The Plant Vascular System: Evolution, Development and FunctionsF

358 Journal of Integrative Plant Biology Vol. 55 No. 4 2013
Shulaev et al. 1995). However, the timeframe of SAR signal
movement precedes that of SA accumulation in the distal
tissues. Moreover, SA-deficient rootstocks of plants expressing
SA hydroxylase or plants suppressed in PAL expression are
capable of activating SAR in the leaves of WT scions. These
data argued against a role for SA as the phloem-mobile SAR
signal (Vernooij et al. 1994; Pallas et al. 1996). Regardless,
SA is required for the proper induction of SAR, and mutations
in either the ICS or PAL pathway are sufficient to compromise
SAR (Vernooij et al. 1994; Pallas et al. 1996; Wildermuth et al.
2001).
Radiolabel feeding experiments suggest that over 50% of
SA in distal leaves is transported from the inoculated leaves
with the remainder being synthesized de novo (Shulaev et al.
1995; Molders et al. 1996). Whether the induced synthesis of
SA in the distal tissues is required for SAR remains unclear.
A marginal difference (∼10 ng/g FW) in SA levels between
SAR-competent WT versus SAR-compromised SA-deficient
scions grafted onto SA-deficient rootstocks suggests that an
increase in SA accumulation may not be a prerequisite for the
normal induction of SAR (Vernooij et al. 1994; Chanda et al.
2011).
In general, most of the endogenous SA is metabolized
to a glucose conjugate, SA 2-O-β-D-glucose (SAG) or SA
glucose ester (SGE), and this reaction is catalyzed by SA
glucosyltransferases (Enyedi et al. 1992; Edwards 1994; Lee
and Raskin 1998; Lee and Raskin 1999; Dean and Delaney
2008; Song et al. 2008). Other derivates of SA include its
methylated ester and methyl SA. (MeSA), and hydroxylated
form gentisic acid (GA), both of which are also present as
glucose conjugates. Exogenous GA induces a specific set of
PR proteins in tomato that are not induced by SA, suggesting
that SA and GA differ in their mode of action (Bellés et al.
1999).
Unlike SA, MeSA is biologically inactive and only functions
when converted back to SA. MeSA is a well-characterized
volatile organic compound that can function as an airborne
defense signal and can mediate plant-plant communication
(Shulaev et al. 1997; Koo et al. 2007). Conversion of SA to
MeSA is mediated by SA methyltransferases (SAMT), also
designated BA (benzoic acid)-/SA-MT because it can utilize
either SA or BA as substrates (Chen et al. 2003; Effmert et al.
2005; Koo et al. 2007). Overexpression of BSMT leads to the
depletion of endogenous SA and SAG, as most of the available
SA is converted to MeSA (Koo et al. 2007). This in turn is
associated with increased susceptibility to bacterial and fungal
pathogens, suggesting that levels of free SA, but not MeSA,
are critical for plant immunity. Likewise, overexpression of the
Arabidopsis SA glucosyltransferase (AtSGT1) also results
in the depletion of SA and an increase in MeSA levels,
which again correlates with increased susceptibility to bacterial
pathogens (Song et al. 2008).
MeSA accumulates in the phloem following induction of SAR,
and this requires SAMT activity. Upon translocation to the distal
tissues, MeSA is converted back to SA via MeSA esterase
(Figure 27). Most of the MeSA accumulating in response to
pathogen inoculation was shown to escape by volatile emissions
(Attaran et al. 2009). Furthermore, Arabidopsis BSMT
mutant plants do not accumulate MeSA, but remain SAR
competent. This discrepancy was attributed to the dependency
of MeSA-derived signaling on light (Liu et al. 2011), which is
well-known to play an important role in plant defense (Karpinski
et al. 2003; Roberts and Park 2006). Notably, the phloem
translocation time of the SAR signal to distal tissues precedes
the time of MeSA requirement; i.e., 48 h and 72 h post primary
infection, respectively (Park et al. 2009; Chanda et al. 2011;
Chaturvedi et al. 2012). This suggests that MeSA is unlikely
to be the primary mobile signal, and possibly might act as a
downstream contributor to SAR.
Recent studies also suggest that defective SAR in dir1 plants
is associated with increased expression of BSMT1, which correlates
with increased accumulation of MeSA and a reduction
in SA and SAG levels (Liu et al. 2011). However, this is in
contrast with two other independent studies that showed normal
SA levels in pathogen inoculated dir1 plants (Maldonado et al.
2002; Chaturvedi et al. 2012). Some possibilities that might
account for these discrepancies are disparate regulation of
BSMT1 expression and the associated changes in MeSA and
SA levels in different ecotypic backgrounds, and/or plant growth
conditions, such as light, humidity, temperature, and wind.
For example, light intensities could affect SA levels/defense
responses since photoreceptors are well known to regulate
both SA- and R-mediated signaling (Genoud et al. 2002; Jeong
et al. 2010).
Components that affect SAR by regulating SA levels
Many proteins known to mediate SA-derived signaling have
been identified as contributors to SAR. These include proteins
involved in SA biosynthesis (including ICS and PAL), transport,
and/or SA-dependent R-mediated signaling (ENHANCED
DISEASE SUSCEPTIBILITY 1 (EDS1), EDS5, PHYTOALEXIN
DEFICIENT 4 (PAD4), and SENESCENCE-ASSOCIATED
gene 101 (SAG101)). The Arabidopsis EDS5 (also called
SA INDUCTION-DEFICIENT 1) encodes a plastid-localized
protein that shows homology to the bacterial multidrug and
toxin extrusion transporter (MATE) proteins. EDS5 is required
for the accumulation of SA after pathogen inoculation (Nawrath
et al. 2002; Ishihara et al. 2008) and, consequently, a mutation
in EDS5 causes enhanced susceptibility against oomycete,
bacterial, and viral pathogens (Rogers and Ausubel 1997;
Nawrath et al. 2002; Chandra-Shekara et al. 2004). Mutations
in ICS1 and EDS5 lead to similar phenotypes (Venugopal
et al. 2009), suggesting that EDS5 might be involved in