ROS Responses in Plants

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (30 December 2019) | Viewed by 68780

Special Issue Editors


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Guest Editor
Science Research Center, Yamaguchi University, Yamaguchi 753-8515, Japan
Interests: reactive oxygen species (ROS) signaling; reactive carbonyl species; oxylipin; environmental stress; programmed cell death
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Guest Editor
Graduate School of Environmental and Life Science, Okayama University, 700-8530 Okayama, Japan
Interests: reactive oxygen species (ROS) signaling; stomatal movement; Ca2+ signaling; guard cell signaling; ion channels
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, 278-8510 Noda, Japan
Interests: reactive oxygen species (ROS) in immunity; stress responses; development; reproduction, and programmed cell death in plants; Ca2+ signaling

Special Issue Information

Dear Colleagues,

Reactive oxygen species (ROS) designates O2-derived reactive molecules including the superoxide anion radical, hydrogen peroxide, singlet oxygen, and the hydroxyl radical. The critical significance of ROS in various aspects of plant life—ranging from the reprogramming during development to the defense response against stress and programmed cell death—is well accepted, and the terms ‘oxidative stress’ and ‘ROS signaling’ are now very often seen in articles in plant sciences. On the other hand, our understanding of the mechanisms of ROS action has been hampered by the nature of ROS in cells: they have high reactivity and their levels are kept very low by abundant antioxidants. The current study of ROS in plants and animals presents many challenges, for example: (i) In which cell compartments (or membranes) are distinct ROS produced and where do they react with their targets? (ii) Is an observed increase in ROS level the cause of cell damage or just a resulting symptom of it? (iii) In ROS-mediated signaling, how can ROS, rather universal species, induce a response specific to the original stimulus? (iv) What is the identity of ROS signal receptors and sensors? (v) By what biochemical mechanisms are ROS signals recognized and transmitted? (vi) How can ROS signal be allowed to travel among organelles and even cells, in a situation in which cells are filled with antioxidants? (vii) What biochemical factors determine cell’s fate, i.e., defense (survival) or death, upon ROS stimulus?

To improve our understanding, several breakthroughs in technology and in knowledge are required. In this Special Issue, we would like to invite research articles and reviews that tackle these challenges and explore new horizons of ROS study in plants.

Prof. Jun’ichi Mano
Prof. Yoshiyuki Murata
Prof. Kazuyuki Kuchitsu
Guest Editors

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Keywords

  • ROS signaling
  • hormonal response
  • environmental stress
  • defense responses and plant immunity
  • programmed cell death
  • plant development
  • reactive electrophiles
  • protein thiol modification
  • apoplast
  • cell wall

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Published Papers (12 papers)

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Research

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14 pages, 1456 KiB  
Article
Photorespiration Enhances Acidification of the Thylakoid Lumen, Reduces the Plastoquinone Pool, and Contributes to the Oxidation of P700 at a Lower Partial Pressure of CO2 in Wheat Leaves
by Shinya Wada, Yuji Suzuki and Chikahiro Miyake
Plants 2020, 9(3), 319; https://doi.org/10.3390/plants9030319 - 3 Mar 2020
Cited by 19 | Viewed by 4340
Abstract
The oxidation of P700 in photosystem I (PSI) is a robust mechanism that suppresses the production of reactive oxygen species. We researched the contribution of photorespiration to the oxidation of P700 in wheat leaves. We analyzed the effects of changes in partial pressures [...] Read more.
The oxidation of P700 in photosystem I (PSI) is a robust mechanism that suppresses the production of reactive oxygen species. We researched the contribution of photorespiration to the oxidation of P700 in wheat leaves. We analyzed the effects of changes in partial pressures of CO2 and O2 on photosynthetic parameters. The electron flux in photosynthetic linear electron flow (LEF) exhibited a positive linear relationship with an origin of zero against the dissipation rate (vH+) of electrochromic shift (ECS; ΔpH across thylakoid membrane), indicating that cyclic electron flow around PSI did not contribute to H+ usage in photosynthesis/photorespiration. The vH+ showed a positive linear relationship with an origin of zero against the H+ consumption rates in photosynthesis/photorespiration (JgH+). These two linear relationships show that the electron flow in LEF is very efficiently coupled with H+ usage in photosynthesis/photorespiration. Lowering the intercellular partial pressure of CO2 enhanced the oxidation of P700 with the suppression of LEF. Under photorespiratory conditions, the oxidation of P700 and the reduction of the plastoquinone pool were stimulated with a decrease in JgH+, compared to non-photorespiratory conditions. These results indicate that the reduction-induced suppression of electron flow (RISE) suppresses the reduction of oxidized P700 in PSI under photorespiratory conditions. Furthermore, under photorespiratory conditions, ECS was larger and H+ conductance was lower against JgH+ than those under non-photorespiratory conditions. These results indicate that photorespiration enhances RISE and ΔpH formation by lowering H+ conductance, both of which contribute to keeping P700 in a highly oxidized state. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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13 pages, 601 KiB  
Article
Stress Responses of Shade-Treated Tea Leaves to High Light Exposure after Removal of Shading
by Satoshi Sano, Tetsuyuki Takemoto, Akira Ogihara, Kengo Suzuki, Takehiro Masumura, Shigeru Satoh, Kazufumi Takano, Yutaka Mimura and Shigeto Morita
Plants 2020, 9(3), 302; https://doi.org/10.3390/plants9030302 - 1 Mar 2020
Cited by 28 | Viewed by 4390
Abstract
High-quality green tea is produced from buds and young leaves grown by the covering-culture method, which employs shading treatment for tea plants (Camellia sinensis L.). Shading treatment improves the quality of tea, but shaded tea plants undergo sudden exposures to high light [...] Read more.
High-quality green tea is produced from buds and young leaves grown by the covering-culture method, which employs shading treatment for tea plants (Camellia sinensis L.). Shading treatment improves the quality of tea, but shaded tea plants undergo sudden exposures to high light (HL) at the end of the treatment by shade removal. In this study, the stress response of shaded tea plants to HL illumination was examined in field condition. Chl a/b ratio was lower in shaded plants than nonshaded control, but it increased due to exposure to HL after 14 days. Rapid decline in Fv/Fm values and increases in carbonylated protein level were induced by HL illumination in the shaded leaves on the first day, and they recovered thereafter between a period of one and two weeks. These results revealed that shaded tea plants temporarily suffered from oxidative damages caused by HL exposure, but they could also recover from these damages in 2 weeks. The activities of antioxidant enzymes, total ascorbate level, and ascorbate/dehydroascorbate ratio were decreased and increased in response to low light and HL conditions, respectively, suggesting that the upregulation of antioxidant defense systems plays a role in the protection of the shaded tea plants from HL stress. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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13 pages, 3652 KiB  
Article
Exogenous Dopamine Application Promotes Alkali Tolerance of Apple Seedlings
by Xueyi Jiao, Yuxing Li, Xiuzhi Zhang, Chenlu Liu, Wei Liang, Chao Li, Fengwang Ma and Cuiying Li
Plants 2019, 8(12), 580; https://doi.org/10.3390/plants8120580 - 7 Dec 2019
Cited by 37 | Viewed by 4204
Abstract
Arid and semiarid apple producing areas suffer from severe alkalinity of soil, which strongly affects the yield and quality of apples. Dopamine (DA) is involved in metabolic activities in response to abiotic stress in plants. To detect the effects of exogenous DA application [...] Read more.
Arid and semiarid apple producing areas suffer from severe alkalinity of soil, which strongly affects the yield and quality of apples. Dopamine (DA) is involved in metabolic activities in response to abiotic stress in plants. To detect the effects of exogenous DA application on the adaption of apple (Malus hupehensis) seedlings to alkali stress and as a protection from oxidative stress, 0.1 mM DA was identified as the most suitable concentration by hydroponic culture. Further experimentation showed that the growth and photosynthesis of apple seedlings were significantly inhibited under alkali stress, and more reactive oxygen species accumulated, compared with control. However, exogenous DA application suppressed the loss of the plant height, root length, chlorophyll levels, and photosynthetic capacity of apple seedlings that were caused by alkali stress. In the leaves of alkali stressed seedlings, the catalase, superoxide dismutase, and peroxidase activities were lower and hydrogen peroxide and malondialdehyde levels were higher than in the untreated plants. The presence of DA significantly alleviated such effects of alkali stress. In addition, exogenous DA application increased the antioxidant capacity of apple seedlings under alkali stress by increasing the level of chlorogenic acid. These results are significant for improving the alkali tolerance of apple in apple-producing areas with alkalized soil. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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17 pages, 1405 KiB  
Article
Exogenous Nitric Oxide Mitigates Nickel-Induced Oxidative Damage in Eggplant by Upregulating Antioxidants, Osmolyte Metabolism, and Glyoxalase Systems
by Mona Soliman, Haifa A. Alhaithloul, Khalid Rehman Hakeem, Basmah M. Alharbi, Mohamed El-Esawi and Amr Elkelish
Plants 2019, 8(12), 562; https://doi.org/10.3390/plants8120562 - 1 Dec 2019
Cited by 82 | Viewed by 4968
Abstract
Nitric oxide (NO) at optimal levels is considered beneficial to plant functioning. The present study was carried out to investigate the role of exogenously applied NO (100 and 150 µM sodium nitropurusside, SNP) in amelioration of nickel (Ni)-mediated oxidative effects in eggplant. Ni [...] Read more.
Nitric oxide (NO) at optimal levels is considered beneficial to plant functioning. The present study was carried out to investigate the role of exogenously applied NO (100 and 150 µM sodium nitropurusside, SNP) in amelioration of nickel (Ni)-mediated oxidative effects in eggplant. Ni stress declined growth and biomass production, relative water content (RWC), and chlorophyll pigment synthesis, thereby affecting the photosynthetic efficiency. Exogenously applied SNP proved beneficial in mitigating the Ni-mediated growth restrictions. NO-treated seedlings exhibited improved photosynthesis, stomatal conductance, and chlorophyll content with the effect of being apparent at lower concentration (100 µM SNP). SNP upregulated the antioxidant system mitigating the oxidative damage on membranes due to Ni stress. The activity of superoxide dismutase, catalase, glutathione S-transferase, ascorbate peroxidase, and glutathione reductase was upregulated due to SNP which also increased the ascorbate and reduced glutathione content. SNP-supplied seedlings also showed higher proline and glycine betaine accumulation, thereby improving RWC and antioxidant system. Glyoxalase I activity was induced due to SNP application declining the accumulation of methylglyoxal. NO-mediated mitigation of Ni toxicity was confirmed using NO scavenger (PTIO, 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide), which reversed the influence of SNP almost entirely on the parameters studied. Uptake of nitrogen (N), potassium (K), and calcium (Ca) was increased due to SNP application and Ni was reduced significantly. Therefore, this study revealed the efficiency of exogenous SNP in enhancing Ni stress tolerance through upregulating antioxidant and glyoxalase systems. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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19 pages, 3580 KiB  
Article
Understanding the Role of the Antioxidant System and the Tetrapyrrole Cycle in Iron Deficiency Chlorosis
by Carla S. Santos, Rengin Ozgur, Baris Uzilday, Ismail Turkan, Mariana Roriz, António O.S.S. Rangel, Susana M.P. Carvalho and Marta W. Vasconcelos
Plants 2019, 8(9), 348; https://doi.org/10.3390/plants8090348 - 13 Sep 2019
Cited by 49 | Viewed by 5578
Abstract
Iron deficiency chlorosis (IDC) is an abiotic stress often experienced by soybean, owing to the low solubility of iron in alkaline soils. Here, soybean lines with contrasting Fe efficiencies were analyzed to test the hypothesis that the Fe efficiency trait is linked to [...] Read more.
Iron deficiency chlorosis (IDC) is an abiotic stress often experienced by soybean, owing to the low solubility of iron in alkaline soils. Here, soybean lines with contrasting Fe efficiencies were analyzed to test the hypothesis that the Fe efficiency trait is linked to antioxidative stress signaling via proper management of tissue Fe accumulation and transport, which in turn influences the regulation of heme and non heme containing enzymes involved in Fe uptake and ROS scavenging. Inefficient plants displayed higher oxidative stress and lower ferric reductase activity, whereas root and leaf catalase activity were nine-fold and three-fold higher, respectively. Efficient plants do not activate their antioxidant system because there is no formation of ROS under iron deficiency; while inefficient plants are not able to deal with ROS produced under iron deficiency because ascorbate peroxidase and superoxide dismutase are not activated because of the lack of iron as a cofactor, and of heme as a constituent of those enzymes. Superoxide dismutase and peroxidase isoenzymatic regulation may play a determinant role: 10 superoxide dismutase isoenzymes were observed in both cultivars, but iron superoxide dismutase activity was only detected in efficient plants; 15 peroxidase isoenzymes were observed in the roots and trifoliate leaves of efficient and inefficient cultivars and peroxidase activity levels were only increased in roots of efficient plants. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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13 pages, 1710 KiB  
Article
Reactive Oxygen Species Alleviate Cell Death Induced by Thaxtomin A in Arabidopsis thaliana Cell Cultures
by Fatima Awwad, Guillaume Bertrand, Michel Grandbois and Nathalie Beaudoin
Plants 2019, 8(9), 332; https://doi.org/10.3390/plants8090332 - 6 Sep 2019
Cited by 10 | Viewed by 3780
Abstract
Thaxtomin A (TA) is a cellulose biosynthesis inhibitor synthesized by the soil actinobacterium Streptomyces scabies, which is the main causal agent of potato common scab. TA is essential for the induction of scab lesions on potato tubers. When added to Arabidopsis thaliana [...] Read more.
Thaxtomin A (TA) is a cellulose biosynthesis inhibitor synthesized by the soil actinobacterium Streptomyces scabies, which is the main causal agent of potato common scab. TA is essential for the induction of scab lesions on potato tubers. When added to Arabidopsis thaliana cell cultures, TA induces an atypical programmed cell death (PCD). Although production of reactive oxygen species (ROS) often correlates with the induction of PCD, we observed a decrease in ROS levels following TA treatment. We show that this decrease in ROS accumulation in TA-treated cells is not due to the activation of antioxidant enzymes. Moreover, Arabidopsis cell cultures treated with hydrogen peroxide (H2O2) prior to TA treatment had significantly fewer dead cells than cultures treated with TA alone. This suggests that H2O2 induces biochemical or molecular changes in cell cultures that alleviate the activation of PCD by TA. Investigation of the cell wall mechanics using atomic force microscopy showed that H2O2 treatment can prevent the decrease in cell wall rigidity observed after TA exposure. While we cannot exclude the possibility that H2O2 may promote cell survival by altering the cellular redox environment or signaling pathways, our results suggest that H2O2 may inhibit cell death, at least partially, by reinforcing the cell wall to prevent or compensate for damages induced by TA. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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17 pages, 1551 KiB  
Article
Hydrogen Peroxide and Superoxide Anion Radical Photoproduction in PSII Preparations at Various Modifications of the Water-Oxidizing Complex
by Andrey Khorobrykh
Plants 2019, 8(9), 329; https://doi.org/10.3390/plants8090329 - 5 Sep 2019
Cited by 17 | Viewed by 3926 | Correction
Abstract
The photoproduction of superoxide anion radical (O2−•) and hydrogen peroxide (H2O2) in photosystem II (PSII) preparations depending on the damage to the water-oxidizing complex (WOC) was investigated. The light-induced formation of O2−• and H [...] Read more.
The photoproduction of superoxide anion radical (O2−•) and hydrogen peroxide (H2O2) in photosystem II (PSII) preparations depending on the damage to the water-oxidizing complex (WOC) was investigated. The light-induced formation of O2−• and H2O2 in the PSII preparations rose with the increased destruction of the WOC. The photoproduction of superoxide both in the PSII preparations holding intact WOC and the samples with damage to the WOC was approximately two times higher than H2O2. The rise of O2−• and H2O2 photoproduction in the PSII preparations in the course of the disassembly of the WOC correlated with the increase in the fraction of the low-potential (LP) Cyt b559. The restoration of electron flow in the Mn-depleted PSII preparations by exogenous electron donors (diphenylcarbazide, Mn2+) suppressed the light-induced formation of O2−• and H2O2. The decrease of O2−• and H2O2 photoproduction upon the restoration of electron transport in the Mn-depleted PSII preparations could be due to the re-conversion of the LP Cyt b559 into higher potential forms. It is supposed that the conversion of the high potential Cyt b559 into its LP form upon damage to the WOC leads to the increase of photoproduction of O2−• and H2O2 in PSII. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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11 pages, 1436 KiB  
Article
Oxidation of P700 Induces Alternative Electron Flow in Photosystem I in Wheat Leaves
by Kanae Kadota, Riu Furutani, Amane Makino, Yuji Suzuki, Shinya Wada and Chikahiro Miyake
Plants 2019, 8(6), 152; https://doi.org/10.3390/plants8060152 - 5 Jun 2019
Cited by 28 | Viewed by 6301
Abstract
Oxygen (O2)-evolving photosynthetic organisms oxidize the reaction center chlorophyll, P700, in photosystem I (PSI) to suppress the production of reactive oxygen species. The oxidation of P700 is accompanied by alternative electron flow in PSI (AEF-I), which is not required for photosynthetic [...] Read more.
Oxygen (O2)-evolving photosynthetic organisms oxidize the reaction center chlorophyll, P700, in photosystem I (PSI) to suppress the production of reactive oxygen species. The oxidation of P700 is accompanied by alternative electron flow in PSI (AEF-I), which is not required for photosynthetic linear electron flow (LEF). To characterize AEF-I, we compared the redox reactions of P700 and ferredoxin (Fd) during the induction of carbon dioxide (CO2) assimilation in wheat leaves, using dark-interval relaxation kinetics analysis. Switching on an actinic light (1000 μmol photons m−2 s−1) at ambient CO2 partial pressure of 40 Pa and ambient O2 partial pressure of 21 kPa gradually oxidized P700 (P700+) and enhanced the reduction rate of P700+ (vP700) and oxidation rate of reduced Fd (vFd). The vFd showed a positive linear relationship with an apparent photosynthetic quantum yield of PSII (Y[II]) originating at point zero; the redox turnover of Fd is regulated by LEF via CO2 assimilation and photorespiration. The vP700 also showed a positive linear relationship with Y(II), but the intercept was positive, not zero. That is, the electron flux in PSI included the electron flux in AEF-I in addition to that in LEF. This indicates that the oxidation of P700 induces AEF-I. We propose a possible mechanism underlying AEF-I and its physiological role in the mitigation of oxidative damage. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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Review

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63 pages, 5275 KiB  
Review
Oxygen and ROS in Photosynthesis
by Sergey Khorobrykh, Vesa Havurinne, Heta Mattila and Esa Tyystjärvi
Plants 2020, 9(1), 91; https://doi.org/10.3390/plants9010091 - 10 Jan 2020
Cited by 169 | Viewed by 14669
Abstract
Oxygen is a natural acceptor of electrons in the respiratory pathway of aerobic organisms and in many other biochemical reactions. Aerobic metabolism is always associated with the formation of reactive oxygen species (ROS). ROS may damage biomolecules but are also involved in regulatory [...] Read more.
Oxygen is a natural acceptor of electrons in the respiratory pathway of aerobic organisms and in many other biochemical reactions. Aerobic metabolism is always associated with the formation of reactive oxygen species (ROS). ROS may damage biomolecules but are also involved in regulatory functions of photosynthetic organisms. This review presents the main properties of ROS, the formation of ROS in the photosynthetic electron transport chain and in the stroma of chloroplasts, and ROS scavenging systems of thylakoid membrane and stroma. Effects of ROS on the photosynthetic apparatus and their roles in redox signaling are discussed. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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23 pages, 2385 KiB  
Review
Reactive Carbonyl Species: A Missing Link in ROS Signaling
by Jun’ichi Mano, Md. Sanaullah Biswas and Koichi Sugimoto
Plants 2019, 8(10), 391; https://doi.org/10.3390/plants8100391 - 30 Sep 2019
Cited by 86 | Viewed by 8081
Abstract
As reactive oxygen species (ROS) play critical roles in plants to determine cell fate in various physiological situations, there is keen interest in the biochemical processes of ROS signal transmission. Reactive carbonyl species (RCS), the α,β-unsaturated aldehydes and ketones produced [...] Read more.
As reactive oxygen species (ROS) play critical roles in plants to determine cell fate in various physiological situations, there is keen interest in the biochemical processes of ROS signal transmission. Reactive carbonyl species (RCS), the α,β-unsaturated aldehydes and ketones produced from lipid peroxides, due to their chemical property to covalently modify protein, can mediate ROS signals to proteins. Comprehensive carbonyl analysis in plants has revealed that more than a dozen different RCS, e.g., acrolein, 4-hydroxy-(E)-2-nonenal and malondialdehyde, are produced from various membranes, and some of them increase and modify proteins in response to oxidative stimuli. At early stages of response, specific subsets of proteins are selectively modified with RCS. The involvement of RCS in ROS signaling can be judged on three criteria: (1) A stimulus to increase the ROS level in plants leads to the enhancement of RCS levels. (2) Suppression of the increase of RCS by scavenging enzymes or chemicals diminishes the ROS-induced response. (3) Addition of RCS to plants evokes responses similar to those induced by ROS. On these criteria, the RCS action as damaging/signaling agents has been demonstrated for root injury, programmed cell death, senescence of siliques, stomata response to abscisic acid, and root response to auxin. RCS thus act as damage/signal mediators downstream of ROS in a variety of physiological situations. A current picture and perspectives of RCS research are presented in this article. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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21 pages, 1419 KiB  
Review
Biotechnological Potential of LSD1, EDS1, and PAD4 in the Improvement of Crops and Industrial Plants
by Maciej Jerzy Bernacki, Weronika Czarnocka, Magdalena Szechyńska-Hebda, Ron Mittler and Stanisław Karpiński
Plants 2019, 8(8), 290; https://doi.org/10.3390/plants8080290 - 16 Aug 2019
Cited by 9 | Viewed by 6280
Abstract
Lesion Simulating Disease 1 (LSD1), Enhanced Disease Susceptibility (EDS1) and Phytoalexin Deficient 4 (PAD4) were discovered a quarter century ago as regulators of programmed cell death and biotic stress responses in Arabidopsis thaliana. Recent studies have demonstrated that these proteins are also [...] Read more.
Lesion Simulating Disease 1 (LSD1), Enhanced Disease Susceptibility (EDS1) and Phytoalexin Deficient 4 (PAD4) were discovered a quarter century ago as regulators of programmed cell death and biotic stress responses in Arabidopsis thaliana. Recent studies have demonstrated that these proteins are also required for acclimation responses to various abiotic stresses, such as high light, UV radiation, drought and cold, and that their function is mediated through secondary messengers, such as salicylic acid (SA), reactive oxygen species (ROS), ethylene (ET) and other signaling molecules. Furthermore, LSD1, EDS1 and PAD4 were recently shown to be involved in the modification of cell walls, and the regulation of seed yield, biomass production and water use efficiency. The function of these proteins was not only demonstrated in model plants, such as Arabidopsis thaliana or Nicotiana benthamiana, but also in the woody plant Populus tremula x tremuloides. In addition, orthologs of LSD1, EDS1, and PAD4 were found in other plant species, including different crop species. In this review, we focus on specific LSD1, EDS1 and PAD4 features that make them potentially important for agricultural and industrial use. Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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Other

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1 pages, 175 KiB  
Correction
Correction: Khorobrykh, A. Hydrogen Peroxide and Superoxide Anion Radical Photoproduction in PSII Preparations at Various Modifications of the Water-Oxidizing Complex. Plants 2019, 8, 329
by Andrey Khorobrykh
Plants 2021, 10(2), 187; https://doi.org/10.3390/plants10020187 - 20 Jan 2021
Cited by 1 | Viewed by 1334
Abstract
In the original article, there was a mistake in the legend for ** Figure 5 ** [...] Full article
(This article belongs to the Special Issue ROS Responses in Plants)
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