Silencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildew

Abstract Background Calcium ions (Ca2+), secondary messengers, are crucial for the signal transduction process of the interaction between plants and pathogens. Ca2+ signaling also regulates autophagy. As plant calcium signal-decoding proteins, calcium-dependent protein kinases (CDPKs) have been foun...

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Main Authors: Jie-yu Yue, Jin-lan Jiao, Wen-wen Wang, Xin-rui Jie, Hua-zhong Wang
Format: Article
Language:English
Published: BMC 2023-03-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04140-y
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author Jie-yu Yue
Jin-lan Jiao
Wen-wen Wang
Xin-rui Jie
Hua-zhong Wang
author_facet Jie-yu Yue
Jin-lan Jiao
Wen-wen Wang
Xin-rui Jie
Hua-zhong Wang
author_sort Jie-yu Yue
collection DOAJ
description Abstract Background Calcium ions (Ca2+), secondary messengers, are crucial for the signal transduction process of the interaction between plants and pathogens. Ca2+ signaling also regulates autophagy. As plant calcium signal-decoding proteins, calcium-dependent protein kinases (CDPKs) have been found to be involved in biotic and abiotic stress responses. However, information on their functions in response to powdery mildew attack in wheat crops is limited. Result In the present study, the expression levels of TaCDPK27, four essential autophagy-related genes (ATGs) (TaATG5, TaATG7, TaATG8, and TaATG10), and two major metacaspase genes, namely, TaMCA1 and TaMCA9, were increased by powdery mildew (Blumeria graminis f. sp. tritici, Bgt) infection in wheat seedling leaves. Silencing TaCDPK27 improves wheat seedling resistance to powdery mildew, with fewer Bgt hyphae occurring on TaCDPK27-silenced wheat seedling leaves than on normal seedlings. In wheat seedling leaves under powdery mildew infection, silencing TaCDPK27 induced excess contents of reactive oxygen species (ROS); decreased the activities of superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT); and led to an increase in programmed cell death (PCD). Silencing TaCDPK27 also inhibited autophagy in wheat seedling leaves, and silencing TaATG7 also enhanced wheat seedling resistance to powdery mildew infection. TaCDPK27-mCherry and GFP-TaATG8h colocalized in wheat protoplasts. Overexpressed TaCDPK27-mCherry fusions required enhanced autophagy activity in wheat protoplast under carbon starvation. Conclusion These results suggested that TaCDPK27 negatively regulates wheat resistance to PW infection, and functionally links with autophagy in wheat.
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spelling doaj.art-0cd19bffbb7840ff8119201db882b5782023-03-22T10:49:28ZengBMCBMC Plant Biology1471-22292023-03-0123111110.1186/s12870-023-04140-ySilencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildewJie-yu Yue0Jin-lan Jiao1Wen-wen Wang2Xin-rui Jie3Hua-zhong Wang4Tianjin Key Laboratory of Animal and Plant Resistance, Tianjin Normal UniversityTianjin Key Laboratory of Animal and Plant Resistance, Tianjin Normal UniversityTianjin Key Laboratory of Animal and Plant Resistance, Tianjin Normal UniversityTianjin Key Laboratory of Animal and Plant Resistance, Tianjin Normal UniversityTianjin Key Laboratory of Animal and Plant Resistance, Tianjin Normal UniversityAbstract Background Calcium ions (Ca2+), secondary messengers, are crucial for the signal transduction process of the interaction between plants and pathogens. Ca2+ signaling also regulates autophagy. As plant calcium signal-decoding proteins, calcium-dependent protein kinases (CDPKs) have been found to be involved in biotic and abiotic stress responses. However, information on their functions in response to powdery mildew attack in wheat crops is limited. Result In the present study, the expression levels of TaCDPK27, four essential autophagy-related genes (ATGs) (TaATG5, TaATG7, TaATG8, and TaATG10), and two major metacaspase genes, namely, TaMCA1 and TaMCA9, were increased by powdery mildew (Blumeria graminis f. sp. tritici, Bgt) infection in wheat seedling leaves. Silencing TaCDPK27 improves wheat seedling resistance to powdery mildew, with fewer Bgt hyphae occurring on TaCDPK27-silenced wheat seedling leaves than on normal seedlings. In wheat seedling leaves under powdery mildew infection, silencing TaCDPK27 induced excess contents of reactive oxygen species (ROS); decreased the activities of superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT); and led to an increase in programmed cell death (PCD). Silencing TaCDPK27 also inhibited autophagy in wheat seedling leaves, and silencing TaATG7 also enhanced wheat seedling resistance to powdery mildew infection. TaCDPK27-mCherry and GFP-TaATG8h colocalized in wheat protoplasts. Overexpressed TaCDPK27-mCherry fusions required enhanced autophagy activity in wheat protoplast under carbon starvation. Conclusion These results suggested that TaCDPK27 negatively regulates wheat resistance to PW infection, and functionally links with autophagy in wheat.https://doi.org/10.1186/s12870-023-04140-yWheatPowdery mildewProgrammed cell deathCalcium-dependent protein kinase TaCDPK27Autophagy
spellingShingle Jie-yu Yue
Jin-lan Jiao
Wen-wen Wang
Xin-rui Jie
Hua-zhong Wang
Silencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildew
BMC Plant Biology
Wheat
Powdery mildew
Programmed cell death
Calcium-dependent protein kinase TaCDPK27
Autophagy
title Silencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildew
title_full Silencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildew
title_fullStr Silencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildew
title_full_unstemmed Silencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildew
title_short Silencing of the calcium-dependent protein kinase TaCDPK27 improves wheat resistance to powdery mildew
title_sort silencing of the calcium dependent protein kinase tacdpk27 improves wheat resistance to powdery mildew
topic Wheat
Powdery mildew
Programmed cell death
Calcium-dependent protein kinase TaCDPK27
Autophagy
url https://doi.org/10.1186/s12870-023-04140-y
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AT jinlanjiao silencingofthecalciumdependentproteinkinasetacdpk27improveswheatresistancetopowderymildew
AT wenwenwang silencingofthecalciumdependentproteinkinasetacdpk27improveswheatresistancetopowderymildew
AT xinruijie silencingofthecalciumdependentproteinkinasetacdpk27improveswheatresistancetopowderymildew
AT huazhongwang silencingofthecalciumdependentproteinkinasetacdpk27improveswheatresistancetopowderymildew