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Authors: Chiara Pucciariello and Pierdomenico Perata.
Journal of Experimental Botany (2024)
Abstract: "Plant quiescence and seed dormancy can be triggered by reduced oxygen availability. Under water, oxygen depletion caused by flooding can culminate in a quiescent state, which is a plant strategy for energy preservation and survival. In adult plants, a quiescent state can be activated by sugar starvation, culminating in metabolic depression. In seeds, secondary dormancy can be activated by reduced oxygen availability, which creates an unfavourable state for germination. The physical dormancy of some seeds and buds includes barriers to external conditions, which indirectly results in hypoxia. The molecular processes that support seed dormancy and plant survival through quiescence under hypoxia include the N-degron pathway, which enables the modulation of ethylene responsive factors of group VII and downstream targets. This oxygen- and nitric oxide-dependent mechanism interacts with phytohormone-related pathways to control growth."
Authors: Yukang Wang, Gaochen Jin, Shuyan Song, Yijun Jin, Xiaowen Wang, Shuaiqi Yang, Xingxing Shen, Yinbo Gan, Yuexing Wang, Ran Li, Jian-Xiang Liu, Jianping Hu and Ronghui Pan.
Developmental Cell (2024)
Editor's view: Wang et al. demonstrated a peroxisomal cinnamate:CoA ligase (CNL)-dependent phytohormone metabolic cascade in rice. Submerged imbibition-induced salicylic acid (SA) biosynthesis promotes anaerobic germination by inducing OsGH3-mediated indole-acetic acid (IAA)-amino acid conjugation, thus releasing IAA’s inhibition of germination under water submergence conditions.
Highlights: • OsCNLs are induced in rice submerged imbibition to synthesize salicylic acid (SA) • Peroxisomal OsCNLs are key enzymes in the SA biosynthetic pathway in rice • SA promotes submerged germination via OsGH3-mediated indole-acetic acid catabolism • SA pretreatment is a cost-effective strategy to improve rice submerged germination
Abstract: "The mechanism underlying the ability of rice to germinate underwater is a largely enigmatic but key research question highly relevant to rice cultivation. Moreover, although rice is known to accumulate salicylic acid (SA), SA biosynthesis is poorly defined, and its role in underwater germination is unknown. It is also unclear whether peroxisomes, organelles essential to oilseed germination and rice SA accumulation, play a role in rice germination. Here, we show that submerged imbibition of rice seeds induces SA accumulation to promote germination in submergence. Two submergence-induced peroxisomal Oryza sativa cinnamate:CoA ligases (OsCNLs) are required for this SA accumulation. SA exerts this germination-promoting function by inducing indole-acetic acid (IAA) catabolism through the IAA-amino acid conjugating enzyme GH3. The metabolic cascade we identified may potentially be adopted in agriculture to improve the underwater germination of submergence-intolerant rice varieties. SA pretreatment is also a promising strategy to improve submerged rice germination in the field."
Authors: Alice Diot, Georg Groth, Simon Blanchet and Christian Chervin.
The FEBS Journal (2024)
Summary: Our viewpoint is that ethanol, at cellular levels (μm), could act as a molecular messenger in animal and plant organisms, during hypoxic or other stressful conditions. We list studies showing the changes generated by small amounts of ethanol, possibly present in animals and plants. We highlight potential mechanisms by which ethanol may be sensed, particularly at the cell membrane level, by modifying protein signals.
Abstract: "Our viewpoint is that ethanol could act as a molecular messenger in animal and plant organisms under conditions of hypoxia or other stresses and could elicit physiological responses to such conditions. There is evidence that both animal and plant organisms have endogenous levels of ethanol, but reports on the changes induced by this alcohol at physiological levels are sparse. Studies have shown that ethanol has different effects on cell metabolism at low and high concentrations, resembling a hormetic response. Further studies have addressed the potential cellular and molecular mechanisms used by organisms to sense changes in physiological concentrations of ethanol. This article summarizes the possible mechanisms by which ethanol may be sensed, particularly at the cell membrane level. Our analysis shows that current knowledge on this subject is limited. More research is required on the effects of ethanol at very low doses, in plants and animals at both molecular and physiological levels. We believe that further research on this topic could lead to new discoveries in physiology and may even help us understand metabolic adjustments related to climate change. As temperatures rise more frequently, dissolved oxygen levels drop, leading to hypoxic conditions and consequently, an increase in cellular ethanol levels."
Authors: Petar Mohorović, Batist Geldhof, Kristof Holsteens, Marilien Rinia, Johan Ceusters and Bram Van de Poel.
Plant Direct (2023)
Abstract: "Salinity, drought, and waterlogging are common environmental stresses that negatively impact plant growth, development, and productivity. One of the responses to abiotic stresses is the production of the phytohormone ethylene, which induces different coping mechanisms that help plants resist or tolerate stress. In this study, we investigated if an ethylene pretreatment can aid plants in activating stress-coping responses prior to the onset of salt, drought, and waterlogging stress. Therefore, we measured real-time transpiration and CO2 assimilation rates and the impact on biomass during and after 3 days of abiotic stress. Our results showed that an ethylene pretreatment of 1 ppm for 4 h did not significantly influence the negative effects of waterlogging stress, while plants were more sensitive to salt stress as reflected by enhanced water losses due to a higher transpiration rate. However, when exposed to drought stress, an ethylene pretreatment resulted in reduced transpiration rates, reducing water loss during drought stress. Overall, our findings indicate that pretreating tomato plants with ethylene can potentially regulate their responses during the forthcoming stress period, but optimization of the ethylene pre-treatment duration, timing, and dose is needed. Furthermore, it remains tested if the effect is related to the stress duration and severity and whether an ethylene pretreatment has a net positive or negative effect on plant vigor during stress recovery. Further investigations are needed to elucidate the mode of action of how ethylene priming impacts subsequent stress responses."
Authors: B. Geldhof, O. Novák and B. Van de Poel.
Journal of Experimental Botany (2024)
Abstract: "Waterlogging leads to hypoxic conditions in the root zone that subsequently cause systemic adaptive responses in the shoot, including leaf epinasty. Waterlogging-induced epinasty in tomato has long been ascribed to the coordinated action of ethylene and auxins. However, other hormonal signals have largely been neglected, despite evidence of their importance in leaf posture control. To cover a large group of growth regulators, we performed a tissue-specific and time-dependent hormonomics analysis. This revealed that multiple hormones are differentially affected throughout a 48 h waterlogging treatment, and that leaf age determines hormone homeostasis and gates their changes during waterlogging. In addition, we distinguished early hormonal signals that contribute to fast responses towards oxygen deprivation from those that potentially sustain the waterlogging response. We found that abscisic acid (ABA) levels peak in petioles within the first 12 h of the treatment, while its precursors only rise much later, suggesting ABA transport is altered. At the same time, cytokinins (CK) and their derivatives drastically decline during waterlogging in leaves of all ages. This drop in CK possibly releases the inhibition of ethylene and auxin mediated cell elongation to establish epinastic bending. Auxins themselves rise substantially in the petiole of mature leaves, but mostly after 48 h of root hypoxia. Based on our hormone profiling, we propose that ethylene and ABA might act synergistically as an early signal to induce epinasty, while the balance of IAA and CK in the petiole ultimately regulates differential growth."
Authors: Lu Yang, Na Li, Yang Liu, Pengfei Miao, Ji Liu, and Zhi Wang.
Agronomy (2023)
Abstract: "With the frequent occurrence of extreme weather such as typhoons and rainstorms, waterlogging has become one of the most important threats to global crop growth and production. Waterlogging limits plants’ access to oxygen and light, leading to disadvantageous changes in metabolism to disturb plant growth and development. To escape the damage of hypoxia or promote the diffusion of oxygen to submerged organs, plants respond to waterlogging stress by regulating their morphological structure, photosynthesis, respiration, energy metabolism, and endogenous plant hormone biosynthesis/signal transduction. The adventitious roots (AR), aerenchyma, and stem internode are the major target structure for waterlogging adaptation. The molecular mechanism of crop survival under waterlogging conditions and the key genes related photosynthesis, reactive oxygen species (ROS) homeostasis, and ethylene signal transduction are reviewed. We also elucidated recent advances in the study of interactions between various regulatory pathways and emphasized the important role of stress memory and cross-stress mechanisms in plant response to abiotic stress, indicating the importance of epigenetic modifications. On the basis of above, the research direction and focus of plants coping with waterlogging stress in the future are proposed. This review provides rich genetic resources and a theoretical basis for improving the genetic breeding of crop resistance to waterlogging."
Authors: Mohammed M. Mira, Eman A. El-Khateeb, Mohamed S. Youssef, Katarzyna Ciacka, Kenny So, Robert W. Duncan, Robert D. Hill and Claudio Stasolla.
Planta (2023)
Main conclusion: Over-expression of phytoglobin mitigates the degradation of the root apical meristem (RAM) caused by waterlogging through changes in nitric oxide and auxin distribution at the root tip.
Abstract: "Plant performance to waterlogging is ameliorated by the over-expression of the Arabidopsis Phytoglobin 1 (Pgb1) which also contributes to the maintenance of a functional RAM. Hypoxia induces accumulation of ROS and damage in roots of wild type plants; these events were preceded by the exhaustion of the RAM resulting from the loss of functionality of the WOX5-expressing quiescent cells (QCs). These phenotypic deviations were exacerbated by suppression of Pgb1 and attenuated when the same gene was up-regulated. Genetic and pharmacological studies demonstrated that degradation of the RAM in hypoxic roots is attributed to a reduction in the auxin maximum at the root tip, necessary for the specification of the QC. This reduction was primarily caused by alterations in PIN-mediated auxin flow but not auxin synthesis. The expression and localization patterns of several PINs, including PIN1, 2, 3 and 4, facilitating the basipetal translocation of auxin and its distribution at the root tip, were altered in hypoxic WT and Pgb1-suppressing roots but mostly unchanged in those over-expressing Pgb1. Disruption of PIN1 and PIN2 signal in hypoxic roots suppressing Pgb1 initiated in the transition zone at 12 h and was specifically associated to the absence of Pgb1 protein in the same region. Exogenous auxin restored a functional RAM, while inhibition of the directional auxin flow exacerbated the degradation of the RAM. The regulation of root behavior by Pgb1 was mediated by nitric oxide (NO) in a model consistent with the recognized function of Pgbs as NO scavengers. Collectively, this study contributes to our understanding of the role of Pgbs in preserving root meristem function and QC niche during conditions of stress, and suggests that the root transition zone is most vulnerable to hypoxia.
Authors: Elena Loreti and Pierdomenico Perata.
Frontiers in Genetics (2023)
Abstract: "In this review, we focus on ethylene transcription factors (ERFs), which are a crucial family of transcription factors that regulate plant development and stress responses. ERFVII transcription factors have been identified and studied in several crop species, including rice, wheat, maize, barley, and soybean. These transcription factors are known to be involved in regulating the plant’s response to low oxygen stress—hypoxia and could thus improve crop yields under suboptimal growing conditions. In rice (Oryza sativa) several ERFVII genes have been identified and characterized, including SUBMERGENCE 1A (SUB1A), which enables rice to tolerate submergence. The SUB1A gene was used in the development of SUB1 rice varieties, which are now widely grown in flood-prone areas and have been shown to improve yields and farmer livelihoods. The oxygen sensor in plants was discovered using the model plant Arabidopsis. The mechanism is based on the destabilization of ERFVII protein via the N-degron pathway under aerobic conditions. During hypoxia, the stabilized ERFVIIs translocate to the nucleus where they activate the transcription of hypoxia-responsive genes (HRGs). In summary, the identification and characterization of ERFVII transcription factors and their mechanism of action could lead to the development of new crop varieties with improved tolerance to low oxygen stress, which could have important implications for global food security."
Authors: Agata Zubrycka, Charlene Dambire, Laura Dalle Carbonare, Gunjan Sharma, Tinne Boeckx, Kamal Swarup, Craig J. Sturrock, Brian S. Atkinson, Ranjan Swarup, Françoise Corbineau, Neil J. Oldham and Michael J. Holdsworth.
Nature Communications (2023)
Editor's view: Oxygen is essential for plant life. Here the authors define new functions and components of the plant oxygen sensing mechanism providing an understanding of the biochemistry of sensing and physiological responses allowing plant roots to survive in the soil.
Abstract: "Oxygen is a key signalling component of plant biology, and whilst an oxygen-sensing mechanism was previously described in Arabidopsis thaliana, key features of the associated PLANT CYSTEINE OXIDASE (PCO) N-degron pathway and Group VII ETHYLENE RESPONSE FACTOR (ERFVII) transcription factor substrates remain untested or unknown. We demonstrate that ERFVIIs show non-autonomous activation of root hypoxia tolerance and are essential for root development and survival under oxygen limiting conditions in soil. We determine the combined effects of ERFVIIs in controlling gene expression and define genetic and environmental components required for proteasome-dependent oxygen-regulated stability of ERFVIIs through the PCO N-degron pathway. Using a plant extract, unexpected amino-terminal cysteine sulphonic acid oxidation level of ERFVIIs was observed, suggesting a requirement for additional enzymatic activity within the pathway. Our results provide a holistic understanding of the properties, functions and readouts of this oxygen-sensing mechanism defined through its role in modulating ERFVII stability."
Authors: Hendrika A.C.F. Leeggangers, Natalia Yaneth Rodriguez-Granados, Monika Gyöngyi Macias-Honti and Rashmi Sasidharan.
Environmental and Experimental Botany (2023)
Highlights: • Ethylene is a major hormonal regulator of plant responses to flooding stress. • Soil flooding or waterlogging elicits various morphological or metabolic adaptations to escape/cope with flooding-associated hypoxia. • Ethylene regulates many survival traits, either locally triggering root responses or long-distance signal for shoot responses. • The versatile role of ethylene in plant responses to waterlogging can be attributed to various factors.
Abstract: "Ethylene plays a very important role as a stress signal for flooded plants, triggering a range of morphological and metabolic changes that help plants acclimate and survive these conditions. The present review surveys the current knowledge on the mechanisms underlying ethylene-dependent survival responses to waterlogging. We untangle the complexity of waterlogging signaling and response, focusing on root and shoot acclimation strategies mediated by ethylene. We describe how ethylene can have versatile roles in waterlogging tolerance, acting both as a local and long-distance signal during soil flooding and reoxygenation. We discuss the internal and external factors contributing to ethylene versatility in waterlogging responses. Finally, we highlight the current challenges and future research directions in the field, focusing not only on ethylene-mediated responses but also on flooding research applications in crop improvement."
Authors: Kuo-Wei Lee, Jeremy J. W. Chen, Chung-Shen Wu, Ho-Chun Chang, Hong-Yue Chen, Hsin-Hao Kuo, Ya-Shan Lee, Yan-Lun Chang, Hung-Chia Chang, Shiau-Yu Shiue, Yi-Chen Wu, Yi-Cheng Ho and Peng-Wen Chen.
Plant, Cell & Environment (2023)
Abstract: "Auxin is well known to stimulate coleoptile elongation and rapid seedling growth in the air. However, its role in regulating rice germination and seedling establishment under submergence is largely unknown. Previous studies revealed that excessive levels of indole-3-acetic acid (IAA) frequently cause the inhibition of plant growth and development. In this study, the high-level accumulation of endogenous IAA is observed under dark submergence, stimulating rice coleoptile elongation but limiting the root and primary leaf growth during anaerobic germination (AG). We found that oxygen and light can reduce IAA levels, promote the seedling establishment and enhance rice AG tolerance. miRNA microarray profiling and RNA gel blot analysis results show that the expression of miR167 is negatively regulated by submergence; it subsequently modulates the accumulation of free IAA through the miR167-ARF-GH3 pathway. The OsGH3-8 encodes an IAA-amido synthetase that functions to prevent free IAA accumulation. Reduced miR167 levels or overexpressing OsGH3-8 increase auxin metabolism, reduce endogenous levels of free IAA and enhance rice AG tolerance. Our studies reveal that poor seed germination and seedling growth inhibition resulting from excessive IAA accumulation would cause intolerance to submergence in rice, suggesting that a certain threshold level of auxin is essential for rice AG tolerance."
Authors: Li-Bing Yuan, Mo-Xian Chen, Lin-Na Wang, Rashmi Sasidharan, Laurentius A. C. J. Voesenek and Shi Xiao.
Plant Biotechnology Journal (2022)
Abstract: "Submergence limits plants’ access to oxygen and light, causing massive changes in metabolism; after submergence, plants experience additional stresses, including reoxygenation, dehydration, photoinhibition, and accelerated senescence. Plant responses to waterlogging and partial or complete submergence, have been well studied, but our understanding of plant responses during post-submergence recovery remains limited. During post-submergence recovery, whether a plant can repair the damage caused by submergence and re-oxygenation and re-activate key processes to continue to grow, determines whether the plant survives. Here, we summarize the challenges plants face when recovering from submergence, primarily focusing on studies of Arabidopsis thaliana and rice (Oryza sativa). We also highlight recent progress in elucidating the interplay among various regulatory pathways, compare post-hypoxia reoxygenation between plants and animals, and provide new perspectives for future studies."
Author: José Manuel Ugalde.
Plant Physiology (2022)
Excerpts: "In this issue of Plant Physiology, (Liu et al., 2022) studied the mechanisms by which ethylene pre-treatments help Arabidopsis root tip survival during hypoxia and re-oxygenation. Because re-oxygenation after hypoxia triggers a ROS burst that could damage the cell, the authors evaluated cell viability at different recovery timepoints after a four-hour hypoxia treatment."
"Most of the genes differentially expressed during hypoxia were already differentially expressed immediately after the ethylene pre-treatment, indicating that ethylene signaling triggers a transcriptome reconfiguration maintained during hypoxia. Enriched gene ontology (GO) terms of genes upregulated by ethylene treatments were linked to hypoxia response and abscisic acid (ABA), among others. In comparison, GO terms enriched in the downregulated genes were related to decreased cellular maintenance and root growth, such as PLETHORA (PLT) 1 and 2, SCARECROW (SCR), and SHORTROOT (SHR). Moreover, ethylene limited the expression of genes related to ROS homeostasis and antioxidant activity, such as peroxidases like ASCORBATE PEROXIDASE 2 (APX2) (Figure 1)."
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Authors: Emese Eysholdt-Derzsó, Bettina Hause, Margret Sauter and Romy R. Schmidt-Schippers.
Plant, Cell & Environment (2024)
Summary Statement: ERFVII pathway actively maintains abscisic acid homoeostasis, enabling a partial control of lateral root development under hypoxic conditions.
Abstract: "Oxygen limitation (hypoxia), arising as a key stress factor due to flooding, negatively affects plant development. Consequently, maintaining root growth under such stress is crucial for plant survival, yet we know little about the root system's adaptions to low-oxygen conditions and its regulation by phytohormones. In this study, we examine the impact of hypoxia and, herein, the regulatory role of group VII ETHYLENE-RESPONSE FACTOR (ERFVII) transcription factors on root growth in Arabidopsis. We found lateral root (LR) elongation to be actively maintained by hypoxia via ERFVII factors, as erfVII seedlings possess hypersensitivity towards hypoxia regarding their LR growth. Pharmacological inhibition of abscisic acid (ABA) biosynthesis revealed ERFVII-driven counteraction of hypoxia-induced inhibition of LR formation in an ABA-dependent manner. However, postemergence LR growth under hypoxia mediated by ERFVIIs was independent of ABA. In roots, ERFVIIs mediate, among others, the induction of ABA-degrading ABA 8′-hydroxylases CYP707A1 expression. RAP2.12 could activate the pCYC707A1:LUC reporter gene, indicating, combined with single mutant analyses, that this transcription factor regulates ABA levels through corresponding transcript upregulation. Collectively, hypoxia-induced adaptation of the Arabidopsis root system is shaped by developmental reprogramming, whereby ERFVII-dependent promotion of LR emergence, but not elongation, is partly executed through regulation of ABA degradation."
Authors: Felix Lutter, Wolfram Brenner, Franziska Krajinski-Barth and Vajiheh Safavi-Rizi.
Plant Signaling & Behavior (2024)
Abstract: "Nitric oxide (NO) and cytokinins (CKs) are known for their crucial contributions to plant development, growth, senescence, and stress response. Despite the importance of both signals in stress responses, their interaction remains largely unexplored. The interplay between NO and CKs emerges as particularly significant not only regarding plant growth and development but also in addressing plant stress response, particularly in the context of extreme weather events leading to yield loss. In this review, we summarize NO and CKs metabolism and signaling. Additionally, we emphasize the crosstalk between NO and CKs, underscoring its potential impact on stress response, with a focus on hypoxia tolerance. Finally, we address the most urgent questions that demand answers and offer recommendations for future research endeavors."
Authors: Md Ibrahim Khalil, Md Mahmudul Hassan, Swadesh Chandra Samanta, Abul Kashem Chowdhury, Md Zahid Hassan, Nasar Uddin Ahmed, Uzzal Somaddar, Sharmistha Ghosal, Arif Hasan Khan Robin, Ujjal Kumar Nath, Mohammad Golam Mostofa, David J. Burritt, Chien Van Ha, Aarti Gupta, Lam-Son Phan Tran and Gopal Saha.
Plant Physiology and Biochemistry (2024)
Highlights • Rice plants having SUB1A-1 endure submergence through a quiescence strategy. • SUB1A-1 mediates inhibition of levels and signaling of ethylene, gibberellin and auxin. • SUB1A-1 increases brassinosteroid biosynthesis and signaling, and JA responsiveness. • SUB1A-1 activates leaf gas film formation and reduces carbohydrate catabolism. • Submergence-tolerant wild rice genotypes lack SUB1A.
Abstract: "The world's low-lying rice (Oryza sativa) cultivation areas have been suffering from the threats of submergence or flash flooding due to global warming. Rice plants manifest a variety of physiological and morphological changes to cope with hypoxia and underwater adversities, including lowering carbohydrate consumption, inhibiting shoot elongation, and forming thicker leaf gas film during submergence. Functional studies have revealed that submergence tolerance in rice is mainly determined by an ethylene response factor (ERF) transcription factor-encoding gene, namely SUBMERGENCE 1A-1 (SUB1A-1) located in the SUB1 quantitative trait locus. The SUB1A-1-dependent submergence tolerance is manifested through hormones such as ethylene, gibberellic acid, brassinosteroid, auxin and jasmonic acid. Considerable progress has been made toward the introduction of SUB1A-1 into rice varieties through a conventional marker-assisted backcrossing strategy. Here, we review the recent advances in the physiological, biochemical and molecular dynamics of rice submergence tolerance mediated by the ‘quiescence strategy’. Thus, the present review aims to provide researchers with insights into the genetics of rice submergence tolerance and future perspectives for designing submergence-resilient plants for sustainable agriculture under the uncertainties of climate change."
Authors: Jagannath Swain, Vinay Shukla, Francesco Licausi and Kapuganti Jagadis Gupta.
Trends in Plant Science (2024)
Abstract: "Group VII ethylene-responsive factor (ERFVII) transcription factors are crucial for the adaption of plants to conditions that limit oxygen availability. A recent study by Zubrycka et al. reveals new aspects of ERFVII stabilization through the PLANT CYSTEINE OXIDASE (PCO)-N degron pathway and non-autonomous regulation in response to different endogenous and exogenous cues."
Authors: Sidra Javed, Xiangzheng Chai, Xiaoming Wang and Shengbao Xu.
Plant and Soil (2023)
Abstract: "Background - Plants rely heavily on the formation of post-embryonic organs, such as leaves, branches, and lateral roots, to adapt to varying soil conditions. Lateral roots (LR) play a crucial role in the plant root system, serving as the primary factor in the exploration of water and nutrients in the soil. The development of LR is meticulously controlled by phytohormones to respond to the information obtained from the surrounding soil. This regulation ensures an optimal arrangement of lateral roots, enabling efficient nutrient absorption and adaptation to the challenging environmental conditions. Scope - This review summarizes recent progress in understanding the mechanisms of lateral root layout in different soil micro-environments and the role of phytohormones in mediating LR development for soil adaptation. Conclusions - The intricate signaling network governing LR layout involves interactions among various soil factors, which are mediated by phytohormones. Despite its complexity, recent studies have yielded significant insights that can be applied to optimize LR arrangement in soil profiles through genetic and cultivation methods to enhance crop yield and stress tolerance."
Authors: Robert D. Hill, Abir U. Igamberdiev and Claudio Stasolla.
Planta (2023)
Main conclusion: The preservation of quiescent center stem cell integrity in hypoxic roots by phytoglobins is exercised through their ability to scavenge nitric oxide and attenuate its effects on auxin transport and cell degradation. Under low oxygen stress, the retention or induction of phytoglobin expression maintains cell viability while loss or lack of induction of phytoglobin leads to cell degradation.
Abstract: "Plants have evolved unique attributes to ensure survival in the environment in which they must exist. Common among the attributes is the ability to maintain stem cells in a quiescent (or low proliferation) state in unfriendly environments. From the seed embryo to meristematic regions of the plant, quiescent stem cells exist to regenerate the organism when environmental conditions are suitable to allow plant survival. Frequently, plants dispose of mature cells or organs in the process of acclimating to the stresses to ensure survival of meristems, the stem cells of which are capable of regenerating cells and organs that have been sacrificed, a feature not generally available to mammals. Most of the research on plant stress responses has dealt with how mature cells respond because of the difficulty of specifically examining plant meristem responses to stress. This raises the question as to whether quiescent stem cells behave in a similar fashion to mature cells in their response to stress and what factors within these critical cells determine whether they survive or degrade when exposed to environmental stress. This review attempts to examine this question with respect to the quiescent center (QC) stem cells of the root apical meristem. Emphasis is put on how varying levels of nitric oxide, influenced by the expression of phytoglobins, affect QC response to hypoxic stress."
Authors: Kevin Daniel and Sjon Hartman.
Journal of Experimental Botany (2024)
Abstract: "Plant submergence is a major abiotic stress that impairs plant performance. Underwater, reduced gas diffusion exposes submerged plant cells to an environment that is enriched in gaseous ethylene and is limited in oxygen (O2) availability (hypoxia). The capacity for plant roots to avoid and/or sustain critical hypoxia damage is essential for plants to survive waterlogging. Plants use spatiotemporal ethylene and O2 dynamics as instrumental flooding signals to modulate potential adaptive root growth and hypoxia stress acclimation responses. However, how non-adapted plant species modulate root growth behaviour during actual waterlogged conditions to overcome flooding stress has hardly been investigated. Here we discuss how changes in the root growth rate, lateral root formation, density and growth angle of non-flood adapted plant species (mainly Arabidopsis) could contribute to avoiding and enduring critical hypoxic conditions. In addition, we discuss the current molecular understanding of how ethylene and hypoxia signalling control these adaptive root growth responses. We propose that future research would benefit from less artificial experimental designs to better understand how plant roots respond to and survive waterlogging. This acquired knowledge would be instrumental to guide targeted breeding of flood-tolerant crops with more resilient root systems."
Author: Françoise Corbineau.
Seed Science Research (2023)
Abstract: "Oxygen is a major factor of seed germination since it allows resumption of respiration and subsequent metabolism reactivation during seed imbibition, thus leading to the production of reducing power and ATP. Most studies carried out in the 60s to 85s indicate that oxygen requirement depends on the species and is modulated by environmental factors. They have also demonstrated that the covering structures mainly inhibit germination by limiting oxygen supply to the embryo during imbibition through enzymatic oxidation of phenolic compounds by polyphenol oxidases (catechol oxidase and laccase) and peroxidases. Recent use of oxygen-sensitive microsensors has allowed to better characterize the oxygen diffusion in the seed and determine the oxygen content at the level of embryo below the covering structures. Here, I will also highlight the major data obtained over the last 30 years indicating the key role of oxygen in the molecular networks regulating seed germination and dormancy through (1) the hormonal balance (ethylene, ABA and GA), the hormone-signalling pathway and, in particular, the ABA sensitivity, (2) the emerging role of mitochondria in ROS production in hypoxia and (3) the involvement of the N-degron pathway in the turnover of proteins involved in seed tolerance to hypoxia."
Authors: Mizuki Murao, Rika Kato, Shuhei Kusano, Rina Hisamatsu, Hitoshi Endo, Yasuki Kawabata, Seisuke Kimura, Ayato Sato, Hitoshi Mori, Kenichiro Itami, Keiko U. Torii, Shinya Hagihara and Naoyuki Uchida.
Plant and Cell Physiology (2023)
Abstract: "Plant seedlings adjust the growth of the hypocotyl in response to surrounding environmental changes. Genetic studies have revealed key players and pathways in hypocotyl growth, such as phytohormones and light signaling. However, because of genetic redundancy in the genome, it is expected that not-yet-revealed mechanisms can be elucidated through approaches different from genetic ones. Here we identified a small compound, HYGIC (HG), that simultaneously induces hypocotyl elongation and thickening, accompanied by increased nuclear size and enlargement of cortex cells. HG-induced hypocotyl growth required the ethylene signaling pathway activated by endogenous ethylene, involving CONSTITUTIVE PHOTOMORPHOGENIC 1, ETHYLENE INSENSITIVE 2, and redundant transcription factors for ethylene responses, ETHYLENE INSENSITIVE 3 (EIN3) and EIN3 LIKE 1. By using EBS:GUS, a transcriptional reporter of ethylene responses based on an EIN3-binding-cis-element, we found that HG treatment ectopically activates ethylene responses at the epidermis and cortex of the hypocotyl. RNA-seq and subsequent gene ontology analysis revealed that a significant number of HG-induced genes are related to responses to hypoxia. Indeed, submergence, a representative environment where the hypoxia response is induced in nature, promoted ethylene-signaling-dependent hypocotyl elongation and thickening accompanied by ethylene responses at the epidermis and cortex, which resembled the HG treatment. Collectively, the identification and analysis of HG revealed that ectopic responsiveness to ethylene promotes hypocotyl growth, and this mechanism is activated under submergence."
Authors: Yiyi Zhang, Yuanfu Xie, Haifan Shi, Yufen Zhuang, Yuan Zheng, Honghui Lin and Huapeng Zhou.
Plant and Cell Physiology (2023)
Abstract: "Floods impose detrimental effects on natural and agro-ecosystems, leading to significant loss of worldwide crop production. Global climate change has even strengthened this situation. Flooding is a continuous process including two stages of submergence and re-oxygenation, and both are harmful to plant growth and development, resulting in a serious decline on crop yield. Therefore, the understanding of plant flooding tolerance and developing flooding-resistant crops are of great significance. Here, we report that the Arabidopsis thaliana (Arabidopsis) R2R3-MYB transcription factor MYB30 participates in plant submergence response through ACS7 by repressing ethylene (ET) biosynthesis. The MYB30 loss-of-function mutant exhibits reduced submergence tolerance with higher level of ET production, whereas the MYB30-overexpressing plant displays enhanced submergence tolerance and repressed ET production. The coding gene of ACC synthase 7 (ACS7) might be a direct target of MYB30 during submergence response. MYB30 binds to the promoter of ACS7 and represses its transcription. ACS7 loss-of-function mutant with defect in ET biosynthesis displays enhanced submergence tolerance, whereas plants overexpressing ACS7 exhibit a submergence-sensitive phenotype. Genetic analysis shows that ACS7 functions downstream of MYB30 both in ET biosynthesis and submergence response. Taken together, our work revealed a novel transcriptional regulation that modulates submergence response in plants."
Authors: Batist Geldhof, Jolien Pattyn, Petar Mohorović, Karlien Van den Broeck, Vicky Everaerts, Ondřej Novák and Bram Van de Poel.
bioRxiv (2022)
Abstract: "Developing leaves undergo a vast array of age-related changes as they mature. These include physiological, hormonal and morphological changes that determine their adaptation plasticity towards adverse conditions. Waterlogging induces leaf epinasty in tomato, and the magnitude of leaf bending is intricately related to the age-dependent cellular and hormonal response. We now show that ethylene, the master regulator of epinasty, is differentially regulated throughout leaf development, giving rise to age-dependent epinastic responses. Young leaves have a higher basal ethylene production, but are less responsive to waterlogging-induced epinasty, as they have a higher capacity to convert the root-borne and mobilized ACC into the inactive conjugate MACC. Ethylene stimulates cell elongation relatively more at the adaxial petiole side, by activating auxin biosynthesis and locally inhibiting its transport through PIN4 and PIN9 in older and mature leaves. As a result, auxins accumulate in the petiole base of these leaves and enforce partially irreversible epinastic bending upon waterlogging. Young leaves maintain their potential to transport auxins, both locally and through the vascular tissue, leading to enhanced flexibility to dampen the epinastic response and a faster upwards repositioning during reoxygenation. This mechanism also explains the observed reduction of epinasty during and its recovery after waterlogging in the anthocyanin reduced (are) and Never ripe (Nr) mutants, both characterized by higher auxin flow. Our work has demonstrated that waterlogging activates intricate hormonal crosstalk between ethylene and auxin, controlled in an age-dependent way."
Authors: Biao Ma, Tian Ma, Wenhao Xian, Bin Hu and Chengcai Chu.
Journal of Integrative Plant Biology (2023)
Abstract: "The stress hormone ethylene plays a key role in plant adaptation to adverse environmental conditions. Nitrogen (N) is the most quantitatively required mineral nutrient for plants, and its availability is a major determinant for crop production. Changes in N availability or N forms can alter ethylene biosynthesis and/or signaling. Ethylene serves as an important cellular signal to mediate root system architecture (RSA) adaptation, N uptake and translocation, ammonium toxicity, anthocyanin accumulation, and premature senescence, thereby adapting plant growth and development to external N status. Here, we review the ethylene-mediated morphological and physiological responses and highlight how ethylene transduces the N signals to the adaptive responses. We specifically discuss the N-ethylene relations in rice, an important cereal crop in which ethylene is essential for its hypoxia survival."
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