Most Oryza sativa cultivars die within a week of complete submergence--a major constraint to rice production in south and southeast Asia that causes annual losses of over US 1 billion dollars and affects disproportionately the poorest farmers in the world. A few cultivars, such as the O. sativa ssp. indica cultivar FR13A, are highly tolerant and survive up to two weeks of complete submergence owing to a major quantitative trait locus designated Submergence 1 (Sub1) near the centromere of chromosome 9 (refs 3, 4, 5-6). Here we describe the identification of a cluster of three genes at the Sub1 locus, encoding putative ethylene response factors. Two of these genes, Sub1B and Sub1C, are invariably present in the Sub1 region of all rice accessions analysed. In contrast, the presence of Sub1A is variable. A survey identified two alleles within those indica varieties that possess this gene: a tolerance-specific allele named Sub1A-1 and an intolerance-specific allele named Sub1A-2. Overexpression of Sub1A-1 in a submergence-intolerant O. sativa ssp. japonica conferred enhanced tolerance to the plants, downregulation of Sub1C and upregulation of Alcohol dehydrogenase 1 (Adh1), indicating that Sub1A-1 is a primary determinant of submergence tolerance. The FR13A Sub1 locus was introgressed into a widely grown Asian rice cultivar using marker-assisted selection. The new variety maintains the high yield and other agronomic properties of the recurrent parent and is tolerant to submergence. Cultivation of this variety is expected to provide protection against damaging floods and increase crop security for farmers.

Flooding is an environmental stress for many natural and man-made ecosystems worldwide. Genetic diversity in the plant response to flooding includes alterations in architecture, metabolism, and elongation growth associated with a low O(2) escape strategy and an antithetical quiescence scheme that allows endurance of prolonged submergence. Flooding is frequently accompanied with a reduction of cellular O(2) content that is particularly severe when photosynthesis is limited or absent. This necessitates the production of ATP and regeneration of NAD(+) through anaerobic respiration. The examination of gene regulation and function in model systems provides insight into low-O(2)-sensing mechanisms and metabolic adjustments associated with controlled use of carbohydrate and ATP. At the developmental level, plants can escape the low-O(2) stress caused by flooding through multifaceted alterations in cellular and organ structure that promote access to and diffusion of O(2). These processes are driven by phytohormones, including ethylene, gibberellin, and abscisic acid. This exploration of natural variation in strategies that improve O(2) and carbohydrate status during flooding provides valuable resources for the improvement of crop endurance of an environmental adversity that is enhanced by global warming.

Plants and animals are obligate aerobes, requiring oxygen for mitochondrial respiration and energy production. In plants, an unanticipated decline in oxygen availability (hypoxia), as caused by root waterlogging or foliage submergence, triggers changes in gene transcription and mRNA translation that promote anaerobic metabolism and thus sustain substrate-level ATP production1. In contrast to animals2, oxygen sensing has not been ascribed to a mechanism of gene regulation in response to oxygen deprivation in plants. Here we show that the N-end rule pathway of targeted proteolysis acts as a homeostatic sensor of severe low oxygen in Arabidopsis, through its regulation of key hypoxia response transcription factors. We found that plants lacking components of the N-end rule pathway constitutively express core hypoxia response genes and are more tolerant of hypoxic stress. We identify the hypoxia-associated Ethylene Response Factor (ERF) Group VII transcription factors of Arabidopsis as substrates of this pathway. Regulation of these proteins by the N-end rule pathway occurs through a characteristic conserved motif at the N-terminus initiating with MetCys- (MC-). Enhanced stability of one of these proteins, HRE2, under low oxygen conditions improves hypoxia survival and reveals a molecular mechanism for oxygen sensing in plants via the evolutionarily conserved N-end rule pathway. SUB1A-1, a major determinant of submergence tolerance in rice3, was shown not to be a substrate for the N-end rule pathway despite containing the N-terminal motif, suggesting that it is uncoupled from N-end rule pathway regulation, and that enhanced stability may relate to the superior tolerance of Sub1 rice varieties to multiple abiotic stresses4.

Multicellular organs are composed of distinct cell types with unique assemblages of translated mRNAs. Here, ribosome-associated mRNAs were immunopurified from specific cell populations of intact seedlings using Arabidopsis thaliana lines expressing a FLAG-epitope tagged ribosomal protein L18 (FLAG-RPL18) via developmentally regulated promoters. The profiling of mRNAs in ribosome complexes, referred to as the translatome, identified differentially expressed mRNAs in 21 cell populations defined by cell-specific expression of FLAG-RPL18. Phloem companion cells of the root and shoot had the most distinctive translatomes. When seedlings were exposed to a brief period of hypoxia, a pronounced reprioritization of mRNA enrichment in the cell-specific translatomes occurred, including a ubiquitous rise in 49 mRNAs encoding transcription factors, signaling proteins, anaerobic metabolism enzymes, and uncharacterized proteins. Translatome profiling also exposed an intricate molecular signature of transcription factor (TF) family member mRNAs that was markedly reconfigured by hypoxia at global and cell-specific levels. In addition to the demonstration of the complexity and plasticity of cell-specific populations of ribosome-associated mRNAs, this study provides an in silico dataset for recognition of differentially expressed genes at the cell-, region-, and organ-specific levels.

Submergence-1 (Sub1), a major quantitative trait locus affecting tolerance to complete submergence in lowland rice (Oryza sativa), contains two or three ethylene response factor (ERF)-like genes whose transcripts are regulated by submergence. In the submergence-intolerant japonica cultivar M202, this locus encodes two ERF genes, Sub1B and Sub1C. In the tolerant near-isogenic line containing the Sub1 locus from the indica FR13A, M202(Sub1), the locus additionally encodes the ERF gene Sub1A. During submergence, the tolerant M202(Sub1) displayed restrained leaf and internode elongation, chlorophyll degradation, and carbohydrate consumption, whereas the enzymatic activities of pyruvate decarboxylase and alcohol dehydrogenase were increased significantly compared with the intolerant M202. Transcript levels of genes associated with carbohydrate consumption, ethanolic fermentation, and cell expansion were distinctly regulated in the two lines. Sub1A and Sub1C transcript levels were shown to be upregulated by submergence and ethylene, with the Sub1C allele in M202 also upregulated by treatment with gibberellic acid (GA). These findings demonstrate that the Sub1 region haplotype determines ethylene-and GA-mediated metabolic and developmental responses to submergence through differential expression of Sub1A and Sub1C. Submergence tolerance in lowland rice is conferred by a specific allele variant of Sub1A that dampens ethylene production and GA responsiveness, causing quiescence in growth that correlates with the capacity for regrowth upon desubmergence.

Crop yield reduction as a consequence of increasingly severe climatic events threatens global food security. Genetic loci that ensure productivity in challenging environments exist within the germplasm of crops, their wild relatives and species that are adapted to extreme environments. Selective breeding for the combination of beneficial loci in germplasm has improved yields in diverse environments throughout the history of agriculture. An effective new paradigm is the targeted identification of specific genetic determinants of stress adaptation that have evolved in nature and their precise introgression into elite varieties. These loci are often associated with distinct regulation or function, duplication and/or neofunctionalization of genes that maintain plant homeostasis.

Climatic stress and disease management The increasing frequency of debilitating heatwaves , droughts, torrential rains and other weather extremes experienced across the globe negatively affects agricultural productivity, and is projected to do so 1,13 (Fig. 1). Climatic constraints can occur independently or together (as with heat and aridity), and in either case reduce the level of productivity that is predicted for a well-managed environment (the yield potential).

Summary Unanticipated flooding challenges plant growth and fitness in natural and agricultural ecosystems. Here we describe mechanisms of developmental plasticity and metabolic modulation that underpin adaptive traits and acclimation responses to waterlogging of root systems and submergence of aerial tissues. This includes insights into processes that enhance ventilation of submerged organs. At the intersection between metabolism and growth, submergence survival strategies have evolved involving an ethylene‐driven and gibberellin‐enhanced module that regulates growth of submerged organs. Opposing regulation of this pathway is facilitated by a subgroup of ethylene‐response transcription factors (ERFs), which include members that require low O2 or low nitric oxide (NO) conditions for their stabilization. These transcription factors control genes encoding enzymes required for anaerobic metabolism as well as proteins that fine‐tune their function in transcription and turnover. Other mechanisms that control metabolism and growth at seed, seedling and mature stages under flooding conditions are reviewed, as well as findings demonstrating that true endurance of submergence includes an ability to restore growth following the deluge. Finally, we highlight molecular insights obtained from natural variation of domesticated and wild species that occupy different hydrological niches, emphasizing the value of understanding natural flooding survival strategies in efforts to stabilize crop yields in flood‐prone environments.