Cargando…

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

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 regul...

Descripción completa

Detalles Bibliográficos
Autores principales: Shim, Jae Sung, Park, Su-Hyun, Lee, Dong-Keun, Kim, Youn Shic, Park, Soo-Chul, Redillas, Mark Christian Felipe R., Seo, Jun Sung, Kim, Ju-Kon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7979854/
https://www.ncbi.nlm.nih.gov/pubmed/33742286
http://dx.doi.org/10.1186/s12284-021-00473-0
_version_ 1783667352325324800
author Shim, Jae Sung
Park, Su-Hyun
Lee, Dong-Keun
Kim, Youn Shic
Park, Soo-Chul
Redillas, Mark Christian Felipe R.
Seo, Jun Sung
Kim, Ju-Kon
author_facet Shim, Jae Sung
Park, Su-Hyun
Lee, Dong-Keun
Kim, Youn Shic
Park, Soo-Chul
Redillas, Mark Christian Felipe R.
Seo, Jun Sung
Kim, Ju-Kon
author_sort Shim, Jae Sung
collection PubMed
description 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(2)O(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.
format Online
Article
Text
id pubmed-7979854
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Springer US
record_format MEDLINE/PubMed
spelling pubmed-79798542021-04-12 The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes Shim, Jae Sung Park, Su-Hyun Lee, Dong-Keun Kim, Youn Shic Park, Soo-Chul Redillas, Mark Christian Felipe R. Seo, Jun Sung Kim, Ju-Kon Rice (N Y) Original Article 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(2)O(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. Springer US 2021-03-19 /pmc/articles/PMC7979854/ /pubmed/33742286 http://dx.doi.org/10.1186/s12284-021-00473-0 Text en © The Author(s) 2021 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/.
spellingShingle Original Article
Shim, Jae Sung
Park, Su-Hyun
Lee, Dong-Keun
Kim, Youn Shic
Park, Soo-Chul
Redillas, Mark Christian Felipe R.
Seo, Jun Sung
Kim, Ju-Kon
The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes
title The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes
title_full The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes
title_fullStr The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes
title_full_unstemmed The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes
title_short The Rice GLYCINE-RICH PROTEIN 3 Confers Drought Tolerance by Regulating mRNA Stability of ROS Scavenging-Related Genes
title_sort rice glycine-rich protein 3 confers drought tolerance by regulating mrna stability of ros scavenging-related genes
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7979854/
https://www.ncbi.nlm.nih.gov/pubmed/33742286
http://dx.doi.org/10.1186/s12284-021-00473-0
work_keys_str_mv AT shimjaesung thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT parksuhyun thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT leedongkeun thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT kimyounshic thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT parksoochul thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT redillasmarkchristianfeliper thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT seojunsung thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT kimjukon thericeglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT shimjaesung riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT parksuhyun riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT leedongkeun riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT kimyounshic riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT parksoochul riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT redillasmarkchristianfeliper riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT seojunsung riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes
AT kimjukon riceglycinerichprotein3confersdroughttolerancebyregulatingmrnastabilityofrosscavengingrelatedgenes