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Flooding stress and O2-shortage in plants: An overview

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Raquel Iglesias‐Fernández1 and Angel Matilla2

Centro de Biotecnología y Genómica de Plantas (UPM‐INIA), Escuela Técnica Superior de Ingenieros Agrónomos, Universidad Politécnica de Madrid, Madrid, Spain 2 Facultad of Farmacia, Departmento de Fisiología Vegetal, Universidad of Santiago de Compostela (USC), Santiago de Compostela, A Coruña, Spain

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More than 300 000 plant species now occupy almost every terrestrial niche. Although their ancestors were aquatic, the land plants derived from them are relatively intolerant to free water in their surroundings, especially if it is slow‐moving or immobile. Therefore, flooding is a major issue for plant survival in many areas of the world. That is, the inability to diffuse gases (i.e. O2 and CO2 among others) turns water into a barrier that encases and kills the affected cells. Gases diffuse 104 faster in air than in water. Thus, gaseous movement through soil pores in waterlogged areas is so strongly inhibited by their water content that it fails to match the needs of growing roots. The maximum amount of O2 dissolved in floodwater in equilibrium with the air is a little over 3% of that in a similar volume of air itself. This small amount is quickly consumed during the early time of flooding by aerobic rhizosphere microorganisms and roots (Matilla‐Vázquez and Matilla, 2014 and references therein). The organs affected must adapt to environments rich in water as the only alternative to the species survival. Growth arrest and death arise principally because demand for ATP exceeds the supply and self‐poisoning by products of anaerobic metabolism. On the other hand, the light levels reaching submerged plants can vary from almost nil in dark, turbid waters to normal levels in clear water (Vervuren et al., 2003). These alterations in photosynthetic light absorption and

decrease in O2 and CO2 diffusion generated by flooding provokes substantial variations in the levels of cellular ATP, NADPH and carbohydrates (Mommer et al., 2005). Two other major changes during flooding are the increases in reactive oxygen species (ROS) formed within plant cells (Fukao et al., 2006; Steffens et al., 2013), as well as the entrapment of the plant hormone ethylene (ET). Flood tolerant species use changes in ET, ROS, O2 and CO2 as signals to induce adaptive processes. Furthermore, these species have the adequate plasticity to adjust their physiology resulting in metabolic, morphological and anatomical adaptation. When plants are waterlogged by flooding, they have lower availability (hypoxia) or total absence of O2 (anoxia), thus severely impairing energy generation through reduced/eliminated mitochondrial oxidative phosphorylation (Voesenek and Bailey‐Serres, 2015). A simple observation of the existing vegetation in the margins of lakes, rivers and flooded environments demonstrate that these plants are well‐adapted to submergence (Jackson 2006). However, rice, through several metabolic adaptations, is the only species able to germinate and survive up to 2 weeks in complete anoxia (Bailey‐Serres and Voesenek, 2008; Nishiuchi et al., 2012). The diffusion in water of the two key gases in the life of autotrophic organisms (i.e. CO2 and O2) together with the added difficulties of its diffusion when the water is immobile or scarcely moves, generates a hardly altered photosynthetic activity and low O2 production.

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21.1 Introduction

Water Stress and Crop Plants: A Sustainable Approach, First Edition. Edited by Parvaiz Ahmad. © 2016 John Wiley & Sons, Ltd. Published 2016 by John Wiley & Sons, Ltd.

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stress and crop plants: A sustainable approach

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As plants are organisms that lack a circulatory system to mobilize photosynthetic O2, flooded organs are very vulnerable to O2 deficiency. Therefore, it is not surprising that some species can be predisposed to endure or avoid a low‐O2 environment (Fukao et al., 2006; Hattori et al., 2009). These organisms perform a series of alterations to adapt to O2 depleted environments (e.g. flooding). But the mechanisms for morphological, metabolic and molecular adaptations responsible for flooding tolerance and sensitivity remain scarcely understood. However, the great plasticity of the flood tolerant species causes at least two adaptive strategies (Bailey‐Serres and Voesenek, 2008): (i) the escape strategy (i.e. endurance or sit and wait), referring to morphological inducible adaptations to low‐O2 stress and includes the formation of aerenchyma and adventitious roots, root cortical air spaces to promote the air transport from shoot to root, and leaf and shoot elongation (Vartapetian and Jackson, 1997; Lorbiecke and Sauter, 1999; Parlanti et al., 2011). This strategy in rice plants (Oriza sativa) involves a fast elongation of internodes (Colmer and Voesenek, 2009). (ii) The quiescence strategy involves the conservation of energy and carbohydrates to prolong underwater survival and enable recovery growth once flood is reduced. The shoot elongation is suppressed in rice plants to preserve carbohydrates for a long period under flash‐flood conditions (Colmer and Voesenek, 2009). As explained next, both adaptive strategies are strictly controlled in rice by the ET response factors (ERFs) encoded by the SNORKEL (SK1 and SK2) and SUBMERGENCE1A (SUB1A) genes. However, current data derived from a flood tolerance screen performed with 109 Oryza genotypes do not suggest that SUB1A

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21.2 How plant species can respond to flooding?

repairs the problems of flooding tolerance (Pena‐Castro et al., 2011; Zhu et al., 2011). Accessions of Oryza rhizomatis and Oryza eichingeri were flood tolerant and lacked SUB1A‐1. In these genotypes, anaerobic genes were only poorly induced. The results indicate that SUB1A‐1 is not essential to confer submergence tolerance in wild rice genotypes (Niroula et al., 2012). At a cellular level, a common eukaryotic response to low‐O2 is the Pasteur Effect, whereby glycolysis and fermentation are promoted and the tricarboxylic acid (TCA/Krebs) cycle and mitochondrial respiration are repressed (Bailey‐Serres and Voesenek, 2008). Metabolic adaptation to anaerobiosis includes the induction of fermentation pathway enzymes (Figure 21.1). The root is the plant organ that is in direct contact with the soil. Anaerobic fermentation yields only 2–3 ATP molecules from each molecule of glucose entering glycolysis. However, aerobic respiration via TCA and mitochondrial electron transport yields 36–38 ATP (Fox et al., 1994). The small yield of ATP in anaerobic cells is insufficient for survival beyond a few hours. That is, the knowledge of cell metabolism under O2 shortage is essential to explain the adaptations to flooding. Therefore, all current research is focused on understanding how the radical system perceives flooding and transforms this signalling into a physiological response. However, a large number of species have been unable to support this stress. The answer may lie in how the changes in water homeostasis are detected by the flooded root cell. But this explanation is still enigmatic. Interestingly, in waterlogged Arabidopsis the carbohydrate transporters were more strongly upregulated in shoots than in roots, suggesting that soluble sugars are transported from shoot to root to maintain the energy metabolism (Figure 21.1). Metabolite studies in waterlogged poplar (Kreuzwieser et al., 2009) indicated that sucrose is transported via phloem to waterlogged roots to support growth and viability. Flooding alters a large number of rhizosphere properties (Dat et al., 2004 and references therein). In other words, the changes in environmental signals near to the root and the reduction of active processes (e.g. osmotic adjustment, nutrient uptake or regulation of cytoplasm pH) can coexist in the flooding response. Together, slow diffusion of O2 during flooding, generates the accumulation of toxic compounds derived of root anaerobic metabolism, such as organic acids, C2H5OH, CH4, H+, Fe+2, Mn+2, H2S, ET and N2, among others

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However, a number of species are perfectly adapted to this environmental stressful situation since they have acquired mechanisms to avoid and escape the flooding stress (such is aerenchyma production and submerged internodes elongation) (Mustroph et al., 2010; Licausi, 2011; Parlanti et al., 2011; Bailey‐Serres et al., 2012; Nishiuchi et al., 2012). In this chapter, knowledge of the most important adaptations to flooding are updated and revised in depth.

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Figure 21.1 Scheme showing the involvement of ABA, ET and GAs in flooding adaptation. AA: Amylase Activity; CW: Cell Wall;

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ADH: Alcohol DeHydrogenase; PDC: Pyruvate DeCarboxylase; SK: Snorkel; SLR: Slender; SUB1: SUBmergence1; SnRK: Sucrose non‐fermenting‐1‐Related protein Kinase); SUS: Sucrose Synthase.

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(Setter et al., 2009; Matilla and Matilla‐Vázquez, 2014). If a percentage of these compounds is excreted to the rhizosphere and then accumulate to toxic concentrations, the physicochemical properties of soil can be negatively altered leading often to plant death (Kirk et al., 2014). Accordingly, there is increasing evidence that changes in soil properties are well capable of stimulating plant responses. However, these alterations are not always sufficient enough to justify the plant changes commonly observed during flooding. Finally, it seems clear the existence in higher plants of a conserved flooding response network that includes alterations in ET‐triggered gene expression. This response leads to growth and carbohydrates stress‐induced catabolism for efficient production and utilization of ATP (for a review see Bailey‐Serres and Voesenek, 2010).

21.2.1 Do plants have mechanisms that sense O2 concentration? The deficiency of O2 is a harmful consequence of flooding, either through flooding of the root system (waterlogging), or partial to complete submergence of the aerial parts (Bailey‐Serres et al., 2012). The existence of plants adapted to low‐O2 environments leads us to

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assume that plants have mechanisms to detect different levels of this gas. Any mechanism must possess an O2 sensor, capable of detecting changes in ambient O2 concentrations, that triggers a signalling cascade leading to the synthesis of specific transcription factors (TFs), which in turn will mediate the cellular response. Recently, compelling evidence for the existence of O2 sensing has been found in plants (Gibbs et al., 2011; Licausi et al., 2011). This sensitivity mechanism in rice and in Arabidopsis involves the regulation of the hypoxia responsive gene expression through the O2‑dependent post‐translational modification of specific TFs (i.e. group VII ERFs family, whose members share an APETALA2 (AP2) DNA binding domain of 60–70 amino acids) via the N‐end rule pathway for protein degradation via the proteasome (Nakano et al., 2006; Sasidharan and Mustroph, 2011; Bailey‐Serres et al., 2012; Voesenek and Bailey‐Serres, 2013). Namely, there is a correlation between the functionality of the group VII ERFs critical for survival at low‐O2 and submergence conditions. The group VII ERFs are part of the ET responsive factors (ERF) family of TFs that play a significant role in transcriptional regulation of plant growth, development and response to abiotic stresses

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control the preparation of group VII ERFs proteins for degradation via the 26S proteasome by oxidizing the Cys‐2 and using O2 as a co‐substrate (Graciet and Wellmer, 2010) (Figre 21.2). That is, PCO act as sensor proteins for O2 in plants. The five members of group VII ERFs in Arabidopsis (i.e. HRE1, HRE2, RAP2.2, RAP2.3 and RAP2.12) were N‐end rule substrates, and displayed how the O2‐dependent degradation of constitutively expressed ERFs controls the responses to hypoxia (Gibbs et al., 2011). Thus, (i) an increased stabilization of the HRE2 protein during low‐O2, triggers transcription of genes associated with anaerobic metabolism and improves the hypoxia survival and (ii) mutants in the HRE2 turnover pathway constitutively produce transcripts associated with anaerobic metabolism and are less sensitive to low O2 stress (Gibbs et al., 2011). On the other hand, it is well known that under normoxia, the ERFs interact with the Acyl CoA binding proteins (ACBPs), whose localization is in the plasmalemma. Recent data suggest that low‐O2 concentrations affects to the ERF‐ACBP interaction and therefore releases the sequestered proteins (Sasidharan and Mustroph, 2011;

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(Nakano et al., 2006; Jung et al., 2010; Yang et al., 2011). This ERF group is characterized by the strong conservation in their ERF domain as well as in the N‑terminal motif MCGGAI (I/L) (Tournier et al., 2003). For better clarity, group VII ERFs of Arabidopsis are stabilized under hypoxia/anoxia, but destabilized under normoxic conditions (normal levels of O2; typically, 20–21% in the atmosphere, or 2–3% in physiological contexts) via the N‐end rule pathway, which controls the degradation of proteins depending on the sequence of their N‐terminal amino acids (Gibbs et al., 2014; Weits et al., 2014) (Figure 21.2). Only 10% of the genes belonging to the ERFs family are ET‐regulated (Nakano et al., 2006). The O2‐dependent targeting of proteins for degradation can occur in proteins containing cysteine as the second amino acid (i.e. Cys‐2). Cys‐2 oxidation is dependent of the intracellular O2 content (Tasaki et al., 2012). However, it is still unresolved as to how the Cys‐2 oxidation of a protein is mediated to adjust the cellular response to O2 availability. Recently, it was shown that the Plant‐Cys‐Oxidases (PCOs) are involved in the N‐end rule pathway‐mediated proteolysis. PCOs

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Figure 21.2 Representative model for the O2 sensitivity under normoxia and hypoxia conditions in Arabidopsis. Under normoxia,

VII ERF transcription factors (TFs) are bound to the acyl‐CoA‐binding proteins (ACBPs) to the membrane to avoid its movement to the nucleus. When O2 concentration decrease, VII ERFs are released from ACBPs and transported to it for activation of expression of the hyoxia response genes. When O2 levels return to normality these TFs are degraded through the N‐end rule pathway: Methionine Endopeptidase (Met‐APS) cleaves the methionine at the N‐terminal of the VII ERFs revealing a Cystein (Cys) destabilizing residue. This C is susceptible of being chemically oxidized by O2 (Cys*). Generation of the oxidized Cys provokes the arginilation of this N‐terminal by the arginyl‐tRNA protein arginyltransferasa (ATE). The E3 ligase proteolysis (PRT6) recognizes this basic amino‐acid terminal and targets it for proteolysis via the 26S proteasome.

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21.2.2 How do plants adapt to flooding?

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21.2.2.1 Enhancing gas exchange at the level of the root system This response is obviously derived from the impediment exerted by waterlogging on the movement of key gases for respiration and photosynthesis (i.e. O2 and CO2). The appearance of the aerenchyma is one of the most important features in the response to the flooding stress (see Section 3). However, some species hardly have, or cannot develop, aerenchyma and are classified as flood intolerant. The efficiency of O2 diffusion in anaerobic soils can be increased when its loss from the root to the soil is prevented. For this, the adapted plants to this kind of stress either have a constitutive O2 impermeable barrier characterised by accumulation of new structural and impermeable components in the exodermis cell walls (CW) (e.g. suberine lamellae; Enstone et al., 2003; Shiono et al., 2011) or have the capacity to develop such a barrier upon flooding (Garthwaite et al., 2006; 2008). These two adaptive mechanisms seem are not controlled or triggered by ET. However, high concentrations of phytotoxins can induce the occurrence of the barrier against radial O2 loss (Armstrong and Armstrong, 2005).

pyrophosphate instead of ATP in some enzymatic reactions, discarding of energetically expensive biosynthetic pathways, increased use of glycolysis and fermentation, sucrose degradation and so on. (Voesenek and Sasidharan, 2013). The importance of fermentation and glycolysis for surviving under low‐O2 has been well established and one of its most important aspects is the regeneration of NAD+ from NADH in the absence of mitochondrial respiration (Liu et al., 2005; Branco‐Price et al., 2008; Van Dongen et al., 2009). The Arabidopsis thaliana ALCOHOL DEHYDROGENASE1 (AtADH1) and the SUCROSE SYNTHASE genes (i.e. AtSUS1 and AtSUS4) are vital for tolerance to low‐O2 conditions (Peng et al., 2001; Ismond et al., 2003; Bieniawska et al., 2007), among other data on alterations at the molecular level (Christianson et al., 2010; Lee et al., 2011; Narsai et al., 2011) (Figure 21.1). Recently, it was hypothesized that hypoxia acts as a positional cue to set germ cell fate (Kelliher and Walbot, 2012). Moreover, exposure of Zea mays root apex cells to hypoxia is sufficient to generate adaptation expressed as fermentative activity in the whole root. Interestingly, cells of the transition zone (TZ) show the highest release of nitric oxide (NO) during hypoxia. Likewise, the use of NO scavengers and donors indicates that the systemic induction of fermentation activity in the whole root requires the NO production in the TZ (Mugnai et al., 2012). Besides, the mitochondria generate ROS during hypoxia as by‐ products of oxidative phosphorylation (Klok et al., 2002). However, this organelle is not the only ROS producer cellular compartment (Marino et al., 2012; Steffens et al., 2013 and references therein). The ROS production and detoxification is likely to play a widespread role in signalling and damage from the onset and release from low‐O2 stress (Bailey‐Serres and Chang, 2005; Semenza, 2007; Marino et al., 2012; Steffens et al., 2013).

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Bailey‐Serres et al., 2012). This could potentially turn on a rapid hypoxia response. Summarizing, when the cell tends to be hypoxic, the ERFs are transported to the nucleus where they initiate transcription of specific downstream target genes that mediate the adaptation and survival to hypoxia. By contrast, when normoxia is restored, the hypoxia response is also rapidly reversed, as oxidised ERFs are targeted to the proteasomal machinery via the N‐end rule pathway (Figure 21.2). Licausi et al. (2011) provides evidence that transcriptional activation of genes associated with anaerobic metabolism is mediated by the O2‐dependent degradation of RAP2.12, most likely through post‐translational oxidation of Cys‐2. Interestingly, group VII ERFs are differentially regulated by O2 and ET (Voesenek and Sasidharan, 2013 and references therein).

21.2.2.2 Acclimation affecting plant metabolism The flooded organs are very vulnerable to O2 deficiency. The O2 shortage in the flooded radical system generates a very low O2 partial pressure in the mitochondria and a strong respiratory crisis (i.e. low ATP production via oxidative phosphorylation). The plant uses a number of strategies to adapt to this ATP shortage, such as use of

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21.3 Aerenchyma and flooding stress Many important crop plants are sensitive to flooding or waterlogging conditions caused by heavy rain or irrigation, and these conditions are also frequently encountered by plants growing in aquatic or semi‐aquatic habitats. The lack of O2 under these environmental conditions affects roots and sometimes shoots (Colmer and Voesenek, 2009) and the most critical challenge encountered is maintaining an energy supply for

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Aerenchyma formation in primary root cortex has been hardly studied in monocots (i.e. primary aerenchyma; Seago et al., 2005; Fagerstedt, 2010; Nishiuchi et al., 2012). In addition to primary aerenchyma, stems, adventitious roots, hypocotyls and nodules of dicots produce large amounts of constitutive secondary aerenchyma under flooding or hypoxia (Youn et al., 2008; Rhine et al., 2010; Shimamura et al., 2010). Secondary aerenchyma (e.g. aerenchymatous phellem), characterized by being spongy and highly porous tissue, is sometimes produced from phellogen secondary cortex (Mochizuki et al., 2000; Stevens et al., 2002; Teakle et al., 2011; Verboven et al., 2012). In other species (e.g. members of the Fabaceae family) the secondary aerenchyma development increases the formation of hypertrophic lenticels on the surface of the stems and roots, and the aerenchyma is brought into contact with the atmosphere through these lenticels (Jackson and Ricard, 2003). Both, secondary aerenchyma and lenticels are produced from phellogen layer and flooding stress quickly induces the development of hypertrophic lenticels. Thus, in the flooded species Alnus glutinosa, the O2 is transported into roots through this hypertrophic tissue just above the water surface. By using 18O2 as tracer, it was shown that the stem phellem was an important entry point for O2 transport to roots in waterlogged soybean plants (Shimamura et al., 2010). Phellem has been also found in the nodules of the annual flood‐tolerant legume Mellilotus siculus. However, the direct intervention on O2 supply to nodules needs to be unequivocally demonstrated. It is interesting to note that blocking of secondary aerenchyma in flooded soybean decreases both root nodulation and nodule activity (Shimamura et al., 2002). In contrast to other plant organs, the root nodules of wetland legumes are much less sensitive to flooding, and can sustain high N2 fixation rates through secondary aerenchyma. Aerenchyma can be formed by schizogeny or lysigeny (Evans, 2003). The formation of schizogenous aerenchyma only involves differential cell expansion and separation, but not cell death. The study of schizogenic process is underdeveloped. On the other hand, the formation of lysigenous aerenchyma is observed in several plants including rice (Figure 1d–f of Steffens et al., 2011), wheat, barley and maize roots, where cortex cells undergo a programmed cell death (PCD). Subsequently, protoplasts and CW are degraded and reabsorbed, resulting in a large gas space (Evans, 2003).

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continued metabolism and growth. As previously indicated Bailey‐Serres and Voesenek (2008) the flooding adaptive response is divided into two main strategies (see Section 2). That is, plant survival under flooding conditions is controlled by a complex and not yet well‐ known balance between both responses network (Fukao and Bailey‐Serres, 2008; Bailey‐Serres and Voesenek, 2010). Plants that adopt the quiescence strategy, use ATP economically, lack underwater growth and conserve substrates to prolong survival during flooding stress. Studies on Arabidopsis hypoxia tolerance have demonstrated that the growth of the radical system is severely inhibited and mechanisms involved in the increase of ATP are upregulated (van Dongen et al., 2009; Mustroph et al., 2009; Lee et al., 2011). Recently, a considerable natural variation in submergence tolerance was observed among Arabidopsis accessions (Vashisht et al., 2011) and this could be related to buffering of underwater growth. By contrast, the escape strategy involves shoot elongation to avoid shortage of O2. Therefore, the plant needs to improve the internal gas diffusion and accordingly develops special anatomical structures (i.e. aerenchyma and adventitious roots among the most important ones) to facilitate gas exchange (Garthwaite et al., 2008; Fagerstedt, 2010; Steffens et al., 2011; Abiko et al., 2012; Dawood et al., 2013). Thus, well‐adapted aquatic and semi‐aquatic plants constitutively develop aerenchyma, enlarged gas‐filled air spaces longitudinally interconnected to ameliorate low‐O2 stress (Yamauchi et al., 2013). Aerenchyma facilitates gas exchange between aerial and submerged plant parts (roots and/or shoots). That is, aerenchimatous tissue allows the roots or stem to maintain aerobic respiration under flooded or hypoxic environmental conditions. Aerenchyma not only improves gas diffusion between and inside plant organs but also conserves O2 by reducing respiratory demand per unit volume. Together, aerenchyma formation is an important plant trait for improving mainly waterlogging tolerance. Alternatively, aerenchyma also facilitates O2 diffusion to roots from submerged organs that generate O2 through underwater photosynthesis or from submerged shoots that are O2‐enriched due to O2 diffusion from the rhizosphere (Sand‐Jensen et al., 2005; Pedersen et al., 2009; 2011). On the other hand, aerenchyma vessel also facilitates depletion of ET accumulated in the root tips and thus alleviates inhibition of root growth (Visser and Pierik, 2007).

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Flooding stress and O2-shortage in plants: An overview 717 net photosynthesis and respiration (Colmer and Pedersen, 2008; Pedersen et al., 2009). It is of interest to note the possible contribution of leaf gas‐films to O2 transport from shoot to root (Winkel et al., 2011).

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21.4 Seed responses under O2-shortage

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One of the most important traits of angiosperm plants is their perpetuation through seeds. The production of seeds represents the main strategy to maintain plant genetic diversity, survival and dispersion. Before germination triggering, the seed is subjected to a strong desiccation process and subsequent dormancy whereby germination is blocked (Bewley et al., 2013; Matilla et al., 2015). The acquisition of desiccation tolerance appears to be a key milestone in plant evolution (Linkies et al., 2010) and the seed responds with strong metabolic and hormonal adjustments under these severe hypoxic conditions (Leprince and Buitink, 2010; Matilla et al., 2014). O2 diffusion during seed development (i.e. final phase of maturation) and early sensu‐stricto germination (i.e. seed imbibition onset) is prevented by seed covering layers and high internal metabolic activity. These features generate a hypoxic environment inside the seed that lead to ATP limitation (Borisjuk and Rolletschek, 2009). Accordingly, it is logical that the seed must adequately respond to this strong O2 restriction.

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Regarding surrounding parenchymal cells, the pre‐ aerenchymal ones have their own characteristics: they are larger and lighter and possess a great vacuole, have an absence of starch and their CWs are thin. This last property is important since they prevent the cell from collapsing in deep water environments. Usually, the lysigenic aerenchyma formation only affects cortical zones of the root (Colmer, 2003a). In rice, this formation is also present in stems and leaves and is constitutively developed (Colmer and Pedersen, 2008). Interestingly, some wetland plants have lysigenic aerenchyma constitutively formed on drained soils, this response being stimulated by flooding (Visser and Bögemann, 2006; Shiono et al., 2011; Abiko et al., 2012). However, there is large variation in the development of adaptive traits, even among different rice cultivars (Fukao et al., 2006; Hattori et al., 2009). Analysis in maize of QTLs associated with constitutive aerenchyma formation suggests that this trait is highly heritable (Mano and Omori, 2009). This feature opens up the exciting possibility of breeding flood tolerance into other economically important species. The number of aerenchyma formed in rice increases from bottom to top in a recurrent pattern that was observed in each internode; nodes did not display gas spaces. Gas flow across the node probably occurs through intercellular spaces (Steffens et al., 2011). On flooding, enhanced aerenchyma formation is observed in semi‐aquatic, but also in nonaquatic species like maize (He et al., 1994), Rumex palustris (Pierik et al., 2009) or Luffa cylindrica (Shimamura et al., 2007), to cite just a few examples. Interestingly, maize can form aerenchyma under drought conditions (Zhu et al., 2010). However, not all species can form aerenchyma under flooding. For example, the porosity value remains constant in Brassica napus (a non‐tolerant species) and increases to 40–50% in rice roots (Steffens et al., 2011). Setter and Waters (2003) suggest that the rate of root aerenchyma formation is correlated with the tolerance to flooding. On the other hand, hypoxic roots can respond favouring the longitudinal diffusion of O2 through the formation of a barrier (Radial O2 Loss; ROL) to prevent its lateral transport (Nishiuchi et al., 2012 and references therein). Probably, ROL also hinders the entrance from the soil of toxic compounds as ET, CH4, CO2 and so on. (Colmer et al., 2003b; Greenway et al., 2006; 2012). Finally, submerged leaves have what are known as gas‐films that aid O2 and CO2 exchange with the surrounding water, and thus increase underwater

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21.4.1 Rice seed germination under flooding The seed of rice is the only known seed that can p erfectly germinate under anoxia. However, its seedlings must possess several characteristics to endure waterlogged conditions (e.g. adventitious root, petiole and coleoptile elongation and so on.) (for a review see Magneschi and Perata, 2009; Angaji et al., 2010; Bailey‐Serres and Voeseneck, 2010; Ismail et al., 2012; Nishiuchi et al., 2012; Miro and Ismail, 2013; Colmer et al., 2014 and references therein). Germinating rice seeds under aerobic conditions obtain ATP from carbohydrate and lipid catabolism (Miro and Ismail, 2013). Rice is a species well adapted to flooding because of its well‐developed aerenchyma (Jackson and Ram, 2003) (also see Section 3). It has been shown that most rice cultivars die within one week of complete submergence due to carbohydrate starvation and an energetic crisis

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widespread in the plant kingdom (Perazzoli et al., 2006; Garrocho‐Villegas et al., 2007; Hoy and Hargrove, 2008; Vinogradov et al., 2011 and references therein). They are cytoplasmic proteins and their long evolutionary history suggests a major role for them in the life cycle of plants. Three kinds of Hbs (i.e. leghaemoglobins, non‐ symbiotic and truncated) have been described. In contrast to symbiotic Hbs (Hoy and Hargrove, 2008), the function of non‐symbiotic haemoglobins (nsHbs) is not fully elucidated (Matilla and Rodríguez‐Gacio, 2013 and references therein). However, there is growing evidence suggesting that structural characteristics are crucial to the function of nsHbs (e.g. the bis‐His‐Fe‐coordination of the haem appears to be a mechanism that regulates chemical processes under specific environmental conditions such as hypoxia). The nsHbs, probably ancestors of leghaemoglobins and highly conserved in higher plants (Vinogradov et al., 2011; Matilla and Rodríguez‐Gacio, 2013), are classified into class‐1 (nsHbs1) and class‐2 (nsHbs2) (Smagghe et al., 2008). Whereas nsHbs1 have moderate rates of O2‐binding and high O2‐affinity, nsHbs2 have high O2‐binding and low O2‐affinity. Current data suggest that nsHbs1and nsHbs2 are involved in O2 scavenging and maintaining of low‐O2 (μM) levels, respectively (Hoy and Hargrove, 2008). Moreover, nsHbs2 appear to have a specific function in facilitating O2 supply to mitochondrial respiration (Smagghe et al., 2009). Interestingly, nsHbs expression is induced under a large number of biotic‐ and abiotic‐ stress conditions (i.e. nutrient deficiency, hypoxia or invasion of pathogens). Thus, several possible roles have been proposed for nsHbs under hypoxic conditions: (i) serve as an O2 carrier as in animal cells (i.e. myoglobin) to help preserve mitochondrial respiration; (ii) act as an electron‐transfer protein; (iii) serve as a O2 sensor capable of regulating gene expression and (vi) help sustain glycolytic metabolism in stressed tissues. On the other hand, nsHbs1 genes are markedly expressed during hypoxia, indicating a highlight role of these proteins in the survival facing a hypoxic challenge (Dordas et al., 2003; Zhao et al., 2008). Understanding of nsHbs1 physiology necessarily requires the determination of spatial expression of their genes, which increases in stressed tissues (Ross et al., 2001). Thus, roots and seeds are the organs in which expression is more positively affected under stress conditions (Parent et al., 2008; 2011; Lira‐ Ruan et al., 2011; Thiel et al., 2011; Matilla and Rodríguez‐Gacio, 2013). Analysis of nsHbs2 expression

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(Fukao et al., 2006; Xu et al., 2006). Other plant species (Arabidopsis, Glycine max and Rumex palustris) have a higher susceptibility to flooding, but they also have some natural genetic factors responsible for tolerance (Vreeburg et al., 2005; Voesenek et al., 2006; Sayama et al., 2009; Chen et al., 2011; Vashisht et al., 2011). Progressive detoxification in seeds of generated O2 radicals and other toxins that develop in anoxic soils, also helps in preventing further injury (Ismail et al., 2012; Colmer et al., 2014; Kirk et al., 2014). Expansins and peroxidases, among other enzymes, play an important role in the CW loosening process under submergence (Figure 21.1) and specifically during coleoptile elongation (Huang et al., 2000; Magneschi and Perata, 2009; Miro and Ismail, 2013 and references therein). However, the main adjustment is determined by the change from the aerobic to the anaerobic metabolism (i.e. Pasteur Effect, use of PPi instead of ATP by certain enzymes as Nucleoside DiPhosphate Kinase; NDPK). NDPK is an enzyme associated with the elongation of the rice coleoptile under submergence (Huang et al., 2005a,b). The important role of the anaerobic Alcohol DeHydrogenase (ADH) enzyme must be also considered. Anaerobic respiration in rice submerged coleoptiles uses mainly the alcohol fermentative pathway to regenerate NAD+ for glycolysis involving Pyruvate DeCarboxylase (PDC), ADH1 and aldehyde dehydrogenase (ALDH) (Kato‐Noguchi, 2006; Kotchoni et al., 2010; Estioko et al., 2014) (Figure 21.1). Moreover, pH control at the cellular level is vital to survive under submergence (Magneschi and Perata, 2009). Thus, v acuolar pH increases in anoxia tolerant rice but not in sensitive wheat roots under submergence (Kulichikhin et al., 2009). The implications of pH regulation under flooding have been reported in various studies, showing that tolerant species are capable of controlling cytoplasmic and vacuolar pH, and can therefore survive longer periods of anoxia (Felle, 2005; Kulichikhin et al., 2009; Greenway et al., 2012).

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21.4.2 Involvement of non-symbiotic haemoglobins under O2-shortage

21.4.2.1 Current background Haemoglobins (Hbs) are globular proteins characterized mainly by: (i) high binding affinity for O2; (ii) affinity for other small gaseous molecules as nitric oxide (NO); (iii) reversible combination with O2 in the Fe++ state; (iv) conserved structure through evolution and (v) being

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21.4.2.2 The relationship between non-symbiotic haemoglobins and seed germination It is well known that NO is a by‐product of a mitochondrial pathway that consumes NO2‐ and produces ATP in hypoxic roots of rice and barley among other species (Stoimenova et al., 2007). In Arabidopsis, NO can be scavenged by nsHbs, and recently it has been demonstrated that the nsHbs/NO cycle participates in O2‐sensing (Igamberdiev et al., 2010; Siddiqui et al., 2010). Besides, it is well known that NO is capable of controlling cellular respiration, preventing anoxia (Borisjuk and Rolletschek, 2009). Likewise, it was demonstrated that: (i) during the onset imbibition of pea seeds a strong internal hypoxia provoked by an active mitochondrial respiration takes place; (ii) the O2 level is controlled by a NO2‐‐dependent NO production and (iii) this mechanism is strongly conserved and has an important role for seed O2‐homeostasis, acting as a negative feedback to prevent anoxia (Benamar et al., 2008). Recently, it was also proven that NO allows the seed to balance its O2 demand avoiding self‐hypoxia (Thiel et al., 2011). On the other hand, ROSs are released during seed hypoxia and ROS‐NO crosstalk plays a prominent role (revised in Matilla‐Vázquez and Matilla, 2012). The over‐expression of nsHbs1 gene in A. thaliana leads to the disappearance of NO production in fruits and an increase in nsHbs1 expression in seeds and fruits due to anoxia and it could be hypothesized that NO influences germination via N‐nitrosylation and that a cross‐talk NO/ nsHBs1 exists in some seeds (Sen, 2010). Under hypoxic conditions and/or when the mitochondrial activity is inhibited, the ATP levels drop and the expression of some nsHbs genes is induced (Borisjuk and Rolletschek, 2009). Interestingly, the nsHbs1 expression is not detected in dry viable seeds subjected to an anoxic atmosphere (Hebelstrup et al., 2007). That is, this gene is induced during hypoxia and its over‐expression permits to maintain high levels of cellular ATP (Dordas, 2009). These data suggest that, under anoxia, nsHbs1 act as part of a NO dioxygenase system, yielding NO3‐ from the reaction of oxyHb with NO and facilitating an alternative type of respiration to the mitochondrial

electron transport (Smagghe et al., 2009; Spyrakis et al., 2011). To fit the physiological nsHbs1 implications with germination several recent results must be taken into account: (i) the nsHbs1 isolated from Medicago sativa seeds was induced by anoxia (Hill, 2012); (ii) in Hordeum vulgare grains, the nsHbs1 transcripts are present at 2 h of imbibition (Hebelstrup et al., 2007) and the expression of nsHbs1 strongly increases in the embryo in an atmosphere of 3% O2 (Guy et al., 2002); (iii) silencing and knockout expression experiments in A. thaliana have demonstrated that at least one functional nsHbs gene is essential for the survival of germinating seeds (Hebelstrup et al., 2006) and (iv) the levels of nsHbs in transgenic maize can be positively correlated with the ATP levels under O2 shortage (Sowa et al., 1998); however, no nsHbs have been found during germination of teosinte seeds, suggesting that they are not needed for germination in this maize ancestor (Arechaga‐Ocampo et al., 2001). Taken together, these results indicate that the over‐expression of nsHbs1 in Arabidopsis allows the seed to respire more intensively, probably due to a decrease in the endogenous NO level, thus avoiding the seed self‐anoxia. Interestingly, nsHbs1 is positively regulated by RAP2.12 (see Section 2.1). Unfortunately, it has not yet been demonstrated the role of nsHb2s, if any, in the physiology of seeds, in spite of some recent promising results (Vigeolas et al., 2011).

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pattern shows the existence of high mRNA levels in flowers, developing seeds, developing leaves and vascular bundles, among others (Heckmann et al., 2006). However, tissue protein distribution of nsHbs2 has been poorly investigated.

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21.5 Hormonal influence in flooding stress Insufficient oxygenation in the root system under submergence is generated because the soil O2 is preferentially consumed by the aerobic bacteria of the rhizosphere (Jackson, 2006; Matilla‐Vázquez and Matilla, 2012; 2014). A decline from 19 to nearly zero kPa O2 in 30 h was observed in soil upon submergence in darkness (mimicking submergence in turbid water; Vashisht et al., 2011). Recently, studies with 86 Arabidopsis accessions submerged under dark conditions demonstrated that they differ strongly in their tolerance to submergence, this tolerance being negatively correlated with rosette growth. That is, lower growth rates improve survival (Vashisht et al., 2011). On the other hand, the O2 partial pressure in the water declines to almost 0% at a depth of 1.8 m and the diurnal pattern ceases (Setter et al., 1987; Vashisht et al., 2011). Roots demonstrate a diurnal

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s ubmergence (i.e. shoot elongation, aerenchyma formation and adventitious root growth; for a review see Bailey‐Serres and Voesenek, 2010; Steffens et al., 2011). ET accumulation occurs rapidly in submerged plant organs, sometimes preceding the onset of hypoxia. Thus, the intracellular ET level is around 1 µl‐1 within 60 min of flooding implying 20‐fold higher values than in non‐ submerged tissues (Banga et al., 1996). Several findings point to trapping as a controlling agent of the ET concentration in the submerged roots (Matilla‐Vázquez and Matilla, 2014 and references therein). The contribution of the covering root water (i.e. gas‐film) is not completely known and the root ET biosynthesis to gas entrapment. However, many experiments strongly support that ET action is involved in the elongation in species adopting the submergence escape strategy (Benschop et al., 2006; Vreeburg et al., 2005; Fukao et al., 2006). The flooding escape involves the ET biosynthesis and the stem elongation facilitating the absorption of atmospheric O2. On the other hand, the ET is also necessary for elongation of the plant organs that do not tolerate submergence (Smalle et al., 1997; Pierik et al., 2004). Quantitative trait locus (QTL) mapping revealed that both submergence tolerance and elongation growth in deepwater rice are controlled by five members of group VII ERFs family (Xu et al., 2006; Hattori et al., 2009; 2011). In the process of low‐O2 adaptation, dark‐ controlled carbohydrate consumption takes place, as well as, ethanolic fermentation metabolism (Magneschi and Perata, 2009) and a complex crosstalk between ABA, GAs and ET (Figure 21.1). In this crosstalk, the following four ERFs are involved: (i) The ET‐regulated SK1 and SK2. The absence of SK1 and SK2 in non‐deepwater rice varieties demonstrates its great relevance in submerged internode elongation. Besides, SK1 and SK2 interact via an unknown pathway with GAs and ABA. (ii) SLENDER RICE‐LIKE 1 (SLRL1) and SLENDER RICE 1 (SLR1) are negative regulators of GA responses (Fukao and Bailey‐Serres, 2008; Hattori et al., 2009; Mustroph et al., 2009; 2010). (iii) SUBMERGENCE1A (SUB1A) (induced by ET and submergence) expression is also correlated with carbohydrate consumption. SUB1A reduces the ET submergence‐induced synthesis, expression of CW loosening proteins (e.g. expansins) and starch and sucrose metabolism transcripts (Fukao et al., 2006; Xu et al., 2006; Jung et al., 2010; Pena‐Castro et al., 2011). Interestingly, SUB1A of rice is not an N‐end rule pathway substrate in vitro, despite the presence of

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pattern in O2 levels related to deepwater photosynthesis (Winkel et al., 2011). The O2 levels in roots decline towards the apex (Colmer, 2003b; Colmer and Greenway, 2005). However, water layers surrounding submerged shoots rarely become anoxic. Many species (e.g. deepwater rice) elongate their internodes to escape from a lack of O2, produced by submergence, by means of a process involving different hormones such ET, GAs and abscisic acid (ABA) (Figure 21.1). By contrast, plant species not adapted to waterlogging die. Waterlogging effects on N2 accumulation and fixation of supernodulating soybean mutants was demonstrated (Young et al., 2008). Recent research has focused on ET as a signal for the regulation of the early response to flooding (Peng et al., 2005). The elongation growth, ET‐mediated, is one of the main mechanisms that plants have to adjust and adapt to continually waterlogged environments and submergence (Kende et al., 1998; Van der Straeten et al., 2001; Vriezen et al., 2003; Voesenek et al., 2004; Benschop et al., 2006; Jackson, 2008; Dubois et al., 2011; Miro and Ismail, 2013). Together, plants appear to have adapted to the limited gas diffusion in an aqueous medium by using ET as an indicator for submergence conditions and as a signal that promotes morphological, anatomical and metabolic changes to ameliorate the stress by a limited O2 supply.

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21.5.1 Ethylene, the main tool to respond to flooding

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ET is an alkene with moderate water solubility that diffuses approximately 104 times more slowly in water than it does in air. This gas is synthesized by almost all plant species (Yoo et al., 2009; Li et al., 2012; Wen, 2015); Potamogeton pectinatus being an exception (Summers et al., 1996). ET cell concentration is mainly determined by the production rate and diffusion towards the atmosphere. However, the process of ET diffusion is severely hindered as soon as the plant organs (e.g. radical system) are surrounded by water (Vandenbussche et al., 2012). That is, the ET levels increase rapidly in submerged plants due to its physical entrapment in the intercellular gas spaces (Musgrave et al., 1972; Métraux and Kende, 1983; Voesenek et al., 2006) and is used by some plants (i.e. rice) to adapt to flooding. Thus, Jackson (2008) proposes a model for ET‐promoted shoot elongation in submerged Rumex palustris. Namely, entrapped ET is sufficient to trigger a fast upward growth and regulate several morphological adaptation responses to flooding and

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ET biosynthesis (increase of OsACS5 expression)

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Increase of GA1 level involving the OsGA20ox1,2 and OsGA3ox2 gene expression

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Figure 21.3 Explanation of the submergence induced elongation

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the required Cys‐2 N‐terminus (Gibbs et al., 2011). Likewise, to economize the carbohydrate reserves under stress, rice plants with SUB1A can reinitiate formation of new leaves and resume vegetative growth upon de‐ submergence (Fukao et al., 2006; Fukao and Bailey‐ Serres, 2008; Fukao et al., 2012) and (iv) other ERFs that provoke prolonged tolerance to submergence (SUB1A‐1 perhaps; Gibbs et al., 2011; Bailey‐Serres and Voesenek, 2010; Nishiuchi et al., 2012; Voesenek and Bailey‐Serres, 2013; Matilla‐Vázquez and Matilla 2014). The five members of group VII ERFs in Arabidopsis (see Section 2.1) are regulated by hypoxia, ET and carbohydrate deprivation darkness‐induced and different responses between roots and shoots were observed (Hinz et al., 2010; Licausi et al., 2010). Shoot and root transcriptomic analyses in plants with O2‐deprived roots, provides evidence of between‐organ communication that assists in the mobilization of shoot carbon to the root system, to facilitate survival. Thus, evaluation of the transcriptomic response of the ET insensitive ein2‐5 mutant reveals a role for ET in this root to shoot systemic signalling (Hsu et al., 2011). Recently, Dubois et al. (2011) from studies with tall lowland rice cv. Bomba concluded that: (i) the effect of submergence was almost absolutely deleted by 1‐methylcyclopropene (1‐MCP; inhibitor of ET action); (ii) the exogenous 1‐aminocyclopropane‐1‐carboxylic acid (ACC) added to non‐submerged seedlings induced sheath elongation to a value similar to that obtained by submergence. But the addition of ACC to submerged seedlings did not generate further elongation; (iii) the ET diffusion doubled upon submergence; (iv) presumably, ET is de novo biosynthesized through induction of ACC‐synthase (OsACS5; short submergence) and OsACS1 gene expression (long‐term submergence) and (v) an increase in the ACC‐oxidase (ACO) genes expression does not seem to be involved. Interestingly, elongation under submergence is not mediated by ET but it is only GAs‐mediated in rice cv. Senia (Dubois et al., 2011) (Figure 21.3). Taking these data together indicates that the presence or absence of ET‐mediated escape delimitates closely related species that can cope or not with submergence stress (Jackson, 2008). Accordingly, ET biosynthesis genes are upregulated under low‐O2 conditions and ET triggers flood‐adaptive signalling in submerged plants except under conditions in which the O2 levels are completely depleted (i.e. true anoxia). It is interesting to note that the submergence‐induced

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in two lowland rice cultivars [i.e. Bomba (tall) and Senia (short)]. In both cultivars, elongation is the result of an increase of active GAs (i.e. GA1) biosynthesis due to enhanced expression of OsGA20ox1, OsGA20ox2 and OsGA3ox2 genes. In Bomba, the induced‐elongation is related to increase of ET biosynthesis due to upregulation of OsACS5 gene expression. However, in Senia cultivar, submergence‐induced elongation does not depend on ET, and the GA‐mediated response is triggered by a still unknown mechanism, probably involving increase of acidity and/or hypoxia. Adapted from Dubois et al. (2011).

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response in Potamogeton pectinatus is not ET‐dependent since it is conducted by the increase in acidity produced by CO2 accumulation (Summers and Jackson, 1996; Voesenek et al., 2004). ET alone cannot induce the expression of the ADH1 gene, a well‐characterized low‐O2 responsive gene (Peng et al., 2001; 2005). That is, ADH1 expression is affected by ET signalling only when hypoxic conditions are present at the same time. Thus, treatments with ET and ACC increased Arabidopsis ADH1 transcript abundance in shoots, while the inhibitors of ET synthesis or signalling, reduced ADH1 expression. ADH1 and RAP2 (belonging to subgroup VII of the AP2/ERF‐TF family, which constitutes 121 members in Arabidopsis; Nakano et al., 2006) are related. Likewise, the Arabidopsis RAP2.2 gene, which is upregulated by ET, shows structural and phylogenetic relationships with the rice SUB1A gene. As for SK1 and SK2, SUB1A‐1 expression is

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and Matilla, 2012; Yamauchi et al., 2011; 2013; Zhu et al., 2013). Although the ET signalling involvement in PCD is scarcely known, H2O2, metallothionein (MT) gene expression and ROS appear to be implicated in the lysis of cortical root cells (Bouranis et al., 2003; Yakimova et al., 2006; Steffens and Sauter, 2009; Steffens et al., 2011; Yamauchi et al., 2013). Thus, ET‐triggered ROS formation promotes the adventitious root growth that provides a spatial signal for the epidermis that enables the PCD necessary for emergence (Voesenek and Bailey‐ Serres, 2013).

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Some old data suggest that GAs are the main hormonal signals for fast flooding elongation (Kende et al., 1998). However, GAs response is slower than that of ET. Thus, short lowland rice cultivars growing under submergence displayed leaves with greater elongation and this process is GA1‐dependent (Dubois et al., 2011). In addition, the OsGA20ox1, OsGA20ox2 and OsGA3ox2 expression are also involved in this rice vegetative development (Oikawa et al., 2004; Dubois et al., 2011). In short, the GAs are considered essential components of a signalling complex chain that is started by entrapped and/or enhanced ET synthesis but they are required for a sustained effectiveness (Vreeburg et al., 2005; Benschop et al., 2006; Jackson, 2008) (Figure 21.1). The following evidence supports it: (i) the inhibition of GAs biosynthesis does not enhance stimulation of elongation under flooding; (ii) the action of GAs does not generate ET biosynthesis; (iii) it is probably that ET serves to sensitize the petiole or internode towards GAs; (iv) GAs‐ dependent processes do not seem to influence the CW apoplastic enzymatic activity; (v) GA1 (the active GA in rice) increases four times in internodes of deep‐water rice during the first 3 h of submergence and (vi) an elevated active GAs synthesis promotes the petiole extension in A. thaliana. For a more detailed view see the following references (Rijnders et al., 1997; Hisamatsu et al., 2005; Benschop et al., 2006; Jackson, 2008). However, the involvement of ET and/or submergence on the expression of certain genes (e.g. expansins, cyclin‐dependent protein kinases, etc.) in deep‐water rice internodes has not been demonstrated and it is only inferred from GA’s positive effects (Fabian et al., 2000; Van Der Knaap et al., 2000; Lee and Kende, 2001; Vreeburg et al., 2005). In the quiescence strategy, growth inhibition by SUB1A‐1 occurs through inhibition of GA

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activated by the accumulated ET in submerged tissue (Nakano et al., 2006). Moreover, ET and RAP2.2, together with O2‐dependent signal transduction, play an important role in the response to hypoxia. RAP2.12, was shown to regulate ADH1 expression through the binding to a cis‐acting ATCTA element of the ADH1 promoter (Papdi et al., 2008). The ATCTA motif was thus proposed as a hypoxia responsive element (Licausi et al., 2011). In relation to this, Hinz et al. (2010) found that: (i) ADH1 is under dual control by low‐O2 signalling and ET signalling; (ii) the overexpression of RAP2.2 result in higher ADH and pyruvate decarboxylase (PDC) activities, indicating that the improved hypoxia survival of plants overexpressing RAP2.2 is in part via enhancement of fermentation and (iii) RAP2.2 mediates ET signalling of ADH1 induction in Arabidopsis shoots. ET is also involved in lysigenous aerenchyma formation through a complex signalling network that induces the activation of some CW degradation enzymes such as cellulases, pectinases, xylanases and xyloglucan endotransglycosylases (Gunawardena et al., 2001; Evans, 2003; Subbaiah and Sachs, 2003). So, the appearance of lysigenous aerenchyma under submergence is an ET‐regulated trait in roots (Watkin et al., 1998; Drew et al., 2000; Gunawardena et al., 2001; Yamauchi et al., 2013), adventitious roots (Steffens and Sauter, 2009; Dawood et al., 2013) and internodes (Hattori et al., 2009; Steffens et al., 2011). Adventitious roots functionally replace primary root systems that may be deteriorated during flooding due to O2 deficiency (Sauter, 2013). However, direct demonstration of adventitious roots effectiveness is still lacking. The apical meristem in adventitious root primordia is activated by flooding. Just before roots emerge, the epidermal cell layers at the primordia apex undergo PCD, which appears to be a necessary process to facilitate protrusion of the roots to the outside (Steffens and Sauter, 2009; Steffens et al., 2012; Dawood et al., 2013). Together, an actual summary on ET involvement in lysigenous aerenchyma formation can be the following: waterlogged soil conditions (i.e. hypoxia) triggers the O2 sensing inside the root and ET is accumulated due to an increase of both ACC synthase (ACS) and ACC oxidase (ACO) activities (Matilla‐Vázquez and Matilla, 2014 and references therein). After ET accumulation, the induction of expression of RBOH (Respiratory Burst Oxidase Homolog) gene follows, as does apoplastic O2‑accumulation and H2O2 production (Matilla‐Vázquez

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about ROS homeostasis in Steffens et al., 2013). In some wetland species, SOD and CAT activities are differentially regulated during flooding depending on the survival strategy (Luo et al., 2012; Bailey‐Serres and Colmer, 2014). Plant hormones produce reactive oxygen species (ROS) as second messengers in signalling cascades that convey information concerning changes in hormone concentrations and/or sensitivity to mediate a whole range of adaptive responses (Bartoli et al., 2012). For example, brassinosteroids can induce plant tolerance to diverse abiotic stresses by triggering H2O2 generation in cucumber leaves (Cui et al., 2011). It is well established that oxidative metabolism, and particularly H2O2, is involved in a wide variety of reactions and signalling cascades necessary for all aspects of plant growth and development. Thus, while the involvement of H2O2 in stress responses is of particular interest, its involvement in normal growth and metabolism must be also considered (Foyer and Noctor, 2012; Matilla and Matilla‐Vázquez, 2012 and references therein). H2O2 can cross membranes by diffusion and it can also be transported by specific aquaporins (Muto et al., 2011; Borisova et al., 2012). Interestingly, the process of stomata closure regulated by ABA in a large sense require the generation of H2O2. Moreover, H2O2 production may be a prerequisite for ABA induced stomatal closure (Zhang et al., 2001). Mutations in genes encoding catalytic subunits of NADPH oxidase will impair ABA‐induced ROS production, as well as the activation of guard cell Ca2+ channels and stomata closure (Kwak et al., 2003). Recently, it was demonstrated that the Arabidopsis calcium‐sensing receptor (CAS) is a crucial regulator of extracellular calcium‐induced stomatal closure. Thus, it has been hypothesized that the extracellular Ca2+ induces H2O2 and NO accumulation in guard cells through the CAS signalling pathway, which further triggers intracellular Ca2+ transients and finally stomatal closure (Wang et al., 2012). On the other hand, the production of H2O2 was also demonstrated when O2 availability is limited because of soil flooding (hypoxia signalling) and it has been suggested that H2O2 acts as a signal component that triggers downstream responses in hypoxia signalling (Pucciariello et al., 2012b). Recent data showed that H2O2 and ET signalling are necessary, but not sufficient, for the control of downstream gene transcription during hypoxic stress (Yang, 2014a,b). Taken together with the available data, we can conclude that regulation of ROS

21.6 ROS involvement under flooding stress

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It has been demonstrated that about 1% of metabolically consumed O2 by aerobic cells goes into ROS generation (Puntarulo et al., 1988). ROS are species of O2 with high reactivity and toxicity resulting from excitation or incomplete reduction of molecular O2. Usually, ROS contains both free radical (O2•−, RO•, HO2•, OH•) and non‐radical forms (H2O2, 1O2). Chloroplasts and mitochondria are the main ROS producers in photo synthetic and non‐photosynthetic tissues, respectively (Shapiguzov et al., 2012 and references therein). Accordingly, networks of ROS/redox signalling in both cell energetic compartments play essential roles in the acclimation of plants to abiotic stresses (Zuzuki et al., 2012 and references therein). Therefore, imbalanced ROS production is highly destructive to lipids, nucleic acids and proteins (Steffens et al., 2013). However, ROS can also affect to gene expression and signalling pathways so activating and regulating several stress‐response processes (Foyer and Noctor, 2009). Thus, ROS have been reported to trigger signalling pathways that interact among others with signalling pathways mediated by NO, lipid messengers and plant hormones. NADPH oxidases (RBOH gene family) are an important ROS‐ generating system at the plasma membrane (Steffens et al., 2012; Matilla and Matilla‐Vázquez, 2012 and references therein). RbohD, one of the 10 RBOH genes of Arabidopsis, is induced at low partial pressure of O2 (Pucciariello et al., 2012a). Superoxide dismutase (SOD) determines the rate of H2O2 production and catalase (CAT) the rate of H2O2 metabolism (see Figure 21.1

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signalling (Fukao et al., 2006). On the other hand, SUB1B and SUB1C genes are present in all indica and japonica varieties tested to date, but SUB1A is limited to a subset of indica varieties (Xu et al., 2006; Singh et al., 2009; 2011). However, their function in the response to submergence is unknown, although Fukao et al. (2006) proposed that SUB1A acts upstream of SUB1C, a GA‐ responsive gene. As stated previously, SK1 and SK2 are included into the ‘escape strategy’ and are upregulated by the submergence‐induced accumulation of ET in internodes, consistent with the essential role of ET in GA‑stimulated underwater shoot elongation (Jackson, 2008; Hattori et al., 2009).

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levels in flooded plants relies on the regulation of ROS producing and ROS scavenging mechanisms. However, it seems clear that ROS abundance is regulated at different levels in different plant species.

well‐known conditions. Therefore, it is of great importance that the effectiveness of flooding tolerance be carried out under authentic field conditions.

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References

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Abiko T, Kotula L, Shiono K, Malik AI, Colmer TD, Nakazono M (2012) Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant Cell Environ 35: 1618–1630. Angaji S, Septiningsih EM, Mackill DJ, Ismail AM (2010) QTLs associated with tolerance of anaerobic conditions during germination in rice (Oryza sativa L.). Euphytica 172: 159–168. Arechaga‐Ocampo E, Saenz‐Rivera J, Sarath G, Klucas RV, Arredondo‐Peter R (2001) Cloning and expression analysis of hemoglobin genes from maize (Zea mays ssp. mays) and teosinte (Zea mays ssp. parviglumis). Biochem Biophys Acta 1552: 1–8. Armstrong J, Armstrong W (2005) Rice: sulphide induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96: 625–638. Bailey‐Serres J, Chang R (2005) Sensing and signalling in response to oxygen deprivation in plants and other organisms. Ann Bot 96: 507–518. Bailey‐Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59: 313–339. Bailey‐Serres J, Voesenek LACJ (2010) Life in the balance: a signaling network controlling survival of flooding. Curr Opin Plant Biol 13: 489–494. Bailey‐Serres J, Fukao T, Gibbs DJ, Holdworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17: 129–138. Bailey‐Serres J, Colmer TD (2014) Plant tolerance of flooding stress – recent advances. Plant Cell Environ doi: 10.1111/ pce.12420. Baltazar MD, Ignacio JCI, Thomson MJ, Ismail AM, Mendioro MS, Septiningsih EM (2014) QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica 197: 251–260. Banga M, Slaa EJ, Blom CWPM, Voesenek LACJ (1996) Ethylene biosynthesis and accumulation under drained and

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Adequate supply of O2 is not always ensured during plant life cycle (Bailey‐Serres et al., 2012). As sessile organisms, plants are constantly adapting to environmental conditions (Voesenek and Bailey‐Serres, 2013). These adaptations are complex and highly sophisticated in the case of severe environmental conditions (i.e. abiotic stress such as flooding) (Licausi et al., 2011). Therefore, it is a great challenge for the research in plant physiology to obtain sufficient knowledge about mechanisms that operate in the flood tolerance. That is, an important scientific challenge is to get sophisticated information under flooded conditions on: (i) the cross‐ talk between ET, ABA and GAs, hormones known to be more related to adaptation to flooding; (ii) the hormonal control of barriers formation to prevent radial O2 loss; (iii) the molecular control of O2 and sugars availability; (iv) the mechanism involved in the O2 sensitiveness (i.e. N‐end rule pathway and NO/nsHbs cycle); (v) the regulation of the hypoxia‐involved key genes shown in Figure 21.1; (vi) the signalling integration to lead to a dynamic network that facilitate survival under flooding‐ stress and (vii) the use of all of this knowledge for the modern agriculture in order to obtain goods and services. That is, the study of genes that can be genetically engineered is the basis to achieve stress‐tolerant transgenic plants. The exact and detailed role of ET in metabolic adjustments during flooded conditions is still under study. Good progress was made in developing breeding lines that are more suitable for direct‐seeded systems. Major QTLs associated with flooding tolerance during germination have been lately identified and are being used for cloning and in marker‐assisted breeding (Angaji et al., 2010; Septiningsih et al., 2013; Baltazar et al., 2014). Satisfactorily, notable progress about flooding‐tolerance was made in this century (Mustroph et al., 2009; 2010; Dubois et al., 2011; Tasaki et al., 2012; Estioko et al., 2013; Miro and Ismail, 2013; Zhu et al., 2013; Colmer et al., 2014; Gibbs et al., 2014; Kirk et al., 2014). Finally, the majority or almost all the data obtained up to now were conducted under controlled or

I am grateful to Dr Voesenek for sending the original publications. We thank Professor Pilar Carbonero for the critical review.

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Acknowledgements

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