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An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields

Drought stress poses a serious threat to global agricultural productivity and food security. Plant resistance to drought is typically accompanied by a growth deficit and yield penalty. Herein, we report a previously uncharacterized, dicotyledon-specific gene, Stress and Growth Interconnector (SGI),...

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Autores principales: Liu, Jun, Liu, Jing, Deng, Linbin, Liu, Hongmei, Liu, Hongfang, Zhao, Wei, Zhao, Yuwei, Sun, Xingchao, Fan, Shihang, Wang, Hanzhong, Hua, Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10152686/
https://www.ncbi.nlm.nih.gov/pubmed/36746783
http://dx.doi.org/10.1093/plphys/kiad074
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author Liu, Jun
Liu, Jing
Deng, Linbin
Liu, Hongmei
Liu, Hongfang
Zhao, Wei
Zhao, Yuwei
Sun, Xingchao
Fan, Shihang
Wang, Hanzhong
Hua, Wei
author_facet Liu, Jun
Liu, Jing
Deng, Linbin
Liu, Hongmei
Liu, Hongfang
Zhao, Wei
Zhao, Yuwei
Sun, Xingchao
Fan, Shihang
Wang, Hanzhong
Hua, Wei
author_sort Liu, Jun
collection PubMed
description Drought stress poses a serious threat to global agricultural productivity and food security. Plant resistance to drought is typically accompanied by a growth deficit and yield penalty. Herein, we report a previously uncharacterized, dicotyledon-specific gene, Stress and Growth Interconnector (SGI), that promotes growth during drought in the oil crop rapeseed (Brassica napus) and the model plant Arabidopsis (Arabidopsis thaliana). Overexpression of SGI conferred enhanced biomass and yield under water-deficient conditions, whereas corresponding CRISPR SGI mutants exhibited the opposite effects. These attributes were achieved by mediating reactive oxygen species (ROS) homeostasis while maintaining photosynthetic efficiency to increase plant fitness under water-limiting environments. Further spatial-temporal transcriptome profiling revealed dynamic reprogramming of pathways for photosynthesis and stress responses during drought and the subsequent recovery. Mechanistically, SGI represents an intrinsically disordered region-containing protein that interacts with itself, catalase isoforms, dehydrins, and other drought-responsive positive factors, restraining ROS generation. These multifaceted interactions stabilize catalases in response to drought and facilitate their ROS-scavenging activities. Taken altogether, these findings provide insights into currently underexplored mechanisms to circumvent trade-offs between plant growth and stress tolerance that will inform strategies to breed climate-resilient, higher yielding crops for sustainable agriculture.
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spelling pubmed-101526862023-05-03 An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields Liu, Jun Liu, Jing Deng, Linbin Liu, Hongmei Liu, Hongfang Zhao, Wei Zhao, Yuwei Sun, Xingchao Fan, Shihang Wang, Hanzhong Hua, Wei Plant Physiol Research Article Drought stress poses a serious threat to global agricultural productivity and food security. Plant resistance to drought is typically accompanied by a growth deficit and yield penalty. Herein, we report a previously uncharacterized, dicotyledon-specific gene, Stress and Growth Interconnector (SGI), that promotes growth during drought in the oil crop rapeseed (Brassica napus) and the model plant Arabidopsis (Arabidopsis thaliana). Overexpression of SGI conferred enhanced biomass and yield under water-deficient conditions, whereas corresponding CRISPR SGI mutants exhibited the opposite effects. These attributes were achieved by mediating reactive oxygen species (ROS) homeostasis while maintaining photosynthetic efficiency to increase plant fitness under water-limiting environments. Further spatial-temporal transcriptome profiling revealed dynamic reprogramming of pathways for photosynthesis and stress responses during drought and the subsequent recovery. Mechanistically, SGI represents an intrinsically disordered region-containing protein that interacts with itself, catalase isoforms, dehydrins, and other drought-responsive positive factors, restraining ROS generation. These multifaceted interactions stabilize catalases in response to drought and facilitate their ROS-scavenging activities. Taken altogether, these findings provide insights into currently underexplored mechanisms to circumvent trade-offs between plant growth and stress tolerance that will inform strategies to breed climate-resilient, higher yielding crops for sustainable agriculture. Oxford University Press 2023-02-07 /pmc/articles/PMC10152686/ /pubmed/36746783 http://dx.doi.org/10.1093/plphys/kiad074 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Liu, Jun
Liu, Jing
Deng, Linbin
Liu, Hongmei
Liu, Hongfang
Zhao, Wei
Zhao, Yuwei
Sun, Xingchao
Fan, Shihang
Wang, Hanzhong
Hua, Wei
An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields
title An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields
title_full An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields
title_fullStr An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields
title_full_unstemmed An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields
title_short An intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields
title_sort intrinsically disordered region-containing protein mitigates the drought–growth trade-off to boost yields
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10152686/
https://www.ncbi.nlm.nih.gov/pubmed/36746783
http://dx.doi.org/10.1093/plphys/kiad074
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