The rice SUB1A gene: Making adaptation to submergence and post‐submergence possible

Rice feeds billions of people in the world. It is grown worldwide, in very diverse environments, from river deltas and coastal areas to highly heterogeneous upland environments. A vast number of varieties, landraces, and wild relatives are grown, reflecting the exceptional adaptability of rice to a range of environments. Flooding represents a significant threat to global rice production, especially in Asia. One-third of the fields cultivated with rice are vulnerable to flash floods (Bailey-Serres et al., 2010), and this scenario is likely to worsen in the context of climate change. Although many people believe that rice is highly tolerant to submergence, given that is often grown in paddy fields, this is only true in terms of shallow submergence. Under such conditions, rice is able to transport oxygen to the submerged parts of the plants thanks to major anatomical modifications of the stems, where an extensive aerenchyma facilitates the flow of air towards the submerged root system. Yet very few rice varieties can withstand complete submergence. The molecular mechanism behind the ability of some rice varieties to withstand submergence has only been understood since 2006. Before this date, only some landraces, such as FR13A, were known to withstand submergence. Unfortunately, FR13A lacks most of the agronomic qualities required for good rice varieties. In fact, FR13A is sensitive to photoperiod for flowering, is too tall, and provides low yields of a poor-quality grain (Bailey-Serres et al., 2010). Genetic studies have led to the identification of a major QTL on chromosome 9, which contributes up to 70% of the phenotypic variation in rice submergence tolerance (Xu & Mackill, 1996). This QTL has been named SUBMERGENCE 1 (SUB1). The molecular identity of SUB1 was revealed in 2006, when a cluster of three genes at the SUB1 locus was identified (Xu et al., 2006). These genes encode for three ethylene response factors (ERFs; Xu et al., 2006), belonging to group VII (ERF-VII; Licausi, Ohme-Takagi, & Perata, 2013). Xu et al. (2006) found that two of these ERF genes, SUB1B and SUB1C, were always present in the SUB1 region of all the rice accessions they analysed, while SUB1A was detected in fewer varieties. SUB1A was not unequivocally associated with submergence tolerance. Two alleles of SUB1A exist in submergence tolerant and intolerant rice accessions, with SUB1A-1 found only in tolerant lines such as FR13A, whereas the SUB1A-2 allele has been found in intolerant indica-type Oryza accessions (Bailey-Serres et al., 2010). It is hypothesized that SUB1A-1 from wild species may have been introgressed into domesticated rice (Pucciariello & Perata, 2013). Besides SUB1A-1, other genes could be important for submergence tolerance, given that some wild species that are tolerant to submergence do not possess SUB1A-1 (Niroula et al., 2012). Remarkably, as highlighted by Locke, Barding Jr., Sathnur, Larive, and Bailey-Serres (2017) in this issue of Plant, Cell and Environment, SUB1A-1 also contributes to desubmergence tolerance. The identification of SUB1A-1 enabled the submergence tolerance trait to be bred within highly productive varieties by marker-assisted backcrossing (Bailey-Serres et al., 2010; Singh, Mackill, & Ismail, 2009). The mechanism by which SUB1A-1 makes rice submergence tolerant was described by Fukao, Xu, Ronald, and Bailey-Serres (2006), who proposed that SUB1A-1 affects the expression of genes involved in anaerobic metabolism, reducing carbohydrate consumption and inhibiting stem elongation. Transgenic rice plants over-expressing SUB1A showed gibberellin (GA)-insensitive phenotypes, suggesting that SUB1A limits the response to GA (Fukao & Bailey-Serres, 2008). It was in fact demonstrated that SUB1A confers tolerance to submergence by limiting ethylene-promoted GA responsiveness by enhancing the accumulation of the GA signalling repressors, SLR1 and SLRL1 (Fukao & Bailey-Serres, 2008). Rice varieties possessing the SUB1A-1 gene are tolerant to submergence because they stop growing when submerged. Their carbohydrate reserves are thus preserved to allow regrowth when the water recedes. This mechanism of submergence tolerance has been defined as the “quiescence strategy” in contrast to the “escape strategy” which many semi-aquatic plant species adopt, based on a highly coordinated enhancement in upward growth of the shoot organs such as stems and petioles (Perata & Voesenek, 2007). The “escape” strategy allows the shoots to regain contact with the atmosphere above the water surface, so that the plant can efficiently resume aerobic metabolic activity. This “escape strategy” is also adopted by some rice varieties, termed “deepwater rice,” which can grow up to 3 m in total height, thanks to a growth rate that can be as high as 30 cm/day when submerged. These varieties are not really tolerant to submergence because they never experience hypoxia as a consequence of flooding, since they are able to keep at least the tips of their leaves above water, thus making the transfer of air by aerenchyma to the submerged parts of the plant possible. Deepwater rice varieties do not possess the SUB1 genes but instead express another group of ERF-VII genes, namely, SNORKEL1 and SNORKEL2 (SK1 and SK2; Hattori et al., 2009). Submergence leads to the entrapment of ethylene, which induces the ERF genes. There is no difference in ethylene accumulation in deepwater and non-deepwater rice (Hattori et al., 2009); however, the presence of the SUB1 or SK genes has a drastically opposite effect on the physiology of the rice plant. In deepwater rice, the accumulated ethylene triggers the expression of the SK genes, leading to the GA-dependent induction of internode elongation in deepwater rice. In contrast, ethylene-induced SUB1A-1 represses growth by interfering with the GA signalling pathway. These two opposite plant responses, which rely on ethylene and on genes belonging to the same group VII of ERF transcription factors, are a perfect example of genetic adaptation to new environments. Group VII ERF genes have recently emerged as oxygen sensors in plants (Gibbs et al., 2011; Licausi et al., 2011). The stability of ERF-VII proteins in Arabidopsis, via the N-end rule pathway, depends upon hypoxia, as the N-terminal cysteine residue in these proteins is enzymatically oxidized by plant cysteine oxidases if oxygen is present (Weits et al., 2014). Arabidopsis ERF-VII proteins, such as RAP2.12, act as transcription factors which activate those genes involved in the adaptation to hypoxia (reviewed in Loreti, van Veen, & Perata, 2016). Interestingly, SUB1A-1 is not a substrate for the N-end rule pathway despite containing the Cys-containing N-terminal motif, thus indicating that it is uncoupled from the oxygen-dependent, N-end rule pathway regulation (Gibbs et al., 2011). The transcription of SUB1A-1 therefore mostly relies on ethylene accumulation under submergence, while its protein stability is not influenced by the presence of oxygen. The enhanced stability of SUB1A-1 may relate to the additional role of SUB1A-1 in inducing tolerance to multiple abiotic stresses (Gibbs et al., 2011). Rice genotypes with SUB1A-1 display enhanced recovery from drought through a reduction in leaf water loss, lipid peroxidation, and increased expression of genes associated with acclimation to dehydration (Fukao, Yeung, & Bailey-Serres, 2011). The overexpression of SUB1A increases ABA responsiveness, thereby activating drought-stress-induced gene expression. It may seem counter-intuitive that a gene playing a major role in submergence tolerance is also involved in drought tolerance. However, it is important to highlight that plant tissue can suffer from dehydration when desubmerged even if the soil contains sufficient water. In fact, desubmergence causes the upregulation of drought-related transcripts, and a higher induction of these genes in SUB1A-1 genotypes has been observed (Fukao et al., 2011). It is therefore possible that SUB1A-1 evolved to ensure that the plant tolerates submergence as a compound stress, which includes a lack of oxygen but also darkness in turbid water and drought during desubmergence. In this issue of Plant, Cell and Environment, Locke et al. (2017) describe the results of transcriptomic and metabolomic analyses that were performed in order to better understand how SUB1A-1 contributes to submergence and desubmergence tolerance. The results show that low energy sensing pathways and sugar metabolism are greatly influenced by SUB1A-1. The levels of trehalose-6-phosphate (T6P), a molecule signalling a high sugar content in the cell, were higher at dusk and dawn in SUB1A-1-containing rice plants that were desubmerged than in control plants, which suggests a better sugar status as the consequence of SUB1A-1 being present. SUB1A-1 plants also showed a lower expression of AMY3D, an α-amylase gene that responds strongly to sugar starvation, again indicating that SUB1A-1 contributes to maintaining sugar homeostasis during desubmergence. The submergence-dependent accumulation of amino acids was reduced by SUB1A-1, indicating a better management of nitrogen metabolism, which is linked to the improved ability of SUB1A-1 plants to control sugar homeostasis. The results of Locke et al. (2017) also show that SUB1A-1 positively impacts the transition from stress amelioration to the return to homeostasis, as plants with SUB1A showed evidence of resumed photosynthesis through improved glucose and sucrose-6-phosphate content within hours of desubmergence. Interestingly, SUB1A-1 limits chloroplast degradation, which is also in line with SUB1A-1 conferring tolerance to extended darkness (Fukao, Yeung, & Bailey-Serres, 2012). These mechanisms may contribute to maintaining photosynthetic capacity and thus regrowth ability after submergence. Overall, the results by Locke et al. (2017) demonstrate that SUB1A promotes the recovery of metabolic homeostasis. This thus confirms that the role of SUB1A-1 in submergence tolerance is not restricted to the submergence of plants but also extends to the recovery phase (Figure 1). Discoveries on plant responses to submergence have dramatically increased over the last decade. The molecular basis of rice tolerance and adaptation to submergence are now known, together with the oxygen sensing mechanism that enables plants to sense molecular oxygen and modify their physiology to better survive hypoxic conditions. Some of these discoveries have already been translated into better crops. However, besides rice, little is known about how other crops adapt to submergence and hypoxia. In the context of the impact of climate change, it is imperative that work performed on Arabidopsis and rice is translated to crops that are intolerant to submergence. I have no conflict of interest to declare.