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Mechanisms for coping with submergence and waterlogging in rice

Rice volume 5, Article number: 2 (2012) Cite this article

Abstract

Rice (Oryza sativa L.), unlike other cereals, can grow well in paddy fields and is highly tolerant of excess water stress, from either submergence (in which part or all of the plant is under water) or waterlogging (in which excess water in soil limits gas diffusion). Rice handles submergence stress by internal aeration and growth controls. A quiescence strategy based on Submergence-1A (SUB1A) or an escape strategy based on SNORKEL1 (SK1) and SNORKEL2 (SK2) is used for the growth controls. On the other hand, rice handles waterlogging stress by forming lysigenous aerenchyma and a barrier to radial O2 loss (ROL) in roots in order to supply O2 to the root tip. In this article, we summarize recent advances in understanding the mechanisms of responding to excess water stresses (i.e., submergence and waterlogging) in rice and other gramineous plants.

Introduction

Plants require water for growth but excess water that occurs during submergence or waterlogging is harmful or even lethal. A submerged plant is defined as "a plant standing in water with at least part of the terminal above the water or completely covered with water" (Figure 1; Catling 1992). Submergence subjects plants to the stresses of low light, limited gas diffusion, effusion of soil nutrients, mechanical damage, and increased susceptibility to pests and diseases (Greenway and Setter 1996; Ram et al. 1999). Basically, flooding (i.e., submergence) can be classified into "flash flooding" and "deepwater flooding" in accordance with the duration of flooding and the water depth (Bailey-Serres et al. 2010; Catling 1992; Jackson and Ram 2003). Flash flooding, which generally lasts less than a few weeks, is caused by heavy rain but the depth is not very deep. On the other hand, deepwater flooding, which lasts for several months, occurs during the rainy season, and the water depth reaches several meters (Catling 1992; Hattori et al. 2011).

Figure 1
figure1

Strategies of adaptation to excess water stresses in the form of submergence or waterlogging in rice plants. Rice can adapt to submergence by internal aeration and growth control. For internal aeration, rice develops longitudinally forming aerenchyma and leaf gas films. On the other hand, some rice cultivars can survive under submergence by using special strategies of growth control: a quiescence strategy or an escape strategy. The Submergence-1A (SUB1A) gene is responsible for the quiescence strategy, which is important for survival under flash-flood conditions. The SNORKEL1 (SK1) and SNORKEL2 (SK2) genes are responsible for the escape strategy, which is important for survival under deepwater-flood conditions. Rice can adapt to soil waterlogging by forming aerenchyma and a barrier to radial O2 loss (ROL) in the roots.

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Waterlogging is defined as a condition of the soil in which excess water limits gas diffusion (Figure 1; Setter and Waters 2003). Oxygen diffusivity in water is approximately 10,000 times slower than in air, and the flux of O2 into soils is approximately 320,000 times less when the soil pores are filled with water than when they are filled with gas (Armstrong and Drew 2002, Colmer and Flowers 2008). The principal cause of damage to plants grown in waterlogged soil is inadequate supply of oxygen to the submerged tissues as a result of slow diffusion of gases in water and rapid consumption of O2 by soil microorganisms. Oxygen deficiency in waterlogged soil occurs within a few hours under some conditions. In addition to the O2 deficiency, production of toxic substances such as Fe2+, Mn2+, and H2S by reduction of redox potential causes severe damage to plants under waterlogged conditions (Drew and Lynch 1980; Setter et al. 2009). Thus, growth and development of most plants, except for rice (Oryza sativa L.) and other wetland species, are impeded under waterlogged conditions.

Unlike other crop plants, rice has some adaptive traits for tolerance of submergence. One of the traits is formation of the longitudinal interconnection of gas spaces, called aerenchyma, that enables internal aeration between shoot and roots (Armstrong 1979; Colmer 2003a; Colmer and Pedersen 2008a) Moreover, leaf gas films, which are a micro-layer of air trapped between submerged leaves and the surrounding water, contribute to the internal aeration during submergence, thereby increasing submergence tolerance in rice (Colmer and Pedersen 2008b; Pedersen et al. 2009; Raskin and Kende 1983).

Many lowland rice cultivars, despite having an ability of internal aeration, are still sensitive to complete submergence. Their leaves and stems moderately elongate under complete submergence to reach the air-water interface, but their elongation growth can exhaust energy reserves and cause death when the flooding depth is deep and the flooding period is long (Bailey-Serres et al. 2010; Jackson and Ram 2003). However, some cultivars use two distinct strategies of growth controls to survive under submerged conditions. One of the strategies is a quiescence strategy [i.e., the low-oxygen quiescence syndrome (Colmer and Voesenek 2009)] (Figure 1), in which shoot elongation is suppressed to preserve carbohydrates for a long period (10-14 days) under flash-flood conditions. Submergence-tolerant cultivars can restart their growth during desubmergence by using preserved carbohydrates. Another strategy is an escape strategy [i.e., the low-oxygen escape syndrome (Bailey-Serres and Voesenek 2008; Colmer and Voesenek 2009)] (Figure 1), which involves fast elongation of internodes to rise above the water level and is used by deepwater rice cultivars. Both strategies depend on ethylene-responsive transcription factors (Hattori et al. 2009; Xu et al. 2006).

The main adaptation of lowland rice to soil waterlogging is the formation of aerenchyma, which permits relatively unhindered transport of O2 from well-aerated shoots to submerged roots (Figures 1, 2; Armstrong 1979; Jackson and Armstrong 1999). Longitudinal diffusion of O2 towards the root apex can be further enhanced by induction of a barrier to radial O2 loss (ROL) that minimizes loss of O2 to the surrounding environment (Figures 1, 2). Furthermore, this barrier may impede the movement of soil-derived toxins (i.e., reduced metal ions) and gases (e.g. methane, CO2, and ethylene) into the roots (Armstrong 1979; Colmer 2003a; Greenway et al. 2006). Both upland and lowland rice species use these traits under waterlogged conditions (Colmer 2003b).

Figure 2
figure2

Differences in lysigenous aerenchyma formation and patterns of radial O 2 loss (ROL) in rice roots under drained soil conditions and waterlogged soil conditions. Under drained soil conditions, lysigenous aerenchyma is constitutively formed, but a barrier to ROL is not formed; thus ROL at the basal part of the root decreases O2 diffusion to the apical part. By contrast, under waterlogged soil conditions lysigenous aerenchyma formation is enhanced and formation of the barrier to ROL is induced, resulting in the promotion of longitudinal O2 diffusion to the root apex. Under drained soil conditions, lysigenous aerenchyma is constitutively formed at the basal part of the roots (a), but it is not usually formed at the apical part of the roots (b). Under waterlogged soil conditions, lysigenous aerenchyma is induced at the basal part (c) and the apical part (d) of the roots. Lysigenous aerenchyma is more highly developed at the basal part of the roots (a, c) than at the apical part (b, d). Arrow thickness reflects the amount of O2 available. Ep, epidermis; Ex, exodermis; Sc, sclerenchyma; Co, cortex; En, endodermis.

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Some recent reviews summarized the mechanisms of flooding tolerance in plants (Bailey-Serres and Voesenek 2008; Bailey-Serres et al. 2010; Colmer and Voesenek 2009; Hattori et al. 2011; Nagai et al. 2010). In this review, we include recent discoveries that were not covered in the previous reviews and summarize what is known about the physiological and molecular mechanisms that contribute to tolerance to, or avoidance of, submergence (i.e., internal aeration and growth controls) and also adaptation to waterlogging (i.e., formations of aerenchyma and a barrier to ROL) in rice and other gramineous plants.

Internal aeration in submerged plants

Effective internal aeration in plants is crucial to survive under submergence. In rice, aerenchyma is well developed in roots, internodes, sheaths, and the mid-rib of leaves (Colmer and Pedersen 2008a; Matsukura et al. 2000; Steffens et al. 2011) and contributes to the effective internal aeration between shoots and roots (Colmer 2003a; Colmer and Pedersen 2008a). Submerged leaves have gas films that aid O2 and CO2 exchange between leaves and the surrounding water, and thus increase underwater net photosynthesis by supplying CO2 during the day (under light conditions) and promote O2 uptake for respiration at night (Colmer and Pedersen 2008b; Pedersen et al. 2009; Raskin and Kende 1983). As a result, leaf gas films contribute to leaf sugar production by photosynthesis when under water, and in turn shoot and root dry mass (Pedersen et al. 2009). Removal of leaf gas films caused a decrease of O2 partial pressure (pO2) in roots when shoots were in darkness, suggesting that leaf gas films partially contribute to O2 transport from shoot to root (Pedersen et al. 2009; Winkel et al. 2011). Taken together, these findings indicate that leaf gas films are important for submergence tolerance in rice (Pedersen et al. 2009; Raskin and Kende 1983).

Strategies of adaptation to flash-flood conditions

Catling (1992) defined submergence tolerance as "the ability of a rice plant to survive 10-14 days of complete submergence and renew its growth when the water subsides; there is no stem elongation during submergence." Under this definition, submergence tolerance indicates flash-flood tolerance. Generally, the seedlings of many lowland rice cultivars elongate their leaves to get oxygen at the water's surface under submerged conditions. However, because this shoot elongation requires large amounts of energy, most rice cultivars (i.e., flash-flood-intolerant cultivars) have poor ability to recover fully after the water recedes and eventually sustain severe damage or die (Jackson and Ram 2003). By contrast, the flash-flood-tolerant East Indian rice cultivar FR13A shows restricted shoot elongation and reduced energy consumption under submergence (Setter and Laureles 1996). The energy in FR13A plants is preserved during submergence, and upon desubmergence their growth can be restarted by using this energy (Fukao et al. 2006; Singh et al. 2001). There is therefore a negative correlation between shoot elongation and survival rate under complete submergence (Setter and Laureles 1996).

FR13A has the Submergence-1 (SUB1) locus on chromosome 9 (Xu and Mackill 1996). Xu et al. (2006) discovered that the SUB1 locus contains SUB1A, SUB1B, and SUB1C, all of which encode ethylene response factors and are upregulated under submergence, but only SUB1A is responsible for the flash-flood tolerance. The near-isogenic line M202(SUB1), which was generated by introgression of the SUB1 region from FR13A into the flash-flood-intolerant cultivar M202, shows restricted shoot elongation under submergence, as does FR13A (Bailey-Serres et al. 2010; Fukao et al. 2006; Xu et al. 2006). To preserve energy and carbohydrates, M202(SUB1) suppresses the expression of genes encoding α-amylase and sucrose synthase, which are involved in starch and sucrose metabolism (Fukao et al. 2006). In addition, SUB1A positively regulates the genes involved in alcohol fermentation and thus promotes acclimation of plants to flash-flood conditions (Fukao et al. 2006). Fukao and Bailey-Serres (2008) reported that SUB1A also enhances the expression of genes encoding SLENDER RICE-1 (SLR1) and SLR1 like 1 (SLRL1), which are key repressors of gibberellin (GA) signaling in rice; it also negatively regulates the GA response in order to restrict shoot elongation under submergence. Recently, it was shown that SUB1A expression is also induced by drought and oxidative stress upon desubmergence (Fukao et al. 2011). SUB1A positively regulates the expressions of genes involved in ABA-mediated acclimation to drought conditions. Moreover, under oxidative stress, SUB1A promotes the expression of genes related to the detoxification of reactive oxygen species (ROS) and reduces the accumulation of ROS. As a result, M202(SUB1) has a higher drought and oxidative tolerance than M202 (Fukao et al. 2011). In rain-fed rice fields, inadequate water management is prone to cause flooding and drought. Thus, as submergence and drought stresses can cause severe decreases in rice production in rain-fed rice fields, introgression of the SUB1A gene into rice cultivars intolerant of submergence and drought is a promising way of increasing rice productivity in these fields (Fukao et al. 2011).

Strategies for adaptation to deepwater-flood conditions

Deepwater flooding lasts for several months, and O2 deficiency causes energy depletion in plants. To survive under deepwater-flood conditions, rice plants must escape from the flooding. A unique trait of deepwater rice is that its internodes rapidly and substantially elongate to avoid deepwater flooding. Remarkably, some deepwater rice cultivars can increase their height by 25 cm/day (Vergara et al. 1976). This rapid elongation allows the leaf tips to extend above the water surface and enables the rice plants to efficiently photosynthesize and exchange gases for respiration (Bailey-Serres and Voesenek 2008). During internode elongation, ethylene biosynthesis is activated and the accumulated ethylene regulates the increases in GA content and decrease in ABA content. As internode elongation is promoted by GA or repressed by ABA, the increased GA/ABA ratio contributes to the elongation (Kende et al. 1998; Sauter 2000). Indeed, GA activates the expression of cell division-related genes (Sauter et al. 1995; van der Knaap et al. 1997), and thus active cell division is observed at the intercalary meristem in the internode under submergence (Métraux and Kende 1984). Moreover, high levels of expression of genes encoding expansin, which is involved in cell-wall loosening (Cho and Kende 1997a, b, c; Lee and Kende 2001), and changes in the orientation of cellulose microfibrils are observed in the internode during internode elongation (Sauter et al. 1993). Aerenchyma formation occurs in the internodes simultaneously with their elongation, and is enhanced by ethylene (Steffens et al. 2011). Growth of adventitious roots, which is preceded by death of epidermal cells that cover the root primordia (Mergemann and Sauter 2000; Steffens and Sauter 2005), is also promoted by ethylene (Steffens et al. 2006).

Recently, Hattori et al. (2009) identified the SNORKEL1 (SK1) and SNORKEL2 (SK2) genes responsible for internode elongation in deepwater rice. Non-deepwater rice (i.e., lowland rice) into which SK1 or SK2 had been introduced showed internode elongation in the same way as deepwater rice, indicating that the SK genes are key factors for the escape strategy of deepwater rice under deepwater-flood conditions. Because of space considerations, details of the function of SK genes have not been included in this review, but they have been summarized by Nagai et al. (2010) and Hattori et al. (2011).

Strategies of adaptation to waterlogging: (1) aerenchyma formation

Formation of aerenchyma is essential to the survival and functioning of plants subjected to waterlogging. The aerenchyma contributes to O2 supply from shoots to roots and to the ventilation of gases (e.g. CO2 and methane) from roots to shoots (Colmer 2003a; Evans 2003). The ventilation of gases in aerenchyma is mainly caused by gas diffusion in rice, but in some wetland species with 'through-flow pathways' (e.g. along rhizomes), gas flows can also occur by humidity- and Venturi-induced pressure flows (e.g. Phragmites australis; Armstrong et al. 1996). The aerenchyma may provide a photosynthetic benefit by concentrating CO2 from root respiration and transporting it to the leaf intercellular spaces in some wetland plant species (Constable and Longstreth 1994).

In general, aerenchyma can be classified into two types: (i) schizogenous aerenchyma, which develops by cell separation and differential cell expansion that creates spaces between cells, in e.g. Rumex palustris; and (ii) lysigenous aerenchyma, formed by the death and subsequent lysis of some cells, e.g., in rice (Jackson et al 1985a), maize (Drew et al 1981), wheat (Trought and Drew 1980), and barley (Arikado and Adachi 1955). In the roots, lysigenous aerenchyma forms in the cortex (Figure 2), whereas in the stems it can form in the cortex and pith cavity (Armstrong 1979).

In some wetland plant species such as rice, root lysigenous aerenchyma is constitutively formed under drained soil conditions (i.e., aerobic conditions; Jackson et al. 1985a), and its formation can be further enhanced during soil waterlogging (Figure 2; Colmer et al 2006; Justin and Armstrong 1991; Shiono et al. 2011; Visser and Bögemann 2006). In rice, aerenchyma formation is initiated at the apical parts of the roots and gradually expands to the basal parts of the roots (Figure 2; Ranathunge et al. 2003). Fully developed aerenchyma, which is observed on the basal parts of roots, separates the inner stele from the outer cell layers (i.e., sclerenchyma, hypodermis/exodermis, and epidermis) of the roots (Figure 2; Armstrong and Armstrong 1994; Kozela and Regan 2003; Ranathunge et al. 2003). Strands of remaining cells and cell walls separate gas spaces in the cortex, forming radial bridges, which are important for the structural integrity of the root and for both apoplastic and symplastic transport of nutrients (Figure 2; Drew and Fourcy 1986). During aerenchyma formation in rice root, cell death begins at the cells in the mid-cortex and then spreads out radially to the surrounding cortical cells (Kawai et al. 1998). The epidermis, hypodermis/exodermis, endodermis, and stele are unaffected, indicating that lysigenous aerenchyma formation occurs by closely controlled mechanisms (Yamauchi et al. 2011).

By contrast, in non-wetland plant species such as maize, wheat, and barley, root lysigenous aerenchyma does not form under well-drained soil conditions, but it may be induced by poor aeration (McDonald et al. 2001; McPherson 1939; Trought and Drew 1980). Generally, induction of aerenchyma formation takes 24-72 hours after the start of anaerobic treatment (Haque et al. 2010; Malik et al. 2003; Rajhi et al. 2011). In addition, aerenchyma formation is less extensive in non-wetland plant species than in wetland plant species (Armstrong 1979; Colmer and Voesenek 2009). Thus, non-wetland plants are less tolerant to waterlogging than wetland plants, such as rice.

Signaling of lysigenous aerenchyma formation

In rice and maize, ethylene is implicated in the induction of lysigenous aerenchyma formation (Drew et al. 2000; Jackson and Armstrong 1999; Justin and Armstrong 1991; Konings 1982; Shiono et al. 2008). Rice roots form lysigenous aerenchyma constitutively even under well-aerated conditions (Jackson et al. 1985a; Justin and Armstrong 1991; Shiono et al. 2011). Lysigenous aerenchyma formation in rice roots can be further increased by ethylene treatment under aerated conditions and decreased by treatment with an ethylene perception inhibitor (e.g. silver ions) under stagnant (0.1% agar) deoxygenated conditions (which mimics hypoxic/anoxic conditions in waterlogged soils; Wiengweera et al. 1997), although cultivars (e.g. Norin 36 and RB3) differ in their sensitivity to ethylene (Justin and Armstrong 1991). Justin and Armstrong (1991) also pointed out that consideration of the lengths of the roots sampled was important for comparison of aerenchyma formations between treatments. More recently, ethylene has been shown to increase root aerenchyma formation in another rice cultivar, Calrose (Colmer et al. 2006). In maize roots, ethylene biosynthesis is stimulated by enhancing the activity of 1-aminocyclopropene-1-carboxylic acid (ACC) synthase and ACC oxidase at the beginning of aerenchyma formation (He et al. 1996a). Thus, treatment of maize roots with inhibitors of ethylene biosynthesis (e.g. aminoethoxyvinylglycine, aminooxyacetic acid (AOA), and cobalt chloride) or action (e.g. silver ions) effectively blocks aerenchyma formation under hypoxic conditions (Drew et al. 1981; Jackson et al. 1985b; Konings 1982). These observations indicate that ethylene works as a trigger for the induction of aerenchyma formation in rice and maize. On the other hand, in the roots of another wetland species (Juncus effusus), lysigenous aerenchyma formation is not affected by treatment with ethylene or the ethylene perception inhibitor 1-methylcyclopropene (1-MCP; Visser and Bögemann 2006). To determine whether ethylene is (or is not) a common factor in regulation of the induction of lysigenous aerenchyma formation in the roots of wetland species, the effect of ethylene on aerenchyma formation should be studied by treatment of a wider range of wetland species while considering the possible influences of root length and tissue age along the root axes (Justin and Armstrong 1991; Visser and Bögemann 2006).

Ethylene-responsive lysigenous aerenchyma formation is affected by chemical inhibitors or stimulators of programmed cell death (PCD) and other signaling pathways. Heterotrimeric G-protein-, phospholipase C (PLC)-, inositol 1,4,5-trisphosphate (IP3)-, or Ca2+-dependent signaling pathways are involved in the process of lysigenous aerenchyma formation in maize roots (Drew et al. 2000; He et al. 1996b). It has been proposed that, under oxygen deprivation, Ca2+ is released from mitochondria into the cytosol (Subbaiah et al. 1994); the elevated cytosolic Ca2+ may provoke subsequent activation of kinases and phosphatases during aerenchyma formation (Subbaiah and Sachs 2003). Lysigenous aerenchyma formation is also induced by okadaic acid, an inhibitor of protein phosphatases, and is repressed by K252a, an inhibitor of protein kinases (Drew et al. 2000; He et al. 1996b). These calcium-dependent signalings may result in activation of expression of the genes responsible for aerenchyma formation (Drew et al. 2000; Subbaiah and Sachs 2003). PCD is a tightly regulated pathway that accompanies the activation of specific biochemical pathways (Greenberg 1996). PCD is distinguished from necrosis, which occurs by uncontrolled, accidental cell death without activation of signaling pathways (Drew et al. 2000; Gunawardena et al. 2001a). Cell death during lysigenous aerenchyma formation is similar to apoptosis in animal cells, which includes DNA fragmentation, nuclear condensation, and nuclear and plasma membrane blebbing (Drew et al. 2000).

One of the final steps in lysigenous aerenchyma formation is degradation of the cell wall, which is mediated by cell-wall modification or degradation enzymes. Changes in esterified and de-esterified pectins in the cell wall of the maize cortex are observed during cell death (Gunawardena et al. 2001b). Subsequently, the cell wall is degraded by the combined action of pectolytic, xylanolytic, and cellulosolytic enzymes (Evans 2003; Jackson and Armstrong 1999). The activity of cellulase (CEL) is increased by treatment with ethylene, okadaic acids, and reagents that increase intracellular Ca2+ levels, whereas CEL activity is decreased by treatment with K252a and inhibitors of Ca2+ increase (He et al. 1996b). In maize roots, expression of a gene encoding xyloglucan endotransglycosylase (XET) is induced by waterlogging, and its induction is inhibited by treatment with the ethylene biosynthesis inhibitor AOA (Saab and Sachs 1996). Treatment with AOA prevents the formation of lysigenous aerenchyma, suggesting that induction of XET production in response to ethylene is involved in aerenchyma formation through cell-wall modification (Saab and Sachs 1996).

On the basis of this evidence, Evans (2003) proposed that cell death in the root cortex during lysigenous aerenchyma formation can be classified into five steps: (1) perception of hypoxia and initiation of ethylene biosynthesis; (2) perception of ethylene signaling by cells of the mid-cortex; (3) initiation of cell death with loss of ions to the surrounding environment, plasma membrane invagination, and formation of small vesicles; (4) chromatin condensation, increased activity of cell-wall hydrolytic enzymes, and the surrounding of organelles by membranes; and (5) cell-wall degradation, cell lysis, and absorption of the cell contents and water by the surrounding cells.

Genes associated with lysigenous aerenchyma formation

So far, studies of lysigenous aerenchyma formation have been done mainly from a physiological perspective. However, the genes involved in lysigenous aerenchyma formation in the root have not been identified. Recently, Rajhi et al. (2011) identified genes associated with lysigenous aerenchyma formation in maize roots by using a microarray analysis combined with laser microdissection. They found that Ca2+ signaling-related genes encoding Calcineurin B-like protein and Calmodulin-like protein were upregulated under waterlogged conditions, and their expression levels were higher in the cortical cells than in the stelar cells. Waterlogging also induces the expression of cell-wall modification-related genes (e.g. XET and CEL). Induction of the expressions of calcium signaling- and cell wall modification-related genes is suppressed by treatment with 1-MCP. These results support the previously proposed mechanism of ethylene-mediated lysigenous aerenchyma formation (Jackson and Armstrong 1999; Drew et al. 2000; Evans 2003).

A gene encoding respiratory burst oxidase homolog (RBOH; a plant homolog of gp91phox in mammalian NADPH oxidase), which has a role in ROS generation (Torres and Dangl 2005), is upregulated strongly in the cortical cells and slightly less strongly in the stelar cells and the outer cell layers of maize roots (Figure 3; Rajhi et al. 2011; Yamauchi et al. 2011). On the other hand, a gene encoding metallothionein (MT), which has a role in ROS scavenging (Wong et al. 2004, Xue et al. 2009), is constitutively expressed in all of the cortical cells, the stelar cells, and the outer cell layers of maize roots under aerobic conditions. By contrast, under waterlogged conditions the MT gene is hardly expressed at all in the cortical cells but is still highly expressed in the stelar cells and the outer cell layers (Figure 3; Rajhi et al. 2011; Yamauchi et al. 2011). These results suggest that H2O2 and other ROS are scavenged by the constitutively expressed MT in stelar cells and the outer cell layers, whereas in the cortical cells decreased MT expression prevents ROS scavenging, thereby leading to greater ROS accumulation, which activates the subsequent processes of PCD (i.e., lysigenous aerenchyma formation) in maize roots (Figure 3). Interestingly, upregulation of RBOH and downregulation of MT also occur in rice roots during inducible aerenchyma formation under anaerobic conditions (Yamauchi and Nakazono, unpublished). Similarly, ethylene-promoted downregulation of expression of a gene encoding MT2b enhances the accumulation of H2O2 produced by NADPH oxidase and thus induces epidermal cell death in rice (Steffens and Sauter 2009) or aerenchyma formation in rice internodes (Steffens et al. 2011). These results suggest that downregulation of MT genes plays an important role in tissue-specific or cell type-specific PCD in rice and maize.

Figure 3
figure3

Model of lysigenous aerenchyma formation. Waterlogging promotes biosynthesis and accumulation of ethylene, followed by induction of RBOH expression. RBOH activity leads to production and accumulation of O2·- at the apoplast. The O2·- is spontaneously or enzymatically converted to H2O2, which can easily diffuse into the cytosol through the plasma membrane. Under waterlogged conditions, in the cytosol of stelar cells and cells in the outer cell layers, H2O2 and other ROS are scavenged by constitutively-expressed MT. By contrast, in the cortical cells, the decreased MT expression prevents ROS scavenging, thereby leading to greater ROS accumulation, which activates the subsequent processes of programmed cell death and lysis of the cortical cells (i.e., lysigenous aerenchyma formation). Under aerobic conditions, the RBOH gene is expressed at low level and the MT gene is constitutively expressed in the cortical cells. WL, waterlogged conditions; Aer, aerobic conditions; OCL, outer cell layers; ap, apoplast; cs, cytosol.

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Strategies of adaptation to waterlogging: (2) formation of a barrier to ROL

Oxygen molecules diffusing longitudinally through aerenchyma toward the root tips may be either consumed by respiration or diffused radially to the rhizosphere (Armstrong 1979; Colmer 2003a). ROL, the flux of O2 from the aerenchyma to the soil, is determined by the concentration gradient, the physical resistance to O2 diffusion in a radial direction, and consumption of O2 by cells along this radial diffusion path (Armstrong 1979; Colmer 2003a). ROL aerates the rhizosphere and is therefore considered to be of adaptive significance in plants growing in waterlogged soil (Armstrong 1979; Blossfeld et al. 2011; Colmer 2003a; Neubauer et al. 2007). However, ROL reduces the supply of O2 to the root apex and thereby causes a decrease in root length in anaerobic soil (Armstrong 1979; Colmer 2003a; Colmer et al. 1998; Jackson and Armstrong 1999).

The roots of many wetland species, including rice, have the ability to prevent ROL to the rhizosphere by forming a barrier in the root peripheral cell layers exterior to the aerenchyma (Figure 2; McDonald et al. 2002; Visser et al. 2000). This adaptive trait enhances longitudinal O2 diffusion through the aerenchyma towards the root apex by diminishing losses of O2 to the rhizosphere, thereby enabling the roots to elongate into anaerobic substrates (Armstrong 1979).

The roots of some wetland species have constitutively present barriers to ROL (e.g. J. effusus; Visser et al. 2000), whereas in other species such as rice and Hordeum marinum the barrier to ROL is induced during growth under anaerobic conditions (Colmer 2003b; Colmer et al. 1998; Garthwaite et al. 2003; Kotula et al. 2009a; Shiono et al. 2011). Analysis of the spatial patterns of ROL along rice roots has revealed that O2 leakage from the basal regions of the long roots under stagnant conditions is quite low (Figure 4), but there are large amounts of O2 flux from the root apexes (Figure 4) and numerous short lateral roots that appear near the base of the main axes (Armstrong 1971a; Armstrong et al. 1996, Colmer 2003b). The barrier to ROL, together with reoxidation of the rhizosphere around the root tips and lateral roots, enables elongation of the roots into the anoxic environment and restricts the entry of toxic compounds from highly reduced soils (Armstrong 1979; Armstrong et al. 1996; Colmer and Voesenek 2009).

Figure 4
figure4

Rates of ROL along intact adventitious roots of rice grown under aerated or stagnant deoxygenated conditions. The experiment was conducted following the methods of Colmer et al. (1998) with minor modifications. Rice (cv. Nipponbare) was grown in a 28°C, continually lit growth chamber. Nine-day-old plants were grown in aerated nutrient solution (Aerated conditions) or stagnant deoxygenated agar solution (Stagnant conditions) for 14 or 15 days before measurements were taken along adventitious roots (80-130 mm long). ROL measurements were performed at 27-29°C under light conditions using cylindrical root-sleeving O2 electrode. Values are means (n = 3) ± SD.

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Despite the importance of the barrier to ROL, there are few data available on the O2 permeability coefficient across the cell layers exterior to the aerenchyma. Recently, Kotula and Steudle (2009) developed a gas perfusion technique to measure the O2 permeability of the outer cell layers of the roots and applied the technique to rice grown under either aerated or stagnant deoxygenated conditions. Plants grown in the stagnant O2-deficient conditions of the external growth medium showed much lower O2 permeability than plants grown in an aerated solution. The variation in O2 permeability, either by blocking apoplastic pores or killing living tissues, indicated that physical resistance is the dominating factor impeding O2 loss from rice roots, although respiratory O2 consumption may contribute to low rates of ROL (Kotula et al. 2009b). Strong physical impedance to radial O2 diffusion in rice roots has already been shown by Armstrong (1971b). In this study, a barrier to ROL was evident in the adventitious roots of rice, even when respiration was inhibited by cooling the root medium to 3°C. Similar findings have been reported by Armstrong et al. (2000) and Garthwaite et al. (2008) in the roots of P. australis and H. marinum, respectively. In H. marinum the physical barrier appeared to account for 84% of the reduction in O2 loss and respiratory activity for 16% (Garthwaite et al. 2008).

Anatomical and chemical nature of the barrier to ROL

It seems that suberization and/or lignification of the cell walls in the root layers exterior to the aerenchyma is implicated in the development of a tight barrier to ROL (Figure 5; Armstrong et al. 2000; Garthwaite et al. 2008; Kotula et al. 2009a; Soukup et al. 2007). In a recent study in rice, rates of ROL from the roots of plants grown under aerated or deoxygenated conditions were quantified, and the results were combined with parallel histochemistry and analytical chemistry (Kotula et al. 2009a). Deoxygenated conditions induced the early development of Casparian bands and suberin lamellae in the exodermis and of lignin in densely packed, uniseriate sclerenchymal cells located interior to the exodermis (Figure 5). In agreement with the results of the histochemical analyses, quantitative analyses using gas chromatography and mass spectrometry have shown that the levels of suberin (both aromatic and aliphatic domains), as well as lignin, released from the outer root sleeves are several times greater in plants grown in oxygen-deprived media compared with plants grown in aerated solution (Kotula et al. 2009a; Ranathunge et al. 2011). Independent of the growth conditions, the total amounts of suberin and lignin increase along the roots towards the basal zones (Kotula et al. 2009a; Ranathunge et al. 2011). Although these studies have shown a direct relationship between changes in O2 permeability and the formation of apoplastic barriers, the precise nature of the ROL barrier remains unclear. Namely, the relative contributions of suberin and lignin in limiting ROL are not well known; potentially, one of the two might not be needed for formation of the barrier (Kotula et al. 2009a). Function of lignin in preventing ROL may not be applied to all plant species. In Amazonian tree species (De Simone et al. 2003), as well as in P. australis (Soukup et al. 2007), resistance to ROL is correlated only with the deposition of suberin, but not lignin. Histochemical solute penetration studies using periodic acid have further confirmed that in the roots of P. australis the suberized exodermis--not the lignified sclerenchyma, which is easily penetrated by periodic acid--is the radial permeation barrier (Soukup et al. 2007). Shiono et al. (2011) found that suberin increased prior to changes in lignin in rice, suggesting that deposition of suberin is more important for the ROL barrier formation than lignin. However, the suberin and lignin deposits were not evident in the roots within the first 2 days of stagnant treatment, during which time barrier induction was already complete. In long adventitious roots (105-130 mm in length), barrier to ROL was well formed within 24 hours under stagnant deoxygenated conditions and dark granules of high-density material were observed by transmission electron microscopy in the spaces between the exodermal cells and also between the sclerenchyma cells in roots at 48 hours after the stagnant treatment (Shiono et al. 2011). This result suggests that these microstructural changes also contribute to the diminution of ROL in the rice root. The precise nature of the barrier to ROL still needs to be more clearly elucidated (see below).

Figure 5
figure5

Staining for suberin and lignin in the outer cell layers of rice roots grown under aerated or stagnant deoxygenated conditions. Nine-day-old rice plants were grown in aerated nutrient solution (Aerated conditions; a, c) or stagnant deoxygenated agar solution (Stagnant conditions; b, d) for 14 days. Basal parts (10-20 mm regions from the root-shoot junction) of the adventitious roots were sliced into 80-μm-thick sections, and were incubated in lactic acid saturated with chloral hydrate at 70°C for 1 h for clearing. For suberin staining, sections were stained with Fluorol Yellow 088 at room temperature for 1 h and observed under UV-light with epifluorescence microscopy (a, b). For lignin staining, sections were stained for 5 min with phloroglucinol/hydrochloride at room temperature to visualize lignin with cinnamyl aldehyde groups (c, d). White arrow indicates yellow-green fluorescence of suberin at hypodermis/exodermis and black arrow indicates orange-red pigmentation of stained lignin at the sclerenchyma. Ep, epidermis; Ex, exodermis; Sc, sclerenchyma; Co, cortex. Scale bars = 50 μm.

Full size image

The barrier to ROL vs. nutrient and water uptake

Although the barrier to ROL helps wetland plants to tolerate waterlogging, it may also reduce water and nutrient uptake (Armstrong 1979; Koncalová 1990). For example, the rates of NH4+ and NO3- net uptake in the basal region of rice roots were about 30% of those in maize, even when the plants were grown in aerated solution (Colmer and Bloom 1998) and the permeability of roots to water is substantially smaller in rice than in maize (Hose et al. 2001; Miyamoto et al. 2001). However, a recent study demonstrated that the early formation of apoplastic barriers in the endodermis and exodermis of rice roots in stagnant solutions does not significantly affect hydraulic conductivity (Ranathunge et al. 2011). This is in agreement with the earlier findings of Garthwaite et al. (2006) in stagnantly grown H. marinum, in which induction of the barrier to ROL did not impede the water permeability of the roots. In contrast to water flow, stagnant growth conditions markedly reduce the permeability of the rice roots to oxygen and to ions such as Fe2+, Cu2+, and NaCl (Armstrong and Armstrong 2005; Kotula et al. 2009b; Krishnamurthy et al. 2009; Ranathunge et al. 2011). The extra suberin and lignin deposited in the roots in stagnant solutions may effectively clog the wall pores, making a barrier sufficient to block the passage of oxygen and ions, but not water, which is mainly bulk and viscous in nature (Kotula et al. 2009b; Ranathunge et al. 2004, 2011). It appears that rice roots living in anaerobic media can retain oxygen in the aerenchyma while taking up sufficient water (Kotula et al. 2009b; Ranathunge et al. 2011). This is achieved because of differences in the transport mechanisms of oxygen and water. When measured with heavy water, the diffusional water permeability of the outer part of the rice root was an order of magnitude smaller than that of oxygen (Ranathunge et al. 2004; Kotula et al. 2009b; Kotula and Steudle 2009). However, diffusional water permeability was smaller than the bulk water permeability by a factor of 600-1400. The latter parameter is the one that is important during water uptake (Steudle and Peterson 1998). This suggests that rice has evolved an optimum balance between water uptake and O2 loss. Water moves predominantly through the porous apoplastic pathway by using a hydrostatic pressure gradient (Ranathunge et al. 2004), whereas the movement of O2 ought to be appreciable over the whole inter-cell interface and is diffusional in nature (Kotula et al. 2009b; Ranathunge et al. 2011).

Formation of the barrier to ROL

There are major uncertainties regarding the signals involved in the formation of an inducible barrier to ROL. Colmer et al. (2006) showed that ethylene, which promotes the induction of lysigenous aerenchyma formation (Justin and Armstrong, 1991), did not induce a tight barrier to ROL in rice roots, indicating that these two root aeration traits, which are considered to act synergistically to enhance O2 diffusion to the root apex, appear to be differentially regulated. By contrast, a significant decline in ROL, which is correlated with suberization and lignification of the outer cell layers, is observed after the exposure of rice roots to carboxylic acids (e.g. acetic acid, propanoic acid, butyric acid, and caproic acid; Armstrong and Armstrong 2001) and sulfide (in the form of phytotoxins produced by micro-organisms in waterlogged soils; Armstrong and Armstrong 2005). Similar effects are found when carboxylic acids are applied to the roots of H. marinum (Kotula, Colmer, and Nakazono, unpublished). However, the reduction in ROL from the roots of rice and H. marinum exposed to toxic levels of carboxylic acids and sulfide was associated with injury, rather than with a specific signal for induction of the barrier to ROL (Armstrong and Armstrong 2001; Colmer 2003a).

Recently, Fleck et al. (2011) showed that Si nutrition increased suberization and lignification of rice roots, which was accompanied by silicic acid-triggered transcription of genes associated with suberin and lignin biosynthesis. As a consequence of suberization and lignification of the outer root cell layers, the oxidation power of the rice roots was reduced. Although it is suggested by Fleck et al. (2011) that altered levels of silicic acid play a role in promoting the biosynthesis of suberin and lignin, the signal involved in inducible ROL barrier formation remains unclear.

Perspectives

Although great progress has been made in our understanding of the mechanisms involved in adaptation to submergence or waterlogging, there are still gaps in our knowledge, mainly in regard to the signaling pathways and molecular processes. The genetic regulation of the formation of lysigenous aerenchyma and the barrier to ROL remains to be determined. Recently, Nakazono and his colleagues (Rajhi et al. 2011; Shiono, Yamazaki, and Nakazono, unpublished) have been investigating the expressions of genes associated with the formation of inducible lysigenous aerenchyma and the barrier to ROL by using laser microdissection-mediated microarray analysis of the cortex in maize roots and the outer cell layers in rice roots, respectively, under anaerobic conditions. This approach should help to identify important genes involved in the formation of these two structures. Further insights into the nature of the barrier to ROL and the molecular mechanism of inducible barrier formation could be achieved from the characterization of suberin or lignin formation-affected rice mutants in comparison with the respective wild types (Ranathunge et al. 2011).

Conclusions

This review summarizes what is known about the physiological and molecular mechanisms used by rice to cope with submergence and waterlogging. For submergence, the mechanisms include internal aeration and growth controls (i.e., a quiescence strategy or an escape strategy). For waterlogging, the mechanisms include formation of aerenchyma and a barrier to ROL. These adaptive traits enable rice plants to have high tolerance to submergence or waterlogging compared with other dryland crops. An advantage of rice is that its genome has been fully sequenced and many tools for studying its molecular biology and genetics (e.g. oligo microarrays, mutant collections, and databases) have been developed. These resources should accelerate our understanding of the mechanisms involved in adaptation of rice to excess water stress and should lead to their introduction into dryland crops.

References

  1. Arikado H, Adachi Y: Anatomical and ecological responses of barley and some forage crops to the flooding treatment. Bulletin Faculty Agriculture, Mie University Tsu Mie 1955, 11: 1–29.

  2. Armstrong J, Armstrong W: Chlorophyll development in mature lysigenous and schizogenous root aerenchyma provides evidence of continuing cortical cell viability. New Phytologist 1994, 126: 493–497. 10.1111/j.1469-8137.1994.tb04246.x

  3. Armstrong J, Armstrong W: Rice and Phragmites : effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. American Journal of Botany 2001, 88: 1359–1370. 10.2307/3558443

  4. Armstrong J, Armstrong W: Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+and water uptake, and lateral root emergence. Annals of Botany 2005, 96: 625–638. 10.1093/aob/mci215

  5. Armstrong J, Armstrong W, Beckett PM, Halder JE, Lythe S, Holt R, Sinclair A: Pathways of aeration and the mechanisms and beneficial effects of humidity- and Venturi-induced convections in Phragmites australis (Cav.) Trin ex Steud. Aquatic Botany 1996, 54: 177–197. 10.1016/0304-3770(96)01044-3

  6. Armstrong W: Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiologia Plantarum 1971a, 25: 192–197. 10.1111/j.1399-3054.1971.tb01427.x

  7. Armstrong W: Oxygen diffusion from the roots of rice grown under non-waterlogged conditions. Physiologia Plantarum 1971b, 24: 242–247. 10.1111/j.1399-3054.1971.tb03487.x

  8. Armstrong W: Aeration in higher plants. Advances in Botanical Research 1979, 7: 236–332.

  9. Armstrong W, Cousins D, Armstrong J, Turner DW, Beckett PM: Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis . Annals of Botany 2000, 86: 687–703. 10.1006/anbo.2000.1236

  10. Armstrong W, Drew MC: Root growth and metabolism under oxygen deficiency. In Plant Roots: The Hidden Half. 3rd edition. Edited by: Waisel Y et al. New York & Basel; 2002:729–761.

  11. Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, Mackill D: Submergence tolerant rice: SUB1 's journey from landrace to modern cultivar. Rice 2010, 3: 138–147. 10.1007/s12284-010-9048-5

  12. Bailey-Serres J, Voesenek LACJ: Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 2008, 59: 313–339. 10.1146/annurev.arplant.59.032607.092752

  13. Blossfeld S, Gansert D, Thiele B, Kuhn AJ, Lösch R: The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp. Soil Biology and Biochemistry 2011, 43: 1186–1197. 10.1016/j.soilbio.2011.02.007

  14. Catling D: Rice in deep water. London: MacMillan Press; 1992.

  15. Cho HT, Kende H: Expansins in deepwater rice internodes. Plant Physiology 1997a, 113: 1137–1143. 10.1104/pp.113.4.1137

  16. Cho HT, Kende H: Expansins and internodal growth of deepwater rice. Plant Physiology 1997b, 113: 1145–1151.

  17. Cho HT, Kende H: Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell 1997c, 9: 1661–1671.

  18. Colmer TD: Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell and Environment 2003a, 26: 17–36. 10.1046/j.1365-3040.2003.00846.x

  19. Colmer TD: Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice ( Oryza sativa L.). Annals of Botany 2003b, 91: 301–309. 10.1093/aob/mcf114

  20. Colmer TD, Bloom AJ: A comparison of NH 4 +and NO 3 -net fluxes along roots of rice and maize. Plant, Cell and Environment 1998, 21: 240–246. 10.1046/j.1365-3040.1998.00261.x

  21. Colmer TD, Cox MCH, Voesenek LACJ: Root aeration in rice ( Oryza sativa ): evaluation of oxygen, carbon dioxide, and ethylene as possible regulators of root acclimatizations. New Phytologist 2006, 170: 767–778. 10.1111/j.1469-8137.2006.01725.x

  22. Colmer TD, Flowers TJ: Flooding tolerance in halophytes. New Phytologist 2008, 179: 964–974. 10.1111/j.1469-8137.2008.02483.x

  23. Colmer TD, Gibberd MR, Wiengweera A, Tinh TK: The barrier to radial oxygen loss from roots of rice ( Oryza sativa L.) is induced by growth in stagnant solution. Journal of Experimental Botany 1998, 49: 1431–1436. 10.1093/jexbot/49.325.1431

  24. Colmer TD, Pedersen O: Oxygen dynamics in submerged rice ( Oryza sativa ). New Phytologist 2008a, 178: 326–334. 10.1111/j.1469-8137.2007.02364.x

  25. Colmer TD, Pedersen O: Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO 2 and O 2 exchange. New Phytologist 2008b, 177: 918–926. 10.1111/j.1469-8137.2007.02318.x

  26. Colmer TD, Voesenek LACJ: Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 2009, 36: 665–681. 10.1071/FP09144

  27. Constable JVH, Longstreth DJ: Aerenchyma carbon dioxide can be assimilated in Typha latifolia L. leaves. Plant Physiology 1994, 106: 1065–1072.

  28. De Simone O, Haase K, Müller E, Junk WJ, Hartmann K, Schreiber L, Schmidt W: Apoplasmic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species. Plant Physiology 2003, 132: 206–217. 10.1104/pp.102.014902

  29. Drew MC, Fourcy A: Radial movement of cations across aerenchymatous roots of Zea mays measured by electron probe X-ray microanalysis. Journal of Experimental Botany 1986, 37: 823–831. 10.1093/jxb/37.6.823

  30. Drew MC, Jackson MB, Giffard SC, Campbell R: Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency. Planta 1981, 153: 217–224.

  31. Drew MC, He CJ, Morgan PW: Programmed cell death and aerenchyma formation in roots. Trends in Plant Science 2000, 5: 123–127. 10.1016/S1360-1385(00)01570-3

  32. Drew MC, Lynch JM: Soil anaerobiosis, microorganisms, and root function. Annual Review of Phytopathology 1980, 18: 37–66. 10.1146/annurev.py.18.090180.000345

  33. Evans DE: Aerenchyma formation. New Phytologist 2003, 161: 35–49. 10.1046/j.1469-8137.2003.00907.x

  34. Fleck AT, Nye T, Repenning C, Stahl F, Zahn M, Schenk MK: Silicon enhances suberization and lignification in roots of rice ( Oryza sativa ). Journal of Experimental Botany 2011, 62: 2001–2011. 10.1093/jxb/erq392

  35. Fukao T, Bailey-Serres J: Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings of the National Academy of Sciences USA 2008, 105: 16814–16819. 10.1073/pnas.0807821105

  36. Fukao T, Xu K, Ronald PC, Bailey-Serres J: A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 2006, 18: 2021–2034. 10.1105/tpc.106.043000

  37. Fukao T, Yeung E, Bailey-Serres J: The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 2011, 23: 412–427. 10.1105/tpc.110.080325

  38. Garthwaite AJ, Armstrong W, Colmer TD: Assessment of O 2 diffusivity across the barrier to radial O 2 loss in adventitious roots of Hordeum marinum . New Phytologist 2008, 179: 405–416. 10.1111/j.1469-8137.2008.02467.x

  39. Garthwaite AJ, Steudle E, Colmer TD: Water uptake by roots of Hordeum marinum : formation of a barrier to radial O 2 loss does not affect root hydraulic conductivity. Journal of Experimental Botany 2006, 57: 655–664. 10.1093/jxb/erj055

  40. Garthwaite AJ, von Bothmer R, Colmer TD: Diversity in root aeration traits associated with waterlogging tolerance in genus Hordeum . Functional Plant Biology 2003, 30: 875–889. 10.1071/FP03058

  41. Greenberg JT: Programmed cell death: a way of life for plants. Proceedings of the National Academy of Sciences USA 1996, 93: 12094–12097. 10.1073/pnas.93.22.12094

  42. Greenway H, Armstrong W, Colmer TD: Conditions leading to high CO 2 (> 5 kPa) in waterlogged-flooded soils and possible effects on root growth and metabolism. Annals of Botany 2006, 98: 9–32. 10.1093/aob/mcl076

  43. Greenway H, Setter TL: Is there anaerobic metabolism in submerged rice plants? a view point. In Physiology of stress tolerance in rice: Proceedings of the international conference on stress physiology of rice Edited by: Singh VP et al. 1996, 11–30. IRRI IRRI

  44. Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE: Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize ( Zea mays L.). Planta 2001a, 212: 205–214. 10.1007/s004250000381

  45. Gunawardena AHLAN, Pearce DME, Jackson MB, Hawes CR, Evans DE: Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize ( Zea mays L.) promoted by ethylene. Plant, Cell and Environment 2001b, 24: 1369–1375. 10.1046/j.1365-3040.2001.00774.x

  46. Haque ME, Abe F, Kawaguchi K: Formation and extension of lysigenous aerenchyma in seminal root cortex of spring wheat ( Triticum aestivum cv. Bobwhite line SH 98 26) seedlings under different strengths of waterlogging. Plant Root 2010, 4: 31–39.

  47. Hattori Y, Nagai K, Ashikari M: Rice growth adapting to deepwater. Current Opinion in Plant Biology 2011, 14: 100–105. 10.1016/j.pbi.2010.09.008

  48. Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsuoka T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M: The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 2009, 460: 1026–1030. 10.1038/nature08258

  49. He CJ, Finlayson SA, Drew MC, Jordan WR, Morgan PW: Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia. Plant Physiology 1996a, 112: 1679–1685.

  50. He CJ, Morgan PW, Drew MC: Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiology 1996b, 112: 463–472.

  51. Hose E, Clarkson DT, Steudle E, Schreiber L, Hartung W: The exodermis: a variable apoplastic barrier. Journal of Experimental Botany 2001, 52: 2245–2264. 10.1093/jexbot/52.365.2245

  52. Jackson MB, Armstrong W: Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1999, 1: 274–287. 10.1111/j.1438-8677.1999.tb00253.x

  53. Jackson MB, Fenning TM, Jenkins W: Aerenchyma (gas-space) formation in adventitious roots of rice ( Oryza sativa L.) is not controlled by ethylene or small partial pressures of oxygen. Journal of Experimental Botany 1985a, 36: 1566–1572. 10.1093/jxb/36.10.1566

  54. Jackson MB, Fenning TM, Drew MC, Saker LR: Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen. Planta 1985b, 165: 486–492. 10.1007/BF00398093

  55. Jackson MB, Ram PC: Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Annals of Botany 2003, 91: 227–241. 10.1093/aob/mcf242

  56. Justin SHFW, Armstrong W: Evidence for the involvement of ethane in aerenchyma formation in adventitious roots of rice ( Oryza sativa L.). New Phytologist 1991, 118: 49–62. 10.1111/j.1469-8137.1991.tb00564.x

  57. Kawai M, Samarajeewa PK, Barrero RA, Nishiguchi M, Uchimiya H: Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta 1998, 204: 277–287. 10.1007/s004250050257

  58. Kende H, van der Knaap E, Cho HT: Deepwater rice: a model plant to study stem elongation. Plant Physiology 1998, 118: 1105–1110. 10.1104/pp.118.4.1105

  59. Koncalová H: Anatomical adaptations to waterlogging in roots of wetland graminoids: limitations and drawbacks. Aquatic Botany 1990, 38: 127–134. 10.1016/0304-3770(90)90102-Q

  60. Konings H: Ethylene-promoted formation of aerenchyma in seedling roots of Zea mays L. under aerated and non-aerated conditions. Physiologia Plantarum 1982, 54: 119–124. 10.1111/j.1399-3054.1982.tb06313.x

  61. Kotula L, Ranathunge K, Schreiber L, Steudle E: Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice ( Oryza sativa L.) grown in aerated or deoxygenated solution. Journal of Experimental Botany 2009a, 60: 2155–2167. 10.1093/jxb/erp089

  62. Kotula L, Ranathunge K, Steudle E: Apoplastic barriers effectively block oxygen permeability across outer cell layers of rice roots under deoxygenated conditions: roles of apoplastic pores and of respiration. New Phytologist 2009b, 184: 909–917. 10.1111/j.1469-8137.2009.03021.x

  63. Kotula L, Steudle E: Measurements of oxygen permeability coefficients of rice ( Oryza sativa L.) roots using a new perfusion technique. Journal of Experimental Botany 2009, 60: 567–580. 10.1093/jxb/ern300

  64. Kozela C, Regan S: How plants make tubes. Trends in Plant Science 2003, 8: 159–164. 10.1016/S1360-1385(03)00050-5

  65. Krishnamurthy P, Ranathunge K, Franke R, Prakash HS, Schreiber L, Mathew MK: The role of root apoplastic transport barriers in salt tolerance of rice ( Oryza sativa L.). Planta 2009, 230: 119–134. 10.1007/s00425-009-0930-6

  66. Lee Y, Kende H: Expression of β-expansins is correlated with internodal elongation in deepwater rice. Plant Physiology 2001, 127: 645–654. 10.1104/pp.010345

  67. Malik AI, Colmer TD, Lambers H, Schortemeyer LM: Aerenchyma formation and radial O 2 loss along adventitious roots of wheat with only the apical root portion exposed to O 2 deficiency. Plant, Cell and Environment 2003, 26: 1713–1722. 10.1046/j.1365-3040.2003.01089.x

  68. Matsukura C, Kawai M, Toyohuku K, Barrero RA, Uchimiya H, Yamaguchi J: Transverse vein differentiation associated with gas space formation--fate of the middle cell layer in leaf sheath development of rice. Annals of Botany 2000, 85: 19–27. 10.1006/anbo.1999.0993

  69. McDonald MP, Galwey NW, Colmer TD: Waterlogging tolerance in the tribe triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant, Cell and Environment 2001, 24: 585–596. 10.1046/j.0016-8025.2001.00707.x

  70. McDonald MP, Galwey NW, Colmer TD: Similarity and diversity in adventitious root anatomy as related to root aeration among a range of wetland and dryland grass species. Plant, Cell and Environment 2002, 25: 441–451. 10.1046/j.0016-8025.2001.00817.x

  71. McPherson DC: Cortical air spaces in the roots of Zea mays L. New Phytologist 1939, 38: 190–202. 10.1111/j.1469-8137.1939.tb07098.x

  72. Mergemann H, Sauter M: Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiology 2000, 124: 609–614. 10.1104/pp.124.2.609

  73. Métraux JP, Kende H: The cellular basis of the elongation response in submerged deep-water rice. Planta 1984, 160: 73–77. 10.1007/BF00392468

  74. Miyamoto N, Steudle E, Hirasawa T, Lafitte R: Hydraulic conductivity of rice roots. Journal of Experimental Botany 2001, 52: 1835–1846. 10.1093/jexbot/52.362.1835

  75. Nagai K, Hattori Y, Ashikari M: Stunt or elongate? two opposite strategies by which rice adapts to floods. Journal of Plant Research 2010, 123: 303–309. 10.1007/s10265-010-0332-7

  76. Neubauer SC, Toledo-Durán GE, Emerson D, Megonigal JP: Returning to their roots: iron-oxidizing bacteria enhance short-term plaque formation in the wetland-plant rhizosphere. Geomicrobiology Journal 2007, 24: 65–73. 10.1080/01490450601134309

  77. Pedersen O, Rich SM, Colmer TD: Surviving floods: leaf gas films improve O 2 and CO 2 exchange root aeration, and growth of completely submerged rice. Plant Journal 2009, 58: 147–156. 10.1111/j.1365-313X.2008.03769.x

  78. Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K, Watanabe R, Mliki A, Nagamura Y, Tsutsumi N, Nishizawa NK, Nakazono M: Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytologist 2011, 190: 351–368. 10.1111/j.1469-8137.2010.03535.x

  79. Ram PC, Singh AK, Singh BB, Singh VK, Singh HP, Setter TL, Singh VP, Singh RK: Environmental characterization of floodwater in eastern India: relevance to submergence tolerance of lowland rice. Experimental Agriculture 1999, 35: 141–152. 10.1017/S0014479799002057

  80. Ranathunge K, Steudle E, Lafitte R: Control of water uptake by rice ( Oryza sativa L.): role of the outer part of the root. Planta 2003, 217: 193–205.

  81. Ranathunge K, Kotula L, Steudle E, Lafitte R: Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. Journal of Experimental Botany 2004, 55: 433–447. 10.1093/jxb/erh041

  82. Ranathunge K, Lin J, Steudle E, Schreiber L: Stagnant deoxygenated growth enhances root suberization and lignifications, but differentially affects water and NaCl permeabilities in rice ( Oryza sativa L.) roots. Plant, Cell and Environment 2011, 34: 1223–1240. 10.1111/j.1365-3040.2011.02318.x

  83. Raskin I, Kende H: How does deep water rice solve its aeration problem. Plant Physiology 1983, 72: 447–454. 10.1104/pp.72.2.447

  84. Saab IN, Sachs MM: A flooding-induced xyloglucan endo-transglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiology 1996, 112: 385–391. 10.1104/pp.112.1.385

  85. Sauter M: Rice in deep water: "how to take heed against a sea of troubles". Naturwissensehaften 2000, 87: 289–303. 10.1007/s001140050725

  86. Sauter M, Seagull RW, Kende H: Internodal elongation and orientation of cellulose microfibrils and microtubules in deepwater rice. Planta 1993, 190: 354–362.

  87. Sauter M, Mekhedov SL, Kende H: Gibberellin promotes histone H1 kinase activity and the expression of cdc2 and cyclin genes during the induction of rapid growth in deepwater rice internodes. Plant Journal 1995, 7: 623–632. 10.1046/j.1365-313X.1995.7040623.x

  88. Setter TL, Laureles EV: The beneficial effect of reduced elongation growth on submergence tolerance of rice. Journal of Experimental Botany 1996, 47: 1551–1559. 10.1093/jxb/47.10.1551

  89. Setter TL, Waters I: Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant and Soil 2003, 253: 1–34.

  90. Setter TL, Waters I, Sharma SK, Singh KN, Kulshreshtha N, Yaduvanshi NPS, Ram PC, Singh BN, Rane J, McDonald G, Khabaz-Saveri H, Biddulph TB, Wilson R, Barclay I, McLean R, Cakir M: Review of wheat improvement for waterlogging tolerance in Australia and India: the importance of anaerobiosis and element toxicities associated with different soils. Annals of Botany 2009, 103: 221–235.

  91. Shiono K, Ogawa S, Yamazaki S, Isoda H, Fujimura T, Nakazono M, Colmer TD: Contrasting dynamics of radial O 2 -loss barrier induction and aerenchyma formation in rice roots of two lengths. Annals of Botany 2011, 107: 89–99. 10.1093/aob/mcq221

  92. Shiono K, Takahashi H, Colmer TD, Nakazono M: Role of ethylene in acclimations to promote oxygen transport in roots of plants in waterlogged soils. Plant Science 2008, 175: 52–58. 10.1016/j.plantsci.2008.03.002

  93. Singh HP, Singh BB, Ram PC: Submergence tolerance of rainfed lowland rice: search for physiological marker traits. Journal of Plant Physiology 2001, 158: 883–889. 10.1078/0176-1617-00036

  94. Soukup A, Armstrong W, Schreiber L, Franke R, Votrubová O: Apoplastic barriers to radial oxygen loss and solute penetration: a chemical and functional comparison of the exodermis of two wetland species, Phragmites australis and Glyceria maxima . New Phytologist 2007, 173: 264–278. 10.1111/j.1469-8137.2006.01907.x

  95. Steffens B, Sauter M: Epidermal cell death in rice ( Oryza sativa L.) is regulated by ethylene, gibberellin and abscisic acid. Plant Physiology 2005, 139: 713–721. 10.1104/pp.105.064469

  96. Steffens B, Sauter M: Epidermal cell death in rice is confined to cells with a distinct molecular identity and is mediated by ethylene and H 2 O 2 through an autoamplified signal pathway. Plant Cell 2009, 21: 184–196. 10.1105/tpc.108.061887

  97. Steffens B, Geske T, Sauter M: Aerenchyma formation in the rice stem and its promotion by H 2 O 2 . New Phytologist 2011, 190: 369–378. 10.1111/j.1469-8137.2010.03496.x

  98. Steffens B, Wang J, Sauter M: Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 2006, 223: 604–612. 10.1007/s00425-005-0111-1

  99. Steudle E, Peterson CA: How does water get through roots? Journal of Experimental Botany 1998, 49: 775–788. 10.1093/jexbot/49.322.775

  100. Subbaiah CC, Bush DS, Sachs MM: Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. Plant Cell 1994, 6: 1747–1762.

  101. Subbaiah CC, Sachs MM: Molecular and cellular adaptations of maize to flooding stress. Annals of Botany 2003, 90: 119–127.

  102. Torres MA, Dangl JL: Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 2005, 8: 397–403. 10.1016/j.pbi.2005.05.014

  103. Trought MCT, Drew MC: The development of waterlogging damage in young wheat plants in anaerobic solution cultures. Journal of Experimental Botany 1980, 31: 1573–1585. 10.1093/jxb/31.6.1573

  104. van der Knaap E, Jagoueix S, Kende H: Expression of an ortholog of replication protein A1 (RPA1) is induced by gibberellin in deepwater rice. Proceedings of the National Academy of Sciences USA 1997, 94: 9979–9983. 10.1073/pnas.94.18.9979

  105. Vergara BS, Jackson B, De Datta SK: Deepwater rice and its response to deepwater stress. In Climate and Rice. International Rice Research Institute; 1976:301–319.

  106. Visser EJW, Bögemann GM: Aerenchyma formation in the wetland plant Juncus effuses is independent of ethylene. New Phytologist 2006, 171: 305–314. 10.1111/j.1469-8137.2006.01764.x

  107. Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ: Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant, Cell and Environment 2000, 23: 1237–1245. 10.1046/j.1365-3040.2000.00628.x

  108. Wiengweera A, Greenway H, Thomson C: The use of agar nutrient solution to simulate lack of convection in waterlogged soils. Annals of Botany 1997, 80: 115–123. 10.1006/anbo.1996.0405

  109. Winkel A, Colmer TD, Pedersen O: Leaf gas films of Spartina anglica enhance rhizome and root oxygen during tidal submergence. Plant, Cell and Environment 2011, 34: 2083–2092. 10.1111/j.1365-3040.2011.02405.x

  110. Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K: Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiology 2004, 135: 1447–1456. 10.1104/pp.103.036384

  111. Xu K, Mackill DJ: A major locus for submergence tolerance mapped on rice chromosome 9. Molecular Breeding 1996, 2: 219–224. 10.1007/BF00564199

  112. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ: Sub1A is an ethylene responsive-factor-like gene that confers submergence tolerance to rice. Nature 2006, 442: 705–708. 10.1038/nature04920

  113. Xue T, Li X, Zhu W, Wu C, Yang G, Zheng C: Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. Journal of Experimental Botany 2009, 60: 339–349.

  114. Yamauchi T, Rajhi I, Nakazono M: Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species. Plant Signaling and Behavior 2011, 6: 759–761. 10.4161/psb.6.5.15417

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Acknowledgements

The authors thank Drs. T. D. Colmer and K. Shiono for stimulating discussions. This work was supported partly by a grant from the Bio-oriented Technology Research Advancement Institution (Promotion of Basic Research Activities for Innovative Biosciences), a grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan (Genomics for Agricultural Innovation, IPG-0012), and grants-in-aid from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. LK is grateful to the Japanese Society for the Promotion of Science for the postdoctoral fellowship.

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  1. Laboratory of Plant Genetics and Breeding, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya, 464-8601, Japan
    • Shunsaku Nishiuchi
    • , Takaki Yamauchi
    • , Hirokazu Takahashi
    • , Lukasz Kotula
    •  & Mikio Nakazono
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  1. Shunsaku Nishiuchi
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Nishiuchi, S., Yamauchi, T., Takahashi, H. et al. Mechanisms for coping with submergence and waterlogging in rice. Rice 5, 2 (2012). https://doi.org/10.1186/1939-8433-5-2

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Keywords

  • Aerenchyma
  • Barrier to radial O2 loss
  • Leaf gas films
  • Rice
  • Submergence
  • Waterlogging