Wassmann und Aulakh - 2000 - The role of rice plants in regulating mechanisms o

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Wassmann und Aulakh - 2000 - The role of rice plants in regulating mechanisms o

Biol Fertil Soils (2000) 31:20–29 Q Springer-Verlag 2000

REVIEW ARTICLE

Reiner Wassmann 7 Milkha S. Aulakh

The role of rice plants in regulating mechanisms of methane missions

Received: 7 April 1999

Abstract Rice plants play a pivotal role in different

levels of the methane (CH 4 ) budget of rice fields. CH 4

production in rice fields largely depends on plant-borne

material that can be either decaying tissue or root exudates.

The quantity and quality of root exudates is affected

by mechanical impedance, presence of toxic elements,

nutrient deficiencies, water status of growing

medium, and nitrogenase activity in the rhizosphere.

CH 4 oxidation in rice fields is localized in the rhizosphere

where the concentration gradients of CH 4 and

oxygen overlap. CH 4 oxidation capacity is a function of

the downward transport of oxygen through the aerenchyma,

which, in turn, also acts as a conduit for CH 4

from the soil to the atmosphere. The decisive step in

the passage of CH 4 through rice plant is the transition

from root to stem. However, rice plants show an enormous

variety of morphological and physiological properties,

including differences in root exudation and gas

transfer capacity. Comparative studies on different cultivars

are deemed crucial for accomplishing a better understanding

of the mechanisms of CH 4 consumption in

the rhizosphere and CH 4 transport through the rice

plant as well as the interaction of these processes. The

results of such studies are considered tools for devising

mitigation options.

Key words Methane production 7 Methane oxidation 7

Methane emission 7 Rice fields 7 Plant-mediated gas

transfer

R. Wassmann (Y) 7 M.S. Aulakh

International Rice Research Institute, P.O. Box 3127,

1271 Makati City, The Philippines

e-mail: R.Wassmann6cgiar.org

Fax: c63-2-891292

R. Wassmann

Institute for Atmospheric Environmental Research,

Garmisch-Partenkirchen, Germany

M.S. Aulakh

Department of Soils, Punjab Agricultural University, Ludhiana,

Punjab, India

Introduction

The atmospheric concentration of the radiative active

methane (CH 4 ) gas has increased at rate of F0.8% per

year during previous decades (IPCC 1994). However,

the concentration increase since 1992 has shown large

interannual variation between 0 and 0.5% (Dlugokencky

et al. 1998). Rice cultivation is one of the most

important anthropogenic sources of atmospheric CH 4

(IPCC 1994). The development of methods and strategies

to reduce the emission of CH 4 from paddy fields is

a central component of the ongoing efforts to protect

the earth’s atmosphere and to avert a possible climatic

change (Rennenberg et al. 1992). Rice plants act in

three key functions regulating the CH 4 budget: (1) as a

source of methanogenic substrate, (2) as a conduit for

CH 4 through a well-developed system of intercellular

air spaces (aerenchyma), and (3) as an active CH 4 oxidizing-site

in rhizosphere by supporting O 2 countertransport

through aerenchyma system (Fig. 1). However,

an assessment of the role of plants has to consider

the enormous genotypic and phenotypic variations. The

genus Oryza comprises approximately 80,000 known

cultivars with large variations in morphology and physiology.

Furthermore, the traits of rice plants are modified

by the growth conditions such as nutrient supply,

climate, local management practices etc., which makes

a generic assessment even more difficult.

Global estimates of CH 4 emission from rice cultivation

vary widely ranging from 20 to 150 Tg CH 4 year –1

(IPCC 1992) while more recent estimates are in the

range of 30–50 Tg CH 4 year –1 (Neue and Sass 1998).

The complexity of the role of rice plants for regulating

CH 4 fluxes to the atmosphere is one of the main reasons

for the uncertainties in the global estimates of this

CH 4 source. Field and laboratory experiments clearly

indicate that there is a cultivar impact (Watanabe et al.

1995b; Butterbach-Bahl et al. 1997; Sigren et al. 1997;

Wang et al. 1997a), but the net-effect of substituting

cultivars, e.g. traditional by modern lines, is still uncer-


21

Fig. 1 Schematic view of the

methane budget of rice fields

with emphasis on plant impacts;

insets depict CH 4 diffusion

through aerenchyma in a

root, b root-stem transition

zone, and c a stem-leaf section

zone (modified from Nouchi

and Mariko 1993; Wassmann

et al. 1998)

tain. This is contrasted by the impact of different management

practices, such as organic versus mineral fertilizer,

continuous flooding versus intermittent drainage,

that can be predicted with reasonable accuracy (Wassmann

et al. 1993a, b; Neue et al. 1997). In view of the

future rice demand for feeding the increasing world

population, the traits of high-yielding rice varieties will

affect the CH 4 source strength of rice cultivation. A

thorough understanding of the mechanisms involved is

required to direct the endeavours of selection – and

possibly breeding – toward high-yielding rice plants

with a limited emission potential. This paper reviews

and compiles the current state of knowledge on mechanisms

and factors that control plant-mediated and

plant-borne CH 4 emissions as well as the significance of

this process for the overall CH 4 flux from rice fields.

Gaps in our knowledge and future research needs are

indicated.

CH 4 production in soil

Strictly anaerobic conditions and availability of readily

decomposable organic substances are essential for the

process of CH 4 production in soil. Rice plants can influence

the CH 4 production by enhancing the anaerobiosis

in soil as well as by supplying organic compounds

through their root exudates, which have the ability to

readily supply C and energy source to the microorganisms

present in the rhizosphere.

Soil redox potential and ecophysiological sequence

of reduction processes

Soil anaerobiosis, measured in terms of redox potential

(Eh), ranging from about –100 to –200 mV, is needed

for the initiation of CH 4 production in paddy soils (Takai

1961, 1966; Cicerone et al. 1983; Yagi and Minami

1990; Lindau et al. 1991; Wang et al. 1993). The intensity

and capacity of soil reduction are controlled by the

nature and extent of organic substances (electron donors),

temperature, degree of waterlogging, and the nature

and quantity of electron acceptors (Ponnamperuma

1972). In laboratory experiments (Takai 1961; Watanabe

1984), it has been demonstrated that the ratio of

CO 2 to CH 4 production in several paddy soils varied by

more than a factor of 10 and correlated with the relative

ratio of total oxidizing (electron-accepting) capacity

to reducing (electron-donating) capacity of the soils.

Soils containing high amounts of readily decomposable

organic substrates (e.g. acetate, formate, methanol, methylated

amines etc.) and low amounts of electron acceptors

(NO 3– , Mn 4c , Fe 3c , SO 4

2–

) are likely to show a

high production of CH 4 (Parashar et al. 1991; Yagi et

al. 1994).

As soon as a soil becomes flooded, the trapped O 2 is

respired and in the following steps, NO 3– , Mn 4c , Fe 3c ,

compounds are reduced successively (Takai and Kamura

1966; Ottow 1969; Yoshida 1975). During these reductive

processes, facultative and obligate anaerobic

bacteria use NO 3– , Mn 4c , Fe 3c , oxides and hydroxides

as alternative electron acceptors to continue their energy-conserving

metabolic reactions at the expense of

easily decomposable organic material (Takai and Kamura

1966; Munch and Ottow 1977; Ottow and Munch

1978). For example, Munch and Ottow (1983) showed

that NO 3– , Mn 4c and Fe 3c are reduced directly by bacterial

reductases and not through chemical processes.

The microbial population may even use non-crystalline

Fe 3c oxides in preference to crystalline forms as external

electron acceptors (Munch and Ottow 1980).

Rice plants can influence the soil Eh by consuming

O 2 from the rhizosphere (root respiration) and by enhancing

the supply of electron donors, i.e. readily decomposable

organic substrates through root exudates,

sloughed-off tissues and debris, and microbially reduced

Mn 2c and Fe 2c ions and chelates. The variability

in content and composition of exudates of different

rice plants could influence soil Eh and CH 4 production


22

differently. For instance, Wang (1995) observed lower

Eh values in soil with Dular, a traditional variety from

the Philippines, than with the modern varieties IR 72

and IR 65538 at heading and ripening growth stages.

Dular showed highest dry matter production resulting

in higher root weight and, as a consequence, larger root

exudation of organic C.

Root exudates

Root exudates contain both high-molecular-weight substances,

mainly mucilage and ecto-enzymes, as well as

low-molecular-weight substances consisting of organic

acids, phenols and amino acids (Andal et al. 1956;

MacRae and Castro 1966; Trolldenier 1977, 1981;

Marschner 1995). The amount of knowledge available

on exudation from rice plants is minute, so that a discussion

on the factors affecting exudation has to rely on

findings obtained with other crops. Total amounts as

well as the proportion of different compounds in root

exudates vary considerably due to various endogenous

and exogenous factors such as mechanical impedance,

presence of toxic elements, nutrient deficiencies, water

status of growing medium, and nitrogenase activity.

Maize grown in a nutrient culture solution exuded a

three times lower amount of sugars and vitamins than

exudation by plants grown in a solid substrate (Schönwitz

and Ziegler 1982). Plants increase their root exudation

to improve their ability to tolerate toxic elements

such as Pb, Cd and Al (Horst et al. 1990). High

exudation restricts the uptake of these elements by preferential

binding and immobilization with mucilage

(Horst et al. 1982). Exudation can also help to cope

with nutrient deficiency through mobilization of nutrients

at the root-soil interface, e.g. phosphate desorption

from clay surfaces by the polygalacturonic acid

component of mucilage (Nagarajah et al. 1970). Under

dry soil condition, high amounts of mucilage facilitate

transport of nutrients from soil particles to the plasma

membrane of root cells (Nambiar 1976).

Plants do not only adjust the quantity but also the

quality of root exudates. In general, nutrient deficiencies

are responded to by higher amounts of low-molecular-weight

organic acids in root exudates (Marschner

1993). If there is a deficiency of Mn and Fe, these acids

increase the solubility of MnO 2 and Fe-oxides by chelation

facilitating root uptake (Godo and Reisenauer

1980; Jauregui and Reisenauer 1982). High excretions

of citric and malic acid result in local acidification of

the rhizosphere which – in turn – mobilizes the sparingly

soluble inorganic compounds such as phosphates, Fe,

Mn and Zn (Hoffland et al. 1989; Marschner 1995).

These few examples illustrate that the total amount and

proportion of different compounds in root exudates

that constitute a dynamic rather than a static plant parameter.

In a study with rice, Lin and You (1989) reported

that root exudates from rice contained varying amounts

of organic acids, carbohydrates and amino acids.

Among organic acids, citric acid had the highest concentration

followed by malic, succinic and lactic acid in

decreasing order. These findings illustrate a large variation

in composition and content of root exudates of different

rice varieties (Fig. 2). They further observed that

inoculation with Alcaligenes faecalis stimulated the excretion

from rice roots which was related to the nitrogenase

activity in the rhizosphere. Nagarajan and Prasad

(1983) also indicated that significant differences

could exist among rice cultivars in supplying different

amounts as well as in the chemical composition of their

exudates. More recently, Wang (1995) compared the

quantities of organic C released by roots of different

cultivars and found that the total amount of C exuded

was closely related to root dry weight (r 2 p0.919) as

well as to above-ground dry matter production

(r 2 p0.954).

These studies help to explain the seasonal variation

in CH 4 emission rates that often follow plant development.

High emission rates at the panicle differentiation/

flowering stage can clearly be attributed to recent

plant-borne material, either root exudates or decaying

root tissue (Watanabe et al. 1997). In laboratory incubations

of soil cores, CH 4 production by soil bacteria

was found to be highest near the soil surface in the rice

row and decreased with depth and distance from the

plant (Sass et al. 1991b). As the season progressed and

the root system expanded to deeper soil and further

away from the plant base, CH 4 production also increased

in these soil regions. Similarly a positive correlation

between rice yield and CH 4 emissions often observed

under field conditions (Neue et al. 1997) could

be due to a close relationship between plant size and C

Fig. 2 Content of different organic acids and carbohydrates in

root exudates of four rice cultivars from China (drawn from data

of Lin and You 1989)


23

excreted from roots which – in turn – influence CH 4

production.

From these studies, it is obvious that rice plants play

a key role in the production of CH 4 in soils. However,

unfortunately most of these studies are based on the

assumption that changes in CH 4 efflux rates reflect

changes in CH 4 production. This conclusion may not be

valid since CH 4 efflux is the net result of two opposite

mechanisms – production and oxidation of CH 4 .

Effects on CH 4 oxidation in soil

CH 4 is consumed in soil by bacteria that are strictly

obligate aerobes (Papen and Rennenberg 1990). These

bacteria can use CH 4 , but also a few other C compounds

such as methanol as a substrate. As they require

molecular O 2 (Bedard and Knowles 1989; King

1992; Knowles 1993), methanotrophs occur and are active

in oxic-anoxic interfaces where concentration gradients

of CH 4 and O 2 overlap. In flooded rice fields,

these conditions are generally confined to the rhizosphere

and a thin layer of the topsoil interfacing with the

water. However, depending on water regime, O 2 -rich

water may intrude into the lower soil layers and temporarily

stimulate CH 4 oxidation.

The estimates of the proportion of locally produced

CH 4 that is oxidized in the soil ranges from 58% (Sass

et al. 1991a, b) to 80% and higher (Holzapfel-Pschorn

et al. 1985; Conrad and Rothfuss 1991; Inubushi et al.

1992). Low CH 4 concentrations in the floodwater in

contrast to high concentrations in the soils (Holzapfel-

Pschorn and Seiler 1986; Nouchi and Mariko 1993) corroborate

the concept of a very efficient removal of CH 4

during the passage through oxidized layers. The rate of

CH 4 oxidation is often higher in rice-planted soil than

in unplanted soil (Inubushi et al. 1992). Rice plants influence

CH 4 oxidation in two ways, i.e. by diffusion of

atmospheric O 2 via aerenchyma into the rhizosphere,

and by enzymatic oxidation as measured by N flush inhibition

technique (Epp and Chanton 1993) and a-

naphthylamine oxidation method (Wang 1995).

Subsequent to flooding, plant roots encounter

anoxic conditions as a result of depletion of soil O 2 by

microbial and plant root respiration (Gambrell and Patrick

1978). In order to adapt to the flooded anoxic conditions,

most hydrophytes, including rice, develop an

aerenchyma system in both root and stem for maintaining

aerobic respiration (van Raalte 1941; Armstrong

1978, 1979; Keeley 1979; Grosse and Schroeder 1985).

O 2 diffuses through the aerenchyma to the roots (Barber

et al. 1962) while CO 2 and CH 4 move in the inverse

direction to the atmosphere. In addition to diffusion,

mass flow could also be an important mechanism of air

movement to the submerged parts of the plant through

the aerenchyma (Raskin and Kende 1985). However,

the pore size of the aerenchyma is the main plant parameter

that controls O 2 transport through the plant to

the rhizosphere and often shows a positive correlation

with O 2 concentration in the rhizosphere (Ueckert et

al. 1990).

Several factors have been reported to affect the O 2

release from the rice roots. For instance, metabolic inhibitors

such as DNP, NaN 3 and KCN could increase

the O 2 release rate (Ando et al. 1983). The soil Eh

could also influence this process (Kludze et al. 1993).

The release rates of O 2 were negatively correlated with

temperature but were unaffected by light conditions,

photosynthesis and respiration rates (Ando et al. 1983;

Nouchi et al. 1990).

The development of the aerenchyma is determined

by the intensity of anaerobiosis. For example, Kludze et

al. (1994) studied the development of aerenchyma in

plants at a soil Eh of –250B10 mV as compared to

plants under well-aerated conditions (515B25 mV). As

a result of enlarged aerenchyma, the root porosity was

increased to 41.4% in the flooded plants as compared

to only 13.3% in non-flooded or drained plants. Increased

porosity enhanced the transport of O 2 from the

atmosphere to the roots; O 2 loss from the roots increased

to 4.6 mmol O 2 g –1 day –1 in the flooded plants

as compared to only 1.4 mmol O 2 g –1 day –1 in drained

plants. Frenzel et al. (1992) detected O 2 down to the

depth of 40 mm in a flooded soil planted with rice

whereas it was confined to a thin surface layer (3.5 mm)

in an unplanted soil. This result illustrates the transport

of O 2 by rice plants to the flooded anaerobic soil. The

supply of O 2 by the plant to the rhizosphere often stimulates

high activities of CH 4 -oxidizing bacteria in the

vicinity of rice roots (Watanabe et al. 1997). De Bont et

al. (1978) counted 10 times more CH 4 -oxidizing bacteria

in the rhizosphere of rice at the tillering stage than

in the bulk of the anaerobic soil and one third more

than in the oxidized surface soil-water interface.

Different rice cultivars can support different rates of

CH 4 oxidation by developing variable root porosity and

oxidation powers. Wang et al. (1997a) found that at the

tillering stage, the root air spaces were small and did

not vary among three rice cultivars. Root air space continued

to increase up to the ripening stage in some cultivars

whereas it decreased in the commonly grown cultivar

IR 72. In the study of Wang et al. (1997a), dry

matter (Fig. 3a) had a direct effect on the CH 4 emission

rate (Fig. 3b) whereas root porosity (Fig. 3c) is not correlated

to the oxidation power of the plant (Fig. 3d).

The process of CH 4 oxidation is generally considered

to be an important in situ sink for CH 4 produced

in paddy soils (King 1992). The ratio of plant-mediated

versus floodwater-mediated oxidation, however, remains

unclear. Several experiments indicated that up to

40% of the potential CH 4 flux could be oxidized in the

rhizosphere (Epp and Chanton 1993; Denier van der

Gon and Neue 1996). Indirect assessments suggested

that 50–90% of the CH 4 transported to the rhizosphere

of the rice plant was oxidized (Frenzel et al. 1992).

However, the impact of rice variety characteristics on

CH 4 oxidation is not well understood. Varietal differences

may also become important when discussing CH 4


24

As mentioned earlier, the amount of CH 4 emitted from

the rice field to the atmosphere is the balance of the

two opposite processes, i.e. CH 4 production and oxidation.

CH 4 escapes from the rice field to the atmosphere

via three processes, viz. ebullition, diffusion, and transport

through the rice plant. The impact of plants on

these processes is discussed below.

Indirect impact of plants on ebullition and diffusion

Fig. 3 Variability among three rice cultivars: IR72 (high-yielding

dwarf), NPT (new plant type IR65598) and Dular (traditional

tall) in a dry matter, b CH 4 emission rate, c root oxidation power

and d root porosity at three growth stages. (Redrawn and modified

from data of Wang et al. 1997a,c)

oxidation within the aerenchyma. Even though recent

results indicate the presence of methanotrophic activity

associated with roots and, to a lesser extent, lower parts

of the stem (Watanabe et al. 1997), the significance of

CH 4 oxidation during passage through the rice plants is

still unknown.

As noted earlier, most of the findings on CH 4 production

and oxidation are based on indirect estimates

from CH 4 efflux rates. This is essentially due to the lack

of appropriate methods. Now techniques for inhibiting

oxidation and monitoring CH 4 production rates are

available, e.g. acetylene, dimethyl ether, nitrapyrin, methyl

fluoride, propylene oxide formation (Oremland

and Culbertson 1992a,b; Epp and Chanton 1993;

Kludze et al. 1993; Oremland and Taylor 1995; Watanabe

et al. 1995a). Therefore, future studies should be

able to address the effects of rice plant traits on both

CH 4 production and oxidation directly. The measurement

of 13 C abundance and 13 C fractionation could improve

knowledge of the function of the rhizosphere in

CH 4 oxidation.

CH 4 emission to the atmosphere

Ebullition and diffusion are purely physical processes

and, thus, are only indirectly affected by rice plants. A

well-developed root system acts as a sink and a barrier

for diffusive upward transport of CH 4 . Ebullition dominates

the overall flux only during the initial plant

growth stage (Wassmann et al. 1996) and upon disturbance

of soil due to weeding, harrowing etc. (Denier

van der Gon et al. 1992). Ebullition rates generally follow

a bimodal pattern over one season with high rates

in the early and late seasons (Wassmann et al. 1996).

The decrease in ebullition rate in mid-season is attributed

to the increasing CH 4 transfer through the aerenchyma,

reducing the pool size of entrapped CH 4 (Wassmann

et al. 1996). During this period, emerging gas

bubbles contain less CH 4 and high amounts of N 2

(Chidthaisong and Watanabe 1997a, b). During the later

growth stage, however, CH 4 production is very intense

due to the release of organic material from the

plant (Chidthaisong and Watanabe 1997a) which results

in increases in the CH 4 pool and the ebullition

rates observed during this period (Wassmann et al.

1996).

The mechanism of CH 4 transport through the rice

plant

The primary function of aerenchyma formation in hydrophilic

plants, including rice, is the delivery of O 2 to

the roots, but several gases are transferred in the inverse

direction. Aerenchyma transport of CO 2 (Higudchi

1982; Higudchi et al. 1984), N 2 and N 2 O (Mosier et

al. 1990; Prade and Trolldenier 1990; Aulakh et al.

1992; Bhadrachalam et al. 1992) and CH 4 (Raimbault et

al. 1977; Cicerone and Shetter 1981; Seiler et al. 1984;

Sebacher et al. 1985; Nouchi et al. 1990; Schütz et al.

1991; Nouchi and Mariko 1993) by rice and other plants

is well documented.

The phenomenon of CH 4 transport through the rice

plant from roots to above-ground portions and release

to the atmosphere has been elucidated by Nouchi et al.

(1990), Butterbach-Bahl (1992), Nouchi and Mariko

(1993), and Wang et al. (1997b). First, the dissolved

CH 4 in soil water surrounding the roots diffuses into

the surface water of the roots and into the cell-wall water

of the root cortex (Fig. 1). This transfer is driven by

the concentration gradient between the soil water surrounding

the roots and the lysigenous intercellular

spaces in the roots. Butterbach-Bahl (1992) identified

the cracks in the junction point of the main root and

the root hairs as predominant entrance ports for CH 4

from surrounding soil solution to the aerenchyma. CH 4

is then gasified in the root cortex and transported to the


25

shoots via the lysigenous intercellular spaces and aerenchyma.

Eventually, CH 4 is released to the atmosphere

from various parts of the rice plant (Fig. 1). Nouchi et

al. (1990) and Nouchi and Mariko (1993) observed that

CH 4 is released mainly through micropores in the leaf

sheath in the lower leaf but not from stomata. They demonstrated

that the closure of stomata openings by application

of abscisic acid did not affect the CH 4 emission

rate although the transpiration rate was decreased

to one-third and stomatal resistance increased threefold.

However, more recently, with the use of 13 C-

labeled CH 4 , Chanton et al. (1997) demonstrated that

although CH 4 is transported by the rice plant predominantly

via molecular diffusion, a small component is

also due to a transpiration-induced flow.

Most of CH 4 release is channelled through the culm

(Nouchi and Mariko 1993) which is an aggregation of

leaf sheaths. In submerged rice plants, many air bubbles

are released from (1) the abaxial epidermis of the

leaf sheath and (2) near the junction of the nodal plate

and leaf sheath (Nouchi and Mariko 1993). Wang et al.

(1997b) observed a shift in the transport pathway with

plant growth; about 50% of the CH 4 was released from

leaf blades before shoot elongation whereas only a

small amount was emitted through leaves as plants

grew older. In addition to the presence of micropores

on the leaf sheath, Wang et al. (1997b) identified cracks

at the junction of internodes. Although CH 4 can also be

released from panicles, this pathway was negligible as

long as leaves and nodes were not submerged. When

the vegetative parts of the plants are submerged, the

number of panicles determines the rate of CH 4 emission

(Wang et al. 1997b).

Factors controlling CH 4 transfer rates through the rice

plant

The actual flux of CH 4 through a rice plant depends on

several factors such as the concentration of CH 4 in soil

water, plant growth, size and shape, and rice cultivar.

Nouchi and Mariko (1993) observed a linear relationship

between CH 4 concentrations in the culture solutions

and CH 4 emission rate from rice plants. CH 4 concentrations

in rice plants show a clear gradient. The

highest concentrations are often found in the aerenchyma

below the water level and highest CH 4 emissions

occur through openings immediately above the water

level (Wang et al. 1997b). The transport capacity of rice

plants also depends on the size and shape of plants.

Emission rates from rice plants with nine tillers were

much larger than those with three tillers while the gap

between flux rates widened with increasing CH 4 concentration

in the soil (Nouchi and Mariko 1993). A similar

relationship was found for leaf area at the tillering

stage when nodes were not yet well developed (Wang

et al. 1997b).

Cutting off the stems of rice plants above the floodwater

did not influence CH 4 emission, indicating that

the rate-limiting step in plant-mediated CH 4 transport

was not located in the cut-off part of the plants (Ando

et al. 1983; Butterbach-Bahl 1992; Denier van der Gon

and van Breemen 1993). In field experiments with cutoff

stems, the pattern and magnitude of CH 4 emissions

remained unaffected over several days (Wassmann et

al. 1994). Tracer gas experiments (Butterbach-Bahl et

al. 1997) provided direct evidence that the root-shoot

transition zone (Fig. 1b) is the main site of resistance to

plant-mediated gas exchange between the soil and the

atmosphere.

Plant-mediated CH 4 transport does not depend on

photosynthetic rates. Ando et al. (1983) demonstrated

that darkening of the plants or increasing CO 2 concentration

in the atmosphere did not significantly affect the

CH 4 emission rates. Partial submergence of stems and

leaves could temporarily reduce the plant-mediated

CH 4 emission while the flux rates readjust within a few

hours (Wang et al. 1997b). From these studies it appears

that once the CH 4 is diffused into the root aerenchyma

and passes through the stem root interception, it

can escape to the atmosphere through one or the other

non-submerged part of the rice plants.

Impact of different rice plant traits

Since up to 90% of CH 4 released from a rice field during

a growing season could be emitted by rice plantmediated

transport, cultivar-specific properties may

have a strong impact on CH 4 emission. In a study with

six rice varieties, semi-dwarf varieties evolved 36% less

CH 4 than tall rice varieties (Lindau et al. 1995). Other

investigations in rice fields of India (Parashar et al.

1991, 1994; Adhya et al. 1994), China (Lin 1993), Japan

(Watanabe et al. 1995b), Italy (Butterbach-Bahl et al.

1997), and Texas, USA (Sigren et al. 1997) have also

indicated differences in the rate of CH 4 emission between

different varieties. These differences in CH 4 flux

rates could be attributed to differences in CH 4 production,

oxidation and gas transport capacities of different

cultivars. Recently Butterbach-Bahl et al. (1997) observed

that two Italian rice varieties differed by

24–31.5% in their CH 4 emission during two seasons.

This relative difference which was observed irrespective

of fertilizer treatment was not related to any difference

in CH 4 production or oxidation, but was attributed

to the different transfer capacities of the two cultivars.

High transfer capacity coincided with an increase in the

relative pore diameter of the root-shoot transition zone

of the aerenchyma system (Butterbach-Bahl et al.

1997).

Many measurements of CH 4 emission in rice fields

revealed seasonal patterns and variations in time and

space. Seasonal CH 4 emission patterns from rice fields

are the net result of the combination of many factors

such as reducing capacity of the soil, C source, nutrient

level, rice plant, temperature, and agricultural practices.

In a recent study, Wang et al. (1997c) observed


26

similar emission patterns for the cultivars Dular and IR

72 with one peak in the early and one in the late stage,

whereas the cultivar IR 65598 did not develop a second

emission peak. The distinct features of the new plant

type IR 65598 were low organic C in root exudates,

high oxidation power, few tillers and low dry matter per

plant. However, these findings (obtained with individual

plants) have to be confirmed for the situation encountered

in the field.

Relative importance of CH 4 transport pathways

The plant-mediated flux increases rapidly within the

first month after planting, which is also reflected in the

relative contribution of this pathway to total emission

(Table 1). In Italian rice fields, the aerenchyma transport

contributed 88–90% of the overall emission

throughout the reproductive and ripening stage (Butterbach-Bahl

et al. 1997). Over the entire season, plantmediated

transport can account for up to 90% of the

total CH 4 emission (Cicerone and Shetter 1981; Holzapfel-Pschorn

et al. 1985, 1986; Schütz et al. 1989; Butterbach-Bahl

et al. 1997). However, the relative contribution

of plant-mediated transfer is much lower under

high organic inputs (Wassmann et al. 1996). Organic

amendments result in high ebullitive fluxes during the

first few weeks when plants are very young and have

not developed their CH 4 transport mechanism. As a

consequence, the relative significance of plant-mediated

transport is decreased to values ranging from

48% to 85% (Table 1).

Conclusions and future research needs

The role of rice plants in the regulation of CH 4 emission

comprises many facets involving virtually every

level of the CH 4 budget in rice fields. However, it

should be noted that most of the findings on the effects

of plants on CH 4 production and oxidation are derived

indirectly from emission rates. With the advent of techniques

for inhibiting CH 4 oxidation, future studies

should address the influence of different plant parameters

on CH 4 production and oxidation. Such information

could be useful for formulating mitigation options

and for future rice breeding programs.

One individual trait of the rice plant can represent

an enhancing as well as a decreasing factor for CH 4 emission.

A high diffusion capacity of the aerenchyma entails

higher efflux of CH 4 plus higher oxidation power

of the root. Therefore, it is imperative to balance the

different impact mechanisms of rice plants for obtaining

a holistic view of the CH 4 budget in rice fields. Recent

achievements have considerably improved our understanding

the three decisive functions of plants, i.e.

(1) root exudation, (2) CH 4 transport to the atmosphere

and (3) CH 4 oxidation in the rhizosphere. But we

are still far away from a comprehensive understanding

of these phenomena, especially with respect to the interactive

relationships between the mechanisms involved.

Considering the enormous variety in physiology and

morphology of the genus Oryza, the impact of different

traits is most important for devising mitigation strategies.

Recent findings provide evidence that the desired

trait of a low emission potential can be reconciled with

a high yield potential (Wang et al. 1997a). High root

exudation rates represent a loss of assimilates for the

rice plants and can therefore be detrimental to yields.

However, information is lacking on the chemical composition

(e.g. amino acids, sugar C, organic acids) of

root exudates of different rice cultivars and its variations

in response to different management practices.

Comparative studies on cultivars may yield decisive

clues as to the identification of favourable traits for mitigation

and – at the same time – to improve our understanding

of the various functions of plants in the CH 4

budget of rice fields. Whereas other mitigation strategies

such as intermittent drainage require substantial

changes in farmers’ practices, new varieties can be introduced

within a given setting. The identification of

cultivars that combine low emissions with high yields is

the most challenging, but probably also the most promising,

strategy for a sustained reduction of CH 4 emissions

from rice fields.

Table 1 Contribution of plant-mediated CH 4 emission at different sites and under different treatments

Site/country Fertilizer/Cultivar Plant

age or

interval

Overall CH 4

emission rate

(mg CH 4 m P2 h P1 )

Plant-mediated

CH 4 emission

(% of overall

emission)

Source

Vercelli/Italy Urea/Roma 25 days 7.8 0 Schütz et al. (1989)

Urea/Roma 54 days 17.0 48

Urea/Roma 76–103 days 23–28 90–97

Vercelli/Italy Unfertilized/Roma Single season 11 88 Butterbach-Bahl (1992)

Unfertilized/Lido Single season 8.1 90

Los Baños/Philippines Urea/IR72 Dry season 1.1 85 Wassmann et al. (1996)

Straw/IR72 Dry season 9.4 65

Urea/IR72 Wet season 1.3 82

Straw/IR72 Wet season 6.3 48


27

Acknowledgement The review was conducted as part of the project

“Reduction of CH 4 emission from rice fields by screening for

low CH 4 transport capacity” funded by the German BMZ/GTZ

(Project No. 95.7860.0–001.05)

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