Flooding Tolerance in Rice: Focus on Mechanisms and Approaches[w1]

Debabrata Panda, Jijnasa Barik

Review

[w1]

Debabrata Panda, Jijnasa Barik

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Flooding is one of the most hazardous natural disasters and a major stress constraint to rice production throughout the world, which results in huge economic loss. Approximately one-fourth of the global rice crops (approximately 40 million hectares) are grown in rainfed lowland plots that are prone to seasonal flooding. A great progress has been made during last two decades in our understanding of the mechanisms involved in adaptation and tolerance to flooding/submergence in rice. In this review, we summarized the physiological and molecular mechanisms that contribute to tolerance of flooding/submergence in rice. We also covered various features of flooding stress with special reference to rice plants,. different types of flooding stress, environmental characterisation of flood water, impact of flooding stress on rice plant and their morphological, physiological and metabolic responses under flooding. A brief discussion on the tolerance mechanism in rice exhibited to different types of flooding will be focused for the future crop improvement programme for development of flooding tolerant rice variety.

flooding stress; submergence tolerance;; rice

Rice (L.) is consumed as the primary source of food in the globe, which provides food and livelihood security to half (about 3.5 billion) of the world population (Samal et al, 2018). It is a semi- aquatic species, cultivated under different climatic conditions, which are subjected to diverse biotic and abiotic stresses. Among different abiotic stresses, flooding is one of the major constraints for rice production particularly in rainfed lowland areas, which threatens global food security (Dar et al, 2017). This is becoming a more serious issue concerning the global climate change as the improved rice varieties are susceptible to flooding (Afrin et al, 2018). A total of 22 million hectares of world’s rice fields are unfavourably submerged annually,which affects the livelihood of more than 100 million people (Singh et al, 2016). The population of world is alarmingly increasing and likely to reach 9 billion by the year 2050 (Lee et al, 2014). Therefore, the present situation demands to increase in food production to overcome food shortage problem in near future (Wang et al, 2016). Due to heterogeneity of flood prone ecosystem in tropical Asian countries like India, few indigenous rice landraces are still maintained and cultivated by poor farmers (Ram et al, 2002; Barik et al, 2020). Although such farming has poor yield capacity, this local landrace has excellent adaptation to extreme water availability, tolerant to different kinds of flooding and very important for QTL mapping and gene discovery (Singh et al, 2017). Therefore, identification of new tolerant rice genotypes having better performance than ‘FR13A’ (flooding tolerant genotype) is agronomically more desirable (Sarkar et al, 2006). This needs exploration of genetic diversity in the rice landraces for identification of new genes and further improvement of germplasm (Ahmed et al, 2016). Therefore, the present review reported the effects of flooding and highlighted the recent development of morphological, physio-biochemical and genetic basis of flooding tolerance in rice.

Flooding stress and flooding affected area[w2]

Although rice plants require large amount of water during growth, flooding stress results in severe loss of the crop as a consequence of anaerobic environment. The crop loss would be more severe on account of unpredictable changes in climatic conditions causing floods (Vergara et al, 2014). The extensive rice growing areas in South and South-East Asia especially India, Bangladesh, Thailand, Vietnam, Myanmar and Indonesia are exposed to flash flooding during monsoon season (Sarkar et al, 2006). Nearly 22 million hectares of rainfed lowland areas of South and South-East Asia get affected due to flooding, out of which about 6.2 million hectares of rice lands are in India (Azarin et al, 2017; Dar et al, 2017). Out of 22 million hectares, 15 million hectares of rainfed lowland are affected only due to short term flash flooding (Singh et al, 2017), and economic loss is estimated to be 1 billion US dollar (Mackill et al, 2012). The flood prone ecosystem comprises about 7% of global rice area and produces 4% of world rice (Yang et al, 2017).

Types of flooding stress

Flooding during germination

Soil water logging normally takes place in case of rainfall after sowing of seeds and particularly where the lands are not properly levelled. The germination during flooding is commonly referred as ‘ANAEROBIC GERMINATION’ (AG), and the seeds have the potential to germinate even under the conditions where no air or oxygen is available. However, slow seed germination, uneven and delayed seedling establishment and high weed infestation are some of the constraints that restrict rice large adaptation of direct seeding in flood prone areas (Ismail et al, 2009, 2012). Almost all varieties of rice are keenly susceptible to flooding and get easily affected or damaged at the time of germination (Yamauchi et al, 1993; Ismail et al, 2009; Angaji et al, 2010; Miro and Ismail, 2013; Lee et al, 2014; Singh et al, 2017). AG is a complex trait governed by various gene families which are linked to many important processes like starch breakdown, glycolysis, fermentation as well as other biochemical and metabolic processes (Ismail et al, 2009, 2012). Hence, AG is thus necessary for homogeneous germination and better crop establishment under flooding condition (Ismail et al, 2009; Magneschi and Perata, 2009; Septiningsih et al, 2013).

Flash flooding

Flash flooding can occur due to heavy rains or overflowing of rivers and streams for a short duration of 1–2 weeks and result in complete submergence of plants (Vergara et al, 2014). Lands in low-lying land areas and near the streams and rivers are generally affected by such flash flooding. Depending on climatic conditions, flash flooding can occur repeatedly in a growing season, damaging the rice cultivation. The flooding depth is not very deep in the flash floodingcondition. Flooding tolerance was defined as ‘the ability of some rice varieties to survive 10–14 d of complete flooding and renew its growth when the flood water subsides’ by Catling (1992).

Stagnant flooding

In stagnant flooding, water depth ranges from 25 to 50 cm, and some parts of the shoot is normally seen over the flood water. Rice production in such cases depends upon the extent of submergence and may vary from 0.5 to 1.5 t/hm2(Kuanar et al, 2017). In this condition, the extended water stagnation remains from a few weeks to several months. This is commonly seen in areaswhere there is no proper drainage system, particularly near the water channels leading to rivers during the monsoon time, due to over flow of excessive rain water. In West Bengal of India, 577 genotypes were studied under stagnant flooding conditions, where genotypic differences between survival and grain yield were observed, but the flooding tolerant cultivars (FR13A and FR43B) were not found to perform well under the aforesaid condition. This suggests that the flash flooding tolerant genotypes may not be the right solution for stagnant flooding (Vergara et al, 2014).

Deep-water flooding

In deep-water flooding, water stagnation continues to remain for a longer time. At times, the water level may rise up to 4 m height(Singh et al, 2017). The flooding stress depending upon the topography and climatic conditions may continue for months together. Adapted rice plants in this type accelerate their growth in commensurate with the increase of flood water level, so as to avoid complete submergence. In deep- water flooding, a portion of plants successfully remains above the water level. The deep-water rice escapes complete flooding by fast internodal elongation growth,which consumes high amount of carbohydrate. Growth is achieved by about 25 cm per day as flood water level increases (Singh et al, 2017) and can reach a height of 5 m with its panicle and top leaves under these circumstances (Jackson and Ram, 2003). Most of the deep-water rice growing areas in India are normally found in several parts of Assam, Bihar, Orissa, West Bengal and Uttar Pradesh (Bin Rahman and Zhang, 2016).

Environmental parameters associated with flooding stress

Flooding causes many complex abiotic stresses (Jackson and Ram, 2003; Sarkar et al, 2006; Bailey-Serres et al, 2010), and the amount of harm that may be caused to the inundated plants varies depending on flood water characteristics like temperature, turbidity, water depth, oxygen, carbon dioxide concentration andlight intensity (Das et al, 2009). These affect importantplant processes like chlorophyll retention, photosynthesis under water, accumulation of carbohydrate, elongation and survival (Das et al, 2009).

Gas diffusion

Gas diffusion under flooding has a key role for plant’s survival since diffusion of oxygen under water takes place slowly compared to open air (approximately 104folds) (Panda et al, 2008). Thus, the oxygen depletion creates hypoxia (low oxygen) and anoxia (no oxygen) around plant tissues during flooding (Ito et al, 1999; Damanik et al, 2012). This reduces the supplies of carbon dioxide (CO2) and oxygen (O2) to the plants. Such reduced supplies of O2and CO2limit respiration and photosynthesis, respectively. Further endogenous concentration of volatile hormone ethylene depends strongly upon its outward diffusion, which is also severely impeded under water. As a result, ethylene is increased in submerged plant tissues. Thus, the reduceddiffusion of ethylene away from plants triggers chlorosisand excessive elongation of leaves in intolerant cultivars (Sarkar et al, 2006).

Light intensity

Poor light transmission under flood water is an important limiting factor. Under these conditions, light reaching the leaves of the flooded plant is impaired by phytoplanktons, water, silt as well as dissolved organic matter suspended in the flood water (Das et al, 2009). Due to this, only a limited amount of sun light reaches leaves and thus decreases the potentiality of plants to photosynthesis (Sarkar et al, 2006). Light intensity is also very important for maintaining O2and CO2concentrations, and therefore greatly affects the physiological status of rice plants under water. Light limitation has been shown to cause severe injuries and accelerate plant mortality (Jackson and Ram, 2003).

Temperature

Temperature is another important factor which plays a vital role in rice plant’s survival under flooding. The low temperatures (20oC) improve plant survival whereas the high temperature (30oC) increases plant mortality. The solubility of O2and CO2in flood water decreases at high temperatures. High temperatures speed up anaerobic respiration, resulting starvation and death of the plants in a short duration (Ram et al, 2002).

pH

Plant survival is also greatly affected by pH values during flooding. Lower flood water pH or enhanced CO2concentration increases photosynthesis during flooding (Sarkar et al, 2006). Although this idea is not practical, it indicates that the tolerant germplasms need to be specific to the location to meet the local variations of the flood water condition (Sarkar et al, 2006).

Toxic substances

Soil oxygen deficiency has indirect effects on plants by promoting the growth of anaerobic bacteria. Some anaerobes reduce ferric ion (Fe3+) to ferrous ion (Fe2+),and due to greater solubility of Fe2+, Fe2+concentrationscan rise to toxic level. Other anaerobic microorganisms may reduce sulfate (SO42-) to hydrogen sulphide (H2S), which is a respiratory poison. These toxic substances cause severe damage to plants by reducing the redox potential under flooding conditions and increase the susceptibility to diseases (Ram et al, 2002). Also, the acetic acids as well as butyric acids released by anaerobic microorganisms are toxic to plants at high concentrations.

Effects of flooding on morphology of rice plants

Leaf traits

Flooding hinders formation of new leaf, and reducestotal leaf area and promotes leaf senescence (Kato et al, 2014). Singh et al (2014) observed that in susceptible varieties, the dry weight of leaf is reduced sharply to the extent of 70%, when it is only 30%–40% in tolerant varieties under 17 d of flooding stress. They found a strong relationship between the dry weight of leaf after flooding and the plant survival in critical flooding conditions. It is noticed that there was no perceptible reduction of leaf area index in tolerant varieties after water recedes, suggesting their stronger ability to recover original leaf area index after flash flooding (Singh et al, 2014).

Plant height

Plant height is a key parameter which influences plant productivity as well as its survival under flooding stress. Most of rice genotypes elongate their shoots under complete flooding (Fig. 1). Flash flooding tolerant varieties reduce shoot growth while remaining in flood, conserving their energy which is used for survival soon after recession flood water (Jackson and Ram, 2003; Bailey-Serres et al, 2010; Goswami et al, 2017; Bui et al, 2019). Particularly-incorporated varieties show lower elongation of shoot in comparison to other varieties (Sarkar and Bhattacharjee, 2011). A study on 903 cultivars from International Rice Research Institute Genebank collections confirmed the negative relationship of shoot elongation and flash flooding tolerance (Setter and Laureles, 1996). Kawano et al (2002) observed that shoot elongation during flooding utilises energy from stored carbohydrate. Singh et al (2014) observed that shoot elongation increases proportionately with flooding, and-introgressed genotypes show slower shoot elongation rates compared to intolerant genotypes. Thus, rice varieties having slower elongation growth under water are preferred for cultivation in the areas affected with flash flooding, and the genotypes having faster elongation capacity are considered appropriate for deep water as well as partially deep-water areas (Sarkar and Bhattacharjee, 2011; Vergara et al, 2014).

Root trait

Root health is vital for survival during flooding and recovery. The roots of sensitive species suffer oxygen deficiency in anoxic soils,which reduce respiration and result in drastic energy crisis, whereas the tolerant species can thrive (Bailey-Serres and Voesnek, 2008). The concentration of potentially toxic compounds also increases in the anaerobic soils, which can enter through roots, damaging both shoot and root tissues. The morphological and anatomical traits of roots determine the root growth and functioning in anoxic soils (Yamauchi et al, 2018). Long term retention of leaf gas films during flooding will likely to improve the supply of carbohydrates for growth and adventitious root regeneration as well as enhance root and rhizosphere aeration. Root porosity is also important for root growth under anoxic soils, which is determined by the extent and rate of aerenchyma formation and to minimize resistance to O2movement down the root. The aeration of root will be improved significantly by induction of barriers to radial oxygen loss, which reduces oxygen loss, promotes aeration to active root tips, and impedes the movement of toxin and gases in anoxic soils (Yamauchi et al, 2018). The root elongation was found to be minimal in all the rice genotypes under flooding when compared with control condition. The positive correlation between survival and root growth is an indication of the capability ofintrogressed varieties to supply the required carbohydrates needed for proper growth of its roots (Singh et al, 2014). Bui et al (2019) highlighted the importance ofQTL in regulation of root physiology of rice under flooding conditions and indicated that the tolerant varieties show higher root activities like root tip viability and root peroxidase, which result in minimum damage in the roots as well as shoots under flooding.

Fig. 1. Morphological, physiological, biochemical and molecular responses of rice plants under flooding stress (Mackill et al, 2012; Upadhyay, 2018).

Biomass

Flooding severely restricts O2and CO2gas exchange between rice tissues and atmosphere, inhibits aerobic respiration as well as photosynthesis, and accelerates the consumption of energy reserves, leading to stunted growth and death (Kato et al, 2014). Flooding inhibits dry matter accumulation in susceptible genotypes (Singh et al, 2014). Reduction in growth is a common phenomenon when plants are flooded with water. However, tolerant rice genotypes have the potentiality to store sufficient amount of dry matter.

Aerenchyma formation and leaf gas film

The major adaptive features of rice to water logging are the formation of aerenchyma. This aerenchyma constitutes the gas spaces and gets interconnected, which becomes the channel for continuous aeration between roots and shoots. In rice, aerenchyma is well developed in leaves, sheaths, roots and internodes (Steffens et al, 2011; Pradhan et al, 2017). Generally, the formation of aerenchyma and its induction occurs within 1–3 dof the anoxic treatment (Pradhan et al, 2017).

In flood water conditions, the presence of leaf gas films enhances the internal aeration and makes the rice tolerant to flood (Pedersen et al, 2009). The leaf gas film facilitates the O2entryfrom surrounding water when in the dark, and the CO2entry in the light for photosynthesis. The role of gas films for flooding tolerance has been confirmed through several studies by artificially induced variation or loss of function mutants (Pedersen et al, 2009). Kurokawa et al (2018) reported the ‘’ () enhances flooding tolerance in rice.

Survival

The extent of visible injury caused by flooding stress is generally used as an indicator of sensitivity of plants to flooding. However, 100% survival is identified in tolerant cultivar FR13A after remaining in flood water for 8 d while only less than 15% in sensitive cultivar (Panda and Sarkar, 2013). In a study among sevenrice cultivars, after 4 d of flooding treatment, the survival rate is more than 80% in tolerant genotypes but only 22% in susceptible ones (Panda et al, 2006). Survival after flooding seems to be associated with the amount of non-structural carbohydrates remaining in the shoots after flooding (Pradhan et al, 2017).

Effects of flooding on physiology of rice plants

Photosynthetic gas exchange

One of the crucial processes for plant growth is ‘Photosynthesis’. By this process, solar energy used by green plants is converted into organic compound releasing oxygen molecule. The adverse impact of flooding on rice is mainly linked to water poor gas exchange through impeding photosynthesis (Colmer and Voesenek, 2009). Inundation of aerial organs under complete flooding drastically reduces gas diffusion rates, restricts uptake of oxygen, thus weakens photosynthesis as well as transpiration and thereby the carbohydrate reserves in the plant get exhausted, resulting in its death (Das et al, 2009). Further turbid flood water can almost completely block light accessibility and slow down photosynthesis (Yang et al, 2017). Factors like chlorophyll degradation, stomatal closure, lipid peroxidationand less intracellular carbon dioxide concentration also cause concomitant reduction in photosynthesis (Panda et al, 2008). Senescence and plant death occur due to decline in CO2concentration and enhancement of leafreactive oxygen species(ROS) level because of continuing of the light reaction. Panda and Sarkar (2013) observed that flooding significantly inhibits the photosynthetic rate along with stomatal conductance and rubisco activity. The maximum reduction (95%) in photosynthetic rate was found in the sensitive genotype IR42, and the least reduction (74.8%) was found in the tolerant genotype FR13A, when compared with non-submerged control plants after 8 d of complete flooding (Panda et al, 2008). The maintenance of higher photosynthetic activity in tolerant cultivars may be due to protection of photosynthetic apparatus, higher amount of chlorophyll and better stomatal conductance during and after flooding compared to susceptible variety IR42 and elongating variety Sabita (Panda and Sarkar, 2013).

Leaf photochemical activity

Photosystem II (PSII) is susceptible to various abiotic stresses. When rice plants were completely submerged,chloroplasts were disintegrated and leaf photosynthetic capacity was decreased (Panda et al, 2008).chlorophyll fluorescence is used as a matter of convenience and non-destructive tool to ascertain the tolerance behaviour of different kinds of species under different environments including flooding conditions (Panda et al, 2006; Panda and Sarkar, 2011, 2012). Changes in chlorophyll fluorescence emissions, mostlyfrom PSII, give all the information about photosynthetic activity (Panda et al, 2008). Flooding affected the photosynthetic apparatus which is evident from the reduced values of chlorophyll fluorescence such as0,mand ratio of variable fluorescence to maximum fluorescence (v/m) in both tolerant and intolerant genotypes (Panda et al, 2006, 2008). A comparison between chlorophyll fluorescence parameters and chlorophyll contents indicates that the chlorophyll fluorescence parameters are more sensitive to submergence (Panda et al, 2006; Sarkar et al, 2006). Thus, various important parameters can be quantified by the measurement of chlorophyll fluorescence for identifying the tolerant and intolerant genotypes within 4–6 d of flooding.

Chlorophyll pigments

Chlorophyll is one of the major plant pigments, supporting the photosynthetic ability. Reduction in chlorophyll content during flooding is common in rice (Panda and Sarkar, 2012). Flooding promotes chlorophylldegradation in sensitive and tolerant genotypes (Sarkar et al, 2006), and this can be used as an index of flooding tolerance. Ethylene stimulates the ‘chlorophyllase’ activity and it accelerates chlorophyll loss in the plants under water. Chlorophyll retention by inhibition of ethylene synthesis and action might improve photosynthesis and supply energy reserve needed for maintenance process (Pradhan et al, 2017).Singh et al (2014) also indicated that the retention of chlorophyll content in and after flooding becomes essential for plant survival, as the same helps photosynthesis under water andhelps in faster recovery on desubmergence. Sarkar et al(2006) observed that the chlorophyll content in Swarna is reduced sharply after 10 d of complete flooding compared to that in Swarna-. Further blocking response of ethylene also reduces leaf chlorosis under flooding (Singh et al, 2014).

Effects of flooding on biochemical characteristics of rice plants

Carbohydrate

Non-structural carbohydrates are essential for plant survival under various stresses (Panda and Sarkar, 2014). Carbohydrate concentration of stem prior to flooding is considered as a major trait for survival of rice plant under water (Panda and Sarkar, 2014). The carbohydrates are consumed while remaining in flooding state to provide requisite energy for the plant’s survival (Nagai et al, 2010), and consumption of carbohydrate by plants under water is essential to tolerate the consequences of flooding. Rice seedlings with high level of carbohydrates before flooding accompanied with less shoot elongation and with the capacity to retain chlorophyll are the essential traits for flooding tolerance. Assessment showed that the tolerant cultivars contain 30%–50% non-structural carbohydrates than the sensitive ones (Sarkar et al, 2006). The genetic differences in flooding tolerance need not be related to the carbohydrate status prior to flooding, instead, it is related to the capability to sustain higher amount of carbohydrates in flooding conditions (Ram et al, 2002).

Anaerobic protein

Protein synthesis is known to be severely affected by flooding. However, certain anaerobic proteins are induced during flooding, and many of them are enzymes of carbohydrate metabolism and alcoholic fermentation (Sarkar et al, 2006). The anoxia tolerant and sensitive cultivars may differ in level of production and number of anaerobic polypeptides due to repression of most aerobic protein synthesis in response to oxygen depletion. Six of the inducible proteins are recognised to be cytosolic enzymes in several crops including rice. Theyare alcohol dehydrogenase, aldolase, glucose phosphate isomerase, sucrose synthase, pyruvate decarboxylase and glyceraldehyde phosphate dehydrogenase (Miro and Ismail, 2013).

Plant hormone

Plant hormones like ethylene, gibberellic acid, abscisic acid and their successive manipulations are considered to have major roles through synergism and antagonism actions for the survival of plants under submergence (Huang et al, 2019). The enhanced elongation growth of deep-water rice varieties is mediated by the action of ethylene and gibberellic acid (Jackson and Ram, 2003; Goswami et al, 2017). But flash flooding tolerance is linked with a reduced level of ethylene. Elongation of stem is not a desirable criterion in flooding condition. Thus, synthesis of gibberellic acid is blocked to reduce elongation and preserve energy for proper growth. Ethylene enhances the responsiveness of internode tissue to gibberellic acid by reducing production of abscisic acid, which is a potent antagonist of gibberellic acid. The survival rate is increased many folds when gibberellin biosynthesisinhibitor is applied before flooding (Pradhan et al, 2013).

Regeneration capacity of rice plants after flooding

The capacity ofplants to regenerate after flooding is vital in order to give high yield. Prompt regeneration of growth following flooding is an important characteristic (Panda et al, 2008). Tolerant genotype showed its ability to regenerate faster by formation of fresh leaves with higher rate of stability to survive (Panda et al, 2008). It was found that recovery becomes faster in tolerant varieties due to efficient ROS scavenging systems and lower in the process of lipid peroxidation on being exposed to air (Kawano et al, 2002; Singh et al, 2014).

Fig. 2.Production and elimination of reactive oxygen species(ROS)responding to adverse flood conditions (Ito et al, 1999; Upadhyay, 2018).

SOD, Superoxide dismutase; CAT, Catalase; APX, Ascorbate peroxidase; GPX,Guaiacol peroxidase; MDAR, Monodehydroascorbate reductase; DHAR, Dehydroascorbate reductase; GR, Glutathione reductase.

Effects of flooding on oxidative metabolism

When flood occurs, rice plants are required to adapt to two extreme environmental conditions, hypoxic condition when flood takes place and aerobic condition after recession of flood (Panda and Sarkar, 2013). The damage of plantssuffered by flood is not perceptible in flooding state but becomes distinct soon after desubmerge (Fig. 2). Plants all in a sudden are required to encounter an environment with higher amount of light intensity and oxygen completely different from the environment prevailing under flooding condition. This post oxygenation causes oxidative stress, resulting in excess ROS production (Panda et al, 2006; Panda and Sarkar, 2013). Such produced ROS acts as signalling molecules inducing the plant to respond to the stresses (Panda and Sarkar, 2013).

Fig. 3.Reactive oxygen species (ROS) and their action in plants under flooding stress (Upadhya, 2018).

ROS are identified as secondary class of smaller molecules which acts as a mediator to the responses of biotic and abiotic stresses including flooding (Fig. 3). ROS are capable of irreversible cellular damage by proteinoxidation, enzyme inactivation, changes in gene expression,and decomposition of biological membranes etc. and results in cell death (Damanik et al, 2012; Jajic et al, 2015). After desubmergence, the submerged rice plants immediately exposed to an environment with high light intensity and oxygen tension, resulting in increased production of ROS and if not detoxified, may cause acute harm to the cellular organisation and plant death (Damanik et al, 2010). Genotypes that are more efficient of mitigating the ROS are more competent in sustaining plant growth. ROS comprises of free radical (hydroxyl radical, superoxide anion etc.) as well as non-radical forms (singlet oxygen, hydrogen peroxide etc.) (Gill and Tuteja, 2010), which are formed as byproducts of different metabolic processes and generated by both enzymatic and non-enzymatic methods (Sasidharan et al, 2018).

Superoxide radical (O2·? )

Superoxide radical is produced in different cell compartments like peroxisome, chloroplast, apoplast, mitochondrial electron transport chain and plasma membrane. The superoxide anion is mainly generated in chloroplast by Mehler reactions, where oxygen is reduced by electrons from photosynthetic electron transport chain under different abiotic stress including flooding (Jajic et al, 2015; Upadhyay, 2018). Superoxide anion is short lived, which is moderately reactive free radical with about 2–4[w3] ms (milli second) of half-life, and it cannot cross the membrane of chloroplast (Jajic et al, 2015).

Hydrogen peroxide (H2O2)

Hydrogen peroxide plays a key role in plants under flooding stress as a signalling molecule, which mediates between various physiological processes (Fukao et al, 2019). It is also associated with the regulation of senescence process (Peng et al, 2005), protection against disease (Kumar et al, 2011), decreasing stress intensity at low light (Zhang et al, 2011), acclimation to drought (Ishibashi et al, 2011), and it can change the expression level of hundreds of genes in plants (Yun et al, 2010). H2O2is the steadiest and firm, and less reactive ROS when compared with other ROS and it can cross the membrane easily. There are two possible pathways of hydrogen peroxide production in plants, one is dismutation of superoxide anion by superoxide dismutase (SOD) and theother is via oxidases like amino and oxalate oxidases. The balance between H2O2scavenging antioxidant enzymes and SOD in cells is believed to be important for determination of the steady state level of H2O2under flooding (Upadhyay, 2018).

Hydroxyl radical (OH?)

Hydroxyl radical is among the most extremely reactive ROS. It is produced from H2O2and O2in the Fenton reaction in the neutral pH and ambient temperature, and these toxic hydroxyl radicals can penetrate the membrane and leaf mitochondrion (Gill and Tuteja, 2010; Sharma et al, 2012). Hydroxylradical is considered to be responsible for mediatingO2toxicity in plants after flood water recedes (Upadhyay, 2018). In higher concentration, this super active hydroxyl radical causes cell death due to lack of enzymatic reaction for its detoxification under flooding stress (You and Chan, 2015; Fukao et al, 2019).

Singlet oxygen (1O2)

This is the highly reactive, excited state of molecular oxygen generated by the reaction of chlorophyll triplet state and O2. Singlet oxygen is formed when one of the unpaired electrons is promoted to a higher energy orbital (Gill and Tuteja, 2010). Under control conditions, singlet oxygen is formed during photosynthesis by the photo activation of photosynthetizers, mostly chlorophyllsand their precursors. It is also produced under different abiotic stresses including submergence (Springer et al, 2015; Upadhyay, 2018). It has dual role as oxidising agent and signalling molecule under flooding stress (Kim et al, 2008; Fukao et al, 2019). Since it is highly reactive and their life span being short by about 3.1 to 3.9 s in pure water, it is able to interact with molecules present mainly in its nearest environment (Jajic et al, 2015).

Lipid peroxidation under flooding stress

Lipid peroxidation produces malondialdehyde (MDA).The amount of MDA indicates the extent of damage resulted by ROS in the tissue (Damanik et al, 2012). This is formed due to oxidative stress which induces membrane damage. Significant negative co-relation has been found between formation of MDA with ascorbate concentration and survival rate in rice plants (Kawano et al, 2002). Damanik et al (2012) indicated the significant difference between MDA content in rice seedlings under anoxic and aerobic conditions, and the extended duration of anaerobic conditions increased the lipid peroxidation. MDA content is significantly higher in sensitive cultivars during flooding and after exposure to air (Panda and Sarkar, 2013).

Effects of flooding on antioxidants defence mechanism

Plant cells are able to neutralise the ROS with efficient oxygen-scavenging machinery consisting of several antioxidants (both non-enzymatic and enzymatic) (Gill and Tuteja, 2010). Thus, induction of antioxidant defense mechanism is essential for protection of plants against different stresses. SOD, catalase (CAT), guaiacolperoxidase (GPX), ascorbate peroxidase (APX), glutathione reductase (GR), dehydroascorbate reductase (DHAR) and monodehydroascorbate reductase(MDAR) are the predominant antioxidant enzymes, which play important roles in protecting plants from oxidative damages (Upadhyay, 2018).

Enzymatic antioxidants

In aerobic organisms,SOD defends and protects from being damaged by oxidative reactions. This is the first antioxidant enzyme in the process of detoxification, transforms superoxide anion to hydrogen peroxide (Gill and Tuteja, 2010; Steffens et al, 2013). SOD is one form of metalloenzymes and it removes superoxide anion by disproportionating it to hydrogen peroxide and oxygen (Sharma et al, 2012). This enzyme existsin three isoforms (Damanik et al, 2012; You and Chan, 2015). SOD activity is increased under stress condition including flooding stress (Mishra et al, 2011). Over production of SOD increases the plant’s tolerance to oxidative stress (Sharma et al, 2012). Damanik et al (2012)studied two Malaysian rice mutants along with FR13A and observed the significant increase in SOD activity in response to flooding.

CAT is identified as the first enzyme among all other antioxidant enzymes (Sharma et al, 2012). CAT carries out dismutation of hydrogen peroxide into H2O and O2(Gill and Tuteja, 2010; Sharma et al, 2012). CATs possess high turnover rate, and each molecule of it converts six million of hydrogen peroxide into water and oxygen in 1 min (Gill and Tuteja, 2010). The major production site of H2O2is peroxisomes. The actions of SOD and CAT when both taken together become critical in elevating the adverse impact of oxidative damage in plants. Damanik et al (2010) observed that the CAT activity was 9-fold higher under flooding as compared to control plants in case of FR13A.

GPX is another antioxidant enzyme containing heme, which prefers to oxidise guaiacol and pyragallol instead of H2O2(Gill and Tuteja, 2010). The enzymes contain two structural Ca2+and four disulfide bridges. Various isoenzymes of GPX are located in different tissues such as cell wall and cytosol. It plays vital roles in various plant processes like decomposition of hormone IAA, lignifications of cell wall, formation of ethylene and lends protection against various stresses including flooding (Gill and Tuteja, 2010; Upadhyay, 2018). Generally, it is known as stress enzyme due to its effective quenching ability of harmful free radical in stress condition (Sharma et al, 2012). GPX activity in rice is increased under different duration of flooding (Panda and Sarkar, 2012)

The Asada-Halliwell pathway or ascorbate glutathione cycle plays an important role in scavenging ROS during and after flooding (Damanik et al, 2012). This pathway regenerates the reduced ascorbate and glutathioneas primary scavengers under flooding stress (Sarkar et al, 2006; Damanik et al, 2010). Glutathione reductase is a key factor associated with recycles of reduced glutathione, maintaining glutathione level in the cell, resulting in supplying the total amount of glutathione to mitigate the damages caused by submergence (Panda and Sarkar, 2013). The ascorbate glutathione cycle includes sequential reduction and oxidation of ascorbic acid, glutathione and nicotinamide adenine dinucleotide phosphate (NADPH) which is catalysed by four antioxidant enzymes i.e. APX, MPAR, DHAR and GR. This Asada-Halliwell pathway is located in sub-cellular sites like cytosol, chloroplast, mitochondria and peroxisome regulate flooding tolerance (Sharma et al, 2012; Upadhyay, 2018). [w4]

APX is a major antioxidant enzyme of Asada-Halliwell pathway and takes the lead role in reduction of enhanced ROS level during and after flooding stress (Sarkar et al, 2006; Upadhyay, 2018). APX catalyses detoxification of hydrogen peroxide by reducing H2O2to H2O utilising the reducing power of ascorbate (Damanik et al, 2010, 2012; Smirnoff, 2018). It is mostly found in both cytosol andchloroplast, and is an important enzyme of glutathione-ascorbate cycle, as its removes peroxides by transforming ascorbic acid into dehydroascorbate (Damanik et al, 2010; Gill and Tuteja, 2010). This enzyme has a greater affinity towards hydrogen peroxide compared to catalase, making the enzyme an efficient scavenger of H2O2under flooding stress (Sarkar et al, 2006; Upadhyay, 2018).

Monodehydroascorbate reductase ([w5] [DP6]

MDAR catalyses the ascorbic acid regeneration from monodehydroascorbate radical using of NADPH. This enzyme exists as cytosolic and chloroplast isozymes (Gill and Tuteja, 2010; Suzuki et al, 2012). Presence of this enzyme in peroxisome and mitochondria decomposes the hydrogen peroxide present therein. The ‘monodehydroascorbate’ is used as a substrate only by this enzyme and the enzyme activity is widespread in plants. The increased MDAR activity was observed in several studies relating to the plants subjected to different kinds of stresses including flooding (Sharma et al, 2012).

DHAR carries out the ‘dehydroascorbate’ reduction to ascorbic acid by using the reducing agent glutathione (Upadhyay, 2018). DHAR has a key role in maintaining reduced ascorbate level. Dehydroascorbate has short life span and it can be either hydrolyse 2,3-diketogluconic acid or convert to ascorbate via DHAR (Sharma et al, 2012). Abiotic stresses such as flooding, drought, chilling and salinity increase the DHAR activity in plants (Chang et al, 2017).

GR is dependent on NADPH, and it reduces the oxidised glutathione (GSSG) to its reduced form (GSH), thus maintaining high GSH/GSSG ratio (Rao and Reddy, 2008). It is a flavo-protein and has an essential disulfide group. Although GR is present in other cell organelles as well as cytosol, its maximum enzyme activity is its chloroplastic isoforms. Reduced glutathione and GR in chloroplast together decomposes hydrogen peroxide produced through Mehler reaction (Sharma et al, 2012) and plays an important role in combating abiotic stress in plants (Gill and Tuteja, 2010). The increased GR activity in plants under stress has been studied by several workers. Damanik et al (2010) revealed that the activity of GR serves as a criterion for evaluation of flooding tolerance in rice. GR sensitivity has been observed in tolerant rice varietiesPanikekoa and T1471 under flooding (Das et al, 2004).

Non-enzymatic antioxidants

Potent non-enzymatic antioxidants help in mitigation of oxdative stress within the cell (Gilland Tuteja, 2010). These non-enzymatic antioxidants interact with various cellular components and in addition to their major roles in providing defense and as cofactors of enzyme, they also involved in various processes relating to plantgrowth and development (Sharma et al, 2012; You and Chan, 2015).

Ascorbic acid is a powerful antioxidant with low molecular weight and is abundantly available. It plays a vital role in giving protection to plants from being adversely affected by oxidative stress caused due to submergence or flooding (Panda and Sarkar, 2013; Steffens et al, 2013). It performs many important roles in plant physiological processes,and is found in all plant tissues, most abundantly in the tissues which carry out photosynthesis. It is considered as a powerful antioxidant because of its power to supply electrons in various reactions catalyzed by both enzymatic and non-enzymatic methods (Gill and Tuteja, 2010). The ascorbate metabolism mostly takes part inside mitochondria, which not only synthesise it but also regenerates it from its oxidised form. Studies showed that higher levels of reduced ascorbate play an important role in creating defense to the plants to fight against damage caused due to flooding (Kawano et al, 2002; Das et al, 2004). Over expression of enzymes linked with ascorbic acid biosynthesis supports plant’s endurance ability to overcome stress (Sharma et al, 2012). It reacts with ROS in both the photosystems I and II through ASC-GSH as well as xanthophyll cycle during flooding (Damanik et al, 2010).

Glutathione is a non-protein thiol which provides intracellular protection against ROS-induced oxidative damages (Gill and Tuteja, 2010; Sharma et al, 2012), and located in all cell compartments, for example,endoplasmic reticulum, vacuole, mitochondria, peroxisomes,chloroplast, cytosol and apoplast. Because of its reducing power glutathione plays crucial roles in diverse physiological processes like regulation of sulfate transport, cell growth and cell division, pathogen resistance,conjugation of metabolites, signal transduction, enzymatic regulation, formation, of protein and nucleic acid, synthesis of phytochelatin, decomposition of xenobiotics as well as the expression of stress responsive genes (Mullineaux and Rausch, 2005). Glutathione acts as a potential scavenger of harmful free radicals like hydrogen peroxide, singlet oxygen and hydroxyl radical. It plays an important role in antioxidant defense system by regenerating ascorbic acid by ASC-GSH cycle (Gill and Tuteja, 2010).

Genetic mechanism of flooding tolerance in rice

The genetic basis of flooding tolerance remained ambiguous until the mid of 1990 (Bailey-Serres et al, 2010). Genetic mechanism of rice for tolerant to flooding/submergence is shown in Fig. 4. ‘Quiescence’ and ‘Elongation’ are two major and opposite strategies to encounter the effects of flooding during flash and deep-water flooding, respectively (Fig. 4). The ‘escape’ type of adaptive response is mostly seen in deep-water lowland rice, where vigorous shoot elongation prevents the plant from complete flooding as flood water level gradually increases. Two ethylene responsive factor genes() and() cloned from a deep-water rice variety C9285 involve in the elongation of shoot in these floating rice (Vergara et al, 2014; Tamang and Fukao, 2015). Both the genes function in contradiction with(). Theempowers the plant to endure flash flooding by limited elongation until flooding water recedes (Xu et al, 2006; Bailey-Serres et al, 2010). The tolerant rice genotype adapted to flash flooding condition is characterised by slow elongation growth and thus conserves accumulated respirable biomass to resume growth after the de-submergence (Bailey-Serres et al, 2012; Azarin et al, 2017). Allelic surveys showed that() genes are present only in deep-water rice varieties which exhibit rapid internode elongation in response to submergence (Tamang and Fukao, 2015).promotethe accumulation of bioactive gibberellic acid in submerged internodes (Ayano et al, 2014). During flooding, ethylene accumulates, triggeringgene expression in C9285 (Minami et al, 2018).It has been observed that ethylene increases biosynthesis of gibberellic acid under flooding, triggering the internode elongation in deep-water rice (Fukao and Bailey-Serres, 2008). Kuroha et al (2018) identified a rare allele of gibberellin biosynthesis gene() which provides adaptation to deepwater. The SD1 protein directs increased gibberellin synthesis, largely GA4, thus resulting in internode elongation.

Fig. 4.Genetic mechanism of rice for tolerant to flooding/submergence.

A,mediated response of submergence tolerance in rice.B,() mediated escape response for tolerance to deep-water flooding in rice (Tamang and Fukao, 2015).

It is reported that a few anaerobic germination tolerance QTLs were found on chromosomes 5 and 11 (Jiang et al, 2004). Five different QTLs were found on chromosomes 1, 3, 7 and 9 identified by crossing IR64 with the tolerant donor Khao All Hlan On (Jiang et al, 2004; Angaji et al, 2010). The QTLorlinked with local modulation of trehalose-6-phosphate (T6P) is the most promising locusfor breeding (Kretzschmar et al, 2015).() gene is involved in metabolism of T6P (Loreti et al, 2018). In a population obtained by crossing sensitiveline IR42 with tolerant variety Ma-Zhan Red (Septiningsih et al, 2013), another anaerobic germination tolerance QTL (or)is found on shoot arm of chromosome 7. Zhang et al (2017) revealedthat_is linked with anaerobic germination tolerance using 5291 single nucleotide polymorphism markers.

Many studies consideredas a typical quantitative trait. This QTL is identified from the rice landrace FR13A on chromosome 9 through molecular mapping. (Ram et al, 2002) indicated that 70% phenotypic variance in flooding tolerance comes from this QTL and the rest 30% were contributed by other secondary minor QTLs located on chromosomes 1, 2, 5, 7,10 and 11. At the molecular level, thelocus contains 3 ethylene responsive factors (ERFs),and, which are upregulated under flooding (Xu et al, 2006).andare found in all rice varieties.is only responsible for transient flooding and it is found atQTL in FR13A and other tolerant genotypes (Bailey-Serres et al, 2010). Xu et al (2000) futher carried out fine mapping ofgene with 3000 F2indivisual to a 0.16-cM region on chromosome 9.is recognised in two allele forms:is located only in tolerant genotype andis found in sensitive ones (Xu et al, 2006; Septiningsih et al, 2012). Both the alleles encode similar proteins, with the exception of Ser186inand Pro186inalleles (Xu et al, 2006; Bailey-Serres et al, 2010).controls shoot elongation, conserves reserve carbohydrates, retains chlorophyll content etc., and as a result, it controls plant survival and resumes tolerant genotype growth when water recedes (Pucciariello and Perata, 2013). Rice varieties having flooding induciblerestricts/limits ethylene production which maintains mRNA and protein accumulation of gibberellic acid signalling repressors during flooding (Singh et al, 2014; Fukao et al, 2019). The inhibition of gibberellic acid responsiveness mediated byrepresses genes needed for catabolism of sucrose and starch, thus restrictingelongation growth in order to conserve precious carbohydrates for its survival under water and recovery. This quiescence is being very useful in plant breeding (Neeraja et al, 2007; Septiningsih et al, 2013).

Marker-assisted breeding (MAB)approaches for flooding tolerance in rice

The success of fine mapping offrom FR13A, a sound QTL has enabled the MAB of modern rice cultivars having the ability to withstand flash flooding (Bailey-Serres et al, 2010). The polygenic QTLwas introduced to eight rice cultivars using marker- assisted backcrossing. International Rice Research Institute has successfully introgressedQTL into high-yielding variety Swarna, which is presently adapted in many states of India (Singh et al, 2013; Dar et al, 2017). Swarna-can endure two weeks of flash flooding and recovers well after receding of flood water. It was released in India in 2009 after few years of successful evaluation in the farmers’ fields. At the same time,was also introgressed into mega rice varieties grown in rainfed ecology in South and South-East Asian countries(Neeraja et al, 2007). Theincorporated popular varieties such as IR64-, Samba Mahsuri-, Thadokkam 1-, BR11-, BINA Dhan11 and CR1009-have been recognized for enhancing rice productivity in less favourable lowland ecosystem of eastern India, Nepal and Bangladesh (Ismail et al, 2013; Ahmed et al, 2016). Singh et al (2016) also reported the transfer ofto 10 highly popular regionally adapted Indian rice varieties. The original andintrogressed varieties show no apparent morphological variation in numerous trials in farmer’s field (Singh et al, 2017).

Breeding for higher germination potential, increased seedling strength and flooding tolerant rice varieties during the period of seed germination was studied in the past (Yamauchi et al, 1993, 1994; Biswas and Yamauchi, 1997), but left with limited results. This is due to lack of suitable genotypes with enhanced tolerance, less available information on genetics of anaerobic germination tolerance and non-availability of clear simplified mechanism (Jiang et al, 2004). Molecular breeding for AG tolerance in rice was started using() detected from Khao Hlan On (Kretzschmar et al, 2015; Kato et al, 2019). AGL was introgressed into some improved varieties or theirderivatives such as IR64, IR64-, PSB Rc18-and PSB Rc82 (Septiningsih et al, 2013). The Chinese traditional rice cultivar Ma-Zhan Red was used as a donor in incorporation of() locus to mega varieties in several studies. Depending upon the population of donor, the transfer ofis monitored by two or three markers (Azarin et al, 2017; Kato et al, 2019).

Prospects

Although remarkable progress has been achieved through marker assisted selection, we still have several critical problems to overcome in molecular breeding of flooding tolerant plants. Our understanding of the whole-plant stress response mechanism is very limited. Therefore, we need to investigate stress responses in differentiated cell, tissues and organs and to connect the data relevantly. Also, there is a need of finding superior alleles of/gene or other novel genes which may provide better protection against different types of flooding stress. The summarized information of this review will facilitate further investigations of signalling mechanisms of flooding tolerance in rice and development of flooding tolerant rice genotypes.

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http://dx.doi.org/10.1016/j.rsci.2020.11.006

9 January 2020;

9 May 2020

Debabrata Panda (dpanda80@gmail.com)

(Managing Editor: Wang Caihong)