Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants

Intercropping with guava (<i>Psidium guajava</i> L.) can assist with the management of Asian citrus psyllid (ACP, <i>Diaphorina citri</i> Kuwayama), the insect vector of the huanglongbing pathogen, in citrus orchards. Sulfur volatiles have a repellent activity and physiologic...

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Main Authors: Siquan Ling, Hualong Qiu, Jinzhu Xu, Yanping Gu, Jinxin Yu, Wei Wang, Jiali Liu, Xinnian Zeng
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/18/10271
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author Siquan Ling
Hualong Qiu
Jinzhu Xu
Yanping Gu
Jinxin Yu
Wei Wang
Jiali Liu
Xinnian Zeng
author_facet Siquan Ling
Hualong Qiu
Jinzhu Xu
Yanping Gu
Jinxin Yu
Wei Wang
Jiali Liu
Xinnian Zeng
author_sort Siquan Ling
collection DOAJ
description Intercropping with guava (<i>Psidium guajava</i> L.) can assist with the management of Asian citrus psyllid (ACP, <i>Diaphorina citri</i> Kuwayama), the insect vector of the huanglongbing pathogen, in citrus orchards. Sulfur volatiles have a repellent activity and physiological effects, as well as being important components of guava volatiles. In this study, we tested whether the sulfur volatiles emitted by guava plants play a role in plant–plant communications and trigger anti-herbivore activities against ACP in sweet orange plants (<i>Citrus sinensis</i> L. Osbeck). Real-time determination using a proton-transfer-reaction mass spectrometer (PTR-MS) showed that guava plants continuously release methanethiol, dimethyl sulfide (DMS), and dimethyl disulfide (DMDS), and the contents increased rapidly after mechanical damage. The exposure of orange plants to DMDS resulted in the suppression of the developmental performance of ACP. The differential elevation of salicylic acid (SA) levels; the expression of phenylalanine ammonia lyase (PAL), salicylate-O-methyl transferase (SMT), and pathogenesis-related (PR1) genes; the activities of defense-related enzymes PAL, polyphenol oxidase (PPO), and peroxidase (POD); and the total polyphenol content were observed in DMDS-exposed orange plants. The emission of volatiles including myrcene, nonanal, decanal, and methyl salicylate (MeSA) was increased. In addition, phenylpropanoid and flavonoid biosynthesis, and aromatic amino acid (such as phenylalanine, tyrosine, and tryptophan) metabolic pathways were induced. Altogether, our results indicated that DMDS from guava plants can activate defense responses in eavesdropping orange plants and boost their herbivore resistance to ACP, which suggests the possibility of using DMDS as a novel approach for the management of ACP in citrus orchards.
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spelling doaj.art-0fb9c885186240c2b5397582dafc92852023-11-23T16:38:56ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-09-0123181027110.3390/ijms231810271Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange PlantsSiquan Ling0Hualong Qiu1Jinzhu Xu2Yanping Gu3Jinxin Yu4Wei Wang5Jiali Liu6Xinnian Zeng7Guangdong Engineering Research Center for Insect Behavior Regulation, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaGuangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou 510520, ChinaGuangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou 510520, ChinaPlant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaGuangdong Engineering Research Center for Insect Behavior Regulation, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaGuangdong Engineering Research Center for Insect Behavior Regulation, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaGuangdong Engineering Research Center for Insect Behavior Regulation, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaGuangdong Engineering Research Center for Insect Behavior Regulation, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaIntercropping with guava (<i>Psidium guajava</i> L.) can assist with the management of Asian citrus psyllid (ACP, <i>Diaphorina citri</i> Kuwayama), the insect vector of the huanglongbing pathogen, in citrus orchards. Sulfur volatiles have a repellent activity and physiological effects, as well as being important components of guava volatiles. In this study, we tested whether the sulfur volatiles emitted by guava plants play a role in plant–plant communications and trigger anti-herbivore activities against ACP in sweet orange plants (<i>Citrus sinensis</i> L. Osbeck). Real-time determination using a proton-transfer-reaction mass spectrometer (PTR-MS) showed that guava plants continuously release methanethiol, dimethyl sulfide (DMS), and dimethyl disulfide (DMDS), and the contents increased rapidly after mechanical damage. The exposure of orange plants to DMDS resulted in the suppression of the developmental performance of ACP. The differential elevation of salicylic acid (SA) levels; the expression of phenylalanine ammonia lyase (PAL), salicylate-O-methyl transferase (SMT), and pathogenesis-related (PR1) genes; the activities of defense-related enzymes PAL, polyphenol oxidase (PPO), and peroxidase (POD); and the total polyphenol content were observed in DMDS-exposed orange plants. The emission of volatiles including myrcene, nonanal, decanal, and methyl salicylate (MeSA) was increased. In addition, phenylpropanoid and flavonoid biosynthesis, and aromatic amino acid (such as phenylalanine, tyrosine, and tryptophan) metabolic pathways were induced. Altogether, our results indicated that DMDS from guava plants can activate defense responses in eavesdropping orange plants and boost their herbivore resistance to ACP, which suggests the possibility of using DMDS as a novel approach for the management of ACP in citrus orchards.https://www.mdpi.com/1422-0067/23/18/10271sulfur volatilesdimethyl disulfideeavesdroppingdefense responseguavasweet orange
spellingShingle Siquan Ling
Hualong Qiu
Jinzhu Xu
Yanping Gu
Jinxin Yu
Wei Wang
Jiali Liu
Xinnian Zeng
Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants
International Journal of Molecular Sciences
sulfur volatiles
dimethyl disulfide
eavesdropping
defense response
guava
sweet orange
title Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants
title_full Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants
title_fullStr Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants
title_full_unstemmed Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants
title_short Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants
title_sort volatile dimethyl disulfide from guava plants regulate developmental performance of asian citrus psyllid through activation of defense responses in neighboring orange plants
topic sulfur volatiles
dimethyl disulfide
eavesdropping
defense response
guava
sweet orange
url https://www.mdpi.com/1422-0067/23/18/10271
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