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Plant Responses to Hypoxia
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Plant Responses to Hypoxia

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Response to Abiotic Stress and Climate Change".

Deadline for manuscript submissions: closed (31 July 2020) | Viewed by 78609

Printed Edition Available!
A printed edition of this Special Issue is available here.

Special Issue Editors

Dr. Elena Loreti

E-Mail Website
Guest Editor
The Institute of Agricultural Biology and Biotechnology, Nationl Research Council, Via G. Moruzzi 1, 56124 Pisa, Italy
Interests: plant responses to hypoxia; miRNA in plants; crosstalk between sugar metabolism and hormone signalling to regulate plant growth
Dr. Gustavo Striker

E-Mail Website
Guest Editor
Agricultural Plant Physiology and Ecology Research Institute, University of Buenos Aires & National Scientific and Technical Research Council, Avenida San Martin 4453, 1417DSE, Argentina
Interests: ecophysiology of plants under low oxygen conditions; crop and forage species responses to waterlogging and submergence; root physiology under hypoxia (root oxygenation, radial oxygen loss and rhizosphere oxidation)

Special Issue Information

Dear Colleagues,

Plants are obligate aerobic organisms and cannot survive for long periods in low-oxygen environments. Oxygen is required for ATP production in the mitochondrial electron transport chain, so a shortage of oxygen (hypoxia) or a total absence of oxygen (anoxia) inhibits aerobic respiration, resulting in an energy crisis. During their life cycle, plants may experience oxygen deprivation due to flooding of the soil or to the anatomical structure of some tissues whose histological properties (e.g., densely packed cells) severely limit the permeability to oxygen, such as in tubers, vascular cambium of trees, meristematic tissues, developing seeds, etc.

Climate change increases the likelihood of sudden floods due to severe rainfall, leading to soil waterlogging or submergence, negatively influencing plant growth and productivity. Plant species differ in their tolerance to waterlogging-induced hypoxia, and some specific traits and responses contribute to tolerance, such as root aerenchyma formation, adventitious rooting, and the formation of physical barriers preventing the loss of oxygen from roots. Plant species can adopt different strategies to deal with submergence; some species display an “escape strategy”, with rapid shoot elongation aimed at restoring leaf contact with the atmosphere, while other species show a “quiescent strategy”, with restrained shoot elongation and conservative use of carbohydrate reserves, which are required for resuming vigorous growth when water recedes. Plants reprogram their gene expression under hypoxia with the synthesis of a set of anaerobic polypeptides (ANPs), mostly involved in glycolysis and ethanol fermentation.

Until a decade ago, little was known about the molecular mechanisms involved in oxygen sensing and signaling in plants. Many researchers have put their efforts into discovering the genes that confer tolerance to submergence, with breakthrough discoveries. However, despite the progress achieved, there are still open questions and challenges in the field of low-oxygen stress responses in plants.

For this Special Issue of Plants about ‘Plant Responses to Hypoxia’, contributions (original research papers, perspectives, hypotheses, opinions, reviews, modeling approaches, and methods) on model plants, crops, trees, and aquatic and wild species from different fields of research, such as biochemistry, physiology, ecophysiology, and molecular biology, are most welcome.

Dr. Elena Loreti
Dr. Gustavo Striker
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Plants is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • anoxia
  • hypoxia metabolism, physiology, ecophysiology
  • molecular biology
  • waterlogging
  • submergence
  • low oxygen responses in plants, crops, forage species, wild species, model species

Published Papers (18 papers)

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Editorial

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4 pages, 211 KiB  
Editorial
Plant Responses to Hypoxia: Signaling and Adaptation
by Elena Loreti and Gustavo G. Striker
Plants 2020, 9(12), 1704; https://doi.org/10.3390/plants9121704 - 03 Dec 2020
Cited by 12 | Viewed by 3157
Abstract
Molecular oxygen deficiency leads to altered cellular metabolism and can dramatically reduce crop productivity [...] Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)

Research

Jump to: Editorial, Review

18 pages, 2880 KiB  
Article
Metabolic Responses to Waterlogging Differ between Roots and Shoots and Reflect Phloem Transport Alteration in Medicago truncatula
by Jérémy Lothier, Houssein Diab, Caroline Cukier, Anis M. Limami and Guillaume Tcherkez
Plants 2020, 9(10), 1373; https://doi.org/10.3390/plants9101373 - 15 Oct 2020
Cited by 36 | Viewed by 2738
Abstract
Root oxygen deficiency that is induced by flooding (waterlogging) is a common situation in many agricultural areas, causing considerable loss in yield and productivity. Physiological and metabolic acclimation to hypoxia has mostly been studied on roots or whole seedlings under full submergence. The [...] Read more.
Root oxygen deficiency that is induced by flooding (waterlogging) is a common situation in many agricultural areas, causing considerable loss in yield and productivity. Physiological and metabolic acclimation to hypoxia has mostly been studied on roots or whole seedlings under full submergence. The metabolic difference between shoots and roots during waterlogging, and how roots and shoots communicate in such a situation is much less known. In particular, the metabolic acclimation in shoots and how this, in turn, impacts on roots metabolism is not well documented. Here, we monitored changes in the metabolome of roots and shoots of barrel clover (Medicago truncatula), growth, and gas-exchange, and analyzed phloem sap exudate composition. Roots exhibited a typical response to hypoxia, such as γ-aminobutyrate and alanine accumulation, as well as a strong decline in raffinose, sucrose, hexoses, and pentoses. Leaves exhibited a strong increase in starch, sugars, sugar derivatives, and phenolics (tyrosine, tryptophan, phenylalanine, benzoate, ferulate), suggesting an inhibition of sugar export and their alternative utilization by aromatic compounds production via pentose phosphates and phosphoenolpyruvate. Accordingly, there was an enrichment in sugars and a decline in organic acids in phloem sap exudates under waterlogging. Mass-balance calculations further suggest an increased imbalance between loading by shoots and unloading by roots under waterlogging. Taken as a whole, our results are consistent with the inhibition of sugar import by waterlogged roots, leading to an increase in phloem sugar pool, which, in turn, exert negative feedback on sugar metabolism and utilization in shoots. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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20 pages, 12278 KiB  
Article
Differential Expression of Maize and Teosinte microRNAs under Submergence, Drought, and Alternated Stress
by Edgar Baldemar Sepúlveda-García, José Francisco Pulido-Barajas, Ariana Arlene Huerta-Heredia, Julián Mario Peña-Castro, Renyi Liu and Blanca Estela Barrera-Figueroa
Plants 2020, 9(10), 1367; https://doi.org/10.3390/plants9101367 - 15 Oct 2020
Cited by 14 | Viewed by 4071
Abstract
Submergence and drought stresses are the main constraints to crop production worldwide. MicroRNAs (miRNAs) are known to play a major role in plant response to various stresses. In this study, we analyzed the expression of maize and teosinte miRNAs by high-throughput sequencing of [...] Read more.
Submergence and drought stresses are the main constraints to crop production worldwide. MicroRNAs (miRNAs) are known to play a major role in plant response to various stresses. In this study, we analyzed the expression of maize and teosinte miRNAs by high-throughput sequencing of small RNA libraries in maize and its ancestor teosinte (Zea mays ssp. parviglumis), under submergence, drought, and alternated stress. We found that the expression patterns of 67 miRNA sequences representing 23 miRNA families in maize and other plants were regulated by submergence or drought. miR159a, miR166b, miR167c, and miR169c were downregulated by submergence in both plants but more severely in maize. miR156k and miR164e were upregulated by drought in teosinte but downregulated in maize. Small RNA profiling of teosinte subject to alternate treatments with drought and submergence revealed that submergence as the first stress attenuated the response to drought, while drought being the first stress did not alter the response to submergence. The miRNAs identified herein, and their potential targets, indicate that control of development, growth, and response to oxidative stress could be crucial for adaptation and that there exists evolutionary divergence between these two subspecies in miRNA response to abiotic stresses. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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14 pages, 2483 KiB  
Article
Potassium Efflux and Cytosol Acidification as Primary Anoxia-Induced Events in Wheat and Rice Seedlings
by Vladislav V. Yemelyanov, Tamara V. Chirkova, Maria F. Shishova and Sylvia M. Lindberg
Plants 2020, 9(9), 1216; https://doi.org/10.3390/plants9091216 - 16 Sep 2020
Cited by 14 | Viewed by 2441
Abstract
Both ion fluxes and changes of cytosolic pH take an active part in the signal transduction of different environmental stimuli. Here we studied the anoxia-induced alteration of cytosolic K+ concentration, [K+]cyt, and cytosolic pH, pHcyt, in [...] Read more.
Both ion fluxes and changes of cytosolic pH take an active part in the signal transduction of different environmental stimuli. Here we studied the anoxia-induced alteration of cytosolic K+ concentration, [K+]cyt, and cytosolic pH, pHcyt, in rice and wheat, plants with different tolerances to hypoxia. The [K+]cyt and pHcyt were measured by fluorescence microscopy in single leaf mesophyll protoplasts loaded with the fluorescent potassium-binding dye PBFI-AM and the pH-sensitive probe BCECF-AM, respectively. Anoxic treatment caused an efflux of K+ from protoplasts of both plants after a lag-period of 300–450 s. The [K+]cyt decrease was blocked by tetraethylammonium (1 mM, 30 min pre-treatment) suggesting the involvement of plasma membrane voltage-gated K+ channels. The protoplasts of rice (a hypoxia-tolerant plant) reacted upon anoxia with a higher amplitude of the [K+]cyt drop. There was a simultaneous anoxia-dependent cytosolic acidification of protoplasts of both plants. The decrease of pHcyt was slower in wheat (a hypoxia-sensitive plant) while in rice protoplasts it was rapid and partially reversible. Ion fluxes between the roots of intact seedlings and nutrient solutions were monitored by ion-selective electrodes and revealed significant anoxia-induced acidification and potassium leakage that were inhibited by tetraethylammonium. The K+ efflux from rice was more distinct and reversible upon reoxygenation when compared with wheat seedlings. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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17 pages, 3014 KiB  
Article
Overexpression of Jatropha curcas ERFVII2 Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes
by Piyada Juntawong, Pimprapai Butsayawarapat, Pattralak Songserm, Ratchaneeporn Pimjan and Supachai Vuttipongchaikij
Plants 2020, 9(9), 1068; https://doi.org/10.3390/plants9091068 - 20 Aug 2020
Cited by 4 | Viewed by 3177
Abstract
Enhancing crop tolerance to waterlogging is critical for improving food and biofuel security. In waterlogged soils, roots are exposed to a low oxygen environment. The group VII ethylene response factors (ERFVIIs) were recently identified as key regulators of plant low oxygen [...] Read more.
Enhancing crop tolerance to waterlogging is critical for improving food and biofuel security. In waterlogged soils, roots are exposed to a low oxygen environment. The group VII ethylene response factors (ERFVIIs) were recently identified as key regulators of plant low oxygen response. Oxygen-dependent N-end rule pathways can regulate the stability of ERFVIIs. This study aims to characterize the function of the Jatropha curcas ERFVIIs and the impact of N-terminal modification that stabilized the protein toward low oxygen response. This study revealed that all three JcERFVII proteins are substrates of the N-end rule pathway. Overexpression of JcERFVII2 conferred tolerance to low oxygen stress in Arabidopsis. In contrast, the constitutive overexpression of stabilized JcERFVII2 reduced low oxygen tolerance. RNA-seq was performed to elucidate the functional roles of JcERFVII2 and the impact of its N-terminal modification. Overexpression of both wildtype and stabilized JcERFVII2 constitutively upregulated the plant core hypoxia-responsive genes. Besides, overexpression of the stabilized JcERFVII2 further upregulated various genes controlling fermentative metabolic processes, oxidative stress, and pathogen responses under aerobic conditions. In summary, JcERFVII2 is an N-end rule regulated waterlogging-responsive transcription factor that modulates the expression of multiple stress-responsive genes; therefore, it is a potential candidate for molecular breeding of multiple stress-tolerant crops. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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15 pages, 2595 KiB  
Article
Jasmonate Signalling Contributes to Primary Root Inhibition Upon Oxygen Deficiency in Arabidopsis thaliana
by Vinay Shukla, Lara Lombardi, Ales Pencik, Ondrej Novak, Daan A. Weits, Elena Loreti, Pierdomenico Perata, Beatrice Giuntoli and Francesco Licausi
Plants 2020, 9(8), 1046; https://doi.org/10.3390/plants9081046 - 17 Aug 2020
Cited by 17 | Viewed by 4483
Abstract
Plants, including most crops, are intolerant to waterlogging, a stressful condition that limits the oxygen available for roots, thereby inhibiting their growth and functionality. Whether root growth inhibition represents a preventive measure to save energy or is rather a consequence of reduced metabolic [...] Read more.
Plants, including most crops, are intolerant to waterlogging, a stressful condition that limits the oxygen available for roots, thereby inhibiting their growth and functionality. Whether root growth inhibition represents a preventive measure to save energy or is rather a consequence of reduced metabolic rates has yet to be elucidated. In the present study, we gathered evidence for hypoxic repression of root meristem regulators that leads to root growth inhibition. We also explored the contribution of the hormone jasmonic acid (JA) to this process in Arabidopsis thaliana. Analysis of transcriptomic profiles, visualisation of fluorescent reporters and direct hormone quantification confirmed the activation of JA signalling under hypoxia in the roots. Further, root growth assessment in JA-related mutants in aerobic and anaerobic conditions indicated that JA signalling components contribute to active root inhibition under hypoxia. Finally, we show that the oxygen-sensing transcription factor (TF) RAP2.12 can directly induce Jasmonate Zinc-finger proteins (JAZs), repressors of JA signalling, to establish feedback inhibition. In summary, our study sheds new light on active root growth restriction under hypoxic conditions and on the involvement of the JA hormone in this process and its cross talk with the oxygen sensing machinery of higher plants. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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14 pages, 2516 KiB  
Article
Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species
by Sjon Hartman, Nienke van Dongen, Dominique M.H.J. Renneberg, Rob A.M. Welschen-Evertman, Johanna Kociemba, Rashmi Sasidharan and Laurentius A.C.J. Voesenek
Plants 2020, 9(8), 1022; https://doi.org/10.3390/plants9081022 - 13 Aug 2020
Cited by 16 | Viewed by 4810
Abstract
The increasing occurrence of floods hinders agricultural crop production and threatens global food security. The majority of vegetable crops are highly sensitive to flooding and it is unclear how these plants use flooding signals to acclimate to impending oxygen deprivation (hypoxia). Previous research [...] Read more.
The increasing occurrence of floods hinders agricultural crop production and threatens global food security. The majority of vegetable crops are highly sensitive to flooding and it is unclear how these plants use flooding signals to acclimate to impending oxygen deprivation (hypoxia). Previous research has shown that the early flooding signal ethylene augments hypoxia responses and improves survival in Arabidopsis. To unravel how cultivated and wild Solanum species integrate ethylene signaling to control subsequent hypoxia acclimation, we studied the transcript levels of a selection of marker genes, whose upregulation is indicative of ethylene-mediated hypoxia acclimation in Arabidopsis. Our results suggest that ethylene-mediated hypoxia acclimation is conserved in both shoots and roots of the wild Solanum species bittersweet (Solanum dulcamara) and a waterlogging-tolerant potato (Solanum tuberosum) cultivar. However, ethylene did not enhance the transcriptional hypoxia response in roots of a waterlogging-sensitive potato cultivar, suggesting that waterlogging tolerance in potato could depend on ethylene-controlled hypoxia responses in the roots. Finally, we show that ethylene rarely enhances hypoxia-adaptive genes and does not improve hypoxia survival in tomato (Solanum lycopersicum). We conclude that analyzing genes indicative of ethylene-mediated hypoxia acclimation is a promising approach to identifying key signaling cascades that confer flooding tolerance in crops. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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14 pages, 2809 KiB  
Article
The Seedlings of Different Japonica Rice Varieties Exhibit Differ Physiological Properties to Modulate Plant Survival Rates under Submergence Stress
by Yu-Syuan Li, Shang-Ling Ou and Chin-Ying Yang
Plants 2020, 9(8), 982; https://doi.org/10.3390/plants9080982 - 03 Aug 2020
Cited by 8 | Viewed by 2899
Abstract
Oryza sativa is a major food crop in Asia. In recent years, typhoons and sudden downpours have caused field flooding, which has resulted in serious harm to the production of rice. In this study, our data revealed that the plant heights of the [...] Read more.
Oryza sativa is a major food crop in Asia. In recent years, typhoons and sudden downpours have caused field flooding, which has resulted in serious harm to the production of rice. In this study, our data revealed that the plant heights of the five Japonica varieties increased during submergence. The elongation rates of TN14, KH139, and TK9 increased significantly during submergence. Chlorophyll contents of the five varieties significantly decreased after submergence and increased after recovery. Moreover, the chlorophyll content of KH139 was significantly higher than those of the other four varieties after recovery. The plant survival rates of the five varieties were higher than 50% after four-day submergence. After eight-day submergence, the survival rate of KH139 remained at 90%, which was the highest among the different varieties. The KH139 presented lower accumulation of hydrogen peroxide and the catalase activity than those of the other four varieties under submergence. The sucrose synthase 1 and alcohol dehydrogenase 1 were induced in KH139 under submergence. The results presented that different varieties of japonica rice have different flood tolerances, especially KH139 under submergence was superior to that of the other four varieties. These results can provide crucial information for future research on japonica rice under flooding stress. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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14 pages, 3297 KiB  
Article
Hypoxic Treatment Decreases the Physiological Action of the Herbicide Imazamox on Pisum sativum Roots
by Miriam Gil-Monreal, Mercedes Royuela and Ana Zabalza
Plants 2020, 9(8), 981; https://doi.org/10.3390/plants9080981 - 03 Aug 2020
Cited by 5 | Viewed by 2674
Abstract
The inhibition of acetolactate synthase (ALS; EC 2.2.1.6), an enzyme located in the biosynthetic pathway of branched-chain amino acids, is the target site of the herbicide imazamox. One of the physiological effects triggered after ALS inhibition is the induction of aerobic ethanol fermentation. [...] Read more.
The inhibition of acetolactate synthase (ALS; EC 2.2.1.6), an enzyme located in the biosynthetic pathway of branched-chain amino acids, is the target site of the herbicide imazamox. One of the physiological effects triggered after ALS inhibition is the induction of aerobic ethanol fermentation. The objective of this study was to unravel if fermentation induction is related to the toxicity of the herbicide or if it is a plant defense mechanism. Pea plants were exposed to two different times of hypoxia before herbicide application in order to induce the ethanol fermentation pathway, and the physiological response after herbicide application was evaluated at the level of carbohydrates and amino acid profile. The effects of the herbicide on total soluble sugars and starch accumulation, and changes in specific amino acids (branched-chain, amide, and acidic) were attenuated if plants were subjected to hypoxia before herbicide application. These results suggest that fermentation is a plant defense mechanism that decreases the herbicidal effect. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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13 pages, 2215 KiB  
Article
Some Accessions of Amazonian Wild Rice (Oryza glumaepatula) Constitutively Form a Barrier to Radial Oxygen Loss along Adventitious Roots under Aerated Conditions
by Masato Ejiri, Yuto Sawazaki and Katsuhiro Shiono
Plants 2020, 9(7), 880; https://doi.org/10.3390/plants9070880 - 13 Jul 2020
Cited by 19 | Viewed by 2525
Abstract
A barrier to radial oxygen loss (ROL), which reduces the loss of oxygen transported via the aerenchyma to the root tips, enables the roots of wetland plants to grow into anoxic/hypoxic waterlogged soil. However, little is known about its genetic regulation. Quantitative trait [...] Read more.
A barrier to radial oxygen loss (ROL), which reduces the loss of oxygen transported via the aerenchyma to the root tips, enables the roots of wetland plants to grow into anoxic/hypoxic waterlogged soil. However, little is known about its genetic regulation. Quantitative trait loci (QTLs) mapping can help to understand the factors that regulate barrier formation. Rice (Oryza sativa) inducibly forms an ROL barrier under stagnant conditions, while a few wetland plants constitutively form one under aerated conditions. Here, we evaluated the formation of a constitutive ROL barrier in a total of four accessions from two wild rice species. Three of the accessions were wetland accessions of O. glumaepatula, and the fourth was a non-wetland species of O. rufipogon. These species have an AA type genome, which allows them to be crossed with cultivated rice. The three O. glumaepatula accessions (W2165, W2149, and W1183) formed an ROL barrier under aerated conditions. The O. rufipogon accession (W1962) did not form a constitutive ROL barrier, but it formed an inducible ROL barrier under stagnant conditions. The three O. glumaepatula accessions should be useful for QTL mapping to understand how a constitutive ROL barrier forms. The constitutive barrier of W2165 was closely associated with suberization and resistance to penetration by an apoplastic tracer (periodic acid) at the exodermis but did not include lignin at the sclerenchyma. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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18 pages, 869 KiB  
Article
Foliar Glycine Betaine or Hydrogen Peroxide Sprays Ameliorate Waterlogging Stress in Cape Gooseberry
by Nicolas E. Castro-Duque, Cristhian C. Chávez-Arias and Hermann Restrepo-Díaz
Plants 2020, 9(5), 644; https://doi.org/10.3390/plants9050644 - 19 May 2020
Cited by 14 | Viewed by 3312
Abstract
Exogenous glycine betaine (GB) or hydrogen peroxide (H2O2) application has not been explored to mitigate waterlogging stress in Andean fruit trees. The objective of this study was to evaluate foliar GB or H2O2 application on the [...] Read more.
Exogenous glycine betaine (GB) or hydrogen peroxide (H2O2) application has not been explored to mitigate waterlogging stress in Andean fruit trees. The objective of this study was to evaluate foliar GB or H2O2 application on the physiological behavior of Cape gooseberry plants under waterlogging. Two separate experiments were carried out. In the first trial, the treatment groups were: (1) plants without waterlogging and with no foliar applications, (2) plants with waterlogging and without foliar applications, and (3) waterlogged plants with 25, 50, or 100 mM of H2O2 or GB, respectively. The treatments in the second trial were: (1) plants without waterlogging and with no foliar applications, (2) plants with waterlogging and without foliar applications, and (3) waterlogged plants with 100 mM of H2O2 or GB, respectively. In the first experiment, plants with waterlogging and with exogenous GB or H2O2 applications at a dose of 100 mM showed higher leaf water potential (−0.5 Mpa), dry weight (1.0 g), and stomatal conductance (95 mmol·m−2·s−1) values. In the second experiment, exogenously supplied GB or H2O2 also increased the relative growth rate, and leaf photosynthesis mitigating waterlogging stress. These results show that short-term GB or H2O2 supply can be a tool in managing waterlogging in Cape gooseberry. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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11 pages, 3211 KiB  
Article
A Role for Auxin in Ethylene-Dependent Inducible Aerenchyma Formation in Rice Roots
by Takaki Yamauchi, Akihiro Tanaka, Nobuhiro Tsutsumi, Yoshiaki Inukai and Mikio Nakazono
Plants 2020, 9(5), 610; https://doi.org/10.3390/plants9050610 - 11 May 2020
Cited by 42 | Viewed by 4814
Abstract
Internal oxygen diffusion from shoot to root tips is enhanced by the formation of aerenchyma (gas space) in waterlogged soils. Lysigenous aerenchyma is created by programmed cell death and subsequent lysis of the root cortical cells. Rice (Oryza sativa) forms aerenchyma [...] Read more.
Internal oxygen diffusion from shoot to root tips is enhanced by the formation of aerenchyma (gas space) in waterlogged soils. Lysigenous aerenchyma is created by programmed cell death and subsequent lysis of the root cortical cells. Rice (Oryza sativa) forms aerenchyma constitutively under aerobic conditions and increases its formation under oxygen-deficient conditions. Recently, we have demonstrated that constitutive aerenchyma formation is regulated by auxin signaling mediated by Auxin/indole-3-acetic acid protein (AUX/IAA; IAA). While ethylene is involved in inducible aerenchyma formation, the relationship of auxin and ethylene during aerenchyma formation remains unclear. Here, we examined the effects of oxygen deficiency and ethylene on aerenchyma formation in the roots of a rice mutant (iaa13) in which auxin signaling is suppressed by a mutation in the degradation domain of IAA13 protein. The results showed that AUX/IAA-mediated auxin signaling contributes to ethylene-dependent inducible aerenchyma formation in rice roots. An auxin transport inhibitor abolished aerenchyma formation under oxygen-deficient conditions and reduced the expression of genes encoding ethylene biosynthesis enzymes, further supporting the idea that auxin is involved in ethylene-dependent inducible aerenchyma formation. Based on these studies, we propose a mechanism that underlies the relationship between auxin and ethylene during inducible aerenchyma formation in rice roots. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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19 pages, 2843 KiB  
Article
Eco-Physiological Traits Related to Recovery from Complete Submergence in the Model Legume Lotus japonicus
by Florencia B. Buraschi, Federico P.O. Mollard, Agustín A. Grimoldi and Gustavo G. Striker
Plants 2020, 9(4), 538; https://doi.org/10.3390/plants9040538 - 21 Apr 2020
Cited by 10 | Viewed by 2484
Abstract
Submergence is a severe form of stress for most plants. Lotus japonicus is a model legume with potential use in assisting breeding programs of closely related forage Lotus species. Twelve L. japonicus genotypes (10 recombinant inbred lines (RILs) and 2 parental accessions) with [...] Read more.
Submergence is a severe form of stress for most plants. Lotus japonicus is a model legume with potential use in assisting breeding programs of closely related forage Lotus species. Twelve L. japonicus genotypes (10 recombinant inbred lines (RILs) and 2 parental accessions) with different constitutive shoot to root dry mass ratios (S:R) were subjected to 7 days of submergence in clear water and allowed to recover for two weeks post-submergence; a set of non-submerged plants served as controls. Relative growth rate (RGR) was used to indicate the recovery ability of the plants. Leaf relative water content (RWC), stomatal conductance (gs), greenness of basal and apical leaves, and chlorophyll fluorescence (Fv/Fm, as a measure of photoinhibition) were monitored during recovery, and relationships among these variables and RGR were explored across genotypes. The main results showed (i) variation in recovery ability (RGR) from short-term complete submergence among genotypes, (ii) a trade-off between growth during vs. after the stress indicated by a negative correlation between RGR during submergence and RGR post-submergence, (iii) an inverse relationship between RGR during recovery and S:R upon de-submergence, (iv) positive relationships between RGR at early recovery and RWC and gs, which were negatively related to S:R, suggesting this parameter as a good estimator of plant water balance post-submergence, (v) chlorophyll retention allowed fast recovery as revealed by the positive relationship between greenness of basal and apical leaves and RGR during the first recovery week, and (vi) full repair of the submergence-damaged photosynthetic apparatus occurred more slowly (second recovery week) than full recovery of plant water relations. The inclusion of these traits contributing to submergence recovery in L. japonicus should be considered to speed up the breeding process of the closely related forage Lotus spp. used in current agriculture. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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13 pages, 3727 KiB  
Article
NADPH Oxidase RbohD and Ethylene Signaling are Involved in Modulating Seedling Growth and Survival Under Submergence Stress
by Chen-Pu Hong, Mao-Chang Wang and Chin-Ying Yang
Plants 2020, 9(4), 471; https://doi.org/10.3390/plants9040471 - 08 Apr 2020
Cited by 16 | Viewed by 3102
Abstract
In higher plants under low oxygen or hypoxic conditions, the phytohormone ethylene and hydrogen peroxide (H2O2) are involved in complex regulatory mechanisms in hypoxia signaling pathways. The respiratory burst oxidase homolog D (RbohD), an NADPH oxidase, is involved in [...] Read more.
In higher plants under low oxygen or hypoxic conditions, the phytohormone ethylene and hydrogen peroxide (H2O2) are involved in complex regulatory mechanisms in hypoxia signaling pathways. The respiratory burst oxidase homolog D (RbohD), an NADPH oxidase, is involved in the primary stages of hypoxia signaling, modulating the expression of downstream hypoxia-inducible genes under hypoxic stress. In this study, our data revealed that under normoxic conditions, seed germination was delayed in the rbohD/ein2-5 double mutant, whereas postgermination stage root growth was promoted. Under submergence, the rbohD/ein2-5 double mutant line had an inhibited root growth phenotype. Furthermore, chlorophyll content and leaf survival were reduced in the rbohD/ein2-5 double mutant compared with wild-type plants under submerged conditions. In quantitative RT-PCR analysis, the induction of Ethylene-responsive factor 73/hypoxia responsive 1 (AtERF73/HRE1) and alcohol dehydrogenase 1 (AtADH1) transcripts was lower in the rbohD/ein2-5 double mutant during hypoxic stress than in wild-type plants and in rbohD and ein2-5 mutant lines. Taken together, our results indicate that an interplay of ethylene and RbohD is involved in regulating seed germination and post-germination stages under normoxic conditions. Moreover, ethylene and RbohD are involved in modulating seedling root growth, leaf chlorophyll content, and hypoxia-inducible gene expression under hypoxic conditions. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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Review

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14 pages, 708 KiB  
Review
The Molecular Regulatory Pathways and Metabolic Adaptation in the Seed Germination and Early Seedling Growth of Rice in Response to Low O2 Stress
by Mingqing Ma, Weijian Cen, Rongbai Li, Shaokui Wang and Jijing Luo
Plants 2020, 9(10), 1363; https://doi.org/10.3390/plants9101363 - 14 Oct 2020
Cited by 26 | Viewed by 3883
Abstract
As sessile organisms, flooding/submergence is one of the major abiotic stresses for higher plants, with deleterious effects on their growth and survival. Therefore, flooding/submergence is a large challenge for agriculture in lowland areas worldwide. Long-term flooding/submergence can cause severe hypoxia stress to crop [...] Read more.
As sessile organisms, flooding/submergence is one of the major abiotic stresses for higher plants, with deleterious effects on their growth and survival. Therefore, flooding/submergence is a large challenge for agriculture in lowland areas worldwide. Long-term flooding/submergence can cause severe hypoxia stress to crop plants and can result in substantial yield loss. Rice has evolved distinct adaptive strategies in response to low oxygen (O2) stress caused by flooding/submergence circumstances. Recently, direct seeding practice has been increasing in popularity due to its advantages of reducing cultivation cost and labor. However, establishment and growth of the seedlings from seed germination under the submergence condition are large obstacles for rice in direct seeding practice. The physiological and molecular regulatory mechanisms underlying tolerant and sensitive phenotypes in rice have been extensively investigated. Here, this review focuses on the progress of recent advances in the studies of the molecular mechanisms and metabolic adaptions underlying anaerobic germination (AG) and coleoptile elongation. Further, we highlight the prospect of introducing quantitative trait loci (QTL) for AG into rice mega varieties to ensure the compatibility of flooding/submergence tolerance traits and yield stability, thereby advancing the direct seeding practice and facilitating future breeding improvement. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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25 pages, 1572 KiB  
Review
Keep Calm and Survive: Adaptation Strategies to Energy Crisis in Fruit Trees under Root Hypoxia
by Ariel Salvatierra, Guillermo Toro, Patricio Mateluna, Ismael Opazo, Mauricio Ortiz and Paula Pimentel
Plants 2020, 9(9), 1108; https://doi.org/10.3390/plants9091108 - 27 Aug 2020
Cited by 19 | Viewed by 4918
Abstract
Plants are permanently facing challenges imposed by the environment which, in the context of the current scenario of global climate change, implies a constant process of adaptation to survive and even, in the case of crops, at least maintain yield. O2 deficiency [...] Read more.
Plants are permanently facing challenges imposed by the environment which, in the context of the current scenario of global climate change, implies a constant process of adaptation to survive and even, in the case of crops, at least maintain yield. O2 deficiency at the rhizosphere level, i.e., root hypoxia, is one of the factors with the greatest impact at whole-plant level. At cellular level, this O2 deficiency provokes a disturbance in the energy metabolism which has notable consequences on the yield of plant crops. In this sense, although several physiological studies describe processes involved in plant adaptation to root hypoxia in woody fruit trees, with emphasis on the negative impacts on photosynthetic rate, there are very few studies that include -omics strategies for specifically understanding these processes in the roots of such species. Through a de novo assembly approach, a comparative transcriptome study of waterlogged Prunus spp. genotypes contrasting in their tolerance to root hypoxia was revisited in order to gain a deeper insight into the reconfiguration of pivotal pathways involved in energy metabolism. This re-analysis describes the classically altered pathways seen in the roots of woody fruit trees under hypoxia, but also routes that link them to pathways involved with nitrogen assimilation and the maintenance of cytoplasmic pH and glycolytic flow. In addition, the effects of root hypoxia on the transcription of genes related to the mitochondrial oxidative phosphorylation system, responsible for providing adenosine triphosphate (ATP) to the cell, are discussed in terms of their roles in the energy balance, reactive oxygen species (ROS) metabolism and aerenchyma formation. This review compiles key findings that help to explain the trait of tolerance to root hypoxia in woody fruit species, giving special attention to their strategies for managing the energy crisis. Finally, research challenges addressing less-explored topics in recovery and stress memory in woody fruit trees are pointed out. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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11 pages, 624 KiB  
Review
Molecular Mechanisms Supporting Rice Germination and Coleoptile Elongation under Low Oxygen
by Chiara Pucciariello
Plants 2020, 9(8), 1037; https://doi.org/10.3390/plants9081037 - 15 Aug 2020
Cited by 19 | Viewed by 5899
Abstract
Rice germinates under submergence by exploiting the starch available in the endosperm and translocating sugars from source to sink organs. The availability of fermentable sugar under water allows germination with the protrusion of the coleoptile, which elongates rapidly and functions as a snorkel [...] Read more.
Rice germinates under submergence by exploiting the starch available in the endosperm and translocating sugars from source to sink organs. The availability of fermentable sugar under water allows germination with the protrusion of the coleoptile, which elongates rapidly and functions as a snorkel toward the air above. Depending on the variety, rice can produce a short or a long coleoptile. Longer length entails the involvement of a functional transport of auxin along the coleoptile. This paper is an overview of rice coleoptiles and the studies undertaken to understand its functioning and role under submergence. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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14 pages, 1912 KiB  
Review
The Many Facets of Hypoxia in Plants
by Elena Loreti and Pierdomenico Perata
Plants 2020, 9(6), 745; https://doi.org/10.3390/plants9060745 - 12 Jun 2020
Cited by 69 | Viewed by 12741
Abstract
Plants are aerobic organisms that require oxygen for their respiration. Hypoxia arises due to the insufficient availability of oxygen, and is sensed by plants, which adapt their growth and metabolism accordingly. Plant hypoxia can occur as a result of excessive rain and soil [...] Read more.
Plants are aerobic organisms that require oxygen for their respiration. Hypoxia arises due to the insufficient availability of oxygen, and is sensed by plants, which adapt their growth and metabolism accordingly. Plant hypoxia can occur as a result of excessive rain and soil waterlogging, thus constraining plant growth. Increasing research on hypoxia has led to the discovery of the mechanisms that enable rice to be productive even when partly submerged. The identification of Ethylene Response Factors (ERFs) as the transcription factors that enable rice to survive submergence has paved the way to the discovery of oxygen sensing in plants. This, in turn has extended the study of hypoxia to plant development and plant–microbe interaction. In this review, we highlight the many facets of plant hypoxia, encompassing stress physiology, developmental biology and plant pathology. Full article
(This article belongs to the Special Issue Plant Responses to Hypoxia)
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