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Journal Article•DOI•

Diverse functional interactions between nitric oxide and abscisic acid in plant development and responses to stress

José León1, Mari Cruz Castillo1, Alberto Coego1, Jorge Lozano-Juste1, Jorge Lozano-Juste2, Ricardo Mir1 •
Polytechnic University of Valencia1, University of California, Riverside2
01 Mar 2014-Journal of Experimental Botany (Oxford University Press)-Vol. 65, Iss: 4, pp 907-921
TL;DR: Several examples of well-documented functional interactions between NO and ABA are analysed in light of the most recent reported data on seed dormancy and germination, stomata movements, leaf senescence, and responses to abiotic and biotic stresses.
Abstract: The extensive support for abscisic acid (ABA) involvement in the complex regulatory networks controlling stress responses and development in plants contrasts with the relatively recent role assigned to nitric oxide (NO). Because treatment with exogenous ABA leads to enhanced production of NO, it has been widely considered that NO participates downstream of ABA in controlling processes such as stomata movement, seed dormancy, and germination. However, data on leaf senescence and responses to stress suggest that the functional interaction between ABA and NO is more complex than previously thought, including not only cooperation but also antagonism. The functional relationship is probably determined by several factors including the time- and place-dependent pattern of accumulation of both molecules, the threshold levels, and the regulatory factors important for perception. These factors will determine the actions exerted by each regulator. Here, several examples of well-documented functional interactions between NO and ABA are analysed in light of the most recent reported data on seed dormancy and germination, stomata movements, leaf senescence, and responses to abiotic and biotic stresses.

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Citations
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Journal Article•DOI•
Nitric Oxide: A Multitasked Signaling Gas in Plants

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Patrícia Domingos1, Ana Margarida Prado1, Aloysius Wong2, Christoph A Gehring2, José A. Feijó3, José A. Feijó1 •
Instituto Gulbenkian de Ciência1, King Abdullah University of Science and Technology2, University of Maryland, College Park3
06 Apr 2015-Molecular Plant
TL;DR: The issues of enzymatic and chemical generation of NO in plants, NO sensing and downstream signaling, namely the putative cGMP and Ca(2+) pathways, ion-channel activity modulation, gene expression regulation, and the interface with other ROS, which can have a profound effect on both NO accumulation and function are addressed.

358 citations

Cites background from "Diverse functional interactions bet..."

  • ...Bursts of NO induced by auxins, ABA, 26 other elicitors,or hydrogen peroxide (H2O2) seem all to be dependent on NR activity (Bright et 27 al., 2006;Yamamoto-Katou et al., 2006;Kolbert et al., 2008; León et al., 2014;)....

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Journal Article•DOI•
Water relations in plants subjected to heavy metal stresses

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Renata Rucińska-Sobkowiak1•
Adam Mickiewicz University in Poznań1
11 Oct 2016-Acta Physiologiae Plantarum
TL;DR: In this paper, the root-derived ABA or ABA-induced signals might play a role in stomatal movement. But the root stomata closure is induced by direct interaction of toxic metals with guard cells and/or as a consequence of the early effects of metal toxicity on roots and stems.
Abstract: Concentrations of heavy metals in soil seldom reach a level sufficient to cause osmotic disturbances in plants. It is likely that water entry to the roots is indirectly governed by other factors which are themselves affected by metals. Decreased elongation of the primary root, impaired secondary growth, increased root dieback, or reduced root hair caused by toxic ions all exert a deleterious effect on the root-absorbing area and water uptake. Moreover, metals are able to decelerate short-distance water transfer both in symplast and apoplast, which in turn reduce the movement of water into the vascular system and affect water supply to the shoot. Long-distance transport is limited also due to decreased hydraulic conductivity in the root, stem and leaf midrib caused by a reduction in the size of vessels and tracheids, and partial blockage of xylem elements by cellular debris or gums. Heavy metals influence water delivery to the shoot due to inhibition of transpiration as they decrease the size of the leaves and the thickness of the lamina, reduce intercellular spaces, affect the density of stomata and decrease their aperture. Stomata closure is induced by direct interaction of toxic metals with guard cells and/or as a consequence of the early effects of metal toxicity on roots and stems. In metal-stressed plants, root-derived ABA or ABA-induced signals might play a role in stomatal movement. Disturbances in water relations trigger differential regulation of aquaporin gene expression, which may contribute to further reductions in water loss.

239 citations

Cites background from "Diverse functional interactions bet..."

  • ...…stresses, ABA has several ameliorative functions that involve a cascade of signaling intermediates, causing rapid induction of stomata closure, which reduce water loss from leaves (Chmielowska-Bąk et al. 2014; León et al. 2014; Neill et al. 2008; Wilkinson and Davies 2010; Yao et al. 2013)....

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  • ...In plants subjected to water and other abiotic stresses, ABA has several ameliorative functions that involve a cascade of signaling intermediates, causing rapid induction of stomata closure, which reduce water loss from leaves (Chmielowska-Bąk et al. 2014; León et al. 2014; Neill et al. 2008; Wilkinson and Davies 2010; Yao et al. 2013)....

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Journal Article•DOI•
The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses.

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Ming Zhang1, J. Andrew C. Smith2, Nicholas P. Harberd2, Caifu Jiang1•
China Agricultural University1, University of Oxford2
27 May 2016-Plant Molecular Biology
TL;DR: A review of recent advances in understanding the linked roles of ethylene and ROS in salt tolerance indicates that ethylene signaling modulates salinity responses largely via regulation of ROS-generating and ROS-scavenging mechanisms.
Abstract: Soil salinity is one of the most commonly encountered environmental stresses affecting plant growth and crop productivity. Accordingly, plants have evolved a variety of morphological, physiological and biochemical strategies that enable them to adapt to saline growth conditions. For example, it has long been known that salinity-stress increases both the production of the gaseous stress hormone ethylene and the in planta accumulation of reactive oxygen species (ROS). Recently, there has been significant progress in understanding how the fine-tuning of ethylene biosynthesis and signaling transduction can promote salinity tolerance, and how salinity-induced ROS accumulation also acts as a signal in the mediation of salinity tolerance. Furthermore, recent advances have indicated that ethylene signaling modulates salinity responses largely via regulation of ROS-generating and ROS-scavenging mechanisms. This review focuses on these recent advances in understanding the linked roles of ethylene and ROS in salt tolerance.

184 citations

Cites background from "Diverse functional interactions bet..."

  • ...In addition, the salinity-induced reactive nitrogen species NO is an important regulator of salinity responses, and likely plays a role downstream of ABA (León et al. 2014)....

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  • ...These signaling molecules, and their downstream signaling components, have been shown to play essential roles in salinity tolerance responses (Matsui et al. 2008; Harberd et al. 2009; León et al. 2014)....

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  • ...These signaling molecules, and their downstream signaling components, have been shown to play essential roles in salinity tolerance responses (Matsui et al. 2008; Harberd et al. 2009; León et al. 2014)....

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  • ...In addition, the salinity-induced reactive nitrogen species NO is an important regulator of salinity responses, and likely plays a role downstream of ABA (León et al. 2014)....

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Journal Article•DOI•
The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12, RAP2.2 and RAP2.3

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Csaba Papdi1, Csaba Papdi2, Imma Pérez-Salamó1, Imma Pérez-Salamó2, Mary Prathiba Joseph2, Beatrice Giuntoli3, László Bögre1, Csaba Koncz2, Csaba Koncz4, László Szabados2 •
Royal Holloway, University of London1, MTA Biological Research Centre2, Sant'Anna School of Advanced Studies3, Max Planck Society4
01 Jun 2015-Plant Journal
TL;DR: It is concluded that the stabilized RAP2 transcription factors can prolong the ABA-mediated activation of a subset of osmotic responsive genes (e.g. ADH1) and the protein level is affected by the REALLY INTERESTING GENE (RING) domain containing SEVEN in ABSENTIA of Arabidopsis thaliana 2 (SINAT2).
Abstract: The ethylene response factor VII (ERF-VII) transcription factor RELATED TO APETALA2.12 (RAP2.12) was previously identified as an activator of the ALCOHOL DEHYDROGENASE1 promoter::luciferase (ADH1-LUC) reporter gene. Here we show that overexpression of RAP2.12 and its homologues RAP2.2 and RAP2.3 sustains ABA-mediated activation of ADH1 and activates hypoxia marker genes under both anoxic and normoxic conditions. Inducible expression of all three RAP2s conferred tolerance to anoxia, oxidative and osmotic stresses, and enhanced the sensitivity to abscisic acid (ABA). Consistently, the rap2.12-2 rap2.3-1 double mutant showed hypersensitivity to both submergence and osmotic stress. These findings suggest that the three ERF-VII-type transcription factors play roles in tolerance to multiple stresses that sequentially occur during and after submergence in Arabidopsis. Oxygen-dependent degradation of RAP2.12 was previously shown to be mediated by the N-end rule pathway. During submergence the RAP2.12, RAP2.2 and RAP2.3 are stabilized and accumulates in the nucleus affecting the transcription of stress response genes. We conclude that the stabilized RAP2 transcription factors can prolong the ABA-mediated activation of a subset of osmotic responsive genes (e.g. ADH1). We also show that RAP2.12 protein level is affected by the REALLY INTERESTING GENE (RING) domain containing SEVEN IN ABSENTIA of Arabidopsis thaliana 2 (SINAT2). Silencing of SINAT1/2 genes leads to enhanced RAP2.12 abundance independently of the presence or absence of its N-terminal degron. Taken together, our results suggest that RAP2.12 and its homologues RAP2.2 and RAP2.3 act redundantly in multiple stress responses. Alternative protein degradation pathways may provide inputs to the RAP2 transcription factors for the distinct stresses.

147 citations

Cites background from "Diverse functional interactions bet..."

  • ...3 were obtained from the TRANSPLANTA collection (Leon et al., 2014), while RAP2....

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Journal Article•DOI•
Ethylene: Traffic Controller on Hormonal Crossroads to Defense

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Colette Broekgaarden1, Lotte Caarls1, Irene A. Vos1, Corné M. J. Pieterse1, Saskia C. M. Van Wees1 •
Utrecht University1
01 Dec 2015-Plant Physiology
TL;DR: Recent findings on the significant role of ET in the plants’ battle against their enemies are summarized.
Abstract: Ethylene (ET) is an important hormone in plant responses to microbial pathogens and herbivorous insects, and in the interaction of plants with beneficial microbes and insects. Early ET signaling events during these biotic interactions involve activities of mitogen-activated protein kinases and ETHYLENE RESPONSE FACTOR transcription factors. Rather than being the principal regulator, ET often modulates defense signaling pathways, including those regulated by jasmonic acid and salicylic acid. Hormonal signal integrations with ET steer the defense signaling network to activate specific defenses that can have direct effects on attackers, or systemically prime distant plant parts for enhanced defense against future attack. ET also regulates volatile signals that attract carnivorous enemies of herbivores or warn neighboring plants. Conversely, ET signaling can also be exploited by attackers to hijack the defense signaling network to suppress effective defenses. In this review, we summarize recent findings on the significant role of ET in the plants' battle against their enemies.

136 citations

Cites background from "Diverse functional interactions bet..."

  • ...Cross communication between the initiated hormone signaling pathways contributes to the activation of attacker-specific defenses (Robert-Seilaniantz et al., 2011; Pieterse et al., 2012; León et al., 2014; Caarls et al., 2015; Fig....

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References
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Journal Article•DOI•
Salt and drought stress signal transduction in plants

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Jian-Kang Zhu1•
University of Arizona1
01 Jan 2002-Annual Review of Plant Biology
TL;DR: Salt and drought stress signal transduction consists of ionic and osmotic homeostasis signaling pathways, detoxification (i.e., damage control and repair) response pathways, and pathways for growth regulation.
Abstract: Salt and drought stress signal transduction consists of ionic and osmotic homeostasis signaling pathways, detoxification (i.e., damage control and repair) response pathways, and pathways for growth regulation. The ionic aspect of salt stress is signaled via the SOS pathway where a calcium-responsive SOS3-SOS2 protein kinase complex controls the expression and activity of ion transporters such as SOS1. Osmotic stress activates several protein kinases including mitogen-activated kinases, which may mediate osmotic homeostasis and/or detoxification responses. A number of phospholipid systems are activated by osmotic stress, generating a diverse array of messenger molecules, some of which may function upstream of the osmotic stress-activated protein kinases. Abscisic acid biosynthesis is regulated by osmotic stress at multiple steps. Both ABA-dependent and -independent osmotic stress signaling first modify constitutively expressed transcription factors, leading to the expression of early response transcriptional activators, which then activate downstream stress tolerance effector genes.

5,328 citations

Additional excerpts

  • ...Zhu JK. 2002....

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Journal Article•DOI•
Plant cellular and molecular responses to high salinity.

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Paul M. Hasegawa1, Ray A. Bressan2, Jian-Kang Zhu, Hans J. Bohnert•
Purdue University1, University of Arizona2
01 Jun 2000
TL;DR: Evidence for plant stress signaling systems is summarized, some of which have components analogous to those that regulate osmotic stress responses of yeast, some that presumably function in intercellular coordination or regulation of effector genes in a cell-/tissue-specific context required for tolerance of plants.
Abstract: ▪ Abstract Plant responses to salinity stress are reviewed with emphasis on molecular mechanisms of signal transduction and on the physiological consequences of altered gene expression that affect biochemical reactions downstream of stress sensing. We make extensive use of comparisons with model organisms, halophytic plants, and yeast, which provide a paradigm for many responses to salinity exhibited by stress-sensitive plants. Among biochemical responses, we emphasize osmolyte biosynthesis and function, water flux control, and membrane transport of ions for maintenance and re-establishment of homeostasis. The advances in understanding the effectiveness of stress responses, and distinctions between pathology and adaptive advantage, are increasingly based on transgenic plant and mutant analyses, in particular the analysis of Arabidopsis mutants defective in elements of stress signal transduction pathways. We summarize evidence for plant stress signaling systems, some of which have components analogous to t...

4,596 citations

Journal Article•DOI•
Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens

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Jane Glazebrook
03 Aug 2005-Annual Review of Phytopathology
TL;DR: This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens.
Abstract: It has been suggested that effective defense against biotrophic pathogens is largely due to programmed cell death in the host, and to associated activation of defense responses regulated by the salicylic acid-dependent pathway. In contrast, necrotrophic pathogens benefit from host cell death, so they are not limited by cell death and salicylic acid-dependent defenses, but rather by a different set of defense responses activated by jasmonic acid and ethylene signaling. This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens. While the model above seems generally correct, there are exceptions and additional complexities.

3,721 citations

"Diverse functional interactions bet..." refers background in this paper

  • ...Necrotrophic pathogens commonly trigger JA and ethylene signalling to activate plant defence responses (Glazebrook, 2005), although they can alter SA signalling to promote disease symptoms in the plant (Rahman et al....

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  • ...Necrotrophic pathogens commonly trigger JA and ethylene signalling to activate plant defence responses (Glazebrook, 2005), although they can alter SA signalling to promote disease symptoms in the plant (Rahman et al., 2012)....

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  • ...SA-related or JA/ethylene-related signalling events have traditionally been described as the major pathways in response to pathogen attack in plants (Glazebrook, 2005)....

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Journal Article•DOI•
Seed dormancy and the control of germination

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William E. Finch-Savage1, Gerhard Leubner-Metzger2•
University of Warwick1, University of Freiburg2
01 Aug 2006-New Phytologist
TL;DR: It is argued that adaptation has taken place on a theme rather than via fundamentally different paths and similarities underlying the extensive diversity in the dormancy response to the environment that controls germination are identified.
Abstract: Seed dormancy is an innate seed property that defines the environmental conditions in which the seed is able to germinate. It is determined by genetics with a substantial environmental influence which is mediated, at least in part, by the plant hormones abscisic acid and gibberellins. Not only is the dormancy status influenced by the seed maturation environment, it is also continuously changing with time following shedding in a manner determined by the ambient environment. As dormancy is present throughout the higher plants in all major climatic regions, adaptation has resulted in divergent responses to the environment. Through this adaptation, germination is timed to avoid unfavourable weather for subsequent plant establishment and reproductive growth. In this review, we present an integrated view of the evolution, molecular genetics, physiology, biochemistry, ecology and modelling of seed dormancy mechanisms and their control of germination. We argue that adaptation has taken place on a theme rather than via fundamentally different paths and identify similarities underlying the extensive diversity in the dormancy response to the environment that controls germination.

2,411 citations

"Diverse functional interactions bet..." refers background in this paper

  • ... 1) where NO produced and perceived in the aleurone/endosperm cell layer is followed by increased ABA catabolism in the aleurone and by the synthesis of active GAs in the embryo....

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  • ...Besides the positive and negative effects exerted by GAs and ABA on these events, several other regulatory components have been identified that influence seed germination....

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  • ...Its regulatory role is often exerted in connection with the classical hormones auxins, cytokinins, gibberellins (GAs), ethylene, and abscisic acid (ABA), as well as the more recently characterized jasmonates, salicylates, brassinosteroids, and strigolactones....

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  • ...It is widely assumed that dormancy is directly promoted by endogenous levels of ABA and also that germination is enhanced by GAs (Finch-Savage and Leubner-Metzger, 2006)....

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Journal Article•DOI•
Nitric oxide functions as a signal in plant disease resistance

[...]

Massimo Delledonne1, Yiji Xia1, Richard A. Dixon, Christopher J. Lamb1•
Salk Institute for Biological Studies1
06 Aug 1998-Nature
TL;DR: It is shown that nitric oxide potentiates the induction of hypersensitive cell death in soybean cells by reactive oxygen intermediates and functions independently of such intermediates to induce genes for the synthesis of protective natural products.
Abstract: Recognition of an avirulent pathogen triggers the rapid production of the reactive oxygen intermediates superoxide (O2-) and hydrogen peroxide (H2O2) This oxidative burst drives crosslinking of the cell wall, induces several plant genes involved in cellular protection and defence, and is necessary for the initiation of host cell death in the hypersensitive disease-resistance response However, this burst is not enough to support a strong disease-resistance response Here we show that nitric oxide, which acts as a signal in the immune, nervous and vascular systems, potentiates the induction of hypersensitive cell death in soybean cells by reactive oxygen intermediates and functions independently of such intermediates to induce genes for the synthesis of protective natural products Moreover, inhibitors of nitric oxide synthesis compromise the hypersensitive disease-resistance response of Arabidopsis leaves to Pseudomonas syringae, promoting disease and bacterial growth We conclude that nitric oxide plays a key role in disease resistance in plants

1,821 citations

"Diverse functional interactions bet..." refers background in this paper

  • ...NO functions as a positive regulator of ETI, as demonstrated by the enhanced susceptibility to P.syringae avrRpm1 and avrRps4 observed in wild-type Arabidopsis plants treated with inhibitors of NO production (Delledonne et  al., 1998), and in NO-deficient Arabidopsis mutants (Mandal et  al., 2012)....

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Radhika Desikan, Rachael Griffiths, John T. Hancock, Steven J. Neill 
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