A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic Acid

Abstract Here, a sucrose non‐fermenting‐1‐related protein kinase alpha subunit (TaSnRK1α‐1A) is identified as associated with cold stress through integration of genome‐wide association study, bulked segregant RNA sequencing, and virus‐induced gene silencing. It is confirmed that TaSnRK1α positively...

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Main Authors: Lingran Zhang, Ning Zhang, Sisheng Wang, Hongyan Tian, Lu Liu, Dan Pei, Xiaodong Yu, Lei Zhao, Feng Chen
Format: Article
Language:English
Published: Wiley 2023-11-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202303478
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author Lingran Zhang
Ning Zhang
Sisheng Wang
Hongyan Tian
Lu Liu
Dan Pei
Xiaodong Yu
Lei Zhao
Feng Chen
author_facet Lingran Zhang
Ning Zhang
Sisheng Wang
Hongyan Tian
Lu Liu
Dan Pei
Xiaodong Yu
Lei Zhao
Feng Chen
author_sort Lingran Zhang
collection DOAJ
description Abstract Here, a sucrose non‐fermenting‐1‐related protein kinase alpha subunit (TaSnRK1α‐1A) is identified as associated with cold stress through integration of genome‐wide association study, bulked segregant RNA sequencing, and virus‐induced gene silencing. It is confirmed that TaSnRK1α positively regulates cold tolerance by transgenes and ethyl methanesulfonate (EMS) mutants. A plastid‐lipid‐associated protein 6, chloroplastic‐like (TaPAP6L‐2B) strongly interacting with TaSnRK1α‐1A is screened. Molecular chaperone DJ‐1 family protein (TaDJ‐1‐7B) possibly bridged the interaction of TaSnRK1α‐1A and TaPAP6L‐2B. It is further revealed that TaSnRK1α‐1A phosphorylated TaPAP6L‐2B. Subsequently, a superior haplotype TaPAP6L‐2B30S/38S is identified and confirmed that both R30S and G38S are important phosphorylation sites that influence TaPAP6L‐2B in cold tolerance. Overexpression (OE) and EMS‐mutant lines verified TaPAP6L positively modulating cold tolerance. Furthermore, transcriptome sequencing revealed that TaPAP6L‐2B‐OE lines significantly increased jasmonic acid (JA) content, possibly by improving precursor α‐linolenic acid contributing to JA synthesis and by repressing JAR1 degrading JA. Exogenous JA significantly improved the cold tolerance of wheat plants. In summary, TaSnRK1α profoundly regulated cold stress, possibly through phosphorylating TaPAP6L to increase endogenous JA content of wheat plants.
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spelling doaj.art-dc11df3d55bf469698df2d5cc5fbbead2023-11-04T08:56:53ZengWileyAdvanced Science2198-38442023-11-011031n/an/a10.1002/advs.202303478A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic AcidLingran Zhang0Ning Zhang1Sisheng Wang2Hongyan Tian3Lu Liu4Dan Pei5Xiaodong Yu6Lei Zhao7Feng Chen8National Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaNational Key Laboratory of Wheat and Maize Crop Science / CIMMYT‐China Wheat and Maize Joint Research Center /Agronomy College Henan Agricultural University Zhengzhou 450046 ChinaAbstract Here, a sucrose non‐fermenting‐1‐related protein kinase alpha subunit (TaSnRK1α‐1A) is identified as associated with cold stress through integration of genome‐wide association study, bulked segregant RNA sequencing, and virus‐induced gene silencing. It is confirmed that TaSnRK1α positively regulates cold tolerance by transgenes and ethyl methanesulfonate (EMS) mutants. A plastid‐lipid‐associated protein 6, chloroplastic‐like (TaPAP6L‐2B) strongly interacting with TaSnRK1α‐1A is screened. Molecular chaperone DJ‐1 family protein (TaDJ‐1‐7B) possibly bridged the interaction of TaSnRK1α‐1A and TaPAP6L‐2B. It is further revealed that TaSnRK1α‐1A phosphorylated TaPAP6L‐2B. Subsequently, a superior haplotype TaPAP6L‐2B30S/38S is identified and confirmed that both R30S and G38S are important phosphorylation sites that influence TaPAP6L‐2B in cold tolerance. Overexpression (OE) and EMS‐mutant lines verified TaPAP6L positively modulating cold tolerance. Furthermore, transcriptome sequencing revealed that TaPAP6L‐2B‐OE lines significantly increased jasmonic acid (JA) content, possibly by improving precursor α‐linolenic acid contributing to JA synthesis and by repressing JAR1 degrading JA. Exogenous JA significantly improved the cold tolerance of wheat plants. In summary, TaSnRK1α profoundly regulated cold stress, possibly through phosphorylating TaPAP6L to increase endogenous JA content of wheat plants.https://doi.org/10.1002/advs.202303478cold stresscommon wheatjasmonic acidphosphorylationTaPAP6LTaSnRK1α
spellingShingle Lingran Zhang
Ning Zhang
Sisheng Wang
Hongyan Tian
Lu Liu
Dan Pei
Xiaodong Yu
Lei Zhao
Feng Chen
A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic Acid
Advanced Science
cold stress
common wheat
jasmonic acid
phosphorylation
TaPAP6L
TaSnRK1α
title A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic Acid
title_full A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic Acid
title_fullStr A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic Acid
title_full_unstemmed A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic Acid
title_short A TaSnRK1α Modulates TaPAP6L‐Mediated Wheat Cold Tolerance through Regulating Endogenous Jasmonic Acid
title_sort tasnrk1α modulates tapap6l mediated wheat cold tolerance through regulating endogenous jasmonic acid
topic cold stress
common wheat
jasmonic acid
phosphorylation
TaPAP6L
TaSnRK1α
url https://doi.org/10.1002/advs.202303478
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