Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factor

Many herbivorous insects exhibit enhanced performance and population dynamics on drought-stressed host plants due to induced changes in plant physiology. However, the underlying mechanisms of how drought regulates plant defense against herbivorous insects are still largely unknown. In this study, we...

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Main Authors: Chan Zhao, Wen-Hao Han, Yu-Die Xiong, Shun-Xia Ji, Hui Du, Yu-Jie Chi, Na Chen, He Wu, Shu-Sheng Liu, Xiao-Wei Wang
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Plant Stress
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667064X25001551
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author Chan Zhao
Wen-Hao Han
Yu-Die Xiong
Shun-Xia Ji
Hui Du
Yu-Jie Chi
Na Chen
He Wu
Shu-Sheng Liu
Xiao-Wei Wang
author_facet Chan Zhao
Wen-Hao Han
Yu-Die Xiong
Shun-Xia Ji
Hui Du
Yu-Jie Chi
Na Chen
He Wu
Shu-Sheng Liu
Xiao-Wei Wang
author_sort Chan Zhao
collection DOAJ
description Many herbivorous insects exhibit enhanced performance and population dynamics on drought-stressed host plants due to induced changes in plant physiology. However, the underlying mechanisms of how drought regulates plant defense against herbivorous insects are still largely unknown. In this study, we found that the survival rate and fecundity of whiteflies, notorious global pests, were significantly higher on drought-stressed tobacco. Drought stress did not affect jasmonic acid (JA) accumulation, whereas it significantly decreased the salicylic acid (SA) content by suppressing its biosynthesis. We further demonstrated that drought-induced abscisic acid (ABA) inhibited the expression of isochorismate synthase 1 (ICS1), a key enzyme in the synthesis of SA. The accumulation of ABA induced the expression of abscisic acid responsive NAC domain containing protein 19 (ANAC019), which directly bound to the promoter of NtICS1 and negatively regulated its expression. Finally, we revealed that drought and ABA could activate abscisic acid responsive elements-binding factor 2 (ABF2) transcription factor to up-regulate the expression of NtANAC019. Our study illustrates the significance of cross-talk between abiotic stress and plant-herbivore interactions and reveals the mechanisms leading to altered herbivore fitness on drought-stressed plants.
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spelling doaj-art-76cb5b11f0624bb1bf86ee327ab0ad092025-08-20T03:48:18ZengElsevierPlant Stress2667-064X2025-06-011610088710.1016/j.stress.2025.100887Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factorChan Zhao0Wen-Hao Han1Yu-Die Xiong2Shun-Xia Ji3Hui Du4Yu-Jie Chi5Na Chen6He Wu7Shu-Sheng Liu8Xiao-Wei Wang9State Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaState Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaCorresponding authors.; State Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, PR ChinaMany herbivorous insects exhibit enhanced performance and population dynamics on drought-stressed host plants due to induced changes in plant physiology. However, the underlying mechanisms of how drought regulates plant defense against herbivorous insects are still largely unknown. In this study, we found that the survival rate and fecundity of whiteflies, notorious global pests, were significantly higher on drought-stressed tobacco. Drought stress did not affect jasmonic acid (JA) accumulation, whereas it significantly decreased the salicylic acid (SA) content by suppressing its biosynthesis. We further demonstrated that drought-induced abscisic acid (ABA) inhibited the expression of isochorismate synthase 1 (ICS1), a key enzyme in the synthesis of SA. The accumulation of ABA induced the expression of abscisic acid responsive NAC domain containing protein 19 (ANAC019), which directly bound to the promoter of NtICS1 and negatively regulated its expression. Finally, we revealed that drought and ABA could activate abscisic acid responsive elements-binding factor 2 (ABF2) transcription factor to up-regulate the expression of NtANAC019. Our study illustrates the significance of cross-talk between abiotic stress and plant-herbivore interactions and reveals the mechanisms leading to altered herbivore fitness on drought-stressed plants.http://www.sciencedirect.com/science/article/pii/S2667064X25001551Abscisic acidDroughtPlant-herbivoreSalicylic acidTranscription regulation
spellingShingle Chan Zhao
Wen-Hao Han
Yu-Die Xiong
Shun-Xia Ji
Hui Du
Yu-Jie Chi
Na Chen
He Wu
Shu-Sheng Liu
Xiao-Wei Wang
Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factor
Plant Stress
Abscisic acid
Drought
Plant-herbivore
Salicylic acid
Transcription regulation
title Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factor
title_full Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factor
title_fullStr Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factor
title_full_unstemmed Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factor
title_short Drought suppresses plant salicylic acid defence against herbivorous insects by down-regulating the expression of ICS1 via NAC transcription factor
title_sort drought suppresses plant salicylic acid defence against herbivorous insects by down regulating the expression of ics1 via nac transcription factor
topic Abscisic acid
Drought
Plant-herbivore
Salicylic acid
Transcription regulation
url http://www.sciencedirect.com/science/article/pii/S2667064X25001551
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