Regulation of Hormones Response in Plant Development and Stress Response: Dilemma or Synergy

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Plant, Algae and Fungi Cell Biology".

Deadline for manuscript submissions: closed (15 January 2023) | Viewed by 31478

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Guest Editor
Laboratoire de Recherche en Sciences Végétales, GBF Team, Université de Toulouse, CNRS, UPS, Toulouse INP, 24 Chemin de Borde Rouge, Auzeville, BP42617, 31326 Castanet-Tolosan, France
Interests: fruit growth and ripening; hormone signaling; fruit set; transcriptional regulation; biotechnology; ethylene response factors
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Department of Horticultural Genetics and Biotechnology, Mediterranean Agronomic Institute of Chania (MAICh), Alsyllio Agrokepiou, Chania, 73100 Crete, Greece
Interests: tomato fruit growth and ripening; hypoxic adaptation; abscission; prolyl 4 hydroxylases; arabinogalactan proteins (AGPs); abiotic stress
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

As sessile organisms, plants grow and develop in a continuously changing environment without any possibility of escaping multiple, overlapping forms of abiotic and biotic stresses. Plant hormones, as molecule signals, will adjust their transcriptome, proteome, and metabolome in accordance with their organ developmental stage and adapt to stress. For most hormones, the different actors have been identified; however, the borders between hormones and molecule signals, such as ROS, are fuzzier, and a great deal of effort is now being made to decipher these pathways.

A plethora of recent research demonstrates the importance of hormonal crosstalk in regulating developmental processes and plants’ response to stress. In this context, hormonal signaling pathways cannot be considered to be isolated without any interaction or overlap with other pathways. Indeed, at each step from biosynthesis to perception and molecular response, there is mounting evidence that chromatin structure modifications, microRNAs, or post-translational modifications play regulatory roles. The between developmental programs and stress adaptation overlap at the molecular mechanism level might be regulated by hormones’ responses to molecular signals in ways not previously known.  

The aim of this Special Issue is to address and summarize recent advances in the role of hormones in plant development and response to stresses. How does the stress response influence the developmental program? How can hormonal response participate in recovery from stress? 

We aim to highlight the molecular mechanisms underlying hormone biosynthesis, perception, transduction, and response, particularly in the context of hormonal interplay and feedback regulatory mechanisms. Reviews and original research focusing on specific hormones are also welcome.

Dr. Julien Pirrello
Dr. Panagiotis Kalaitzis
Guest Editors

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Keywords

  • hormone
  • plants
  • crosstalk
  • biosynthesis
  • perception
  • signaling
  • biotic stress
  • abiotic stress
  • development
  • signal transduction
  • transcription factors
  • molecule signal
  • transcriptome
  • metabolome
  • proteome
  • post-translational modification

Related Special Issue

Published Papers (11 papers)

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Research

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29 pages, 10676 KiB  
Article
Response of Prolyl 4 Hydroxylases, Arabinogalactan Proteins and Homogalacturonans in Four Olive Cultivars under Long-Term Salinity Stress in Relation to Physiological and Morphological Changes
by Aristotelis Azariadis, Filippos Vouligeas, Elige Salame, Mohamed Kouhen, Myrto Rizou, Kostantinos Blazakis, Penelope Sotiriou, Lamia Ezzat, Khansa Mekkaoui, Aline Monzer, Afroditi Krokida, Ioannis-Dimosthenis Adamakis, Faten Dandachi, Boushra Shalha, George Kostelenos, Eleftheria Figgou, Eleni Giannoutsou and Panagiotis Kalaitzis
Cells 2023, 12(11), 1466; https://doi.org/10.3390/cells12111466 - 24 May 2023
Viewed by 1291
Abstract
Olive (Olea europeae L.) salinity stress induces responses at morphological, physiological and molecular levels, affecting plant productivity. Four olive cultivars with differential tolerance to salt were grown under saline conditions in long barrels for regular root growth to mimic field conditions. Arvanitolia [...] Read more.
Olive (Olea europeae L.) salinity stress induces responses at morphological, physiological and molecular levels, affecting plant productivity. Four olive cultivars with differential tolerance to salt were grown under saline conditions in long barrels for regular root growth to mimic field conditions. Arvanitolia and Lefkolia were previously reported as tolerant to salinity, and Koroneiki and Gaidourelia were characterized as sensitive, exhibiting a decrease in leaf length and leaf area index after 90 days of salinity. Prolyl 4-hydroxylases (P4Hs) hydroxylate cell wall glycoproteins such as arabinogalactan proteins (AGPs). The expression patterns of P4Hs and AGPs under saline conditions showed cultivar-dependent differences in leaves and roots. In the tolerant cultivars, no changes in OeP4H and OeAGP mRNAs were observed, while in the sensitive cultivars, the majority of OeP4Hs and OeAGPs were upregulated in leaves. Immunodetection showed that the AGP signal intensity and the cortical cell size, shape and intercellular spaces under saline conditions were similar to the control in Arvanitolia, while in Koroneiki, a weak AGP signal was associated with irregular cells and intercellular spaces, leading to aerenchyma formation after 45 days of NaCl treatment. Moreover, the acceleration of endodermal development and the formation of exodermal and cortical cells with thickened cell walls were observed, and an overall decrease in the abundance of cell wall homogalacturonans was detected in salt-treated roots. In conclusion, Arvanitolia and Lefkolia exhibited the highest adaptive capacity to salinity, indicating that their use as rootstocks might provide increased tolerance to irrigation with saline water. Full article
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21 pages, 5365 KiB  
Article
BRI1 and BAK1 Canonical Distribution in Plasma Membrane Is HSP90 Dependent
by Despina Samakovli, Loukia Roka, Panagiota Konstantinia Plitsi, Georgia Drakakaki, Kosmas Haralampidis, Dimitrios J. Stravopodis, Polydefkis Hatzopoulos and Dimitra Milioni
Cells 2022, 11(21), 3341; https://doi.org/10.3390/cells11213341 - 22 Oct 2022
Cited by 3 | Viewed by 1902
Abstract
The activation of BRASSINOSTEROID INSENSITIVE1 (BRI1) and its association with the BRI1 ASSOCIATED RECEPTOR KINASE1 (BAK1) are key steps for the initiation of the BR signaling cascade mediating hypocotyl elongation. Heat shock protein 90 (HSP90) is crucial in the regulation of signaling processes [...] Read more.
The activation of BRASSINOSTEROID INSENSITIVE1 (BRI1) and its association with the BRI1 ASSOCIATED RECEPTOR KINASE1 (BAK1) are key steps for the initiation of the BR signaling cascade mediating hypocotyl elongation. Heat shock protein 90 (HSP90) is crucial in the regulation of signaling processes and the activation of hormonal receptors. We report that HSP90 is required for the maintenance of the BRI1 receptor at the plasma membrane (PM) and its association with the BAK1 co-receptor during BL-ligand stimulation. HSP90 mediates BR perception and signal transduction through physical interactions with BRI1 and BAK1, while chaperone depletion resulted in lower levels of BRI1 and BAK1 receptors at the PM and affected the spatial partitioning and organization of BRI1/BAK1 heterocomplexes at the PM. The BRI1/BAK1 interaction relies on the HSP90-dependent activation of the kinase domain of BRI1 which leads to the confinement of the spatial dynamics of the membrane resident BRI1 and the attenuation of the downstream signaling. This is evident by the impaired activation and transcriptional activity of BRI1 EMS SUPPRESSOR 1 (BES1) upon HSP90 depletion. Our findings provide conclusive evidence that further expands the commitment of HSP90 in BR signaling through the HSP90-mediated activation of BRI1 in the control of the BR signaling cascade in plants. Full article
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15 pages, 4160 KiB  
Article
GhWRKY33 Interacts with GhTIFY10A to Synergistically Modulate Both Ageing and JA-Mediated Leaf Senescence in Arabidopsis
by Songguo Wu, Huimin Zhang, Ruling Wang, Guimei Chang, Yifen Jing, Zhifang Li and Ligang Chen
Cells 2022, 11(15), 2328; https://doi.org/10.3390/cells11152328 - 29 Jul 2022
Cited by 1 | Viewed by 1517
Abstract
WRKY transcription factors play critical roles in the modulation of transcriptional changes during leaf senescence, but the underlying mechanisms controlled by them in this progress still remain enigmatic. In this study, Gossypium hirsutum WRKY DNA-binding protein 33 (GhWRKY33) was characterized as [...] Read more.
WRKY transcription factors play critical roles in the modulation of transcriptional changes during leaf senescence, but the underlying mechanisms controlled by them in this progress still remain enigmatic. In this study, Gossypium hirsutum WRKY DNA-binding protein 33 (GhWRKY33) was characterized as a negative regulator of both ageing and JA-mediated leaf senescence. The overexpression of GhWRKY33 in Arabidopsis greatly delayed leaf senescence, as determined by elevated chlorophyll content, lower H2O2 content, and reduced expression of several senescence-associated genes (SAGs). An electrophoretic mobility shift assay (EMSA) and transient dual–luciferase reporter assay revealed that GhWRKY33 could bind to the promoters of both AtSAG12 and Ghcysp and suppress their expression. Yeast two-hybrid (Y2H) and firefly luciferase complementation imaging (LUC) assays showed that GhWRKY33 could interact with GhTIFY10A. Similarly, the overexpression of GhTIFY10A in Arabidopsis also dramatically delayed leaf senescence. Furthermore, both GhWRKY33 and GhTIFY10A negatively regulate JA-mediated leaf senescence. In addition, a transientdual-luciferase reporter assay indicated that GhWRKY33 and GhTIFY10A could function synergistically to inhibit the expression of both AtSAG12 and Ghcysp. Thus, our work suggested that GhWRKY33 may function as a negative regulator to modulate both ageing and JA-mediated leaf senescence and also contributes to a basis for further functional studies on cotton leaf senescence. Full article
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20 pages, 4429 KiB  
Article
Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants
by Yuzhu Wang, Yeling Zhou and Jiansheng Liang
Cells 2022, 11(13), 2039; https://doi.org/10.3390/cells11132039 - 27 Jun 2022
Cited by 4 | Viewed by 2143
Abstract
Abscisic acid (ABA) is a critical phytohormone involved in multifaceted processes in plant metabolism and growth under both stressed and nonstressed conditions. Its accumulation in various tissues and cells has long been established as a biomarker for plant stress responses. To date, a [...] Read more.
Abscisic acid (ABA) is a critical phytohormone involved in multifaceted processes in plant metabolism and growth under both stressed and nonstressed conditions. Its accumulation in various tissues and cells has long been established as a biomarker for plant stress responses. To date, a comprehensive understanding of ABA distribution and dynamics at subcellular resolution in response to environmental cues is still lacking. Here, we modified the previously developed ABA sensor ABAleon2.1_Tao3 (Tao3) and targeted it to different organelles including the endoplasmic reticulum (ER), chloroplast/plastid, and nucleus through the addition of corresponding signal peptides. Together with the cytosolic Tao3, we show distinct ABA distribution patterns in different tobacco cells with the chloroplast showing a lower level of ABA in both cell types. In a tobacco mesophyll cell, organellar ABA displayed specific alterations depending on osmotic stimulus, with ABA levels being generally enhanced under a lower and higher concentration of salt and mannitol treatment, respectively. In Arabidopsis roots, cells from both the meristem and elongation zone accumulated ABA considerably in the cytoplasm upon mannitol treatment, while the plastid and nuclear ABA was generally reduced dependent upon specific cell types. In Arabidopsis leaf tissue, subcellular ABA seemed to be less responsive when stressed, with notable increases of ER ABA in epidermal cells and a reduction of nuclear ABA in guard cells. Together, our results present a detailed characterization of stimulus-dependent cell type-specific organellar ABA responses in tobacco and Arabidopsis plants, supporting a highly coordinated regulatory network for mediating subcellular ABA homeostasis during plant adaptation processes. Full article
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Review

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14 pages, 1042 KiB  
Review
Nitrate, Auxin and Cytokinin—A Trio to Tango
by Rashed Abualia, Stefan Riegler and Eva Benkova
Cells 2023, 12(12), 1613; https://doi.org/10.3390/cells12121613 - 13 Jun 2023
Cited by 4 | Viewed by 1613
Abstract
Nitrogen is an important macronutrient required for plant growth and development, thus directly impacting agricultural productivity. In recent years, numerous studies have shown that nitrogen-driven growth depends on pathways that control nitrate/nitrogen homeostasis and hormonal networks that act both locally and systemically to [...] Read more.
Nitrogen is an important macronutrient required for plant growth and development, thus directly impacting agricultural productivity. In recent years, numerous studies have shown that nitrogen-driven growth depends on pathways that control nitrate/nitrogen homeostasis and hormonal networks that act both locally and systemically to coordinate growth and development of plant organs. In this review, we will focus on recent advances in understanding the role of the plant hormones auxin and cytokinin and their crosstalk in nitrate-regulated growth and discuss the significance of novel findings and possible missing links. Full article
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21 pages, 1108 KiB  
Review
Jasmonic Acid as a Mediator in Plant Response to Necrotrophic Fungi
by Violetta Katarzyna Macioszek, Tomasz Jęcz, Iwona Ciereszko and Andrzej Kiejstut Kononowicz
Cells 2023, 12(7), 1027; https://doi.org/10.3390/cells12071027 - 27 Mar 2023
Cited by 6 | Viewed by 2433
Abstract
Jasmonic acid (JA) and its derivatives, all named jasmonates, are the simplest phytohormones which regulate multifarious plant physiological processes including development, growth and defense responses to various abiotic and biotic stress factors. Moreover, jasmonate plays an important mediator’s role during plant interactions with [...] Read more.
Jasmonic acid (JA) and its derivatives, all named jasmonates, are the simplest phytohormones which regulate multifarious plant physiological processes including development, growth and defense responses to various abiotic and biotic stress factors. Moreover, jasmonate plays an important mediator’s role during plant interactions with necrotrophic oomycetes and fungi. Over the last 20 years of research on physiology and genetics of plant JA-dependent responses to pathogens and herbivorous insects, beginning from the discovery of the JA co-receptor CORONATINE INSENSITIVE1 (COI1), research has speeded up in gathering new knowledge on the complexity of plant innate immunity signaling. It has been observed that biosynthesis and accumulation of jasmonates are induced specifically in plants resistant to necrotrophic fungi (and also hemibiotrophs) such as mostly investigated model ones, i.e., Botrytis cinerea, Alternaria brassicicola or Sclerotinia sclerotiorum. However, it has to be emphasized that the activation of JA-dependent responses takes place also during susceptible interactions of plants with necrotrophic fungi. Nevertheless, many steps of JA function and signaling in plant resistance and susceptibility to necrotrophs still remain obscure. The purpose of this review is to highlight and summarize the main findings on selected steps of JA biosynthesis, perception and regulation in the context of plant defense responses to necrotrophic fungal pathogens. Full article
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18 pages, 3007 KiB  
Review
Melatonin and Indole-3-Acetic Acid Synergistically Regulate Plant Growth and Stress Resistance
by Min Zhang, Chunxue Gao, Ling Xu, Hui Niu, Qian Liu, Yixiao Huang, Guoshuai Lv, Hengshan Yang and Minhui Li
Cells 2022, 11(20), 3250; https://doi.org/10.3390/cells11203250 - 16 Oct 2022
Cited by 15 | Viewed by 3164
Abstract
Plant growth and development exhibit plasticity, and plants can adapt to environmental changes and stress. Various phytohormones interact synergistically or antagonistically to regulate these responses. Melatonin and indole-3-acetic acid (IAA) are widespread across plant kingdom. Melatonin, an important member of the neuroendocrine immune [...] Read more.
Plant growth and development exhibit plasticity, and plants can adapt to environmental changes and stress. Various phytohormones interact synergistically or antagonistically to regulate these responses. Melatonin and indole-3-acetic acid (IAA) are widespread across plant kingdom. Melatonin, an important member of the neuroendocrine immune regulatory network, can confer autoimmunity and protect against viral invasion. Melatonin functions as a plant growth regulator and biostimulant, with an important role in enhancing plant stress tolerance. IAA has a highly complex stress response mechanism, which participates in a series of stress induced physiological changes. This article reviews studies on the signaling pathways of melatonin and IAA, focusing on specific regulatory mechanisms. We discuss how these hormones coordinate plant growth and development and stress responses. Furthermore, the interactions between melatonin and IAA and their upstream and downstream transcriptional regulation are discussed from the perspective of modulating plant development and stress adaptation. The reviewed studies suggest that, at low concentrations, melatonin promotes IAA synthesis, whereas at high levels it reduces IAA levels. Similarly to IAA, melatonin promotes plant growth and development. IAA suppresses the melatonin induced inhibition of germination. IAA signaling plays an important role in plant growth and development, whereas melatonin signaling plays an important role in stress responses. Full article
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12 pages, 614 KiB  
Review
Progress in Salicylic Acid-Dependent Signaling for Growth–Defense Trade-Off
by Ching Chan
Cells 2022, 11(19), 2985; https://doi.org/10.3390/cells11192985 - 25 Sep 2022
Cited by 5 | Viewed by 2636
Abstract
One grand challenge for studying plant biotic and abiotic stress responses is to optimize plant growth and plasticity under variable environmental constraints, which in the long run benefits agricultural production. However, efforts in promoting plant immunity are often accompanied by compromised morphological “syndromes” [...] Read more.
One grand challenge for studying plant biotic and abiotic stress responses is to optimize plant growth and plasticity under variable environmental constraints, which in the long run benefits agricultural production. However, efforts in promoting plant immunity are often accompanied by compromised morphological “syndromes” such as growth retardation, sterility, and reduced yield. Such a trade-off is dictated by complex signaling driven by secondary messengers and phytohormones. Salicylic acid (SA) is a well-known phytohormone essential for basal immunity and systemic acquired resistance. Interestingly, recent updates suggest that external environmental cues, nutrient status, developmental stages, primary metabolism, and breeding strategies attribute an additional layer of control over SA-dependent signaling, and, hence, plant performance against pathogens. In this review, these external and internal factors are summarized, focusing on their specific roles on SA biosynthesis and downstream signaling leading to immunity. A few considerations and future opportunities are highlighted to improve plant fitness with minimal growth compensation. Full article
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15 pages, 1327 KiB  
Review
Roles of Auxin in the Growth, Development, and Stress Tolerance of Horticultural Plants
by Qiongdan Zhang, Min Gong, Xin Xu, Honghai Li and Wei Deng
Cells 2022, 11(17), 2761; https://doi.org/10.3390/cells11172761 - 05 Sep 2022
Cited by 20 | Viewed by 6206
Abstract
Auxin, a plant hormone, regulates virtually every aspect of plant growth and development. Many current studies on auxin focus on the model plant Arabidopsis thaliana, or on field crops, such as rice and wheat. There are relatively few studies on what role auxin [...] Read more.
Auxin, a plant hormone, regulates virtually every aspect of plant growth and development. Many current studies on auxin focus on the model plant Arabidopsis thaliana, or on field crops, such as rice and wheat. There are relatively few studies on what role auxin plays in various physiological processes of a range of horticultural plants. In this paper, recent studies on the role of auxin in horticultural plant growth, development, and stress response are reviewed to provide novel insights for horticultural researchers and cultivators to improve the quality and application of horticultural crops. Full article
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21 pages, 2586 KiB  
Review
Contrasting Roles of Ethylene Response Factors in Pathogen Response and Ripening in Fleshy Fruit
by Shan Li, Pan Wu, Xiaofen Yu, Jinping Cao, Xia Chen, Lei Gao, Kunsong Chen and Donald Grierson
Cells 2022, 11(16), 2484; https://doi.org/10.3390/cells11162484 - 10 Aug 2022
Cited by 9 | Viewed by 3312
Abstract
Fleshy fruits are generally hard and unpalatable when unripe; however, as they mature, their quality is transformed by the complex and dynamic genetic and biochemical process of ripening, which affects all cell compartments. Ripening fruits are enriched with nutrients such as acids, sugars, [...] Read more.
Fleshy fruits are generally hard and unpalatable when unripe; however, as they mature, their quality is transformed by the complex and dynamic genetic and biochemical process of ripening, which affects all cell compartments. Ripening fruits are enriched with nutrients such as acids, sugars, vitamins, attractive volatiles and pigments and develop a pleasant taste and texture and become attractive to eat. Ripening also increases sensitivity to pathogens, and this presents a crucial problem for fruit postharvest transport and storage: how to enhance pathogen resistance while maintaining ripening quality. Fruit development and ripening involve many changes in gene expression regulated by transcription factors (TFs), some of which respond to hormones such as auxin, abscisic acid (ABA) and ethylene. Ethylene response factor (ERF) TFs regulate both fruit ripening and resistance to pathogen stresses. Different ERFs regulate fruit ripening and/or pathogen responses in both fleshy climacteric and non-climacteric fruits and function cooperatively or independently of other TFs. In this review, we summarize the current status of studies on ERFs that regulate fruit ripening and responses to infection by several fungal pathogens, including a systematic ERF transcriptome analysis of fungal grey mould infection of tomato caused by Botrytis cinerea. This deepening understanding of the function of ERFs in fruit ripening and pathogen responses may identify novel approaches for engineering transcriptional regulation to improve fruit quality and pathogen resistance. Full article
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21 pages, 2452 KiB  
Review
PYR/PYL/RCAR Receptors Play a Vital Role in the Abscisic-Acid-Dependent Responses of Plants to External or Internal Stimuli
by Justyna Fidler, Jakub Graska, Marta Gietler, Małgorzata Nykiel, Beata Prabucka, Anna Rybarczyk-Płońska, Ewa Muszyńska, Iwona Morkunas and Mateusz Labudda
Cells 2022, 11(8), 1352; https://doi.org/10.3390/cells11081352 - 15 Apr 2022
Cited by 22 | Viewed by 3961
Abstract
Abscisic acid (ABA) is a phytohormone that plays a key role in regulating several developmental processes as well as in response to stressful conditions such as drought. Activation of the ABA signaling cascade allows the induction of an appropriate physiological response. The basic [...] Read more.
Abscisic acid (ABA) is a phytohormone that plays a key role in regulating several developmental processes as well as in response to stressful conditions such as drought. Activation of the ABA signaling cascade allows the induction of an appropriate physiological response. The basic components of the ABA signaling pathway have been recognized and characterized in recent years. Pyrabactin resistance, pyrabactin resistance-like, and the regulatory component of ABA receptors (PYR/PYL/RCAR) are the major components responsible for the regulation of the ABA signaling pathway. Here, we review recent findings concerning the PYR/PYL/RCAR receptor structure, function, and interaction with other components of the ABA signaling pathway as well as the termination mechanism of ABA signals in plant cells. Since ABA is one of the basic elements related to abiotic stress, which is increasingly common in the era of climate changes, understanding the perception and transduction of the signal related to this phytohormone is of paramount importance in further increasing crop tolerance to various stress factors. Full article
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