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Journal Article•DOI•

Temporal-Spatial Interaction between Reactive Oxygen Species and Abscisic Acid Regulates Rapid Systemic Acclimation in Plants

Nobuhiro Suzuki1, Gad Miller2, Carolina Salazar1, Hossain Ali Mondal1, Elena Shulaev1, Diego F. Cortes3, Joel L. Shuman3, Xiaozhong Luo1, Jyoti Shah1, Karen Schlauch4, Vladimir Shulaev1, Ron Mittler1 •
University of North Texas1, Bar-Ilan University2, Virginia Bioinformatics Institute3, University of Nevada, Reno4
01 Sep 2013-The Plant Cell (American Society of Plant Biologists)-Vol. 25, Iss: 9, pp 3553-3569
TL;DR: It is demonstrated that SAA is stress specific and that a temporal–spatial interaction between ROS and abscisic acid regulates rapid SAA to heat stress in plants, and that the rapid ROS signal is associated with the propagation of electric signals in Arabidopsis thaliana.
Abstract: Being sessile organisms, plants evolved sophisticated acclimation mechanisms to cope with abiotic challenges in their environment. These are activated at the initial site of exposure to stress, as well as in systemic tissues that have not been subjected to stress (termed systemic acquired acclimation [SAA]). Although SAA is thought to play a key role in plant survival during stress, little is known about the signaling mechanisms underlying it. Here, we report that SAA in plants requires at least two different signals: an autopropagating wave of reactive oxygen species (ROS) that rapidly spreads from the initial site of exposure to the entire plant and a stress-specific signal that conveys abiotic stress specificity. We further demonstrate that SAA is stress specific and that a temporal–spatial interaction between ROS and abscisic acid regulates rapid SAA to heat stress in plants. In addition, we demonstrate that the rapid ROS signal is associated with the propagation of electric signals in Arabidopsis thaliana. Our findings unravel some of the basic signaling mechanisms underlying SAA in plants and reveal that signaling events and transcriptome and metabolome reprogramming of systemic tissues in response to abiotic stress occur at a much faster rate than previously envisioned.

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Citations
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Journal Article•DOI•
Reactive oxygen species, abiotic stress and stress combination.

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Feroza K. Choudhury1, Rosa M. Rivero2, Eduardo Blumwald3, Ron Mittler1•
Florida State University College of Arts and Sciences1, Spanish National Research Council2, University of California, Davis3
01 Jun 2017-Plant Journal
TL;DR: ROS is beneficial to plants during abiotic stress enabling them to adjust their metabolism and mount a proper acclimation response, as long as cells maintain high enough energy reserves to detoxify ROS.
Abstract: Reactive oxygen species (ROS) play a key role in the acclimation process of plants to abiotic stress. They primarily function as signal transduction molecules that regulate different pathways during plant acclimation to stress, but are also toxic byproducts of stress metabolism. Because each subcellular compartment in plants contains its own set of ROS-producing and ROS-scavenging pathways, the steady-state level of ROS, as well as the redox state of each compartment, is different at any given time giving rise to a distinct signature of ROS levels at the different compartments of the cell. Here we review recent studies on the role of ROS in abiotic stress in plants, and propose that different abiotic stresses, such as drought, heat, salinity and high light, result in different ROS signatures that determine the specificity of the acclimation response and help tailor it to the exact stress the plant encounters. We further address the role of ROS in the acclimation of plants to stress combination as well as the role of ROS in mediating rapid systemic signaling during abiotic stress. We conclude that as long as cells maintain high enough energy reserves to detoxify ROS, ROS is beneficial to plants during abiotic stress enabling them to adjust their metabolism and mount a proper acclimation response.

1,462 citations

Cites background from "Temporal-Spatial Interaction betwee..."

  • ...Although it does not convey abiotic stress specificity to the systemic response, the ROS wave is absolutely required for it (Suzuki et al., 2013)....

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  • ...At least when it comes to heat stress, the ROS wave was also shown to be coordinated with ABA function in systemic leaves (Suzuki et al., 2013)....

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  • ...Furthermore, the ROS wave was shown to be required to induce a systemic acclimation response to light or heat stress (Suzuki et al., 2013)....

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  • ...Accordingly, mutants impaired in ROS production or ROS scavenging were found to be more sensitive to abiotic stresses as well as unable to mediate systemic signaling during abiotic stress (Davletova et al., 2005; Suzuki et al., 2013; reviewed in Mittler et al., 2004; Suzuki et al., 2011)....

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  • ...In addition, the ROS wave was shown to be required for the generation of some electric signals during abiotic stress (Suzuki et al., 2013)....

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Journal Article•DOI•
ROS as key players in plant stress signalling

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Aaron Baxter1, Ron Mittler1, Nobuhiro Suzuki1•
Florida State University College of Arts and Sciences1
01 Mar 2014-Journal of Experimental Botany
TL;DR: This review will provide an update of recent findings related to the integration of ROS signals with an array of signalling pathways aimed at regulating different responses in plants and address signals that confer systemic acquired resistance (SAR) or systemic acquired acclimation (SAA) in plants.
Abstract: Reactive oxygen species (ROS) play an integral role as signalling molecules in the regulation of numerous biological processes such as growth, development, and responses to biotic and/or abiotic stimuli in plants. To some extent, various functions of ROS signalling are attributed to differences in the regulatory mechanisms of respiratory burst oxidase homologues (RBOHs) that are involved in a multitude of different signal transduction pathways activated in assorted tissue and cell types under fluctuating environmental conditions. Recent findings revealed that stress responses in plants are mediated by a temporal-spatial coordination between ROS and other signals that rely on production of stress-specific chemicals, compounds, and hormones. In this review we will provide an update of recent findings related to the integration of ROS signals with an array of signalling pathways aimed at regulating different responses in plants. In particular, we will address signals that confer systemic acquired resistance (SAR) or systemic acquired acclimation (SAA) in plants.

1,414 citations

Cites background from "Temporal-Spatial Interaction betwee..."

  • ...In particular, induction of heat-responsive proteins in systemic tissue was shown to be ROS wave dependent (Suzuki et al., 2013)....

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  • ...Our recent study demonstrated that SAA of plants to heat stress was correlated with activation of the ROS wave and transient accumulation of ABA in systemic tissues, and these responses were suppressed in a mutant lacking RBOHD (Suzuki et al., 2013)....

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  • ...Our recent findings suggest that these two phases of the ROS burst are linked via the ROS wave that communicates the initial ROS burst in the local tissue to the systemic tissue via a cell to cell relay mechanism (Miller et al., 2009; Suzuki et al., 2013)....

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  • ...These results indicate that temporal–spatial interactions between RBOHDdependent ROS and ABA mediate SAA to heat stress (Suzuki et al., 2013)....

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  • ...Our recent study demonstrated that amino acids involved in the photorespiratory pathway such as glycine, serine, and glycerate are similarly altered in both local and systemic tissues in response to local application of high light (Suzuki et al., 2013)....

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Journal Article•DOI•
Abscisic Acid and Abiotic Stress Tolerance in Crop Plants

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Saroj Kumar Sah1, K. R. Reddy1, Jiaxu Li1•
Mississippi State University1
04 May 2016-Frontiers in Plant Science
TL;DR: The role of ABA in response to abiotic stress at the molecular level and ABA signaling is discussed and the effect of A BA in respect to gene expression is dealt with.
Abstract: Abiotic stress is a primary threat to fulfill the demand of agricultural production to feed the world in coming decades. Plants reduce growth and development process during stress conditions, which ultimately affect the yield. In stress conditions, plants develop various stress mechanism to face the magnitude of stress challenges, although that is not enough to protect them. Therefore, many strategies have been used to produce abiotic stress tolerance crop plants, among them, ABA (abscisic acid) phytohormone engineering could be one of the methods of choice. ABA is an isoprenoid phytohormone, which regulates various physiological processes ranging from stomatal opening to protein storage and provides adaptation to many stresses like drought, salt, and cold stresses. ABA is also called an important messenger that acts as the signaling mediator for regulating the adaptive response of plants to different environmental stress conditions. In this review, we will discuss the role of ABA in response to abiotic stress at the molecular level and ABA signaling. The review also deals with the effect of ABA in respect to gene expression.

805 citations

Cites background or result from "Temporal-Spatial Interaction betwee..."

  • ...Foliar spraying with ABA has been revealed to promote leaf senescence in rice (Ray et al., 1983) and similar results were shown in maize by He and Jin (1999)....

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  • ...During stomatal closure, decreased gas exchange results in the reduction of photosynthate production while decreased transpiration can reduce water loss from leaves (Suzuki et al., 2013; Mittler and Blumwald, 2015)....

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Journal Article•DOI•
Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants

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Won-Gyu Choi1, Masatsugu Toyota1, Su-Hwa Kim1, Richard Hilleary1, Simon Gilroy1 •
University of Wisconsin-Madison1
29 Apr 2014-Proceedings of the National Academy of Sciences of the United States of America
TL;DR: Plants possess a rapid stress signaling system based on Ca2+ waves that propagate through the plant at rates of up to ∼400 µm/s, and this system likely elicits systemic molecular responses in target organs and may contribute to whole-plant stress tolerance.
Abstract: Their sessile lifestyle means that plants have to be exquisitely sensitive to their environment, integrating many signals to appropriate developmental and physiological responses. Stimuli ranging from wounding and pathogen attack to the distribution of water and nutrients in the soil are frequently presented in a localized manner but responses are often elicited throughout the plant. Such systemic signaling is thought to operate through the redistribution of a host of chemical regulators including peptides, RNAs, ions, metabolites, and hormones. However, there are hints of a much more rapid communication network that has been proposed to involve signals ranging from action and system potentials to reactive oxygen species. We now show that plants also possess a rapid stress signaling system based on Ca2+ waves that propagate through the plant at rates of up to ∼400 µm/s. In the case of local salt stress to the Arabidopsis thaliana root, Ca2+ wave propagation is channeled through the cortex and endodermal cell layers and this movement is dependent on the vacuolar ion channel TPC1. We also provide evidence that the Ca2+ wave/TPC1 system likely elicits systemic molecular responses in target organs and may contribute to whole-plant stress tolerance. These results suggest that, although plants do not have a nervous system, they do possess a sensory network that uses ion fluxes moving through defined cell types to rapidly transmit information between distant sites within the organism.

519 citations

Journal Article•DOI•
Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance

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Xiao-Jian Xia1, Yan-Hong Zhou1, Kai Shi1, Jie Zhou1, Christine H. Foyer2, Jing-Quan Yu1 •
Zhejiang University1, University of Leeds2
01 May 2015-Journal of Experimental Botany
TL;DR: This review provides an overview of current knowledge of how ROS production and signalling are integrated with the action of auxin, brassinosteroids, gibberellins, abscisic acid, ethylene, strigolactones, salicylic acid, and jasmonic acid in the coordinate regulation of plant growth and stress tolerance.
Abstract: As a consequence of a sessile lifestyle, plants are continuously exposed to changing environmental conditions and often life-threatening stresses caused by exposure to excessive light, extremes of temperature, limiting nutrient or water availability, and pathogen/insect attack. The flexible coordination of plant growth and development is necessary to optimize vigour and fitness in a changing environment through rapid and appropriate responses to such stresses. The concept that reactive oxygen species (ROS) are versatile signalling molecules in plants that contribute to stress acclimation is well established. This review provides an overview of our current knowledge of how ROS production and signalling are integrated with the action of auxin, brassinosteroids, gibberellins, abscisic acid, ethylene, strigolactones, salicylic acid, and jasmonic acid in the coordinate regulation of plant growth and stress tolerance. We consider the local and systemic crosstalk between ROS and hormonal signalling pathways and identify multiple points of reciprocal control, as well as providing insights into the integration nodes that involve Ca(2+)-dependent processes and mitogen-activated protein kinase phosphorylation cascades.

511 citations

Cites background from "Temporal-Spatial Interaction betwee..."

  • ...However, ABA accumulation in systemic tissues that are distant from the perceived heat stress is abolished in Arabidopsis rbohD mutants (Suzuki et al., 2013)....

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References
More filters
Journal Article•DOI•
Exploration, normalization, and summaries of high density oligonucleotide array probe level data

[...]

Rafael A. Irizarry1, Bridget G. Hobbs1, Francois Collin1, Yasmin Beazer-Barclay1, Kristen J. Antonellis1, Uwe Scherf1, Terence P. Speed1 •
Johns Hopkins University1
01 Apr 2003-Biostatistics
TL;DR: There is no obvious downside to using RMA and attaching a standard error (SE) to this quantity using a linear model which removes probe-specific affinities, and the exploratory data analyses of the probe level data motivate a new summary measure that is a robust multi-array average (RMA) of background-adjusted, normalized, and log-transformed PM values.
Abstract: SUMMARY In this paper we report exploratory analyses of high-density oligonucleotide array data from the Affymetrix GeneChip R � system with the objective of improving upon currently used measures of gene expression. Our analyses make use of three data sets: a small experimental study consisting of five MGU74A mouse GeneChip R � arrays, part of the data from an extensive spike-in study conducted by Gene Logic and Wyeth’s Genetics Institute involving 95 HG-U95A human GeneChip R � arrays; and part of a dilution study conducted by Gene Logic involving 75 HG-U95A GeneChip R � arrays. We display some familiar features of the perfect match and mismatch probe ( PM and MM )v alues of these data, and examine the variance–mean relationship with probe-level data from probes believed to be defective, and so delivering noise only. We explain why we need to normalize the arrays to one another using probe level intensities. We then examine the behavior of the PM and MM using spike-in data and assess three commonly used summary measures: Affymetrix’s (i) average difference (AvDiff) and (ii) MAS 5.0 signal, and (iii) the Li and Wong multiplicative model-based expression index (MBEI). The exploratory data analyses of the probe level data motivate a new summary measure that is a robust multiarray average (RMA) of background-adjusted, normalized, and log-transformed PM values. We evaluate the four expression summary measures using the dilution study data, assessing their behavior in terms of bias, variance and (for MBEI and RMA) model fit. Finally, we evaluate the algorithms in terms of their ability to detect known levels of differential expression using the spike-in data. We conclude that there is no obvious downside to using RMA and attaching a standard error (SE) to this quantity using a linear model which removes probe-specific affinities. ∗ To whom correspondence should be addressed

10,711 citations

"Temporal-Spatial Interaction betwee..." refers methods in this paper

  • ...Array data were analyzed as previously described (Irizarry et al., 2003; Gautier et al., 2004; Davletova et al., 2005a, 2005b; Miller et al., 2009; Suzuki et al., 2011a) and deposited in Array Express (E-MEXP-3754)....

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Journal Article•DOI•
affy---analysis of Affymetrix GeneChip data at the probe level

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Laurent Gautier1, Leslie Cope2, Benjamin M. Bolstad3, Rafael A. Irizarry2•
Technical University of Denmark1, Johns Hopkins University2, University of California, Berkeley3
12 Feb 2004-Bioinformatics
TL;DR: The affy package is an R package of functions and classes for the analysis of oligonucleotide arrays manufactured by Affymetrix that provides the user with extreme flexibility when carrying out an analysis and make it possible to access and manipulate probe intensity data.
Abstract: Motivation: The processing of the Affymetrix GeneChip data has been a recent focus for data analysts. Alternatives to the original procedure have been proposed and some of these new methods are widely used. Results: The affy package is an R package of functions and classes for the analysis of oligonucleotide arrays manufactured by Affymetrix. The package is currently in its second release, affy provides the user with extreme flexibility when carrying out an analysis and make it possible to access and manipulate probe intensity data. In this paper, we present the main classes and functions in the package and demonstrate how they can be used to process probe-level data. We also demonstrate the importance of probe-level analysis when using the Affymetrix GeneChip platform.

4,822 citations

"Temporal-Spatial Interaction betwee..." refers methods in this paper

  • ...Array data were analyzed as previously described (Irizarry et al., 2003; Gautier et al., 2004; Davletova et al., 2005a, 2005b; Miller et al., 2009; Suzuki et al., 2011a) and deposited in Array Express (E-MEXP-3754)....

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Book•
Biochemistry & Molecular Biology of Plants

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Bob B. Buchanan, Wilhelm Gruissem, Russell L. Jones
01 Jan 2002
TL;DR: This edition of Biochemistry & Molecular Biology of Plants holds a unique place in the plant sciences literature as it provides the only comprehensive, authoritative, integrated single volume book in this essential field of study.
Abstract: Since its publication in 2000, Biochemistry & Molecular Biology of Plants, has been hailed as a major contribution to the plant sciences literature and critical acclaim has been matched by global sales success. Maintaining the scope and focus of the first edition, the second will provide a major update, include much new material and reorganise some chapters to further improve the presentation. This book is meticulously organised and richly illustrated, having over 1,000 full-colour illustrations and 500 photographs. It is divided into five parts covering: Compartments: Cell Reproduction: Energy Flow; Metabolic and Developmental Integration; and Plant Environment and Agriculture. Specific changes to this edition include: Completely revised with over half of the chapters having a major rewrite. Includes two new chapters on signal transduction and responses to pathogens. Restructuring of section on cell reproduction for improved presentation. Dedicated website to include all illustrative material. Biochemistry & Molecular Biology of Plants holds a unique place in the plant sciences literature as it provides the only comprehensive, authoritative, integrated single volume book in this essential field of study.

3,439 citations

Journal Article•DOI•
Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling

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Paul D. Ray1, Bo-Wen Huang1, Yoshiaki Tsuji1•
North Carolina State University1
01 May 2012-Cellular Signalling
TL;DR: This review focuses on the molecular mechanisms through which ROS directly interact with critical signaling molecules to initiate signaling in a broad variety of cellular processes, such as proliferation and survival, ROS homeostasis and antioxidant gene regulation, mitochondrial oxidative stress, apoptosis, and aging.

3,372 citations

"Temporal-Spatial Interaction betwee..." refers background in this paper

  • ...Reactive oxygen species (ROS) function as important signaling molecules in bacteria, plants, animals, and humans (Bae et al., 2011; Halliwell, 2012; Ray et al., 2012)....

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Journal Article•DOI•
ROS signaling: the new wave?

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Ron Mittler1, Ron Mittler2, Sandy Vanderauwera3, Nobuhiro Suzuki1, Gad Miller4, Vanesa B. Tognetti3, Klaas Vandepoele3, Marty Gollery, Vladimir Shulaev1, Frank Van Breusegem3 •
Florida State University College of Arts and Sciences1, Hebrew University of Jerusalem2, Ghent University3, Bar-Ilan University4
01 Jun 2011-Trends in Plant Science
TL;DR: This review will attempt to address several key questions related to the use of ROS as signaling molecules in cells, including the dynamics and specificity of ROS signaling, networking of ROS with other signaling pathways, ROS signaling within and across different cells, ROS waves and the evolution of the ROS gene network.

1,879 citations

"Temporal-Spatial Interaction betwee..." refers background or methods in this paper

  • ...The ROS wave may therefore directly promote electric signals at the PM along its path (Mittler et al., 2011)....

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  • ...…ROS at the outer surface of the plasma membrane (PM) during the progression of the ROS wave along its systemic path could cause membrane depolarization and the generation and/or propagation of electric signals (DeCoursey, 2003; Matoba and Shimokawa, 2003; Miller et al., 2010; Mittler et al., 2011)....

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  • ...The accumulation of ROS at the outer surface of the plasma membrane (PM) during the progression of the ROS wave along its systemic path could cause membrane depolarization and the generation and/or propagation of electric signals (DeCoursey, 2003; Matoba and Shimokawa, 2003; Miller et al., 2010; Mittler et al., 2011)....

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  • ...In plant tissues, a burst of ROS production, often occurring as two distinct peaks, accompanies the onset of several different abiotic stresses (Nishimura and Dangl, 2010; Mittler et al., 2011)....

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  • ...Mittler et al., 2011; Dubiella et al., 2013)....

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Related Papers (5)
The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.

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18 Aug 2009-Science Signaling
Gad Miller, Karen Schlauch, Rachel Tam, Diego F. Cortes, Miguel A. Torres, Vladimir Shulaev, Jeffery L. Dangl, Ron Mittler, Ron Mittler 
ROS signaling: the new wave?

[...]

01 Jun 2011-Trends in Plant Science
Ron Mittler, Ron Mittler, Sandy Vanderauwera, Nobuhiro Suzuki, Gad Miller, Vanesa B. Tognetti, Klaas Vandepoele, Marty Gollery, Vladimir Shulaev, Frank Van Breusegem 
ROS as key players in plant stress signalling

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01 Mar 2014-Journal of Experimental Botany
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Reactive oxygen gene network of plants

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01 Oct 2004-Trends in Plant Science
Ron Mittler, Sandy Vanderauwera, Martin Gollery, Frank Van Breusegem 
NADPH oxidase AtrbohD and AtrbohF genes function in ROS‐dependent ABA signaling in Arabidopsis

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01 Jun 2003-The EMBO Journal
June M. Kwak, Izumi C. Mori, Zhen-Ming Pei, Nathalie Leonhardt, Miguel Angel Torres, Jeffery L. Dangl, Rachel E. Bloom, Sara Bodde, Jonathan D. G. Jones, Julian I. Schroeder