A point mutation in LTT1 enhances cold tolerance at the booting stage in rice

The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance genes have been identified that can be effectively used in breeding programmes. Here, we show that a point mutation in the low‐temperature tol...

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Published inPlant, cell and environment Vol. 43; no. 4; pp. 992 - 1007
Main Authors Xu, Yufang, Wang, Ruci, Wang, Yueming, Zhang, Li, Yao, Shanguo
Format Journal Article
LanguageEnglish
Published Chichester, UK John Wiley & Sons, Ltd 01.04.2020
Wiley Subscription Services, Inc
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ISSN0140-7791
1365-3040
1365-3040
DOI10.1111/pce.13717

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Abstract The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance genes have been identified that can be effectively used in breeding programmes. Here, we show that a point mutation in the low‐temperature tolerance 1 (LTT1) gene improves cold tolerance by maintaining tapetum degradation and pollen development, by activation of systems that metabolize reactive oxygen species (ROS). Cold‐induced ROS accumulation is therefore prevented in the anthers of the ltt1 mutants allowing correct development. In contrast, exposure to cold stress dramatically increases ROS accumulation in the wild type anthers, together with the expression of genes encoding proteins associated with programmed cell death and with the accelerated degradation of the tapetum that ultimately leads to pollen abortion. These results demonstrate that appropriate ROS management is critical for the cold tolerance of rice at the booting stage. Hence, the ltt1 mutation can significantly improve the seed setting ability of cold‐sensitive rice varieties under low‐temperature stress conditions, with little yield penalty under optimal temperature conditions. This study highlights the importance of a valuable genetic resource that may be applied in rice breeding programmes to enhance cold tolerance. Understanding how rice plants respond to the changing environmental temperature is one of the most important biological subjects. By functional analysis of the cold tolerant ltt1 mutant, we demonstrate that acclimation to high endogenous reactive oxygen species level is critical for rice plants to cope with the coming low‐temperature stress. Our results provide a novel strategy for genetic improvement of booting stage cold tolerance in rice.
AbstractList The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance genes have been identified that can be effectively used in breeding programmes. Here, we show that a point mutation in the low-temperature tolerance 1 (LTT1) gene improves cold tolerance by maintaining tapetum degradation and pollen development, by activation of systems that metabolize reactive oxygen species (ROS). Cold-induced ROS accumulation is therefore prevented in the anthers of the ltt1 mutants allowing correct development. In contrast, exposure to cold stress dramatically increases ROS accumulation in the wild type anthers, together with the expression of genes encoding proteins associated with programmed cell death and with the accelerated degradation of the tapetum that ultimately leads to pollen abortion. These results demonstrate that appropriate ROS management is critical for the cold tolerance of rice at the booting stage. Hence, the ltt1 mutation can significantly improve the seed setting ability of cold-sensitive rice varieties under low-temperature stress conditions, with little yield penalty under optimal temperature conditions. This study highlights the importance of a valuable genetic resource that may be applied in rice breeding programmes to enhance cold tolerance.
The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance genes have been identified that can be effectively used in breeding programmes. Here, we show that a point mutation in the low‐temperature tolerance 1 ( LTT1 ) gene improves cold tolerance by maintaining tapetum degradation and pollen development, by activation of systems that metabolize reactive oxygen species (ROS). Cold‐induced ROS accumulation is therefore prevented in the anthers of the ltt1 mutants allowing correct development. In contrast, exposure to cold stress dramatically increases ROS accumulation in the wild type anthers, together with the expression of genes encoding proteins associated with programmed cell death and with the accelerated degradation of the tapetum that ultimately leads to pollen abortion. These results demonstrate that appropriate ROS management is critical for the cold tolerance of rice at the booting stage. Hence, the ltt1 mutation can significantly improve the seed setting ability of cold‐sensitive rice varieties under low‐temperature stress conditions, with little yield penalty under optimal temperature conditions. This study highlights the importance of a valuable genetic resource that may be applied in rice breeding programmes to enhance cold tolerance. Understanding how rice plants respond to the changing environmental temperature is one of the most important biological subjects. By functional analysis of the cold tolerant ltt1 mutant, we demonstrate that acclimation to high endogenous reactive oxygen species level is critical for rice plants to cope with the coming low‐temperature stress. Our results provide a novel strategy for genetic improvement of booting stage cold tolerance in rice.
The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance genes have been identified that can be effectively used in breeding programmes. Here, we show that a point mutation in the low-temperature tolerance 1 (LTT1) gene improves cold tolerance by maintaining tapetum degradation and pollen development, by activation of systems that metabolize reactive oxygen species (ROS). Cold-induced ROS accumulation is therefore prevented in the anthers of the ltt1 mutants allowing correct development. In contrast, exposure to cold stress dramatically increases ROS accumulation in the wild type anthers, together with the expression of genes encoding proteins associated with programmed cell death and with the accelerated degradation of the tapetum that ultimately leads to pollen abortion. These results demonstrate that appropriate ROS management is critical for the cold tolerance of rice at the booting stage. Hence, the ltt1 mutation can significantly improve the seed setting ability of cold-sensitive rice varieties under low-temperature stress conditions, with little yield penalty under optimal temperature conditions. This study highlights the importance of a valuable genetic resource that may be applied in rice breeding programmes to enhance cold tolerance.The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance genes have been identified that can be effectively used in breeding programmes. Here, we show that a point mutation in the low-temperature tolerance 1 (LTT1) gene improves cold tolerance by maintaining tapetum degradation and pollen development, by activation of systems that metabolize reactive oxygen species (ROS). Cold-induced ROS accumulation is therefore prevented in the anthers of the ltt1 mutants allowing correct development. In contrast, exposure to cold stress dramatically increases ROS accumulation in the wild type anthers, together with the expression of genes encoding proteins associated with programmed cell death and with the accelerated degradation of the tapetum that ultimately leads to pollen abortion. These results demonstrate that appropriate ROS management is critical for the cold tolerance of rice at the booting stage. Hence, the ltt1 mutation can significantly improve the seed setting ability of cold-sensitive rice varieties under low-temperature stress conditions, with little yield penalty under optimal temperature conditions. This study highlights the importance of a valuable genetic resource that may be applied in rice breeding programmes to enhance cold tolerance.
The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance genes have been identified that can be effectively used in breeding programmes. Here, we show that a point mutation in the low‐temperature tolerance 1 (LTT1) gene improves cold tolerance by maintaining tapetum degradation and pollen development, by activation of systems that metabolize reactive oxygen species (ROS). Cold‐induced ROS accumulation is therefore prevented in the anthers of the ltt1 mutants allowing correct development. In contrast, exposure to cold stress dramatically increases ROS accumulation in the wild type anthers, together with the expression of genes encoding proteins associated with programmed cell death and with the accelerated degradation of the tapetum that ultimately leads to pollen abortion. These results demonstrate that appropriate ROS management is critical for the cold tolerance of rice at the booting stage. Hence, the ltt1 mutation can significantly improve the seed setting ability of cold‐sensitive rice varieties under low‐temperature stress conditions, with little yield penalty under optimal temperature conditions. This study highlights the importance of a valuable genetic resource that may be applied in rice breeding programmes to enhance cold tolerance. Understanding how rice plants respond to the changing environmental temperature is one of the most important biological subjects. By functional analysis of the cold tolerant ltt1 mutant, we demonstrate that acclimation to high endogenous reactive oxygen species level is critical for rice plants to cope with the coming low‐temperature stress. Our results provide a novel strategy for genetic improvement of booting stage cold tolerance in rice.
Author Xu, Yufang
Wang, Yueming
Wang, Ruci
Yao, Shanguo
Zhang, Li
AuthorAffiliation 1 State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design Chinese Academy of Sciences Beijing China
2 Genome Biology Center University of Chinese Academy of Sciences Beijing China
AuthorAffiliation_xml – name: 1 State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design Chinese Academy of Sciences Beijing China
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Issue 4
Keywords booting stage
cold tolerance
rice
ROS acclimation
LTT1
Language English
License Attribution-NonCommercial-NoDerivs
2020 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.
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SSID ssj0001479
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Snippet The cold tolerance of rice at the booting stage is a main factor determining sustainability and regional adaptability. However, relatively few cold tolerance...
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pubmed
crossref
wiley
SourceType Open Access Repository
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Enrichment Source
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StartPage 992
SubjectTerms abortion (plants)
Accumulation
Adaptability
Anthers
Apoptosis
Apoptosis - genetics
Apoptosis - physiology
booting stage
breeding programs
Cell death
Cold
cold stress
Cold Temperature
Cold tolerance
Degradation
Gene expression
Genes
Genes, Plant - genetics
Genes, Plant - physiology
Genetic resources
In Situ Nick-End Labeling
LTT1
Microscopy, Electron, Scanning
Mutants
Mutation
Original
Oryza - genetics
Oryza - metabolism
Oryza - physiology
Oryza - ultrastructure
Oryza sativa
Peroxidases - metabolism
Plant breeding
Point mutation
Point Mutation - genetics
Pollen
programmed cell death
proteins
Quantitative Trait, Heritable
Reactive oxygen species
Reactive Oxygen Species - metabolism
Rice
ROS acclimation
seed set
Superoxide Dismutase - metabolism
temperature
Temperature tolerance
Title A point mutation in LTT1 enhances cold tolerance at the booting stage in rice
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpce.13717
https://www.ncbi.nlm.nih.gov/pubmed/31922260
https://www.proquest.com/docview/2383457891
https://www.proquest.com/docview/2336260109
https://www.proquest.com/docview/2439428372
https://pubmed.ncbi.nlm.nih.gov/PMC7154693
Volume 43
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