The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes

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Abstract

Background

Plant glycine-rich proteins are categorized into several classes based on their protein structures. The glycine-rich RNA binding proteins (GRPs) are members of class IV subfamily possessing N-terminus RNA-recognition motifs (RRMs) and proposed to be involved in post-transcriptional regulation of its target transcripts. GRPs are involved in developmental process and cellular stress responses, but the molecular mechanisms underlying these regulations are still elusive.

Results

Here, we report the functional characterization of rice GLYCINE-RICH PROTEIN 3 ( OsGRP3) and its physiological roles in drought stress response. Both drought stress and ABA induce the expression of OsGRP3. Transgenic plants overexpressing OsGRP3 ( OsGRP3 ^OE) exhibited tolerance while knock-down plants ( OsGRP3 ^KD) were susceptible to drought compared to the non-transgenic control. In vivo , subcellular localization analysis revealed that OsGRP3-GFP was transported from cytoplasm/nucleus into cytoplasmic foci following exposure to ABA and mannitol treatments. Comparative transcriptomic analysis between OsGRP3 ^OE and OsGRP3 ^KD plants suggests that OsGRP3 is involved in the regulation of the ROS related genes. RNA-immunoprecipitation analysis revealed the associations of OsGRP3 with PATHOGENESIS RELATED GENE 5 ( PR5), METALLOTHIONEIN 1d ( MT1d), 4,5-DOPA-DIOXYGENASE ( DOPA), and LIPOXYGENASE ( LOX) transcripts. The half-life analysis showed that PR5 transcripts decayed slower in OsGRP3 ^OE but faster in OsGRP3 ^KD, while MT1d and LOX transcripts decayed faster in OsGRP3 ^OE but slower in OsGRP3 ^KD plants. H ₂O ₂ accumulation was reduced in OsGRP3 ^OE and increased in OsGRP3 ^KD plants compared to non-transgenic plants (NT) under drought stress.

Conclusion

OsGRP3 plays a positive regulator in rice drought tolerance and modulates the transcript level and mRNA stability of stress-responsive genes, including ROS-related genes. Moreover, OsGRP3 contributes to the reduction of ROS accumulation during drought stress. Our results suggested that OsGRP3 alleviates ROS accumulation by regulating ROS-related genes’ mRNA stability under drought stress, which confers drought tolerance.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12284-021-00473-0.

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Most cited references 63

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Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel (2014)

Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.

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Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.

Sarvajeet Singh Gill, Narendra Tuteja (2010)

Various abiotic stresses lead to the overproduction of reactive oxygen species (ROS) in plants which are highly reactive and toxic and cause damage to proteins, lipids, carbohydrates and DNA which ultimately results in oxidative stress. The ROS comprises both free radical (O(2)(-), superoxide radicals; OH, hydroxyl radical; HO(2), perhydroxy radical and RO, alkoxy radicals) and non-radical (molecular) forms (H(2)O(2), hydrogen peroxide and (1)O(2), singlet oxygen). In chloroplasts, photosystem I and II (PSI and PSII) are the major sites for the production of (1)O(2) and O(2)(-). In mitochondria, complex I, ubiquinone and complex III of electron transport chain (ETC) are the major sites for the generation of O(2)(-). The antioxidant defense machinery protects plants against oxidative stress damages. Plants possess very efficient enzymatic (superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; glutathione reductase, GR; monodehydroascorbate reductase, MDHAR; dehydroascorbate reductase, DHAR; glutathione peroxidase, GPX; guaicol peroxidase, GOPX and glutathione-S- transferase, GST) and non-enzymatic (ascorbic acid, ASH; glutathione, GSH; phenolic compounds, alkaloids, non-protein amino acids and α-tocopherols) antioxidant defense systems which work in concert to control the cascades of uncontrolled oxidation and protect plant cells from oxidative damage by scavenging of ROS. ROS also influence the expression of a number of genes and therefore control the many processes like growth, cell cycle, programmed cell death (PCD), abiotic stress responses, pathogen defense, systemic signaling and development. In this review, we describe the biochemistry of ROS and their production sites, and ROS scavenging antioxidant defense machinery. Copyright © 2010 Elsevier Masson SAS. All rights reserved.

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ROS Regulation During Abiotic Stress Responses in Crop Plants

Jun Myeong You, Zhulong Chan (2015)

Abiotic stresses such as drought, cold, salt and heat cause reduction of plant growth and loss of crop yield worldwide. Reactive oxygen species (ROS) including hydrogen peroxide (H2O2), superoxide anions (O2 •-), hydroxyl radical (OH•) and singlet oxygen (1O2) are by-products of physiological metabolisms, and are precisely controlled by enzymatic and non-enzymatic antioxidant defense systems. ROS are significantly accumulated under abiotic stress conditions, which cause oxidative damage and eventually resulting in cell death. Recently, ROS have been also recognized as key players in the complex signaling network of plants stress responses. The involvement of ROS in signal transduction implies that there must be coordinated function of regulation networks to maintain ROS at non-toxic levels in a delicate balancing act between ROS production, involving ROS generating enzymes and the unavoidable production of ROS during basic cellular metabolism, and ROS-scavenging pathways. Increasing evidence showed that ROS play crucial roles in abiotic stress responses of crop plants for the activation of stress-response and defense pathways. More importantly, manipulating ROS levels provides an opportunity to enhance stress tolerances of crop plants under a variety of unfavorable environmental conditions. This review presents an overview of current knowledge about homeostasis regulation of ROS in crop plants. In particular, we summarize the essential proteins that are involved in abiotic stress tolerance of crop plants through ROS regulation. Finally, the challenges toward the improvement of abiotic stress tolerance through ROS regulation in crops are discussed.

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Author and article information

Contributors

Jun Sung Seo: xfiles96@snu.ac.kr

Ju-Kon Kim:

ORCID: http://orcid.org/0000-0001-8905-7617

jukon@snu.ac.kr

Journal

Journal ID (nlm-ta): Rice (N Y)

Journal ID (iso-abbrev): Rice (N Y)

Title: Rice

Publisher: Springer US (New York )

ISSN (Print): 1939-8425

ISSN (Electronic): 1939-8433

Publication date (Electronic): 19 March 2021

Publication date PMC-release: 19 March 2021

Publication date Collection: 2021

Volume: 14

Electronic Location Identifier: 31

Affiliations

[1 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, Crop Biotechnology Institute, GreenBio Science and Technology, , Seoul National University, ; Pyeongchang, 25354 South Korea

[2 ]GRID grid.14005.30, ISNI 0000 0001 0356 9399, School of Biological Sciences and Technology, , Chonnam National University, ; Gwangju, 61186 South Korea

[3 ]GRID grid.4280.e, ISNI 0000 0001 2180 6431, Temasek Life Sciences Laboratory, 1 Research Link, , National University of Singapore, ; Singapore, 117604 Singapore

[4 ]E GREEN GLOBAL, Gunpo, 15843 South Korea

[5 ]GRID grid.412010.6, ISNI 0000 0001 0707 9039, Agriculture and Life Sciences Research Institute, , Kangwon National University, ; Chuncheon, 24341 South Korea

[6 ]GRID grid.420186.9, ISNI 0000 0004 0636 2782, Department of Agricultural Biotechnology, , National Academy of Agricultural Science, Rural Development Administration, ; Jeonju, 54874 South Korea

[7 ]GRID grid.411987.2, ISNI 0000 0001 2153 4317, Biology Department, , De La Salle University, ; 0922 Manila, Philippines

Author information

Ju-Kon Kim http://orcid.org/0000-0001-8905-7617

Article

Publisher ID: 473

DOI: 10.1186/s12284-021-00473-0

PMC ID: 7979854

PubMed ID: 33742286

SO-VID: e9ef4489-051f-44cf-a1f7-716b1c85944d

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 23 October 2020

Date accepted : 10 March 2021

Funding

Funded by: Rural Development Administration, Republic of Korea

Award ID: PJ01477201

Award Recipient : Ju-Kon Kim

Custom metadata

ScienceOpen disciplines: Agriculture

Keywords: osgrp3,drought tolerance,cytoplasmic foci,rna-ip,mrna stability

Data availability:

ScienceOpen disciplines: Agriculture

Keywords: osgrp3, drought tolerance, cytoplasmic foci, rna-ip, mrna stability

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The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes

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Abstract

Background

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Supplementary Information

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Algerian Journal of Natural Products

Most cited references 63

Trimmomatic: a flexible trimmer for Illumina sequence data

Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.

ROS Regulation During Abiotic Stress Responses in Crop Plants

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Cited by 11

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