Possible Roles of Carbohydrate Management and Cytokinin in the Process of Defoliation-Regrowth Cycles in Rice.

Defoliation is an inevitable abiotic stress for forage and turf grasses because harvesting, grazing, and mowing are general processes for their production and management. Vegetative regrowth occurs upon defoliation, a crucial trait determining the productivity and persistence of these grasses. However, the information about the molecular regulation of this trait is limited because it is still challenging to perform molecular analyses in forage and turf grasses. Here, we used rice as a model to investigate vegetative regrowth upon defoliation at physiological and molecular levels. This study analyzed stubble and regrown leaves following periodic defoliation using two rice varieties with contrasting regrowth vigor. Vigorous regrowth was associated with maintained chlorophyll content and photosystem II performance; a restricted and promoted mRNA accumulation of sucrose synthase (SUS) I and III subfamilies, respectively; and reduced enzymatic activity of SUS. These results suggest that critical factors affecting vegetative regrowth upon defoliation are de novo carbohydrate synthesis by newly emerged leaves and proper carbohydrate management in leaves and stubble. Physiological and genetic analyses have demonstrated that the reduced sensitivity to and inhibited biosynthesis of cytokinin enhance regrowth vigor. Proper regulation of these metabolic and hormonal pathways identified in this study can lead to the development of new grass varieties with enhanced regrowth vigor following defoliation.

The submergence tolerance regulator SUB1A differentially coordinates molecular adaptation to submergence in mature and growing leaves of rice (Oryza sativa L.).

A typical adaptive response to submergence regulated by SUB1A, the ethylene-responsive transcription factor gene, is the restricted elongation of the uppermost leaves. However, the molecular and physiological functions of SUB1A have been characterized using entire shoot tissues, most of which are mature leaves that do not elongate under submergence. We aimed to identify leaf-type-specific and overlapping adaptations coordinated in SUB1A-dependent and -independent manners. To this end, we compared the transcriptomic and hormonal responses to submergence between mature and growing leaves using rice genotypes with and without SUB1A. Monosaccharide, branched-chain amino acid, and nucleoside metabolism, associated with ATP synthesis, were commonly activated in both leaf types regardless of genotype. In both leaf types, pathways involved in carbohydrate and nitrogen metabolism were suppressed by SUB1A, with more severe restriction in growing leaves that have a greater energy demand if SUB1A is absent. In growing leaves, accumulation of and responsiveness to growth-regulating hormones were properly modulated by SUB1A, which correlated with restricted elongation. In mature leaves, submergence-induced auxin accumulation was suppressed by SUB1A. This study demonstrates that different sets of hormonal pathways, both of which are modulated by SUB1A, contribute to distinct adaptive responses to submergence in mature and growing rice leaves.

Overlapping and stress-specific transcriptomic and hormonal responses to flooding and drought in soybean.

Flooding and drought are serious constraints that reduce crop productivity worldwide. Previous studies identified genes conferring tolerance to both water extremes in various plants. However, overlapping responses to flooding and drought at the genome-scale remain obscure. Here, we defined overlapping and stress-specific transcriptomic and hormonal responses to submergence, drought and recovery from these stresses in soybean (Glycine max). We performed comparative RNA-sequencing and hormone profiling, identifying genes, hormones and biological processes that are differentially regulated in an overlapping or stress-specific manner. Overlapping responses included positive regulation of trehalose and sucrose metabolism and negative regulation of cellulose, tubulin, photosystem II and I, and chlorophyll biosynthesis, facilitating the economization of energy reserves under both submergence and drought. Additional energy-consuming pathways were restricted in a stress-specific manner. Downregulation of distinct pathways for energy saving under each stress suggests energy-consuming processes that are relatively unnecessary for each stress adaptation are turned down. Our newly developed transcriptomic-response analysis revealed that abscisic acid and ethylene responses were activated in common under both stresses, whereas stimulated auxin response was submergence-specific. The energy-saving strategy is the key overlapping mechanism that underpins adaptation to both submergence and drought in soybean. Abscisic acid and ethylene are candidate hormones that coordinate transcriptomic energy-saving processes under both stresses. Auxin may be a signaling component that distinguishes submergence-specific regulation of the stress response.

A barrier to radial oxygen loss helps the root system cope with waterlogging-induced hypoxia.

Internal aeration is crucial for root growth under waterlogged conditions. Many wetland plants have a structural barrier that impedes oxygen leakage from the basal part of roots called a radial oxygen loss (ROL) barrier. ROL barriers reduce the loss of oxygen transported via the aerenchyma to the root tips, enabling long-distance oxygen transport for cell respiration at the root tip. Because the root tip does not have an ROL barrier, some of the transferred oxygen is released into the waterlogged soil, where it oxidizes and detoxifies toxic substances (e.g., sulfate and Fe2+) around the root tip. ROL barriers are located at the outer part of roots (OPRs). Their main component is thought to be suberin. Suberin deposits may block the entry of potentially toxic compounds in highly reduced soils. The amount of ROL from the roots depends on the strength of the ROL barrier, the length of the roots, and environmental conditions, which causes spatiotemporal changes in the root system's oxidization pattern. We summarize recent achievements in understanding how ROL barrier formation is regulated and discuss opportunities for breeding waterlogging-tolerant crops.

Physiology, gene expression, and metabolome of two wheat cultivars with contrasting submergence tolerance.

Responses of wheat (Triticum aestivum) to complete submergence are not well understood as research has focused on waterlogging (soil flooding). The aim of this study was to characterize the responses of 2 wheat cultivars differing vastly in submergence tolerance to test if submergence tolerance was linked to shoot carbohydrate consumption as seen in rice. Eighteen-day-old wheat cultivars Frument (intolerant) and Jackson (tolerant) grown in soil were completely submerged for up to 19 days while assessing responses in physiology, gene expression, and shoot metabolome. Results revealed 50% mortality after 9.3 and 15.9 days of submergence in intolerant Frument and tolerant Jackson, respectively, and significantly higher growth in Jackson during recovery. Frument displayed faster leaf degradation as evident from leaf tissue porosity, chlorophylla , and metabolomic fingerprinting. Surprisingly, shoot soluble carbohydrates, starch, and individual sugars declined to similarly low levels in both cultivars by day 5, showing that cultivar Jackson tolerated longer periods of low shoot carbohydrate levels than Frument. Moreover, intolerant Frument showed higher levels of phytol and the lipid peroxidation marker malondialdehyde relative to tolerant Jackson. Consequently, we propose to further investigate the role of ethylene sensitivity and deprivation of reactive O2 species in submerged wheat.

Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants.

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 roots becoming waterlogged or foliage submergence, triggers changes in gene transcription and messenger RNA translation that promote anaerobic metabolism and thus sustain substrate-level ATP production. In contrast to animals, 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 levels 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 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 amino terminus initiating with Met-Cys. 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 rice, was shown not to be a substrate for the N-end rule pathway despite containing the N-terminal motif, indicating 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 stresses.

The key regulator of submergence tolerance, SUB1A, promotes photosynthetic and metabolic recovery from submergence damage in rice leaves.

The submergence-tolerance regulator, SUBMERGENCE1A (SUB1A), of rice (Oryza sativa L.) modulates gene regulation, metabolism and elongation growth during submergence. Its benefits continue during desubmergence through protection from reactive oxygen species and dehydration, but there is limited understanding of SUB1A's role in physiological recovery from the stress. Here, we investigated the contribution of SUB1A to desubmergence recovery using the two near-isogenic lines, submergence-sensitive M202 and tolerant M202(Sub1). No visible damage was detected in the two genotypes after 3 d of submergence, but the sublethal stress differentially altered photosynthetic parameters and accumulation of energy reserves. Submergence inhibited photosystem II photochemistry and stimulated breakdown of protein and accumulation of several amino acids in both genotypes at similar levels. Upon desubmergence, however, more rapid return to homeostasis of these factors was observed in M202(Sub1). Submergence considerably restrained non-photochemical quenching (NPQ) in M202, whereas the value was unaltered in M202(Sub1) during the stress. Upon reaeration, submerged plants encounter sudden exposure to higher light. A greater capability for NPQ-mediated photoprotection can benefit the rapid recovery of photosynthetic performance and energy reserve metabolism in M202(Sub1). Our findings illuminate the significant role of SUB1A in active physiological recovery upon desubmergence, a component of enhanced tolerance to submergence.

Plant Adaptation to Multiple Stresses during Submergence and Following Desubmergence.

Plants require water for growth and development, but excessive water negatively affects their productivity and viability. Flash floods occasionally result in complete submergence of plants in agricultural and natural ecosystems. When immersed in water, plants encounter multiple stresses including low oxygen, low light, nutrient deficiency, and high risk of infection. As floodwaters subside, submerged plants are abruptly exposed to higher oxygen concentration and greater light intensity, which can induce post-submergence injury caused by oxidative stress, high light, and dehydration. Recent studies have emphasized the significance of multiple stress tolerance in the survival of submergence and prompt recovery following desubmergence. A mechanistic understanding of acclimation responses to submergence at molecular and physiological levels can contribute to the deciphering of the regulatory networks governing tolerance to other environmental stresses that occur simultaneously or sequentially in the natural progress of a flood event.

Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings.

Complete inundation at the early seedling stage is a common environmental constraint for soybean production throughout the world. As floodwaters subside, submerged seedlings are subsequently exposed to reoxygenation stress in the natural progression of a flood event. Here, we characterized the fundamental acclimation responses to submergence and reoxygenation in soybean at the seedling establishment stage. Approximately 90% of seedlings succumbed during 3 d of inundation under constant darkness, whereas 10 d of submergence were lethal to over 90% of seedlings under 12 h light/12 h dark cycles, indicating the significance of underwater photosynthesis in seedling survival. Submergence rapidly decreased the abundance of carbohydrate reserves and ATP in aerial tissue of seedlings although chlorophyll breakdown was not observed. The carbohydrate and ATP contents were recovered upon de-submergence, but sudden exposure to oxygen also induced lipid peroxidation, confirming that reoxygenation induced oxidative stress. Whole transcriptome analysis recognized genome-scale reconfiguration of gene expression that regulates various signalling and metabolic pathways under submergence and reoxygenation. Comparative analysis of differentially regulated genes in shoots and roots of soybean and other plants defines conserved, organ-specific and species-specific adjustments which enhance adaptability to submergence and reoxygenation through different metabolic pathways.

The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice.

Submergence and drought are major constraints to rice (Oryza sativa) production in rain-fed farmlands, both of which can occur sequentially during a single crop cycle. SUB1A, an ERF transcription factor found in limited rice accessions, dampens ethylene production and gibberellic acid responsiveness during submergence, economizing carbohydrate reserves and significantly prolonging endurance. Here, we evaluated the functional role of SUB1A in acclimation to dehydration. Comparative analysis of genotypes with and without SUB1A revealed that SUB1A enhanced recovery from drought at the vegetative stage through reduction of leaf water loss and lipid peroxidation and increased expression of genes associated with acclimation to dehydration. Overexpression of SUB1A augmented ABA responsiveness, thereby activating stress-inducible gene expression. Paradoxically, vegetative tissue undergoes dehydration upon desubmergence even though the soil contains sufficient water, indicating that leaf desiccation occurs in the natural progression of a flooding event. Desubmergence caused the upregulation of gene transcripts associated with acclimation to dehydration, with higher induction in SUB1A genotypes. SUB1A also restrained accumulation of reactive oxygen species (ROS) in aerial tissue during drought and desubmergence. Consistently, SUB1A increased the abundance of transcripts encoding ROS scavenging enzymes, resulting in enhanced tolerance to oxidative stress. Therefore, in addition to providing robust submergence tolerance, SUB1A improves survival of rapid dehydration following desubmergence and water deficit during drought.

Comparison of GC-MS and NMR for metabolite profiling of rice subjected to submergence stress.

Natural disasters such as drought, extreme temperatures, and flooding can severely impact crop production. Understanding the metabolic response of crops threatened with these disasters provides insights into biological response mechanisms that can influence survival. In this study, a comparative analysis of GC-MS and (1)H NMR results was conducted for wild-type and tolerant rice varieties stressed by up to 3 days of submergence and allowed 1 day of postsubmergence recovery. Most metabolomics studies are conducted using a single analytical platform. Each platform, however, has inherent advantages and disadvantages that can influence the analytical coverage of the metabolome. In this work, a more thorough analysis of the plant stress response was possible through the use of both (1)H NMR and GC-MS. Several metabolites, such as S-methyl methionine and the dipeptide alanylglycine, were only detected and quantified by (1)H NMR. The high dynamic range of NMR, as compared with that of the GC-TOF-MS used in this study, provided broad coverage of the metabolome in a single experiment. The sensitivity of GC-MS facilitated the quantitation of sugars, organic acids, and amino acids, some of which were not detected by NMR, and provided additional insights into the regulation of the TCA cycle. The combined metabolic information provided by (1)H NMR and GC-MS was essential for understanding the complex biochemical and molecular response of rice plants to submergence.

SUB1A-dependent and -independent mechanisms are involved in the flooding tolerance of wild rice species.

Crop tolerance to flooding is an important agronomic trait. Although rice (Oryza sativa) is considered a flood-tolerant crop, only limited cultivars display tolerance to prolonged submergence, which is largely attributed to the presence of the SUB1A gene. Wild Oryza species have the potential to unveil adaptive mechanisms and shed light on the basis of submergence tolerance traits. In this study, we screened 109 Oryza genotypes belonging to different rice genome groups for flooding tolerance. Oryza nivara and Oryza rufipogon accessions, belonging to the A-genome group, together with Oryza sativa, showed a wide range of submergence responses, and the tolerance-related SUB1A-1 and the intolerance-related SUB1A-2 alleles were found in tolerant and sensitive accessions, respectively. Flooding-tolerant accessions of Oryza rhizomatis and Oryza eichingeri, belonging to the C-genome group, were also identified. Interestingly, SUB1A was absent in these species, which possess a SUB1 orthologue with high similarity to O. sativa SUB1C. The expression patterns of submergence-induced genes in these rice genotypes indicated limited induction of anaerobic genes, with classical anaerobic proteins poorly induced in O. rhizomatis under submergence. The results indicated that SUB1A-1 is not essential to confer submergence tolerance in the wild rice genotypes belonging to the C-genome group, which show instead a SUB1A-independent response to submergence.

The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice.

Leaf senescence is a natural age-dependent process that is induced prematurely by various environmental stresses. Typical alterations during leaf senescence include breakdown of chlorophyll, a shift to catabolism of energy reserves, and induction of senescence-associated genes, all of which can occur during submergence, drought, and constant darkness. Here, we evaluated the influence of the submergence tolerance regulator, SUBMERGENCE1A (SUB1A), in the acclimation responses during leaf senescence caused by prolonged darkness in rice (Oryza sativa). SUB1A messenger RNA was highly induced by prolonged darkness in a near-isogenic line containing SUB1A. Genotypes with conditional and ectopic overexpression of SUB1A significantly delayed loss of leaf color and enhanced recovery from dark stress. Physiological analysis revealed that SUB1A postpones dark-induced senescence through the maintenance of chlorophyll and carbohydrate reserves in photosynthetic tissue. This delay allowed leaves of SUB1A genotypes to recover photosynthetic activity more quickly upon reexposure to light. SUB1A also restricted the transcript accumulation of representative senescence-associated genes. Jasmonate and salicylic acid are positive regulators of leaf senescence, but ectopic overexpression of SUB1A dampened responsiveness to both hormones in the context of senescence. We found that ethylene accelerated senescence stimulated by darkness and jasmonate, although SUB1A significantly restrained dark-induced ethylene accumulation. Overall, SUB1A genotypes displayed altered responses to prolonged darkness by limiting ethylene production and responsiveness to jasmonate and salicylic acid, thereby dampening the breakdown of chlorophyll, carbohydrates, and the accumulation of senescence-associated messenger RNAs. A delay of leaf senescence conferred by SUB1A can contribute to the enhancement of tolerance to submergence, drought, and oxidative stress.

The Impact of Carbohydrate Management on Coleoptile Elongation in Anaerobically Germinating Seeds of Rice (Oryza sativa L.) under Light and Dark Cycles.

The ability of rice to elongate coleoptiles under oxygen deprivation is a determinant of anaerobic germination tolerance, critical for successful direct seeding. Most studies on anaerobic coleoptile elongation have been performed under constant darkness or in flooded soils because a drilling method was the primary approach for direct seeding of rice. However, aerial seeding is becoming popular, in which seeds which land on flooded soils are exposed to light during the daytime. Here, we investigated physiological mechanisms underlying anaerobic elongation of coleoptiles under light and dark cycles. This study identified two novel varieties, LG and L202, enabling the development of long coleoptiles under oxygen limitation, comparable to well-characterized varieties with strong anaerobic germination tolerance. Germination experiments using these two tolerant and two intolerant varieties, including Takanari and IR64, revealed that light and dark cycles increased coleoptile length in LG, Takanari, and IR64 relative to constant darkness. Interestingly, even in intolerant lines, dramatic starch breakdown and soluble carbohydrate accumulation occurred under oxygen limitation. However, intolerant lines were more susceptible to a representative soluble sugar, glucose, than tolerant lines under oxygen deprivation, suggesting that coleoptile growth can be inhibited in intolerant lines due to hypersensitivity to soluble sugars accumulated in anaerobically germinating seeds.

Differential metabolic regulation governed by the rice SUB1A gene during submergence stress and identification of alanylglycine by 1H NMR spectroscopy.

Although the genetic mechanism of submergence survival for rice varieties containing the SUB1A gene has been elucidated, the downstream metabolic effects have not yet been evaluated. In this study, the metabolomes of Oryza sativa ssp. japonica cv. M202 and cv. M202(Sub1) were profiled using (1)H NMR spectroscopy to compare the metabolic effect of submergence stress and recovery on rice in the presence or absence of SUB1A. Significant changes were observed in the NMR resonances of compounds in pathways important for carbohydrate metabolism. The presence of SUB1A in M202(Sub1) was correlated with suppression of carbohydrate metabolism in shoot tissue, consistent with the role of SUB1A in limiting starch catabolism to fuel elongation growth. The absence of SUB1A in M202 was correlated with greater consumption of sucrose stores and accumulation of amino acids that are synthesized from glycolysis intermediates and pyruvate. Under submergence conditions, alanine, a product of pyruvate metabolism, showed the largest difference between the two varieties, but elevated levels of glutamine, glutamate, leucine, isoleucine, threonine, and valine were also higher in M202 compared with the M202(Sub1) variety. The identification and characterization of alanylglycine (AlaGly) in rice is also reported. After 3 days of submergence stress, AlaGly levels decreased significantly in both genotypes but did not recover within 1 day of desubmergence with the other metabolites evaluated. The influence of SUB1A on dynamic changes in the metabolome during complete submergence provides new insights into the functional roles of a single gene in invoking a quiescence strategy that helps stabilize crop production in submergence-prone fields.

Expression of rice SUB1A and SUB1C transcription factors in Arabidopsis uncovers flowering inhibition as a submergence tolerance mechanism.

Submergence of plant organs perturbs homeostasis by limiting diffusion of oxygen, carbon dioxide and ethylene. In rice (Oryza sativa L.), the haplotype at the multigenic SUBMERGENCE1 (SUB1) locus determines whether plants survive prolonged submergence. SUB1 encodes two or three transcription factors of the group VII ethylene response factor family: SUB1A, SUB1B and SUB1C. The presence of SUB1A-1 and its strong submergence-triggered ethylene-mediated induction confers submergence tolerance through a quiescence survival strategy that inhibits gibberellin (GA)-induced carbohydrate consumption and elongation growth. SUB1C is invariably present and acts downstream of the enhancement of GA responsiveness during submergence. In this study, heterologous ectopic expression of rice SUB1A and SUB1C in Arabidopsis thaliana was used to explore conserved mechanisms of action associated with these genes using developmental, physiological and molecular metrics. As in rice transgenic plants that ectopically express SUB1A-1, Arabidopsis transgenic plants that constitutively express SUB1A displayed GA insensitivity and abscisic acid hypersensitivity. Ectopic SUB1C expression had more limited effects on development, stress responses and the transcriptome. Observation of a delayed flowering phenotype in lines over-expressing SUB1A led to the finding that inhibition of floral initiation is a component of the quiescence survival strategy in rice. Together, these analyses demonstrate conserved as well as specific roles for group VII ethylene response factors in integration of abiotic responses with development.

Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice.

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.

Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater.

Submergence during germination impedes aerobic metabolisms and limits the growth of most higher plants. However, some wetland plants including rice can germinate under submerged conditions. It has long been hypothesized that the first elongating shoot tissue, the coleoptile, acts as a snorkel to acquire atmospheric oxygen (O2) to initiate the first leaf elongation and seminal root emergence. Here, we obtained direct evidence for this hypothesis by visualizing the spatiotemporal O2 dynamics during submerged germination in rice using a planar O2 optode system. In parallel with the O2 imaging, we tracked the anatomical development of shoot and root tissues in real-time using an automated flatbed scanner. Three hours after the coleoptile tip reached the water surface, O2 levels around the embryo transiently increased. At this time, the activity of alcohol dehydrogenase (ADH), an enzyme critical for anaerobic metabolism, was significantly reduced, and the coleorhiza covering the seminal roots in the embryo was broken. Approximately 10 h after the transient burst in O2, seminal roots emerged. A transient O2 burst around the embryo was shown to be essential for seminal root emergence during submerged rice germination. The parallel application of a planar O2 optode system and automated scanning system can be a powerful tool for examining how environmental conditions affect germination in rice and other plants.

Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses.

High-throughput technology has facilitated genome-scale analyses of transcriptomic adjustments in response to environmental perturbations with an oxygen deprivation component, such as transient hypoxia or anoxia, root waterlogging, or complete submergence. We showed previously that Arabidopsis (Arabidopsis thaliana) seedlings elevate the levels of hundreds of transcripts, including a core group of 49 genes that are prioritized for translation across cell types of both shoots and roots. To recognize low-oxygen responses that are evolutionarily conserved versus species specific, we compared the transcriptomic reconfiguration in 21 organisms from four kingdoms (Plantae, Animalia, Fungi, and Bacteria). Sorting of organism proteomes into clusters of putative orthologs identified broadly conserved responses associated with glycolysis, fermentation, alternative respiration, metabolite transport, reactive oxygen species amelioration, chaperone activity, and ribosome biogenesis. Differentially regulated genes involved in signaling and transcriptional regulation were poorly conserved across kingdoms. Strikingly, nearly half of the induced mRNAs of Arabidopsis seedlings encode proteins of unknown function, of which over 40% had up-regulated orthologs in poplar (Populus trichocarpa), rice (Oryza sativa), or Chlamydomonas reinhardtii. Sixteen HYPOXIA-RESPONSIVE UNKNOWN PROTEIN (HUP) genes, including four that are Arabidopsis specific, were ectopically overexpressed and evaluated for their effect on seedling tolerance to oxygen deprivation. This allowed the identification of HUPs coregulated with genes associated with anaerobic metabolism and other processes that significantly enhance or reduce stress survival when ectopically overexpressed. These findings illuminate both broadly conserved and plant-specific low-oxygen stress responses and confirm that plant-specific HUPs with limited phylogenetic distribution influence low-oxygen stress endurance.