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<strong>A<strong>biotic</strong></strong> <strong>and</strong> <strong>biotic</strong> <strong>stresses</strong> <strong>and</strong> <strong>changes</strong> <strong>in</strong> <strong>the</strong> lign<strong>in</strong> content <strong>and</strong><br />
composition <strong>in</strong> plants<br />
Runn<strong>in</strong>g title: Lign<strong>in</strong> <strong>changes</strong> caused by <strong>stresses</strong><br />
Jullyana Crist<strong>in</strong>a Magalhães Silva Moura 1 , Cesar Augusto Valencise Bon<strong>in</strong>e 2 , Juliana<br />
de Oliveira Fern<strong>and</strong>es Viana 1,2 , Marcelo Carnier Dornelas 1 <strong>and</strong> Paulo Mazzafera 1 *<br />
1 Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de<br />
Camp<strong>in</strong>as, CP 6109, 13083-970, Camp<strong>in</strong>as, SP, Brazil<br />
2 Votorantim Celulose e Papel S.A., Rodovia SP 255, Km 41,2, s/nº, 14210-000, Luis<br />
Antonio, SP, Brazil<br />
*Correspond<strong>in</strong>g author:<br />
email: pmazza@unicamp.br<br />
Tel: +55 19 3521 6358
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Abbreviations: PAL - phenylalan<strong>in</strong>e ammonia-lyase; C4H - c<strong>in</strong>namate 4-hydroxylase;<br />
C3H - c<strong>in</strong>namate 3-hydroxylase or p-coumaroyl shikimic acid/qu<strong>in</strong>ic acid 3-<br />
hydroxylase; OMT - O-methyltransferase; HCT - p-hydroxy c<strong>in</strong>namoyl-CoA:<br />
shikimate/qu<strong>in</strong>ate p-hydroxy c<strong>in</strong>namoyl transferase; CCoAOMT - caffeoyl coenzyme A<br />
O-methyltransferase; F5H - ferulate 5-hydroxylase; 4CL - 4-coumarate: coenzyme A<br />
ligase; CCR - c<strong>in</strong>namoyl coenzyme A reductase; Cald5H - coniferaldehyde 5-<br />
hydroxylase; AldOMT - 5-hydroxy coniferaldehyde O-methyltransferase; SAD -<br />
s<strong>in</strong>apyl alcohol dehydrogenase; CAD - c<strong>in</strong>namyl alcohol dehydrogenase.<br />
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Abstract: Lign<strong>in</strong> is a polymer of phenylpropanoid compounds formed through a<br />
complex biosyn<strong>the</strong>sis route, represented by a metabolic grid for which most of <strong>the</strong> genes<br />
<strong>in</strong>volved have been sequenced <strong>in</strong> several plants, ma<strong>in</strong>ly <strong>in</strong> <strong>the</strong> model-plants Arabidopsis<br />
thaliana <strong>and</strong> Populus. Plants are exposed to different <strong>stresses</strong>, which may change lign<strong>in</strong><br />
content <strong>and</strong> composition. In many cases, particularly for plant-microbe <strong>in</strong>teractions, this<br />
has been suggested as defence responses of plants to <strong>the</strong> stress. Thus, underst<strong>and</strong><strong>in</strong>g<br />
how a stressor modulates expression of <strong>the</strong> genes related with lign<strong>in</strong> biosyn<strong>the</strong>sis may<br />
allow us to develop study-models to <strong>in</strong>crease our knowledge on <strong>the</strong> metabolic control of<br />
lign<strong>in</strong> deposition <strong>in</strong> <strong>the</strong> cell wall. This review focuses on recent literature report<strong>in</strong>g on<br />
<strong>the</strong> ma<strong>in</strong> types of a<strong>biotic</strong> <strong>and</strong> <strong>biotic</strong> <strong>stresses</strong> that alter <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> <strong>in</strong> plants.<br />
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Key words: disease, drought, light stress, low temperature, m<strong>in</strong>eral nutrition, plant<br />
growth, plant breed<strong>in</strong>g, reaction wood.<br />
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Introduction<br />
Lign<strong>in</strong> (from <strong>the</strong> Lat<strong>in</strong> word lignum, wood) is a highly branched polymer of<br />
phenylpropanoid compounds, <strong>and</strong> a component of <strong>the</strong> plant cell wall. After cellulose,<br />
lign<strong>in</strong> is <strong>the</strong> second most abundant organic compound <strong>in</strong> plants, represent<strong>in</strong>g<br />
approximately 30% of <strong>the</strong> organic carbon <strong>in</strong> <strong>the</strong> biosphere (Boerjan et al., 2003).<br />
The lignification process seems to have appeared on Earth 430 million years ago<br />
(Boudet, 2000) among <strong>the</strong> possible strategies that allowed plants to adapt to terrestrial<br />
life. The functional significance of lign<strong>in</strong> is associated ma<strong>in</strong>ly with <strong>the</strong> mechanical<br />
support allow<strong>in</strong>g plants to st<strong>and</strong>, with water transport <strong>in</strong> <strong>the</strong> xylem vases <strong>and</strong> as a<br />
defence aga<strong>in</strong>st pests <strong>and</strong> microorganisms (Boudet, 2000). The first two characteristics<br />
are related to <strong>the</strong> way lign<strong>in</strong> <strong>in</strong>teracts with o<strong>the</strong>r molecules of <strong>the</strong> cell wall,<br />
streng<strong>the</strong>n<strong>in</strong>g <strong>the</strong> whole structure.<br />
Despite <strong>the</strong> importance of lign<strong>in</strong> <strong>in</strong> plant evolution <strong>and</strong> development, it<br />
represents a problem for <strong>the</strong> agro-<strong>in</strong>dustrial application of several plants, particularly <strong>in</strong><br />
<strong>the</strong> papermak<strong>in</strong>g <strong>in</strong>dustry. The processes used for <strong>the</strong> separation of lign<strong>in</strong> from <strong>the</strong><br />
cellulose pulp are <strong>the</strong> most costly <strong>and</strong> pollut<strong>in</strong>g parts of <strong>the</strong> whole process (Hatfield <strong>and</strong><br />
Fukushima, 2005). Consequently, several studies have <strong>in</strong>vestigated how to improve<br />
pulp<strong>in</strong>g efficiency (Akgül et al., 2007), as well as alternative pulp<strong>in</strong>g methods<br />
(Khristova et al., 2006; Huang et al., 2007).<br />
In addition to <strong>the</strong> chemical studies try<strong>in</strong>g to f<strong>in</strong>d more efficient <strong>and</strong><br />
environmentally friendly methods for lign<strong>in</strong> extraction, <strong>the</strong>re are also several<br />
laboratories around <strong>the</strong> world seek<strong>in</strong>g to genetically manipulate lign<strong>in</strong> structure <strong>and</strong><br />
content. Genetically modified plants with less lign<strong>in</strong> <strong>and</strong>/or with a different structural<br />
lign<strong>in</strong> composition may allow for improved cellulose yield dur<strong>in</strong>g pulp<strong>in</strong>g <strong>and</strong>, at <strong>the</strong>
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same time, reduce <strong>the</strong> level of pollutants released to <strong>the</strong> environment. Arabidopsis<br />
thaliana <strong>and</strong> Populus have been used as model-plants <strong>in</strong> most of <strong>the</strong>se studies.<br />
With<strong>in</strong> this context, lign<strong>in</strong> biosyn<strong>the</strong>sis has been shown to be <strong>the</strong> result of a<br />
complex genetic network (Rogers <strong>and</strong> Campbel, 2004), where several enzymes are<br />
<strong>in</strong>volved <strong>and</strong> may respond differently to <strong>biotic</strong> <strong>and</strong> a<strong>biotic</strong> effects (Figure 1). In this<br />
regard, <strong>the</strong> literature is rich with examples where lign<strong>in</strong> content <strong>in</strong> <strong>the</strong> plant body is<br />
<strong>in</strong>creased or exhibits a change <strong>in</strong> chemical composition due to stressors, suggest<strong>in</strong>g<br />
complex genetic <strong>and</strong> physiological control. It is possible that underst<strong>and</strong><strong>in</strong>g how a<br />
stressor “modulates” <strong>the</strong> expression of “lign<strong>in</strong> genes” would allow us to develop studymodels<br />
to elucidate genetic control of lign<strong>in</strong> syn<strong>the</strong>sis <strong>and</strong> its deposition <strong>in</strong> <strong>the</strong> cell wall.<br />
Different types of a<strong>biotic</strong> <strong>stresses</strong>, such as m<strong>in</strong>eral deficiency, drought, UV-B<br />
radiation <strong>and</strong> low temperatures, as well as <strong>biotic</strong> <strong>stresses</strong>, such as <strong>in</strong>fection by fungi,<br />
bacteria <strong>and</strong> viruses, cause <strong>changes</strong> <strong>in</strong> <strong>the</strong> lign<strong>in</strong> contents of several plants. Thus, this<br />
review focuses on <strong>the</strong> recent literature report<strong>in</strong>g on <strong>the</strong> ma<strong>in</strong> types of a<strong>biotic</strong> <strong>and</strong> <strong>biotic</strong><br />
<strong>stresses</strong> that alter <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> <strong>in</strong> plants.<br />
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Insert Figure 1<br />
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Low temperatures<br />
Low temperature is an important factor limit<strong>in</strong>g <strong>the</strong> extension of cultivat<strong>in</strong>g<br />
areas <strong>and</strong> <strong>the</strong>refore <strong>the</strong> productivity of grow<strong>in</strong>g several plants. It is known that, <strong>in</strong> many<br />
species, a prior exposure to non-freez<strong>in</strong>g low temperatures allows survival follow<strong>in</strong>g<br />
fur<strong>the</strong>r exposure to freez<strong>in</strong>g temperatures (Ch<strong>in</strong>nusamy et al., 2007). Underst<strong>and</strong><strong>in</strong>g<br />
which mechanisms are <strong>in</strong>volved <strong>in</strong> <strong>the</strong> acclimation to cold would allow researchers to<br />
produce genetically modified plants with greater resistance to low temperatures. This
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would m<strong>in</strong>imize <strong>the</strong> impact of cold on <strong>the</strong> productivity of agriculturally important plants<br />
<strong>and</strong> would also allow <strong>the</strong> expansion of agricultural areas <strong>in</strong> several countries.<br />
The acclimation to cold is a process that <strong>in</strong>volves <strong>changes</strong> <strong>in</strong> gene expression<br />
associated with physiological <strong>and</strong> biochemical <strong>changes</strong>. Dur<strong>in</strong>g cold acclimation of<br />
Arabidopsis, 3379 genes, <strong>in</strong>clud<strong>in</strong>g those cod<strong>in</strong>g for several transcription factors,<br />
exhibit altered expression patterns (Hannah et al., 2005).<br />
In below-zero temperatures, <strong>the</strong> membranes are <strong>the</strong> most <strong>in</strong>jured regions of <strong>the</strong><br />
cell. This damage occurs ma<strong>in</strong>ly due to dehydration caused by <strong>the</strong> formation of<br />
extracellular ice (Steponkus, 1984; Steponkus et al., 1993). O<strong>the</strong>r <strong>in</strong>juries are caused by<br />
reactive oxygen species (Suzuki <strong>and</strong> Mittler, 2006). Therefore, it may be possible to<br />
improve cold tolerance by exam<strong>in</strong><strong>in</strong>g <strong>changes</strong> <strong>in</strong> lipid composition (Thomashow, 1999),<br />
as well as <strong>the</strong> accumulation of sugars, am<strong>in</strong>o acids <strong>and</strong> anti-freeze compounds, such as<br />
anti-freeze prote<strong>in</strong>s (Atici <strong>and</strong> Nalbantoglu, 2003) <strong>and</strong> antioxidant enzymes <strong>and</strong><br />
compounds (Gratão et al., 2005).<br />
Even though we do not know <strong>the</strong> role of lign<strong>in</strong> <strong>in</strong> <strong>the</strong> acclimation to cold, low<br />
temperatures can cause <strong>changes</strong> <strong>in</strong> plant lign<strong>in</strong> content. Ex vitro poplar (Populus<br />
tremula x P. tremuloides L. cv. Muhs1) seedl<strong>in</strong>gs grown at 10 o C showed an <strong>in</strong>crease <strong>in</strong><br />
lign<strong>in</strong> content, but <strong>the</strong> same was not true for <strong>in</strong> vitro seedl<strong>in</strong>gs (Hausman et al., 2000).<br />
The amount of lign<strong>in</strong> <strong>in</strong> latewood Picea abies may be positively correlated with <strong>the</strong><br />
annual average temperature (G<strong>in</strong>dl et al., 2000). Monocots <strong>in</strong> temperate climate regions<br />
exhibit an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> amounts of lign<strong>in</strong>, cellulose <strong>and</strong> hemicellulose with <strong>in</strong>creas<strong>in</strong>g<br />
temperature (Ford et al., 1979).<br />
O<strong>the</strong>r studies showed variation <strong>in</strong> <strong>the</strong> level of phenylpropanoid lign<strong>in</strong> precursors<br />
<strong>and</strong> <strong>in</strong> <strong>the</strong> activities of related enzymes <strong>in</strong> plants exposed to low temperatures. Brassica<br />
napus plants exposed to cold (3 weeks to 2 o C followed by a rapid decl<strong>in</strong>e to -5ºC for
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18h, <strong>the</strong>n followed by 6h at 2 o C) did not show any change <strong>in</strong> <strong>the</strong> levels of lign<strong>in</strong> or cell<br />
wall-bound phenols (Solecka et al., 1999). However, <strong>the</strong>re was an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> levels<br />
of ρ-coumaric acid, ferulic acid <strong>and</strong> synapic acid <strong>in</strong> <strong>the</strong> cells of <strong>the</strong> leaf mesophyll, as<br />
well as an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> esterified soluble forms of <strong>the</strong>se acids, which may be<br />
associated with an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> activity of phenylalan<strong>in</strong>e ammonia-lyase (PAL).<br />
Previous studies showed that B. napus exposed to low temperatures demonstrated<br />
<strong>in</strong>creased PAL activity (Solecka <strong>and</strong> Kacperska, 1995). The <strong>in</strong>crease <strong>in</strong> phenolic acid<br />
esterified soluble forms observed by Solecka et al. (1999) might be a mechanism to<br />
avoid <strong>the</strong> toxic effect on plant cells of free phenols (Whetten <strong>and</strong> Sederoff, 1995). This<br />
would also allow <strong>the</strong>ir transport to <strong>the</strong> vacuoles (Dixon <strong>and</strong> Paiva, 1995), where <strong>the</strong>y<br />
could be used as substrates for peroxidase (Takahama, 1988) to protect <strong>the</strong> cells aga<strong>in</strong>st<br />
reactive oxygen species, s<strong>in</strong>ce this enzyme uses peroxide as oxidiz<strong>in</strong>g substrate<br />
(Takahama <strong>and</strong> Oniki, 1997).<br />
Glyc<strong>in</strong>e max roots also showed <strong>in</strong>creased PAL activity dur<strong>in</strong>g acclimation to<br />
cold (10 o C), accompanied by a significant <strong>in</strong>crease <strong>in</strong> <strong>the</strong> levels of esterified forms of<br />
ferulic, syr<strong>in</strong>gic <strong>and</strong> p-hydroxybenzoic acids (Janas et al., 2000). Such <strong>in</strong>creases were<br />
also suggested to be a mechanism to prevent cell damage, <strong>in</strong>volv<strong>in</strong>g transport to <strong>the</strong><br />
vacuole <strong>and</strong> peroxidase activity as scavenger mechanisms to protect aga<strong>in</strong>st generated<br />
reactive oxygen species.<br />
Peroxidase activity also <strong>in</strong>creased <strong>in</strong> wheat (Taşgına et al., 2006; J<strong>and</strong>a et al.,<br />
2007) <strong>and</strong> Saccharum spp. hybrid (Ja<strong>in</strong> et al., 2007) exposed to low temperature.<br />
Levels of lign<strong>in</strong> <strong>and</strong> soluble phenols were closely related <strong>in</strong> leaves <strong>and</strong> roots of<br />
Triticum aestivum plants at 2 o C (Olenichenko <strong>and</strong> Zagosk<strong>in</strong>a, 2005). While leaves<br />
showed an <strong>in</strong>crease of soluble phenols <strong>and</strong> a decrease of lign<strong>in</strong>, <strong>the</strong> opposite was<br />
observed <strong>in</strong> roots. The accumulation of soluble phenolic compounds was argued to
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correlate with <strong>changes</strong> <strong>in</strong> CO 2 exchange, as <strong>the</strong>re was a smaller reduction <strong>in</strong><br />
photosyn<strong>the</strong>sis as compared to respiration, s<strong>in</strong>ce photosyn<strong>the</strong>sis is less sensitive to low<br />
temperatures. The <strong>in</strong>crease of <strong>the</strong>se compounds was considered a cellular adaptation to<br />
stress, act<strong>in</strong>g as endogenous antioxidant. O<strong>the</strong>r studies with wheat also showed an<br />
<strong>in</strong>crease <strong>in</strong> <strong>the</strong> accumulation of soluble phenolic compounds <strong>in</strong> leaves, but no change <strong>in</strong><br />
lign<strong>in</strong> content was detected (Olenichenko <strong>and</strong> Zagosk<strong>in</strong>a, 2005). However, lign<strong>in</strong><br />
accumulated <strong>in</strong> tiller<strong>in</strong>g nodes; <strong>in</strong> contrast to o<strong>the</strong>r studies where <strong>the</strong> <strong>in</strong>creased amount<br />
of soluble phenolic compounds was correlated with <strong>in</strong>creased PAL activity (Solecka<br />
<strong>and</strong> Kacperska, 1995; Janas et al., 2000), <strong>in</strong> this case less activity was observed <strong>in</strong> both<br />
tissues with a concomitant <strong>in</strong>crease of free L-phenylalan<strong>in</strong>e.<br />
Curiously, some studies have shown that although no <strong>changes</strong> <strong>in</strong> <strong>the</strong> levels of<br />
lign<strong>in</strong> or its precursors were observed <strong>in</strong> plants ma<strong>in</strong>ta<strong>in</strong>ed at low temperatures, <strong>the</strong>re<br />
was an <strong>in</strong>crease <strong>in</strong> related enzyme activities as well as an <strong>in</strong>crease <strong>in</strong> gene expression.<br />
Dur<strong>in</strong>g acclimation of Rhododendron to cold, <strong>the</strong>re was an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> expression of<br />
<strong>the</strong> gene cod<strong>in</strong>g for C3H, a cytochrome P450-dependent monooxygenase <strong>in</strong>volved <strong>in</strong><br />
<strong>the</strong> biosyn<strong>the</strong>sis of phenylpropanoids <strong>and</strong> lign<strong>in</strong> (El Kayal et al., 2006). Accord<strong>in</strong>g to<br />
<strong>the</strong>se authors, <strong>in</strong>creased expression of C3H could result <strong>in</strong> <strong>changes</strong> <strong>in</strong> <strong>the</strong> composition<br />
of lign<strong>in</strong>, alter<strong>in</strong>g <strong>the</strong> stiffness of <strong>the</strong> cell wall.<br />
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Water deficit<br />
Water deficit occurs <strong>in</strong> plants when <strong>the</strong> water supply is <strong>in</strong>sufficient to ma<strong>in</strong>ta<strong>in</strong><br />
growth, photosyn<strong>the</strong>sis <strong>and</strong> transpiration (Fan et al., 2006). This is one of <strong>the</strong> ma<strong>in</strong><br />
problems affect<strong>in</strong>g food production <strong>in</strong> <strong>the</strong> world, reduc<strong>in</strong>g crop productivity (V<strong>in</strong>cent et<br />
al., 2005).
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Very little is known about <strong>the</strong> effects of drought on lign<strong>in</strong> biosyn<strong>the</strong>sis. A<br />
reduction <strong>in</strong> <strong>the</strong> amount of ferulic acid <strong>and</strong> an <strong>in</strong>crease of p-coumaric <strong>and</strong> caffeic acids<br />
<strong>in</strong> <strong>the</strong> xylem sap of maize was observed after 12 days of water uphold<strong>in</strong>g (Alvarez et al.,<br />
2008). It was also detected decreased anionic peroxidase activity <strong>and</strong> <strong>in</strong>creased cationic<br />
peroxidase activity. Accord<strong>in</strong>g to <strong>the</strong> authors, <strong>the</strong> <strong>in</strong>crease of free lign<strong>in</strong> precursors <strong>in</strong><br />
<strong>the</strong> xylem sap as well as <strong>the</strong> reduced anionic peroxidase activity could be an <strong>in</strong>dication<br />
that drought decreases <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> <strong>in</strong> maize (Alvarez et al., 2008).<br />
Different regions of <strong>the</strong> maize root may respond differently to drought, as <strong>the</strong><br />
deposition of lign<strong>in</strong> may be greater <strong>in</strong> a specific region of <strong>the</strong> root or at certa<strong>in</strong> times of<br />
stress (Fan et al., 2006; Yang et al., 2006; Yoshimura et al., 2008).<br />
It has been shown that <strong>the</strong> basal part of <strong>the</strong> roots of maize plants under water<br />
stress exhibit a greater reduction <strong>in</strong> growth than <strong>the</strong> apical region (Fan et al., 2006).<br />
Such a reduction was associated with an <strong>in</strong>creased expression of two genes <strong>in</strong>volved <strong>in</strong><br />
<strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong>: c<strong>in</strong>namoyl-CoA reductase 1 <strong>and</strong> 2. The reduction was also<br />
associated with <strong>in</strong>creased deposition of lign<strong>in</strong>, which stiffened cell wall extensibility<br />
<strong>and</strong> decreased cell wall expansion. In <strong>the</strong>se plants, reduced growth of <strong>the</strong> basal root<br />
might improve <strong>the</strong> availability of water, m<strong>in</strong>erals <strong>and</strong> sugars, factors necessary to<br />
ma<strong>in</strong>ta<strong>in</strong> m<strong>in</strong>imum growth <strong>and</strong> survival of young cells <strong>in</strong> <strong>the</strong> most apical portion,<br />
facilitat<strong>in</strong>g renewed growth after rehydration (Fan et al., 2006).<br />
Researches have shown an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> expression of genes related to cell<br />
growth <strong>and</strong> extensibility <strong>in</strong> <strong>the</strong> roots of rice (Oryza sativa L.) plants dur<strong>in</strong>g <strong>the</strong> <strong>in</strong>itial<br />
stages (16 hours) of water stress, enabl<strong>in</strong>g root growth <strong>in</strong> <strong>the</strong>se plants (Yang et al.,<br />
2006). It was also observed that <strong>the</strong>re was an <strong>in</strong>creased expression of genes <strong>in</strong>volved <strong>in</strong><br />
lign<strong>in</strong> biosyn<strong>the</strong>sis dur<strong>in</strong>g <strong>the</strong> <strong>in</strong>termediate <strong>and</strong> f<strong>in</strong>al stages of water stress (from 48 to<br />
72 hours), such as those cod<strong>in</strong>g for PAL, C3H, 4CL, CCoAOMT, CAD <strong>and</strong> peroxidase.
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Similar results were obta<strong>in</strong>ed with Citrullus lanatus sp., which shows an extraord<strong>in</strong>ary<br />
resistance to drought (Yoshimura et al., 2008). In <strong>the</strong> early stages of stress, this plant<br />
showed an <strong>in</strong>crease <strong>in</strong> root growth, which was associated with <strong>the</strong> <strong>in</strong>duction of <strong>the</strong><br />
syn<strong>the</strong>sis of prote<strong>in</strong>s <strong>in</strong>volved <strong>in</strong> morphogenesis (act<strong>in</strong>, α-tubul<strong>in</strong> <strong>and</strong> Ran GTPase) as<br />
well as <strong>the</strong> metabolism of carbon <strong>and</strong> nitrogen (isoforms of triose-phosphate isomerase,<br />
malate dehydrogenase, α-mannosidase, UDP-sugar pyrophosphorylase, NADP-malic<br />
enzymes, phosphoglucomutase <strong>and</strong> UDP glucose-6-phosphate dehydrogenase). In <strong>the</strong><br />
f<strong>in</strong>al stages of <strong>the</strong> stress, however, <strong>the</strong>re was a reduction <strong>in</strong> root growth <strong>and</strong> <strong>in</strong>duction of<br />
lign<strong>in</strong> biosyn<strong>the</strong>sis, with <strong>in</strong>creas<strong>in</strong>g expression of CCoAOMT <strong>and</strong> a large number of<br />
isoenzymes compris<strong>in</strong>g class III peroxidases. Growth reduction <strong>and</strong> tolerance to<br />
desiccation were associated with more lign<strong>in</strong> <strong>in</strong> <strong>the</strong> roots.<br />
O<strong>the</strong>r plant organs such as leaves may show marked physiological <strong>changes</strong><br />
dur<strong>in</strong>g drought stress. Grow<strong>in</strong>g leaves of maize plants accumulated more COMT,<br />
mostly at 10 to 20 cm from <strong>the</strong> po<strong>in</strong>t of leaf <strong>in</strong>sertion; drought resulted <strong>in</strong> a shift of this<br />
region of maximal accumulation toward basal regions (V<strong>in</strong>cent et al., 2005). The lign<strong>in</strong><br />
content <strong>in</strong> leaves of maize plants subjected to water stress was lower than <strong>in</strong> <strong>the</strong> wellwatered<br />
control plants, suggest<strong>in</strong>g an adaptation to drought, s<strong>in</strong>ce <strong>the</strong> ma<strong>in</strong>tenance of<br />
high levels of lign<strong>in</strong> <strong>in</strong> <strong>the</strong> region of leaf elongation region might negatively affect<br />
growth after rehydration (V<strong>in</strong>cent et al., 2005).<br />
The biosyn<strong>the</strong>sis of lign<strong>in</strong> <strong>and</strong> its functional significance dur<strong>in</strong>g water stress was<br />
studied <strong>in</strong> <strong>the</strong> leaves of Trifolium repens plants subjected to 28 days of drought (Bok-<br />
Rye et al., 2007). Reduced leaf growth occurred concurrently with <strong>the</strong> <strong>in</strong>crease <strong>in</strong> lign<strong>in</strong><br />
biosyn<strong>the</strong>sis. The activities of enzymes <strong>in</strong>volved <strong>in</strong> <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> revealed<br />
that <strong>the</strong> enzyme responses to drought might differ, depend<strong>in</strong>g on <strong>the</strong> period for which<br />
plants are exposed to drought. Overall, <strong>the</strong>re was a large <strong>in</strong>crease <strong>in</strong> <strong>the</strong> activities of
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PAL <strong>and</strong> ascorbate peroxidase <strong>in</strong> <strong>the</strong> early stages of stress (0-14 days), with activity<br />
levels decreas<strong>in</strong>g gradually as <strong>the</strong> period of stress was extended. On <strong>the</strong> o<strong>the</strong>r h<strong>and</strong>,<br />
o<strong>the</strong>r enzymes such as guaiacol peroxidase, coniferyl alcohol peroxidase <strong>and</strong><br />
syr<strong>in</strong>galdaz<strong>in</strong>e peroxidase exhibited greater activity dur<strong>in</strong>g <strong>the</strong> f<strong>in</strong>al stages of stress (14-<br />
28 days).<br />
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Light is essential for plants to ensure normal growth. However, an excess of<br />
light has <strong>the</strong> potential to cause cellular damage, ma<strong>in</strong>ly due to <strong>the</strong> formation of reactive<br />
oxygen species (ROS). To cope with this degenerative stress, plants have evolved<br />
strategies to protect <strong>the</strong>mselves aga<strong>in</strong>st ROS, such as <strong>in</strong>creased peroxidase activity,<br />
accumulation of anthocyan<strong>in</strong>s <strong>and</strong> reduction of <strong>the</strong> antenna systems components to<br />
dissipate <strong>the</strong> energy of absorbed light (Kimura et al., 2003).<br />
Light itself has an effect on lign<strong>in</strong> biosyn<strong>the</strong>sis. Ebenus cretica L. seedl<strong>in</strong>gs<br />
grown <strong>in</strong> <strong>the</strong> light had 2.5 times more lign<strong>in</strong> than seedl<strong>in</strong>gs grown <strong>in</strong> <strong>the</strong> dark (Syros et<br />
al., 2005).<br />
The control of lign<strong>in</strong> biosyn<strong>the</strong>sis by light was <strong>in</strong>vestigated <strong>in</strong> 3-day-old soybean<br />
seedl<strong>in</strong>gs, which were divided <strong>in</strong> three groups: seedl<strong>in</strong>gs kept <strong>in</strong> <strong>the</strong> dark, seedl<strong>in</strong>gs<br />
exposed to light (340 µmol m -2 s -1 ) <strong>and</strong> seedl<strong>in</strong>gs exposed to light (340 µmol m -2 s -1 ,<br />
16h per day) plus diam<strong>in</strong>e oxidase <strong>in</strong>hibitors (Andersson-Gunneras et al., 2006). Plants<br />
<strong>in</strong> <strong>the</strong> light showed <strong>in</strong>creased levels of H 2 O 2 <strong>and</strong> lign<strong>in</strong>, as well as higher levels of<br />
diam<strong>in</strong>e oxidase <strong>and</strong> POD activity. The light plus <strong>in</strong>hibitor condition reduced <strong>the</strong><br />
amount of H 2 O 2 <strong>and</strong> lign<strong>in</strong>.<br />
Dur<strong>in</strong>g <strong>the</strong> differentiation of cultured calli of P<strong>in</strong>us radiata <strong>in</strong>to tracheids, it was<br />
found a positive effect of light on <strong>the</strong> activity of <strong>the</strong> enzymes PAL <strong>and</strong> CAD, which
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resulted <strong>in</strong> an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> concentration of lign<strong>in</strong> when <strong>the</strong> calli were transferred<br />
from dark to a photoperiod of 16 hours (Möller et al., 2006). Cont<strong>in</strong>uous light (16.7 W<br />
m -2 ) <strong>in</strong>creased <strong>the</strong> activity of anionic <strong>and</strong> cationic PODs <strong>and</strong> laccases <strong>in</strong> mungbean<br />
hypocotyls, result<strong>in</strong>g <strong>in</strong> an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> lign<strong>in</strong> content (Chen et al., 2002).<br />
Phalaenopsis orchids ma<strong>in</strong>ta<strong>in</strong>ed for one month at 25ºC ± 2°C at different light<br />
<strong>in</strong>tensities (60, 160 <strong>and</strong> 300 µmol m -2 s -1 ) tended to <strong>in</strong>crease <strong>the</strong> lign<strong>in</strong> content <strong>in</strong> leaves<br />
<strong>and</strong> roots with <strong>in</strong>creas<strong>in</strong>g light <strong>in</strong>tensity, which was associated with <strong>the</strong> <strong>in</strong>duction of<br />
PAL, CAD <strong>and</strong> POD activities (Akgül et al., 2007). It was concluded that <strong>the</strong> <strong>in</strong>crease<br />
<strong>in</strong> <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong>, probably not only provided cell wall rigidity, but also<br />
provided protection aga<strong>in</strong>st radiation stress.<br />
In Arabidopsis thaliana, 7,000 genes exhibited altered expression when plants<br />
were submitted to high light <strong>in</strong>tensity. Among <strong>the</strong>se, 110 showed <strong>in</strong>creased expression,<br />
<strong>and</strong> several of <strong>the</strong>m are <strong>in</strong>volved <strong>in</strong> <strong>the</strong> lign<strong>in</strong> biosyn<strong>the</strong>sis pathway (Kimura et al.,<br />
2003).<br />
The accumulation of gene transcripts cod<strong>in</strong>g for enzymes <strong>in</strong>volved <strong>in</strong> lign<strong>in</strong><br />
biosyn<strong>the</strong>sis <strong>in</strong> A. thaliana varies dur<strong>in</strong>g <strong>the</strong> diurnal cycle, stimulated by light provided<br />
that <strong>the</strong>re is a prior period of darkness (Rogers et al., 2005). It was also observed that <strong>in</strong><br />
<strong>the</strong> sex1 mutant, which is deficient <strong>in</strong> starch metabolism, <strong>the</strong>re was lower expression of<br />
genes <strong>in</strong>volved <strong>in</strong> lign<strong>in</strong> syn<strong>the</strong>sis dur<strong>in</strong>g <strong>the</strong> day, <strong>in</strong>dicat<strong>in</strong>g that <strong>the</strong> availability of<br />
carbohydrate may regulate lign<strong>in</strong> biosyn<strong>the</strong>sis. These mutants accumulated less lign<strong>in</strong><br />
than wild type; lign<strong>in</strong> composition was also changed, with a higher proportion of lign<strong>in</strong>type<br />
S as compared with type G type H (of which <strong>the</strong>re was none). This resulted <strong>in</strong><br />
lign<strong>in</strong> that was easier to extract from <strong>the</strong> cell wall. It was concluded that at least three<br />
factors could affect <strong>the</strong> syn<strong>the</strong>sis of lign<strong>in</strong> <strong>in</strong> <strong>the</strong>se plants: light, circadian rhythms <strong>and</strong><br />
sugar perception.
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UV-B (280-320nm)<br />
In recent years, <strong>the</strong>re has been <strong>in</strong>creased <strong>in</strong>terest <strong>in</strong> <strong>the</strong> biological effects of UV<br />
radiation on liv<strong>in</strong>g organisms, <strong>in</strong> part due to <strong>the</strong> reduction of <strong>the</strong> atmospheric ozone<br />
layer caused by anthropogenic actions, lead<strong>in</strong>g to an <strong>in</strong>crease <strong>in</strong> UV rays reach<strong>in</strong>g <strong>the</strong><br />
Earth’s surface.<br />
Plants <strong>and</strong> animals both undergo morphological, anatomical, physiological <strong>and</strong><br />
biochemical <strong>changes</strong> follow<strong>in</strong>g exposure to UV rays. Among <strong>the</strong> <strong>changes</strong> caused by<br />
UV-B radiation are <strong>in</strong>hibition of growth, <strong>in</strong>creased thickness of leaf blades, reduced<br />
biomass, damage to <strong>the</strong> photosyn<strong>the</strong>sis apparatus, altered membrane composition <strong>and</strong><br />
modifications to <strong>the</strong> balance of phytohormones (Zagosk<strong>in</strong>a et al., 2003). Structural<br />
damage to <strong>the</strong> DNA is also observed, reflected <strong>in</strong> <strong>the</strong> formation of cyclobutane<br />
pyrimid<strong>in</strong>e dimers (CDPs) <strong>and</strong> pyrimid<strong>in</strong>e-(6-4)-pyrimidone (Yamasaki et al., 2007).<br />
Thus, to protect <strong>the</strong>mselves from UV damage, plants produce mechanical<br />
barriers, such as thicker cuticles <strong>and</strong> trichomes; <strong>the</strong>y also syn<strong>the</strong>size protective<br />
substances, such as secondary compounds (Yamasaki et al., 2007). UV-B affects <strong>the</strong><br />
production of several secondary compounds such as flavonoids, tann<strong>in</strong>s <strong>and</strong> lign<strong>in</strong>,<br />
which are thought to have played an important role <strong>in</strong> <strong>the</strong> transition of aquatic plants to<br />
l<strong>and</strong>, when <strong>the</strong>y became more exposed to UV-B radiation (Rozema et al., 1997).<br />
UV-B radiation affected <strong>the</strong> morphogenesis of trichomes <strong>in</strong> <strong>the</strong> cotyledons of<br />
Cucumis sativus L. <strong>and</strong> <strong>in</strong>duced <strong>the</strong> accumulation of lign<strong>in</strong> <strong>in</strong> <strong>the</strong>se structures<br />
(Yamasaki et al., 2007). In a study with two types of Camellia s<strong>in</strong>ensis L. cell cultures<br />
that differed <strong>in</strong> <strong>the</strong>ir capacity to biosyn<strong>the</strong>size <strong>the</strong> phenolic compounds ChS1 <strong>and</strong> ChS-<br />
2, <strong>the</strong> latter had greater capacity for production of phenolic compounds (Zagosk<strong>in</strong>a et<br />
al., 2003). It was observed that under exposure to UV-B radiation, ChS2 demonstrated
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greater accumulation of lign<strong>in</strong> <strong>in</strong> <strong>the</strong> cell walls of <strong>the</strong> parenchyma of tracheid elements<br />
<strong>and</strong> <strong>in</strong> <strong>the</strong> <strong>in</strong>tercellular space, <strong>in</strong> addition to <strong>the</strong> formation of a layer of lign<strong>in</strong>-likematerial<br />
on <strong>the</strong> surface of <strong>the</strong> callus. The ChS2 l<strong>in</strong>eage was also more resistant to UV-<br />
B, suggest<strong>in</strong>g <strong>the</strong> <strong>in</strong>volvement of lign<strong>in</strong> <strong>in</strong> cell protection aga<strong>in</strong>st this type of stress.<br />
Cotyledons of Chenopodium qu<strong>in</strong>oa exposed to UV-B radiation exhibited <strong>in</strong>creased<br />
epidermal cell wall thickness; this was associated with a large accumulation of lign<strong>in</strong><br />
due to <strong>in</strong>creased peroxidase activity (Hilal et al., 2004). Additionally, <strong>changes</strong> <strong>in</strong> <strong>the</strong><br />
ultrastructure of chloroplasts rendered <strong>the</strong>m similar to <strong>the</strong> chloroplasts of shaded plants.<br />
It was suggested that such alterations <strong>in</strong> <strong>the</strong> chloroplast were caused by reduced light<br />
penetration <strong>in</strong> <strong>the</strong> cells of <strong>the</strong> mesophyll, due to <strong>the</strong> protective effect of lign<strong>in</strong><br />
deposition. Therefore, lign<strong>in</strong> <strong>in</strong> epidermal tissue may attenuate radiation.<br />
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Mechanical <strong>in</strong>juries<br />
Injuries <strong>in</strong>duce specific reactions <strong>in</strong> <strong>the</strong> wood which can be restricted to <strong>the</strong> bark<br />
or might extend to <strong>the</strong> cambium <strong>and</strong> xylem (Frankenste<strong>in</strong> et al., 2006). Several studies,<br />
if not most of <strong>the</strong>m, have focused on characteriz<strong>in</strong>g histological <strong>and</strong> anatomical wood<br />
<strong>changes</strong> produced by a particular type of <strong>in</strong>jury, <strong>and</strong> <strong>the</strong> obta<strong>in</strong>ed <strong>in</strong>formation is <strong>the</strong>n<br />
used to expla<strong>in</strong> <strong>the</strong> roles of <strong>the</strong>se <strong>changes</strong> <strong>in</strong> adaptation <strong>and</strong> resistance to stress. In<br />
general, attention has been paid to <strong>the</strong> <strong>changes</strong> occurr<strong>in</strong>g after <strong>in</strong>sect attack or after<br />
microorganism <strong>in</strong>fection. Some species have defence mechanisms that range from<br />
physical barriers <strong>in</strong>clud<strong>in</strong>g cuticle formation, lignification, sp<strong>in</strong>es <strong>and</strong> trichomes to <strong>the</strong><br />
biosyn<strong>the</strong>sis of toxic compounds such as alkaloids <strong>and</strong> tann<strong>in</strong>s (Delessert et al., 2004).<br />
Electron microscopy has demonstrated that <strong>in</strong>juries to <strong>the</strong> stem of Populus spp.<br />
<strong>in</strong>duce <strong>the</strong> thicken<strong>in</strong>g of <strong>the</strong> xylem fibre cell wall <strong>in</strong> three ways: syn<strong>the</strong>sis of an<br />
additional S2 layer, thicken<strong>in</strong>g of <strong>the</strong> exist<strong>in</strong>g cell wall or syn<strong>the</strong>sis of a sclereid-like
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sublayer (Frankenste<strong>in</strong> et al., 2006). The authors also showed, from <strong>the</strong> UVmicrospectrophotometric<br />
determ<strong>in</strong>ations, that cell walls of <strong>the</strong>se xylem modified-fibres<br />
had a higher content of lign<strong>in</strong> <strong>and</strong> uneven distribution of this polymer <strong>in</strong> <strong>the</strong> middle<br />
lamella <strong>and</strong> secondary wall. They concluded that <strong>the</strong> observed <strong>changes</strong> might enable<br />
<strong>the</strong>se plants to resist stress.<br />
Histochemical (phlorogluc<strong>in</strong>ol-HCL) <strong>and</strong> quantitative (acetyl bromide) studies<br />
on <strong>the</strong> accumulation of lign<strong>in</strong> <strong>and</strong> ferulic acid <strong>in</strong> <strong>the</strong> phloem of Chamaecyparis obtusa<br />
exposed to <strong>in</strong>jury (<strong>in</strong>jury of <strong>the</strong> bark near <strong>the</strong> base of <strong>the</strong> stem) reported <strong>the</strong> formation of<br />
a parenchymal zone <strong>and</strong> <strong>in</strong>duction of lignification <strong>in</strong> <strong>the</strong> necrotic phloem (Kusumoto,<br />
2005) after 7 days. The formation of a ligno-suberized layer between <strong>the</strong> necrotic tissue<br />
<strong>and</strong> <strong>the</strong> parenchymatous area was observed after 14 days. It was also observed <strong>the</strong><br />
formation of a callus (due to hyperplasia of cells <strong>in</strong> <strong>the</strong> parenchyma <strong>and</strong> cambium),<br />
which became lignified. The concentration of lign<strong>in</strong> measured <strong>in</strong> <strong>the</strong> cell walls of<br />
necrotic tissues was significantly higher at 28 <strong>and</strong> 56 days after <strong>in</strong>jury. The<br />
concentration of ferulic acid was significantly higher from <strong>the</strong> seventh day after <strong>in</strong>jury,<br />
which suggests that <strong>the</strong> accumulation of ferulic acid occurred before <strong>the</strong> accumulation<br />
of lign<strong>in</strong>.<br />
Given <strong>the</strong> complexity of responses to <strong>in</strong>jury, it is not surpris<strong>in</strong>g that genes of<br />
different metabolic pathways are <strong>in</strong>duced. Thus, various studies have aimed at<br />
identify<strong>in</strong>g which genes are <strong>in</strong>volved <strong>in</strong> this response <strong>and</strong> many have already<br />
demonstrated <strong>the</strong> <strong>in</strong>duction of genes related to lign<strong>in</strong> biosyn<strong>the</strong>sis. The expression of<br />
genes of <strong>the</strong> At4CL family (At4CL1-i), which codes for <strong>the</strong> enzyme 4CL, was studied <strong>in</strong><br />
Arabidopsis thaliana <strong>in</strong> response to <strong>in</strong>jury caused by perforation of <strong>the</strong> leaf with <strong>the</strong> tip<br />
of a pipette (Soltani et al., 2006). 4CL catalyzes <strong>the</strong> conversion of hydroxyc<strong>in</strong>namic<br />
acids <strong>in</strong> CoA esters, which are subsequently reduced to <strong>the</strong> correspond<strong>in</strong>g monolignol
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precursors of lign<strong>in</strong>. The results showed <strong>in</strong>creased expression of At4CL1 <strong>and</strong> At4CL2<br />
dur<strong>in</strong>g two dist<strong>in</strong>ct phases, at 2.5 hours (early phase) <strong>and</strong> 48-72 hours (late) after <strong>in</strong>jury.<br />
The level of At4CL4 transcripts also <strong>in</strong>creased dur<strong>in</strong>g <strong>the</strong> first 2.5 hours, but was later<br />
reduced to lower levels. The expression of At4CL3 was rapidly reduced <strong>in</strong> response to<br />
<strong>in</strong>jury, <strong>and</strong> returned to <strong>in</strong>itial levels after 4 hours; from that po<strong>in</strong>t on, expression<br />
gradually <strong>in</strong>creased. The construction of vectors conta<strong>in</strong><strong>in</strong>g At4CL::GUS showed that<br />
At4CL1::GUS <strong>and</strong> At4CL2::GUS were specific to <strong>the</strong> vascular regions of <strong>the</strong> root <strong>and</strong><br />
aerial parts of <strong>the</strong> plant, unlike AT4CL3::GUS <strong>and</strong> At4CL4::GUS.<br />
The expression of CaF5H1, which codes for F5H, <strong>in</strong>creased <strong>in</strong> detached leaf<br />
discs of Campto<strong>the</strong>ca acum<strong>in</strong>ata plants (Kim et al., 2006). F5H is a cytochrome P450-<br />
dependent monooxygenase that catalyzes <strong>the</strong> hydroxylation of ferulic acid,<br />
coniferaldehyde <strong>and</strong> coniferyl alcohol, promot<strong>in</strong>g <strong>the</strong> biosyn<strong>the</strong>sis of syr<strong>in</strong>gyl lign<strong>in</strong>.<br />
The results suggested that such a response represented protection from mechanical<br />
stress.<br />
As a strategy to avoid pathogen <strong>in</strong>fection <strong>and</strong> water loss, <strong>in</strong>jured leaves of<br />
Arabidopsis thaliana showed <strong>in</strong>creased expression of genes related to lign<strong>in</strong><br />
biosyn<strong>the</strong>sis, cod<strong>in</strong>g for <strong>the</strong> enzymes 4CL, CAD <strong>and</strong> CCR (Delessert et al., 2004). It<br />
was suggested that lign<strong>in</strong> was formed <strong>in</strong> <strong>the</strong> cells surround<strong>in</strong>g <strong>the</strong> wound site.<br />
The removal of <strong>the</strong> stem apex <strong>in</strong> Eucalyptus gunnii caused an <strong>in</strong>crease <strong>in</strong> <strong>the</strong><br />
activities of CAD <strong>and</strong> SAD, enzymes <strong>in</strong>volved <strong>in</strong> <strong>the</strong> f<strong>in</strong>al steps of lign<strong>in</strong> biosyn<strong>the</strong>sis<br />
(Hawk<strong>in</strong>s <strong>and</strong> Boudet, 2003). Microscopy <strong>and</strong> histochemical analyses also detected <strong>the</strong><br />
formation of a "barrier zone" where <strong>the</strong> cell walls exhibited a clear <strong>in</strong>tensification of<br />
lign<strong>in</strong> deposition. This lign<strong>in</strong> was poor <strong>in</strong> S units <strong>and</strong> differed from <strong>the</strong> usual quantity of<br />
G-S that has been reported for this species.<br />
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Reaction wood: tension wood <strong>and</strong> compression wood<br />
Reaction wood (RW) is a type of wood that occurs <strong>in</strong> lean<strong>in</strong>g stems <strong>and</strong><br />
branches <strong>in</strong> order to force <strong>the</strong>m <strong>in</strong>to <strong>the</strong> normal position. Therefore, <strong>in</strong> some way<br />
reaction wood may represent a stress<strong>in</strong>g situation.<br />
In angiosperms, RW develops above <strong>the</strong> lean<strong>in</strong>g region, pull<strong>in</strong>g it up: <strong>in</strong> this<br />
context, it is called tension wood. In gymnosperms, this wood develops below <strong>the</strong><br />
lean<strong>in</strong>g region <strong>and</strong> it is called compression wood; it pushes <strong>the</strong> plant up (Paux et al.,<br />
2005). The wood reaction <strong>in</strong>volves a marked reprogramm<strong>in</strong>g of <strong>the</strong> genes <strong>in</strong>volved <strong>in</strong><br />
cell wall formation <strong>and</strong> <strong>the</strong>refore significantly affects <strong>the</strong> properties of <strong>the</strong> wood<br />
(Déjard<strong>in</strong> et al., 2004).<br />
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Tension wood: A wide variety of characteristics are observed <strong>in</strong> <strong>the</strong> tension wood (TW)<br />
of various angiosperms, but <strong>the</strong> most common type of TW is characterized by hav<strong>in</strong>g<br />
fewer xylem vessel elements, which have a smaller diameter <strong>and</strong> a higher proportion of<br />
fibres with thick walls, more cellulose <strong>and</strong> less lign<strong>in</strong> (Wilson <strong>and</strong> White, 1986). In<br />
addition, TW fibres often develop an additional <strong>in</strong>ternal layer of <strong>the</strong> cell wall called <strong>the</strong><br />
gelat<strong>in</strong>ous layer or G-layer, with higher amounts of cellulose, low microfibril angles<br />
(MFA: angle that <strong>the</strong> cellulose microfibrils form with <strong>the</strong> longitud<strong>in</strong>al axis of <strong>the</strong> fibre)<br />
<strong>and</strong> low levels of lign<strong>in</strong> (Qiu et al., 2008). Normal wood fibres conta<strong>in</strong> a middle<br />
lamella, a th<strong>in</strong> primary wall <strong>and</strong> a thicker secondary wall, which is made of 3 sublayers:<br />
S1, S2 <strong>and</strong> S3 (Clair et al., 2005). In different trees, TW conta<strong>in</strong>s fibres with a<br />
special morphology <strong>and</strong> chemical composition due to <strong>the</strong> development of <strong>the</strong> G-layer,<br />
which replaces <strong>the</strong> S2-layer <strong>and</strong> ei<strong>the</strong>r partially or completely substitutes <strong>the</strong> S3-layer<br />
(Clair et al., 2005).
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The lower amount of lign<strong>in</strong> <strong>in</strong> TW has been attributed ma<strong>in</strong>ly to <strong>the</strong> reduction of<br />
lign<strong>in</strong> <strong>in</strong> <strong>the</strong> G-layer <strong>and</strong> to <strong>changes</strong> <strong>in</strong> <strong>the</strong> relative proportions of monolignols. Dur<strong>in</strong>g<br />
<strong>the</strong> development of TW <strong>in</strong> Eucalyptus vim<strong>in</strong>alis, <strong>the</strong>re is a reduction <strong>in</strong> <strong>the</strong> amount of<br />
lign<strong>in</strong> <strong>and</strong> an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> level of S residues, <strong>in</strong>creas<strong>in</strong>g <strong>the</strong> ratio of syr<strong>in</strong>gyl/guaiacyl<br />
monolignol units (Aoyama et al., 2001). Ultrastructural studies on <strong>the</strong> distribution of<br />
lign<strong>in</strong> <strong>in</strong> cell walls of TW <strong>in</strong> Populus deltoides us<strong>in</strong>g polyclonal antibodies specific to<br />
syn<strong>the</strong>tic polymers of lign<strong>in</strong> showed that, <strong>in</strong> <strong>the</strong>se plants, <strong>the</strong> additional G-layer conta<strong>in</strong>s<br />
low amounts of guaiacyl lign<strong>in</strong> <strong>and</strong> greater amounts of syr<strong>in</strong>gyl lign<strong>in</strong> (Joseleau et al.,<br />
2004). In contrast, <strong>changes</strong> <strong>in</strong> <strong>the</strong> proportion of monolignols <strong>in</strong> <strong>the</strong> lign<strong>in</strong> have not been<br />
observed <strong>in</strong> <strong>the</strong> TW of different eucalyptus species (Rodrigues et al., 2001).<br />
In species that do not have <strong>the</strong> G layer, <strong>the</strong> S2-layer of <strong>the</strong> cell wall has similar<br />
characteristics to those found <strong>in</strong> <strong>the</strong> G-layer. Incl<strong>in</strong>ed branches of two angiosperm<br />
species of <strong>the</strong> primitive genus Magnolia, which does not form a gelat<strong>in</strong>ous layer, have<br />
fewer <strong>and</strong> smaller vessel elements <strong>and</strong> no S3-layer <strong>in</strong> <strong>the</strong> cell walls of xylem tracheids<br />
(Yoshizawa et al., 2000). As expected, <strong>the</strong> presence of a G-layer was not observed;<br />
however, <strong>the</strong> more <strong>in</strong>ternal layer of secondary cell wall (S2-layer) showed<br />
characteristics of a G-layer, with smaller cellulose microfibril angles. Additionally it<br />
was noted that <strong>the</strong> amount of lign<strong>in</strong> sta<strong>in</strong>ed by <strong>the</strong> Wiesner reaction was lower <strong>in</strong> TW<br />
fibres as compared with regions of normal wood, suggest<strong>in</strong>g that <strong>the</strong> amount of lign<strong>in</strong><br />
(ma<strong>in</strong>ly <strong>the</strong> guaiacyl type) would have been reduced. In Liriodendron tulipifera, which<br />
does not form a G-layer <strong>in</strong> TW, it was observed a decrease <strong>in</strong> <strong>the</strong> lign<strong>in</strong> content of<br />
secondary cell walls, while <strong>the</strong> syr<strong>in</strong>gyl/guaiacyl proportion <strong>in</strong>creased. Additionally, it<br />
was also observed an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> amount of cellulose <strong>and</strong> smaller cellulose<br />
microfibril angles (Yoshida et al., 2002).
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Eucalyptus nitens, which rarely exhibits a G-layer, was bent to 45 o . These plants<br />
displayed a TW with high cellulose content, reduced microfibril angle, <strong>and</strong> less Klason<br />
lign<strong>in</strong> (Qiu et al., 2008).<br />
Laeta procera TW has a peculiar polylam<strong>in</strong>ate secondary wall, formed by th<strong>in</strong><br />
lignified layers with small microfibril angles alternat<strong>in</strong>g with layers that are still th<strong>in</strong> but<br />
exhibit greater lignification (Ruelle et al., 2007).<br />
Most of <strong>the</strong> work on TW has focused on anatomical <strong>and</strong> biochemical<br />
characterization of <strong>the</strong> wood, fail<strong>in</strong>g to consider <strong>the</strong> physiological <strong>and</strong> molecular<br />
mechanisms <strong>in</strong>volved. These studies refer only to <strong>changes</strong> <strong>in</strong> quantity or quality<br />
(syr<strong>in</strong>gyl <strong>and</strong> guaiacyl) of lign<strong>in</strong> <strong>and</strong> do not explore which factors are responsible for<br />
<strong>the</strong>se <strong>changes</strong> <strong>in</strong> <strong>the</strong> lignifications process, whe<strong>the</strong>r hormones, prote<strong>in</strong>s or genes.<br />
Aux<strong>in</strong> was thought to be <strong>the</strong> ma<strong>in</strong> hormone <strong>in</strong>volved <strong>in</strong> <strong>in</strong>duc<strong>in</strong>g <strong>the</strong> formation<br />
of reaction wood (Déjard<strong>in</strong> et al., 2004). For years, experiments with exogenous<br />
supplies of aux<strong>in</strong> <strong>and</strong> aux<strong>in</strong> transport <strong>in</strong>hibitors showed that TW can be <strong>in</strong>duced by a<br />
deficiency of aux<strong>in</strong> (Little <strong>and</strong> Savidge, 1987). However, reaction wood (from both<br />
tension <strong>and</strong> compression) can be formed without obvious <strong>changes</strong> <strong>in</strong> <strong>the</strong> balance of<br />
aux<strong>in</strong>. This f<strong>in</strong>d<strong>in</strong>g <strong>in</strong>dicated <strong>the</strong> importance of <strong>in</strong>vestigat<strong>in</strong>g o<strong>the</strong>r factors, such as<br />
mechanisms of aux<strong>in</strong> perception or even o<strong>the</strong>r signall<strong>in</strong>g molecules (Hellgren et al.,<br />
2004). Ethylene appeared as a strong c<strong>and</strong>idate s<strong>in</strong>ce it was observed that this hormone<br />
is distributed asymmetrically <strong>in</strong> <strong>the</strong> TW <strong>and</strong> that expression of a 1-am<strong>in</strong>ocyclopropane-<br />
1-carboxylate oxidase gene (PttACO1) controls <strong>the</strong> process (Andersson-Gunnerås et al.,<br />
2003). In addition, <strong>the</strong>re is a connection between ethylene <strong>and</strong> lignification, as observed<br />
<strong>in</strong> <strong>the</strong> phenotype of Arabidopsis mutants, where a mutation <strong>in</strong> a chit<strong>in</strong>ase gene causes<br />
<strong>the</strong> ectopic expression of CCoAOMT, ectopic deposition of lign<strong>in</strong> <strong>and</strong> <strong>the</strong><br />
overproduction of ethylene (Zhong et al., 2002).
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In addition to ethylene, gibberell<strong>in</strong>s also seem to be related to <strong>the</strong> formation of<br />
reaction wood. It was observed that <strong>the</strong> application of gibberell<strong>in</strong>s to <strong>the</strong> stems of some<br />
angiosperms <strong>in</strong>duces <strong>the</strong> formation of wood with characteristics similar to tension<br />
wood: fibres have <strong>in</strong>ner layers similar to a G-layer, with high cellulose content, small<br />
microfibril angles <strong>and</strong> low lign<strong>in</strong> content (Funada et al., 2008).<br />
In addition to studies of plant hormones, important research has characterized<br />
<strong>the</strong> prote<strong>in</strong>s <strong>in</strong>volved <strong>in</strong> reaction wood formation. SDS-PAGE comparisons of <strong>the</strong><br />
pattern of prote<strong>in</strong> accumulation <strong>in</strong> TW <strong>and</strong> normal wood showed <strong>the</strong> presence of at least<br />
five prote<strong>in</strong>s <strong>in</strong>duced dur<strong>in</strong>g <strong>the</strong> formation of TW (Baba et al., 2000). The extraction<br />
conditions used <strong>in</strong> <strong>the</strong> protocols led <strong>the</strong> authors to suggest that <strong>the</strong>se five prote<strong>in</strong>s were<br />
cell wall- or membrane-bound prote<strong>in</strong>s. Additionally, a study on peroxidase activity<br />
showed that <strong>the</strong> <strong>in</strong>crease <strong>in</strong> <strong>the</strong> S/G ratio, generally observed <strong>in</strong> TW, could be partly<br />
attributed to <strong>the</strong> <strong>in</strong>creased activity of a syr<strong>in</strong>galdaz<strong>in</strong>e peroxidase ionically l<strong>in</strong>ked to <strong>the</strong><br />
cell wall (Aoyama et al., 2001).<br />
The molecular mechanisms <strong>in</strong>volved <strong>in</strong> <strong>the</strong> formation reaction wood <strong>and</strong> <strong>the</strong>ir<br />
relationship to metabolomics data have been <strong>in</strong>vestigated. However, due to <strong>the</strong><br />
complexity of differential accumulation of lign<strong>in</strong> <strong>in</strong> TW, very little is known about <strong>the</strong><br />
genes <strong>in</strong>volved <strong>in</strong> <strong>the</strong> process.<br />
ESTs obta<strong>in</strong>ed from different wood tissues, among <strong>the</strong>m TW <strong>and</strong> opposite wood<br />
from <strong>the</strong> poplar (Populus tremula x P. alba), <strong>in</strong>dicated <strong>the</strong> presence of some genes<br />
specific to <strong>the</strong>se tissues (Déjard<strong>in</strong> et al., 2004). In tissues under tension, ESTs related to<br />
arab<strong>in</strong>ogalactan prote<strong>in</strong>-like (AGP), fructok<strong>in</strong>ase <strong>and</strong> sucrose synthase were abundant.<br />
In contrast, <strong>the</strong> opposite wood exhibited greater CCoA-OMT expression, which is<br />
consistent with <strong>the</strong> high levels of lign<strong>in</strong> syn<strong>the</strong>sis observed <strong>in</strong> this wood.
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The <strong>in</strong>creased expression of fascicl<strong>in</strong>-like arab<strong>in</strong>ogalactan prote<strong>in</strong>s was also<br />
observed <strong>in</strong> G-fibres <strong>in</strong> ano<strong>the</strong>r poplar hybrid (Populus tremula x P. tremuloides)<br />
(Andersson-Gunneras et al., 2006). In addition, several genes <strong>in</strong>volved <strong>in</strong> lign<strong>in</strong><br />
biosyn<strong>the</strong>sis exhibited reduced expression <strong>in</strong> <strong>the</strong> TW: PttPAL1, PttCCoAOMT1, 4CL,<br />
HCT, C3H, CCR, F5H, COMT <strong>and</strong> CAD. A MYB transcription factor (PttMYB21a)<br />
previously shown to repress biosyn<strong>the</strong>sis of lign<strong>in</strong> displayed elevated expression levels.<br />
Branches of artificially <strong>in</strong>cl<strong>in</strong>ed Eucalyptus globulus showed that <strong>the</strong> expression<br />
of a cellulose synthase gene (EgCesA) was correlated with <strong>the</strong> appearance of <strong>the</strong> G-<br />
layer (Paux et al., 2005). The lign<strong>in</strong> biosyn<strong>the</strong>sis genes for which expression changed<br />
dur<strong>in</strong>g TW formation <strong>in</strong>cluded: 4CL, CCR, CAD, COMT, <strong>and</strong> CCoAOMT. The response<br />
of <strong>the</strong>se genes was varied <strong>and</strong> complex, with different patterns of expression for each<br />
gene. The 4CL, CCR <strong>and</strong> CAD genes exhibited reduced expression dur<strong>in</strong>g <strong>the</strong> first 6 h<br />
of stress but <strong>the</strong> transcript levels were similar to those observed <strong>in</strong> control plants after a<br />
week. Accord<strong>in</strong>g to <strong>the</strong> authors, this variation could not expla<strong>in</strong> <strong>the</strong> reduced amount of<br />
lign<strong>in</strong> often observed <strong>in</strong> tension wood; <strong>the</strong> lower amount of lign<strong>in</strong>, ma<strong>in</strong>ly G-type, was<br />
probably due to <strong>the</strong> differential expression of CCoAOMT <strong>and</strong> COMT, genes that encode<br />
methylation enzymes.<br />
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Compression wood: Compression wood (CW) has small <strong>and</strong> rounded tracheids with<br />
thicker cell walls, higher lign<strong>in</strong> content, less cellulose, large microfibril angles, <strong>and</strong><br />
typically lacks <strong>the</strong> S3 layer (McDougall, 2000; Donaldson et al., 2004; Yeh et al., 2005;<br />
Yeh et al., 2006). Additionally, <strong>the</strong> lign<strong>in</strong> <strong>in</strong> this wood has high levels of p-<br />
hydroxyphenylpropane units (Monties, 1989) <strong>and</strong> alterations <strong>in</strong> <strong>the</strong> chemical l<strong>in</strong>ks<br />
between lign<strong>in</strong> units, when compared with normal wood (Nimz et al., 1981).
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As <strong>in</strong> TW, <strong>the</strong> chemical <strong>and</strong> anatomical characteristics of <strong>the</strong> CW are <strong>the</strong> results<br />
of various altered molecular <strong>and</strong> physiological factors. Unravell<strong>in</strong>g <strong>the</strong>se factors will be<br />
necessary to underst<strong>and</strong> <strong>the</strong> mechanisms <strong>in</strong>volved <strong>and</strong> elucidate lign<strong>in</strong> biosyn<strong>the</strong>sis <strong>in</strong><br />
wood. Many studies have already identified prote<strong>in</strong>s <strong>and</strong> genes potentially responsible<br />
for <strong>the</strong> different characteristics of CW, <strong>in</strong>clud<strong>in</strong>g <strong>the</strong> high amount of lign<strong>in</strong>.<br />
The comparison of prote<strong>in</strong>s <strong>in</strong> CW <strong>and</strong> <strong>in</strong> <strong>the</strong> opposite normal wood showed that<br />
<strong>the</strong> presence of a dioxygenase related to <strong>the</strong> biosyn<strong>the</strong>sis of anthocyan<strong>in</strong>s<br />
(leucoanthocyanid<strong>in</strong> dioxygenase) might contribute to <strong>the</strong> colour of this reddish wood<br />
(Gion et al., 2005).<br />
O<strong>the</strong>r prote<strong>in</strong>s abundant <strong>in</strong> this type of wood are: 1-am<strong>in</strong>ocyclopropane-1-<br />
carboxylate oxidase, an enzyme that catalyzes <strong>the</strong> conversion of 1-am<strong>in</strong>ocyclopropane-<br />
1-carboxylate to ethylene; glutam<strong>in</strong>e syn<strong>the</strong>tase <strong>and</strong> fructok<strong>in</strong>ase, enzymes <strong>in</strong>volved <strong>in</strong><br />
<strong>the</strong> assimilation of nitrogen <strong>and</strong> carbon; malate dehydrogenase, an enzyme of <strong>the</strong> Krebs<br />
cycle (Plomion et al., 2000); glyceraldehyde-3-phosphate dehydrogenase (G3PDH), an<br />
enzyme related to energy production <strong>and</strong> metabolism; <strong>and</strong> α-tubul<strong>in</strong>, <strong>the</strong> ma<strong>in</strong><br />
component of cortical microtubules (Le Provost et al., 2003).<br />
O<strong>the</strong>r studies have reported on prote<strong>in</strong>s possibly more directly <strong>in</strong>volved <strong>in</strong> <strong>the</strong><br />
differential accumulation of lign<strong>in</strong>. A polypeptide correspond<strong>in</strong>g to a laccase-type of<br />
polyphenol oxidase, which is <strong>in</strong>volved <strong>in</strong> <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong>, has higher activity<br />
<strong>in</strong> develop<strong>in</strong>g xylem <strong>in</strong> <strong>the</strong> CW of Picea sitchensis, as compared to non-compressed<br />
wood (McDougall, 2000).<br />
Twenty-six prote<strong>in</strong>s whose expression was correlated with an <strong>in</strong>crease <strong>in</strong> <strong>the</strong><br />
degree of compression were identified <strong>in</strong> P<strong>in</strong>us p<strong>in</strong>aster, <strong>in</strong>clud<strong>in</strong>g two methylat<strong>in</strong>g<br />
enzymes <strong>in</strong>volved <strong>in</strong> lign<strong>in</strong> biosyn<strong>the</strong>sis - COMT <strong>and</strong> CCoAOMT – <strong>and</strong> members of <strong>the</strong><br />
S-adenosyl-L-methion<strong>in</strong>e syn<strong>the</strong>tase gene family. In addition to be<strong>in</strong>g enzymes
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<strong>in</strong>volved <strong>in</strong> <strong>the</strong> response to ethylene, this gene family also plays a role <strong>in</strong> <strong>the</strong><br />
methylation of monolignols dur<strong>in</strong>g <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> (Plomion et al., 2000).<br />
Sequenced cDNAs from CW <strong>and</strong> normal wood of P<strong>in</strong>us taeda showed that <strong>the</strong><br />
genes that were most abundant <strong>in</strong> <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> code for <strong>the</strong> enzymes PAL,<br />
C4H, OMT, 4CL, CAD, diphenol oxidase (laccase) <strong>and</strong> POD (Allona et al., 1998).<br />
The R2R3-MYB transcription factors, which have been associated with <strong>the</strong><br />
biosyn<strong>the</strong>sis of lign<strong>in</strong>, also display elevated expression <strong>in</strong> CW (Bedon et al., 2007).<br />
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M<strong>in</strong>eral nutrition <strong>and</strong> heavy metals<br />
Deficiency disability <strong>and</strong> abnormally high concentrations of a nutrient can both<br />
cause abnormalities <strong>in</strong> <strong>the</strong> accumulation of lign<strong>in</strong>, where this has been documented by<br />
many studies. Most of <strong>the</strong>se, however, do not <strong>in</strong>clude a study of <strong>the</strong> physiological or<br />
molecular causes of <strong>the</strong>ir f<strong>in</strong>d<strong>in</strong>gs. Recent reports have also shown that lign<strong>in</strong> content<br />
may be affected by toxic heavy metals.<br />
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Nitrogen (N): Few studies were conducted to assess <strong>the</strong> impact of fertilization with N<br />
on <strong>the</strong> properties of wood (Luo et al., 2005; Liberloo et al., 2006); most of <strong>the</strong>se<br />
<strong>in</strong>vestigated grasses used as forage for animal feed<strong>in</strong>g, show<strong>in</strong>g that lign<strong>in</strong> content was<br />
<strong>in</strong>creased by N due to elevated PAL activity (Pitre et al., 2007).<br />
Moreover, <strong>the</strong> effect of N seems to vary with <strong>the</strong> type, degree of development<br />
<strong>and</strong> tissue exam<strong>in</strong>ed. In p<strong>in</strong>e (P<strong>in</strong>us palustris) seedl<strong>in</strong>gs, high-N fertilization reduced<br />
<strong>the</strong> lign<strong>in</strong> content <strong>in</strong> roots but had no effect on <strong>the</strong> lign<strong>in</strong> concentration <strong>in</strong> aerial parts of<br />
<strong>the</strong> plant (Entry et al., 1998).
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In red p<strong>in</strong>e (P<strong>in</strong>us res<strong>in</strong>osa), comb<strong>in</strong>ed nitrogen-phosphorus-potassium (NPK)<br />
fertilization reduced <strong>the</strong> lign<strong>in</strong> content of branches (Blodgett et al., 2005) but had an<br />
opposite effect on <strong>the</strong> ma<strong>in</strong> stem of Picea abies (Kostia<strong>in</strong>en et al., 2004).<br />
Populus plants receiv<strong>in</strong>g high concentrations of nitrogen (10 mM NH 4 NO 3 ) had<br />
less lign<strong>in</strong>, reduced β-O-4 l<strong>in</strong>kage, <strong>in</strong>creased frequency of ρ-hydroxyphenyl units <strong>and</strong> a<br />
tendency toward low S/G ratios (Pitre et al., 2007).<br />
At <strong>the</strong> molecular level, <strong>the</strong> expression of <strong>the</strong> pot171 gene, which encodes a<br />
prote<strong>in</strong> similar to CCoAOMT, is negatively regulated <strong>in</strong> response to nitrogen <strong>in</strong> Populus<br />
trichocarpa x deltoid hybrids (Cooke et al., 2003).<br />
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Calcium (Ca): The effect of Ca on <strong>the</strong> biosyn<strong>the</strong>sis of phenylpropanoids is not<br />
sufficiently clear. Some studies have shown that Ca <strong>in</strong>creases <strong>the</strong> activity of guaiacol-<br />
POD <strong>and</strong> PAL (Castañeda <strong>and</strong> Pérez, 1996; Kolupaev et al., 2005); however, a<br />
reduction <strong>in</strong> <strong>the</strong> amount of phenolic compounds has also been reported (de Obeso et al.,<br />
2003). O<strong>the</strong>r authors observed a reduction <strong>in</strong> PAL <strong>and</strong> POD activity (soluble <strong>and</strong> cell<br />
wall-bound), as well as reductions <strong>in</strong> <strong>the</strong> levels of phenolic compounds, <strong>in</strong>clud<strong>in</strong>g lign<strong>in</strong><br />
(Teixeira et al., 2006). No substantial <strong>changes</strong> <strong>in</strong> <strong>the</strong> amounts of <strong>the</strong>se compounds was<br />
observed (Tomas-Barberan et al., 1997).<br />
In Populus tremula x Populus tremuloides, Ca deficiency was responsible for<br />
wood deformation, which <strong>in</strong>cluded smaller diameter of xylem vessels, shorter fibre<br />
length <strong>and</strong> reduced levels of S units <strong>in</strong> lign<strong>in</strong> (Lautner et al., 2007). Therefore, it seems<br />
that Ca is necessary for <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> <strong>in</strong> plants. It is important to note that<br />
several PODs are l<strong>in</strong>ked to <strong>the</strong> galacturonic doma<strong>in</strong>s of pect<strong>in</strong> <strong>in</strong> <strong>the</strong> presence of Ca<br />
(Penel <strong>and</strong> Grepp<strong>in</strong>, 1996) <strong>and</strong> such a l<strong>in</strong>k occurs only <strong>in</strong> <strong>the</strong> pect<strong>in</strong> cha<strong>in</strong> that is crossl<strong>in</strong>ked<br />
to Ca, known as Ca-pectates (Carp<strong>in</strong> et al., 2001). S<strong>in</strong>ce <strong>the</strong> middle lamella <strong>and</strong>
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cell corners are rich <strong>in</strong> Ca-pectates (Carpita <strong>and</strong> Gibeaut, 1993) <strong>and</strong> are <strong>the</strong> first places<br />
to be lignified, POD l<strong>in</strong>ked to <strong>the</strong>se cha<strong>in</strong>s of Ca-pectates might play a role <strong>in</strong><br />
controll<strong>in</strong>g <strong>the</strong> spatial deposition of lign<strong>in</strong>, <strong>and</strong> <strong>changes</strong> <strong>in</strong> <strong>the</strong> concentrations of Ca<br />
would def<strong>in</strong>e <strong>the</strong> location of <strong>the</strong>se PODs (Carp<strong>in</strong> et al., 2001).<br />
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Copper (Cu): It is known that copper has a positive effect on <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong>.<br />
Thus, Cu deficiency results <strong>in</strong> less lign<strong>in</strong> (Robson et al., 1981), <strong>and</strong> excess Cu results <strong>in</strong><br />
more lign<strong>in</strong>.<br />
Capsicum annuum hypocotyls grown <strong>in</strong> a nutrient solution with excess copper<br />
(50 mM CuSO 4 ) showed higher levels of shikimate dehydrogenase <strong>and</strong> POD activity<br />
<strong>and</strong> greater accumulation of soluble phenolic compounds <strong>and</strong> lign<strong>in</strong> (Diaz et al., 2001).<br />
Roots of Raphanus sativus grown <strong>in</strong> <strong>the</strong> presence of Cu (1-10 mM CuSO 4 ) showed<br />
higher levels of cationic <strong>and</strong> anionic POD activities <strong>and</strong> higher levels of lign<strong>in</strong> <strong>in</strong><br />
comparison with plants grown <strong>in</strong> <strong>the</strong> absence of this element; <strong>the</strong> <strong>in</strong>creases were dosedependent<br />
(Chen et al., 2002).<br />
Laccases were responsible for <strong>the</strong> extracellular polymerization of monolignols <strong>in</strong><br />
<strong>the</strong> roots of soybean plants dur<strong>in</strong>g <strong>the</strong> early stages of Cu exposure. Later, POD activity<br />
<strong>in</strong>creases, work<strong>in</strong>g cooperatively with laccases <strong>in</strong> <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> (Barnes et<br />
al., 1997).<br />
Exposure of Panax g<strong>in</strong>seng root suspension cultures to <strong>in</strong>creas<strong>in</strong>g concentrations<br />
of Cu led to an enhancement of <strong>the</strong> activities of glucose-6-phosphate dehydrogenase,<br />
shikimate dehydrogenase, PAL <strong>and</strong> CAD <strong>and</strong> to <strong>the</strong> accumulation of phenolic<br />
compounds <strong>and</strong> lign<strong>in</strong>. It also caused an <strong>in</strong>crease <strong>in</strong> levels of caffeic acid-POD,<br />
polyphenol oxidase <strong>and</strong> β-glucosidase (Akgül et al., 2007).
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Thus, lign<strong>in</strong> accumulates <strong>in</strong> plant cell walls <strong>in</strong> <strong>the</strong> presence of Cu. This process<br />
is correlated with enhanced activities of several enzymes, <strong>in</strong>clud<strong>in</strong>g POD <strong>and</strong> laccases,<br />
which are enzymes that carry out <strong>the</strong> polymerization of monolignol precursors of lign<strong>in</strong>.<br />
This could be partly expla<strong>in</strong>ed by <strong>the</strong> fact that Cu is structurally important for laccases<br />
(Claus, 2004). It appears also that Cu has functional importance <strong>in</strong> terms of peroxidase<br />
activity, s<strong>in</strong>ce an am<strong>in</strong>e oxidase conta<strong>in</strong><strong>in</strong>g Cu that generates H 2 O 2 by oxidis<strong>in</strong>g<br />
putresc<strong>in</strong>e has been co-located with lign<strong>in</strong> <strong>and</strong> with POD activity <strong>in</strong> tracheid elements<br />
of xylem <strong>in</strong> Arabidopsis (Møller <strong>and</strong> McPherson, 1998).<br />
However, Cu also mediates an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> activity of o<strong>the</strong>r enzymes of <strong>the</strong><br />
lign<strong>in</strong> biosyn<strong>the</strong>sis pathway, such as PAL <strong>and</strong> CAD. This could be an <strong>in</strong>direct effect of<br />
this metal, which enhances oxidation <strong>and</strong> polymerization of monolignols via laccases;<br />
peroxidase would stimulate (by feedback) <strong>the</strong> syn<strong>the</strong>sis of <strong>the</strong>se monolignols.<br />
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Boron <strong>and</strong> Z<strong>in</strong>c: Boric acid at 5 mM <strong>in</strong>creased <strong>the</strong> activities of PAL <strong>and</strong><br />
syr<strong>in</strong>galdaz<strong>in</strong>e-POD <strong>and</strong> <strong>in</strong>creased <strong>the</strong> lign<strong>in</strong> content <strong>in</strong> soybean (Ghanati et al., 2005).<br />
At high concentrations of Zn, both A. thaliana <strong>and</strong> Thlaspi caeru lescens showed<br />
<strong>in</strong>creased expression of genes related to <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> (van de Mortel et al.,<br />
2006). However, <strong>in</strong> T. Caerulescens, a Zn hyper-accumulator, <strong>the</strong> expression of <strong>the</strong>se<br />
genes was even greater. This could be related to <strong>the</strong> ability of this species to adapt to<br />
higher concentrations of Zn. Among <strong>the</strong> genes that had higher expression <strong>in</strong> T.<br />
caerulescens than <strong>in</strong> A. thaliana were genes related to dirigent prote<strong>in</strong>s, 4CL, CCR,<br />
F5H, CAD, CCoAOMT <strong>and</strong> laccase.<br />
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Metals - Alum<strong>in</strong>ium (Al) <strong>and</strong> Cadmium: Al is one of <strong>the</strong> ma<strong>in</strong> factors <strong>in</strong>hibit<strong>in</strong>g plant<br />
growth <strong>in</strong> acidic tropical soils. A typical symptom of Al toxicity is <strong>the</strong> <strong>in</strong>hibition of root
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growth (Tahara et al., 2005). Excess of Al causes <strong>in</strong>creased lign<strong>in</strong> deposition <strong>in</strong> <strong>the</strong> cell<br />
walls of some plant species (Sasaki et al., 1996; Budíková, 1999). In plants susceptible<br />
to Al, lign<strong>in</strong> accumulation is even higher, dramatically reduc<strong>in</strong>g growth; growth<br />
<strong>in</strong>hibition is strongly correlated with <strong>the</strong> extent to which lign<strong>in</strong> is deposited <strong>in</strong> <strong>the</strong> cell<br />
wall, <strong>in</strong>dependently of <strong>the</strong> tolerance to this metal (Sasaki et al., 1996).<br />
Among several species of Myrtaceae, only <strong>the</strong> most sensitive to Al shows<br />
<strong>in</strong>creased lign<strong>in</strong> content when exposed to high concentrations of alum<strong>in</strong>ium (Tahara et<br />
al., 2005).<br />
Camellia s<strong>in</strong>ensis is know to be highly tolerant to Al, <strong>and</strong> its growth is<br />
stimulated by high concentrations of this element (Lima et al., 2009). When this species<br />
was grown <strong>in</strong> high concentrations of Al, <strong>the</strong>re was a reduction <strong>in</strong> <strong>the</strong> activities of PAL<br />
<strong>and</strong> POD bound to <strong>the</strong> cell wall, as well as a reduction <strong>in</strong> lign<strong>in</strong> content, which might<br />
expla<strong>in</strong> enhanced growth of <strong>the</strong>se plants <strong>in</strong> <strong>the</strong> presence of Al (Ghanati et al., 2005).<br />
It was also demonstrated that Al <strong>in</strong>duces <strong>the</strong> expression of genes cod<strong>in</strong>g for<br />
enzymes of <strong>the</strong> lign<strong>in</strong> biosyn<strong>the</strong>sis pathway. Both resistant <strong>and</strong> sensitive rice (Oriza<br />
sativa) plants under Al stress exhibited <strong>in</strong>creased expression of 4CL, PAL, CAD <strong>and</strong><br />
C3H (Chuanzao et al., 2004). Nor<strong>the</strong>rn blot analysis <strong>in</strong>dicated that <strong>the</strong> temporal patterns<br />
of expression differ between <strong>the</strong> two varieties <strong>and</strong>, additionally, that transcripts of PAL<br />
accumulated more <strong>in</strong>tensively <strong>in</strong> <strong>the</strong> sensitive variety. Al also <strong>in</strong>duces expression of<br />
PAL <strong>in</strong> wheat (Snowden <strong>and</strong> Gardner, 1993).<br />
Cd is a heavy metal pollutant, not essential for plants, which enters <strong>the</strong><br />
environment primarily through <strong>in</strong>dustrial processes <strong>and</strong> phosphate fertilizers. Among its<br />
many effects on plants, Cd may <strong>in</strong>duce <strong>the</strong> syn<strong>the</strong>sis of lign<strong>in</strong>. This was observed <strong>in</strong><br />
roots of Phragmites australis (Ederli et al., 2004) <strong>and</strong> callus tissue culture from <strong>the</strong><br />
roots <strong>and</strong> branches of C. s<strong>in</strong>ensis (Zagosk<strong>in</strong>a et al., 2007).
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Cd concentrations vary<strong>in</strong>g from 0.2 mM to 1 mM reduced <strong>the</strong> growth of soybean<br />
roots <strong>and</strong> <strong>in</strong>creased <strong>the</strong> lign<strong>in</strong> content (Bhuiyan et al., 2007). This was accompanied by<br />
<strong>in</strong>creased POD (cationic <strong>and</strong> anionic) activity, elevated laccase activity, <strong>and</strong> <strong>in</strong>creased<br />
expression of genes related to POD. The authors also noted that <strong>the</strong> laccases are<br />
responsible for <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong> dur<strong>in</strong>g <strong>the</strong> <strong>in</strong>itial stages of treatment with Cd<br />
<strong>and</strong> that POD participation become important at later stages.<br />
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Gases (CO 2 <strong>and</strong> Ozone)<br />
It is expected that atmospheric concentrations of CO 2 will change from 360<br />
μmol -1 to 550-1000 μmol -1 <strong>in</strong> <strong>the</strong> next 100 years. This will probably <strong>in</strong>terfere with <strong>the</strong><br />
primary <strong>and</strong> secondary metabolism of plants (Davey et al., 2004).<br />
With respect to secondary metabolism, it is known that high concentrations of<br />
CO 2 <strong>in</strong>terfere with <strong>the</strong> biosyn<strong>the</strong>sis of lign<strong>in</strong>. But it has been observed both <strong>in</strong>creases <strong>in</strong><br />
(Koricheva et al., 1998; Richard et al., 2001), reduction <strong>in</strong> (Knops et al., 2007) or even<br />
no effect on <strong>the</strong> concentration of lign<strong>in</strong> (Cotrufo et al., 2005) with <strong>in</strong>creas<strong>in</strong>g rates of<br />
CO 2 . Moreover, <strong>the</strong> response to high CO 2 concentrations is <strong>in</strong>fluenced by fertilization<br />
with N (Matros et al., 2006). Accord<strong>in</strong>gly, high concentrations of CO 2 <strong>in</strong> <strong>the</strong> roots of<br />
Nicotiana tabacum cv. Samsun-NN grown <strong>in</strong> 5 mM of NH 4 NO 3 led to an <strong>in</strong>crease <strong>in</strong><br />
lign<strong>in</strong> content; however, under 8 mM of NH 4 NO 3 , no <strong>changes</strong> <strong>in</strong> <strong>the</strong> levels of lign<strong>in</strong><br />
were observed (Matros et al., 2006).<br />
Plantago maritima ma<strong>in</strong>ta<strong>in</strong>ed for a year <strong>in</strong> an atmosphere of 600 μmol CO 2<br />
638<br />
mol -1<br />
showed an <strong>in</strong>crease <strong>in</strong> <strong>the</strong> biomass of stems <strong>and</strong> roots <strong>and</strong> <strong>changes</strong> <strong>in</strong><br />
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vascularization <strong>and</strong> lignification when compared with plants kept <strong>in</strong> normal<br />
concentrations of CO 2 (Davey et al., 2004). An atmosphere rich <strong>in</strong> CO 2 resulted <strong>in</strong> a
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higher concentration of caffeic acid <strong>in</strong> <strong>the</strong> leaves, while <strong>the</strong>re was an <strong>in</strong>crease of p-<br />
coumaric acid <strong>in</strong> <strong>the</strong> roots.<br />
Both <strong>the</strong> enzyme activity <strong>and</strong> gene expression of PAL (Paakkonen et al., 1998),<br />
4CL (Booker <strong>and</strong> Miller, 1998), COMT (Koch et al., 1998) <strong>and</strong> CAD (Booker <strong>and</strong><br />
Miller, 1998; Z<strong>in</strong>ser et al., 1998) are stimulated by exposure to ozone. It was also<br />
observed <strong>in</strong>creased shikimate dehydrogenase activity <strong>in</strong> leaves of Populus tremula X<br />
alba, as well as elevated lign<strong>in</strong> content <strong>and</strong> <strong>changes</strong> <strong>in</strong> lign<strong>in</strong> structure (Cabane et al.,<br />
2004).<br />
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Biotic <strong>stresses</strong> (bacteria, fungi <strong>and</strong> virus)<br />
An <strong>in</strong>crease <strong>in</strong> lignification is often observed <strong>in</strong> response to attack by pathogen.<br />
The response is believed to represent one of a plethora of mechanisms designed to block<br />
parasite <strong>in</strong>vasion, thus reduc<strong>in</strong>g <strong>the</strong> susceptibility of <strong>the</strong> host, s<strong>in</strong>ce lign<strong>in</strong> is a nondegradable<br />
mechanical barrier for most microorganisms.<br />
Two genes cod<strong>in</strong>g for CCR (AtCCR1 <strong>and</strong> AtCCR2) <strong>in</strong> A. thaliana are<br />
differentially expressed upon <strong>in</strong>fection with Xanthomonas campestris. AtCCR1 is<br />
preferentially expressed <strong>in</strong> <strong>the</strong> normal development of tissues, while AtCCR2 shows<br />
lower expression. However, this relation is reversed <strong>in</strong> response to <strong>the</strong> attack by X.<br />
Campestris, <strong>in</strong>dicat<strong>in</strong>g that <strong>the</strong>se genes might participate <strong>in</strong> <strong>the</strong> hypersensitive response<br />
to <strong>the</strong> pathogen.<br />
Agrobacterium <strong>in</strong>duces <strong>the</strong> production of ferulic acid <strong>in</strong> wheat. Ferulic acid is a<br />
precursor <strong>in</strong> lign<strong>in</strong> biosyn<strong>the</strong>sis, suggest<strong>in</strong>g <strong>the</strong> existence of a defence response<br />
prevent<strong>in</strong>g <strong>in</strong>fection by <strong>the</strong> bacteria <strong>in</strong> <strong>the</strong>se plants (Parrott et al., 2002).<br />
No <strong>changes</strong> occurred <strong>in</strong> <strong>the</strong> lign<strong>in</strong> content of wheat leaves <strong>in</strong>fected with mosaic<br />
virus (Kofalvi <strong>and</strong> Nassuth, 1995).
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Several authors have shown <strong>changes</strong> <strong>in</strong> lign<strong>in</strong> content due to attack by fungi, but<br />
not all of <strong>the</strong>se studies have sufficiently demonstrated <strong>the</strong> importance of lign<strong>in</strong> dur<strong>in</strong>g<br />
<strong>the</strong>se processes. In addition, fewer still are <strong>the</strong> works that analyze <strong>the</strong> <strong>changes</strong> <strong>in</strong> plant<br />
metabolism <strong>and</strong> gene expression responsible for this differential accumulation of lign<strong>in</strong>.<br />
The <strong>in</strong>fection of P<strong>in</strong>us nigra by Sphaeropsis sap<strong>in</strong>ea <strong>in</strong>duces an <strong>in</strong>crease <strong>in</strong> <strong>the</strong><br />
deposition of lign<strong>in</strong> (Bonello <strong>and</strong> Blodgett, 2003). Lignification is a defence response <strong>in</strong><br />
<strong>the</strong> hypersensitive reaction of wheat to Pucc<strong>in</strong>ia gram<strong>in</strong>is (Moerschbacher et al., 1990).<br />
Dur<strong>in</strong>g such a response <strong>in</strong> wheat, lign<strong>in</strong> rich <strong>in</strong> syr<strong>in</strong>gyl units accumulates (Menden et<br />
al., 2007).<br />
The deposition of lign<strong>in</strong> <strong>in</strong> necrophylatic periderm <strong>in</strong> <strong>the</strong> early stages of<br />
<strong>in</strong>fection by Mycosphaerella expla<strong>in</strong>s <strong>the</strong> greater resistance of E. nitens as compared to<br />
E. globulus, as this response may prevent <strong>the</strong> spread of tox<strong>in</strong>s <strong>and</strong> fungal enzymes to <strong>the</strong><br />
host, <strong>the</strong>reby prevent<strong>in</strong>g <strong>the</strong> displacement of water <strong>and</strong> nutrients from <strong>the</strong> host cell to<br />
<strong>the</strong> fungus (Smith et al., 2007).<br />
Metabolic studies on <strong>the</strong> <strong>changes</strong> <strong>in</strong> <strong>the</strong> xylem tissues of Ulmus m<strong>in</strong>or <strong>and</strong><br />
Ulmus m<strong>in</strong>or x Ulmus pumila after <strong>in</strong>oculation with Ophiostomis new-ulmi showed that<br />
<strong>the</strong> hybrid has a faster defence response, which is characterized by an <strong>in</strong>crease <strong>in</strong> <strong>the</strong><br />
amount of lign<strong>in</strong>, dim<strong>in</strong>ish<strong>in</strong>g <strong>the</strong> probability of pathogen <strong>in</strong>vasion (Mart<strong>in</strong> et al., 2007).<br />
Regard<strong>in</strong>g physiological <strong>and</strong> molecular aspects, <strong>the</strong> differential accumulation of<br />
lign<strong>in</strong> <strong>and</strong> lignans <strong>in</strong> cell suspension cultures of L<strong>in</strong>um usitatissimum was studied, <strong>in</strong><br />
response to Botrytis c<strong>in</strong>erea, Fusarium oxysporum <strong>and</strong> Phoma exigua mycelium<br />
extracts (Hano et al., 2006). In this study, genes cod<strong>in</strong>g for PAL, CCR <strong>and</strong> CAD<br />
showed elevated expression; PAL activity was enhanced as well.<br />
F<strong>in</strong>ally, COMT expression <strong>in</strong> diploid wheat (Triticum monococcum) is elevated<br />
follow<strong>in</strong>g <strong>in</strong>oculation with Blumeria gram<strong>in</strong>is (Bhuiyan et al., 2007).
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Conclud<strong>in</strong>g Remarks<br />
Figure 1 shows <strong>the</strong> ma<strong>in</strong> route of lign<strong>in</strong> biosyn<strong>the</strong>sis <strong>in</strong> plants <strong>and</strong> <strong>the</strong> enzymes<br />
<strong>in</strong>volved <strong>in</strong> each metabolic step (adapted from Rastogi <strong>and</strong> Dwivedi, 2008). For most of<br />
<strong>the</strong> genes cod<strong>in</strong>g for <strong>the</strong>se enzymes, transgenic plants have been produced us<strong>in</strong>g genesilenc<strong>in</strong>g<br />
techniques (Anterola <strong>and</strong> Lewis, 2002). The aim of <strong>the</strong>se works was to reduce<br />
lign<strong>in</strong> content or to change <strong>the</strong> structure of lign<strong>in</strong>, goals which have economical <strong>and</strong><br />
environmental implications: cheaper <strong>and</strong> more process-amenable trees for pulp <strong>and</strong><br />
paper manufacture with less pollution, more readily digestible forage for livestock <strong>and</strong><br />
improved feedstock for fuel/chemical production (Anterola <strong>and</strong> Lewis, 2002).<br />
The potential applications of chang<strong>in</strong>g or silenc<strong>in</strong>g <strong>the</strong> expression of <strong>the</strong>se genes<br />
were comprehensively discussed by Anterola <strong>and</strong> Lewis (2002). Some questions<br />
discussed by <strong>the</strong>se authors were, “why do vascular plants consistently produce various<br />
types of cell walls with lign<strong>in</strong>s from ei<strong>the</strong>r two or three monolignols, <strong>and</strong> how does this<br />
occur <strong>in</strong> vivo? Why are <strong>the</strong>se moieties also differentially deposited <strong>in</strong>to specific regions<br />
of develop<strong>in</strong>g cell wall types?” Despite <strong>the</strong> complexity of <strong>the</strong> lign<strong>in</strong> biosyn<strong>the</strong>sis<br />
network, Anterola <strong>and</strong> Lewis (2002) used accumulated knowledge obta<strong>in</strong>ed with<br />
mutants or transgenic plants (<strong>in</strong> which levels of particular enzymes of <strong>the</strong> pathway have<br />
been modified <strong>in</strong> some way) to show that monolignol biosyn<strong>the</strong>sis is under f<strong>in</strong>e<br />
metabolic <strong>and</strong> transcriptional coord<strong>in</strong>ation.<br />
For several of <strong>the</strong>se genes, repressed expression led to diverse <strong>and</strong> undesirable<br />
impacts on plant physiology due to <strong>the</strong> multiple products that orig<strong>in</strong>ate from <strong>the</strong><br />
phenylpropanoid pathway. Therefore, <strong>the</strong> PAL, C4H, C3H <strong>and</strong> 4CL genes (see Figure 1)<br />
are not good targets for genetic manipulation aim<strong>in</strong>g to reduce lign<strong>in</strong>, while CCoAOMT,
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COMT <strong>and</strong> CAD genes can be used to reduce <strong>and</strong> change lign<strong>in</strong> composition (Rastogi<br />
<strong>and</strong> Dwivedi, 2008).<br />
The biosyn<strong>the</strong>sis of monolignols <strong>in</strong> phenylpropanoid metabolism is a metabolic<br />
grid; that is, different routes may be used to syn<strong>the</strong>size a compound. This gives plants<br />
<strong>the</strong> plasticity to produce lign<strong>in</strong> when a step is <strong>in</strong>hibited for whatever reason such as<br />
when a specific gene is silenced. In addition, enzymes related to lign<strong>in</strong> biosyn<strong>the</strong>sis<br />
usually derive from multigene families; depend<strong>in</strong>g on <strong>the</strong> stress<strong>in</strong>g situation (<strong>biotic</strong> or<br />
a<strong>biotic</strong>), different genes for different isozymes can be activated. For <strong>the</strong> sake of<br />
complexity, it is also well known that <strong>the</strong> relative proportions of <strong>the</strong> monolignols may<br />
vary due to environmental <strong>in</strong>fluence (Boudet, 1998). It has been suggested that plants<br />
are versatile <strong>in</strong> <strong>the</strong>ir ability to tolerate substantial <strong>changes</strong> <strong>in</strong> lign<strong>in</strong> structure <strong>and</strong><br />
<strong>in</strong>corporate phenolic compounds o<strong>the</strong>r than <strong>the</strong> three known monolignols (Ralph et al.,<br />
2004). Recently, it was shown that acylated monolignols could also serve as lign<strong>in</strong><br />
precursors (Lu <strong>and</strong> Ralph, 2003). This can make lign<strong>in</strong> more recalcitrant to disruption<br />
dur<strong>in</strong>g pulp<strong>in</strong>g <strong>in</strong> <strong>the</strong> paper <strong>in</strong>dustry, for example (Lapierre et al., 1999). However, it<br />
does not appear that “non-traditional” phenolics, o<strong>the</strong>r than <strong>the</strong> monolignols, are<br />
<strong>in</strong>corporated <strong>in</strong>to lign<strong>in</strong> (Anterola <strong>and</strong> Lewis, 2002).<br />
There are several examples <strong>in</strong>dicat<strong>in</strong>g that lign<strong>in</strong> found <strong>in</strong> nature may comprise<br />
modified molecules (Lu et al., 2004; Morreel et al., 2004). Phenolic amides may also be<br />
part of <strong>the</strong> cell wall, as proven by over-expression of <strong>the</strong> enzyme responsible for <strong>the</strong>ir<br />
biosyn<strong>the</strong>sis, which caused an <strong>in</strong>crease <strong>in</strong> <strong>the</strong>ir <strong>in</strong>corporation <strong>in</strong>to <strong>the</strong> cell wall matrix<br />
(Hagel <strong>and</strong> Facch<strong>in</strong>i, 2005). Recent research also showed that acetylation of syr<strong>in</strong>gyl<br />
units seems to be an exclusive characteristic of angiosperms, as <strong>the</strong> process was<br />
observed among 11 angiosperm species but not <strong>in</strong> 2 gymnosperm species (Del Rio et<br />
al., 2007).
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This review showed that lign<strong>in</strong> biosyn<strong>the</strong>sis <strong>in</strong> nature can <strong>in</strong>crease complexity<br />
depend<strong>in</strong>g on <strong>the</strong> <strong>stresses</strong> <strong>and</strong> whe<strong>the</strong>r <strong>the</strong> stressor is act<strong>in</strong>g dur<strong>in</strong>g plant growth <strong>and</strong><br />
development. Unfortunately, little has been done to elucidate how such stress<strong>in</strong>g<br />
situations can change lign<strong>in</strong> content or alter its composition with regard to <strong>the</strong> build<strong>in</strong>g<br />
blocks called monolignols, or o<strong>the</strong>r phenolics enter<strong>in</strong>g <strong>the</strong> polymeric structure. Reaction<br />
wood has proven to be an important model for underst<strong>and</strong><strong>in</strong>g lign<strong>in</strong> formation <strong>in</strong> plants<br />
(Mellerowicz <strong>and</strong> Sundberg, 2008). O<strong>the</strong>r <strong>stresses</strong> may also become excellent models<br />
that will yield important clues for underst<strong>and</strong><strong>in</strong>g such complex metabolic pathways, as<br />
well as <strong>the</strong> <strong>in</strong>tricacies of genetic <strong>and</strong> metabolic control.<br />
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Acknowledgments<br />
The authors (J.C.M.S.M., M.C.D. <strong>and</strong> P.M.) thank CNPq for research fellowships.<br />
Votorantim Celulose e Papel S.A. is acknowledged for f<strong>in</strong>ancial support.<br />
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Figure 1. Biosyn<strong>the</strong>sis pathway of lign<strong>in</strong> <strong>in</strong> plants (adapted from Rastogi <strong>and</strong> Dwivedi,<br />
2008). PAL - phenylalan<strong>in</strong>e ammonia-lyase; C4H - c<strong>in</strong>namate 4-hydroxylase; C3H -<br />
c<strong>in</strong>namate 3-hydroxylase or p-coumaroyl shikimic acid/qu<strong>in</strong>ic acid 3-hydroxylase;<br />
OMT - O-methyltransferase; HCT - p-hydroxy c<strong>in</strong>namoyl-CoA: shikimate/qu<strong>in</strong>ate p-<br />
hydroxy c<strong>in</strong>namoyl transferase; CCoAOMT - caffeoyl coenzyme A O-<br />
methyltransferase; F5H - ferulate 5-hydroxylase; 4CL - 4-coumarate: coenzyme A<br />
ligase; CCR - c<strong>in</strong>namoyl coenzyme A reductase; Cald5H - coniferaldehyde 5-<br />
hydroxylase; AldOMT - 5-hydroxy coniferaldehyde O-methyltransferase; SAD -<br />
s<strong>in</strong>apyl alcohol dehydrogenase; CAD - c<strong>in</strong>namyl alcohol dehydrogenase.<br />
C<strong>in</strong>namate<br />
PAL<br />
Phenylalan<strong>in</strong>e<br />
C4H<br />
C3H (?) OMT F5H OMT<br />
4-Coumarate Caffeate Ferulate 5-Hydroxyferulate S<strong>in</strong>apate<br />
4CL<br />
4CL 4CL 4CL 4CL (?)<br />
CCoAOM<br />
CCoAOM<br />
HCT<br />
C3H<br />
HCT<br />
COMT F5H (?) COMT<br />
4-Coumaryl-CoA 4-Coumaryl Caffeoyl Caffeoyl-CoA Feruloyl-CoA 5-Hydroxyferuolyl-CoA S<strong>in</strong>apyl-CoA<br />
shikimic acid / shikimic acid /<br />
4-Coumaryl<br />
Caffeoyl<br />
CCR<br />
qu<strong>in</strong>ic acid<br />
qu<strong>in</strong>ic acid<br />
CCR CC CC CC<br />
(?)<br />
OMT F5H OMT<br />
4-Coumaraldehyde Caffeoyl aldehyde Coniferaldehyde 5-Hydroxyconiferaldehyde S<strong>in</strong>apaldehyde<br />
CAD/SAD<br />
CAD/SAD CAD/SAD CAD/SAD CAD/SAD<br />
(?) OMT<br />
F5H<br />
OMT<br />
Cald5h<br />
AldOM<br />
4-Coumaryl alcohol Caffeoyl alcohol Coniferyl alcohol 5-Hydroxyconiferyl S<strong>in</strong>apyl alcohol<br />
alcohol<br />
p-Hydroxypnehyl Guaiacyl Syr<strong>in</strong>gil<br />
(H unit) (G unit) (S unit)<br />
R1 = R2 = H p-coumaryl alcohol (p-hydroxy phenyl, H unit)<br />
R1 = H, R2 = OCH 3 coniferyl alcohol (guayacyl, G unit)<br />
R1 = R2 = OCH 3 s<strong>in</strong>apyl alcohol (syr<strong>in</strong>gyl, S unit)