Summary
Amphibious plants thrive in areas with fluctuating water levels, partly as a result of their capacity to make specialized leaves when submerged or emerged. The tailor‐made leaves improve gas ...exchange underwater or prevent aerial desiccation. Aquatic leaves are thin with narrow or dissected forms, thin cuticles and fewer stomata. These traits can combine with carbon‐concentrating mechanisms and various inorganic carbon utilization strategies. Signalling networks underlying this plasticity include conserved players like abscisic acid and ethylene, but closer inspection reveals greater variation in regulatory behaviours. Moreover, it seems that amphibious leaf development overrides and reverses conserved signalling pathways of their terrestrial counterparts. The diversity of physiology and signalling makes plant amphibians particularly attractive for gaining insights into the evolution of signalling and crop improvement.
See also the Editorial on this article by Sasidharan et al., 229: 5–7.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
Summary
The molecular mechanisms controlling underwater elongation are based extensively on studies on internode elongation in the monocot rice (Oryza sativa) and petiole elongation in Rumex rosette ...species. Here, we characterize underwater growth in the dicot Nasturtium officinale (watercress), a wild species of the Brassicaceae family, in which submergence enhances stem elongation and suppresses petiole growth.
We used a genome‐wide transcriptome analysis to identify the molecular mechanisms underlying the observed antithetical growth responses. Though submergence caused a substantial reconfiguration of the petiole and stem transcriptome, only little qualitative differences were observed between both tissues. A core submergence response included hormonal regulation and metabolic readjustment for energy conservation, whereas tissue‐specific responses were associated with defense, photosynthesis, and cell wall polysaccharides.
Transcriptomic and physiological characterization suggested that the established ethylene, abscisic acid (ABA), and GA growth regulatory module for underwater elongation could not fully explain underwater growth in watercress.
Petiole growth suppression is likely attributed to a cell cycle arrest. Underwater stem elongation is driven by an early decline in ABA and is not primarily mediated by ethylene or GA. An enhanced stem elongation observed in the night period was not linked to hypoxia and suggests an involvement of circadian regulation.
See also the Editorial on this article by Sasidharan et al., 229: 5–7.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, ...limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.
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Plants growing at high densities elongate their shoots to reach for light, a response known as the shade avoidance syndrome (SAS). Phytochrome-mediated detection of far-red light reflection from ...neighboring plants activates growth-promoting molecular pathways leading to SAS. However, it is unknown how plants that complete their life cycle in the forest understory and are shade tolerant prevent SAS when exposed to shade. Here, we show how two wild Geranium species from different native light environments regulate contrasting responses to light quality cues. A comparative RNA sequencing approach unveiled the molecular underpinnings of their contrasting growth responses to far-red light enrichment. It also identified differential phytochrome control of plant immunity genes and confirmed that far-red enrichment indeed contrastingly affects resistance against Botrytis cinerea between the two species. Furthermore, we identify a number of candidate regulators of differential shade avoidance. Three of these, the receptor-like kinases FERONIA and THESEUS1 and the non-DNA binding bHLH protein KIDARI, are functionally validated in Arabidopsis thaliana through gene knockout and/or overexpression studies. We propose that these components may be associated with either showing or not showing shade avoidance responses.
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Plants use light as a resource and signal. Photons within the 400–700 nm waveband are considered photosynthetically active. Far‐red photons (FR, 700–800 nm) are used by plants to detect nearby ...vegetation and elicit the shade avoidance syndrome. In addition, FR photons have also been shown to contribute to photosynthesis, but knowledge about these dual effects remains scarce. Here, we study shoot‐architectural and photosynthetic responses to supplemental FR light during the photoperiod in several rice varieties. We observed that FR enrichment only mildly affected the rice transcriptome and shoot architecture as compared to established model species, whereas leaf formation, tillering and biomass accumulation were clearly promoted. Consistent with this growth promotion, we found that CO2‐fixation in supplemental FR was strongly enhanced, especially in plants acclimated to FR‐enriched conditions as compared to control conditions. This growth promotion dominates the effects of FR photons on shoot development and architecture. When substituting FR enrichment with an end‐of‐day FR pulse, this prevented photosynthesis‐promoting effects and elicited shade avoidance responses. We conclude that FR photons can have a dual role, where effects depend on the environmental context: in addition to being an environmental signal, they are also a potent source of harvestable energy.
Summary statement
The ratio of red: far‐red (FR) light is monitored by phytochrome photoreceptors as a cue for neighbour proximity, and a drop in this ratio plants elicit so‐called shade avoidance responses. Here we show in a number of rice varieties that FR enrichment triggers only marginal shade avoidance but contributes significantly to leaf‐level photosynthesis and whole‐plant biomass accumulation.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
Flooding events negatively affect plant performance and survival. Flooding gradients thereby determine the dynamics in vegetation composition and species abundance. In adaptation to flooding, the ...group VII Ethylene Response Factor genes (ERF‐VIIs) play pivotal roles in rice and Arabidopsis through regulation of anaerobic gene expression and antithetical survival strategies. We investigated if ERF‐VIIs have a similar role in mediating survival strategies in eudicot species from flood‐prone environments. Here, we studied the evolutionary origin and regulation of ERF‐VII transcript abundance and the physiological responses in species from two genera of divergent taxonomic lineages (Rumex and Rorippa). Synteny analysis revealed that angiosperm ERF‐VIIs arose from two ancestral loci and that subsequent diversification and duplication led to the present ERF‐VII variation. We propose that subtle variation in the regulation of ERF‐VII transcript abundance could explain variation in tolerance among Rorippa species. In Rumex, the main difference in flood tolerance correlated with the genetic variation in ERF‐VII genes. Large transcriptional differences were found by comparing the two genera: darkness and dark submergence‐induced Rumex ERF‐VIIs, whereas HRE2 expression was increased in submerged Rorippa roots. We conclude that the involvement of ERF‐VIIs in flooding tolerance developed in a phylogenetic‐dependent manner, with subtle variations within taxonomic clades.
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Flooding is detrimental for nearly all higher plants, including crops. The compound stress elicited by slow gas exchange and low light levels under water is responsible for both a carbon and an ...energy crisis ultimately leading to plant death. The endogenous concentrations of four gaseous compounds, oxygen, carbon dioxide, ethylene, and nitric oxide, change during the submergence of plant organs in water. These gases play a pivotal role in signal transduction cascades, leading to adaptive processes such as metabolic adjustments and anatomical features. Of these gases, ethylene is seen as the most consistent, pervasive, and reliable signal of early flooding stress, most likely in tight interaction with the other gases. The production of reactive oxygen species (ROS) in plant cells during flooding and directly after subsidence, during which the plant is confronted with high light and oxygen levels, is characteristic for this abiotic stress. Low, well-controlled levels of ROS are essential for adaptive signaling pathways, in interaction with the other gaseous flooding signals. On the other hand, excessive uncontrolled bursts of ROS can be highly damaging for plants. Therefore, a fine-tuned balance is important, with a major role for ROS production and scavenging. Our understanding of the temporal dynamics of the four gases and ROS is basal, whereas it is likely that they form a signature readout of prevailing flooding conditions and subsequent adaptive responses.
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Timely perception of adverse environmental changes is critical for survival. Dynamic changes in gases are important cues for plants to sense environmental perturbations, such as submergence. In ...Arabidopsis thaliana, changes in oxygen and nitric oxide (NO) control the stability of ERFVII transcription factors. ERFVII proteolysis is regulated by the N-degron pathway and mediates adaptation to flooding-induced hypoxia. However, how plants detect and transduce early submergence signals remains elusive. Here we show that plants can rapidly detect submergence through passive ethylene entrapment and use this signal to pre-adapt to impending hypoxia. Ethylene can enhance ERFVII stability prior to hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO depletion and consequent ERFVII accumulation pre-adapts plants to survive subsequent hypoxia. Our results reveal the biological link between three gaseous signals for the regulation of flooding survival and identifies key regulatory targets for early stress perception that could be pivotal for developing flood-tolerant crops.
Limited aeration that is caused by tissue geometry, diffusion barriers, high elevation, or a flooding event poses major challenges to plants and is often, but not exclusively, associated with low ...oxygen. These processes span a broad interest in the research community ranging from whole plant and crop responses, post‐harvest physiology, plant morphology and anatomy, fermentative metabolism, plant developmental processes, oxygen sensing by ERF‐VIIs, gene expression profiles, the gaseous hormone ethylene, and O2 dynamics at cellular resolution. The International Society for Plant Anaerobiosis (ISPA) gathers researchers from all over the world contributing to understand the causes, responses, and consequences of limited aeration in plants. During the 14th ISPA meeting, major research progress was related to the evolution of O2 sensing mechanisms and the intricate network that balances low O2 signaling. Here, the work moved beyond flooding stress and emphasized novel underexplored roles of low O2 and limited aeration in altitude adaptation, fruit development and storage, and the vegetative development of growth apices. Regarding tolerance towards flooding, the meeting stressed the relevance and regulation of developmental plasticity, aerenchyma, and barrier formation to improve internal aeration. Additional newly explored flood tolerance traits concerned resource balance, senescence, and the exploration of natural genetic variation for novel tolerance loci. In this report, we summarize and synthesize the major progress and future challenges for low O2 and aeration research presented at the conference.
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