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The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube

Jujube witches’ broom disease (JWB), one of the most serious phytoplasma diseases, usually results in the destruction of Chinese jujube (Ziziphus jujuba Mill.). Although most jujube cultivars are sensitive to JWB, we found a few genotypes that are highly resistant to JWB. However, the molecular mech...

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Autores principales: Wang, Lixin, Liu, Shiyan, Gao, Mengjiao, Wang, Lihu, Wang, Linxia, Wang, Yunjie, Dai, Li, Zhao, Jin, Liu, Mengjun, Liu, Zhiguo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8971994/
https://www.ncbi.nlm.nih.gov/pubmed/35369447
http://dx.doi.org/10.3389/fmicb.2022.800762
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author Wang, Lixin
Liu, Shiyan
Gao, Mengjiao
Wang, Lihu
Wang, Linxia
Wang, Yunjie
Dai, Li
Zhao, Jin
Liu, Mengjun
Liu, Zhiguo
author_facet Wang, Lixin
Liu, Shiyan
Gao, Mengjiao
Wang, Lihu
Wang, Linxia
Wang, Yunjie
Dai, Li
Zhao, Jin
Liu, Mengjun
Liu, Zhiguo
author_sort Wang, Lixin
collection PubMed
description Jujube witches’ broom disease (JWB), one of the most serious phytoplasma diseases, usually results in the destruction of Chinese jujube (Ziziphus jujuba Mill.). Although most jujube cultivars are sensitive to JWB, we found a few genotypes that are highly resistant to JWB. However, the molecular mechanism of phytoplasma resistance has seldom been studied. Here, we used Chinese jujube “T13,” which has strong resistance to JWB, and a typical susceptible cultivar, “Pozao” (“PZ”), as materials to perform comparative transcriptome, hormone, and regulation analyses. After phytoplasma infection, the differential expression genes (DEGs) were detected at all three growth phases (S1, S2, and S3) in “PZ,” but DEGs were detected only at the first growth phase in “T13.” Meanwhile, no phytoplasma was detected, and the symptoms especially witches’ broom caused by JWB were not observed at the last two growth phases (S2 and S3) in “T13.” Protein–protein interaction analysis also showed that the key genes were mainly involved in hormone and reactive oxygen species (ROS) signaling. In addition, during the recovered growth phase in “T13” from S1 to S2, the level of hydrogen peroxide (H(2)O(2)) was significantly increased and then decreased from S2 to S3. Moreover, jasmonic acid (JA) was significantly accumulated in “PZ” diseased plants, especially at the S2 phase and at the S2 phase in “T13,” while the content of salicylic acid (SA) decreased significantly at the S2 phase of “T13” compared to that in “PZ.” The changes in H(2)O(2) and JA or SA were consistent with the changes in their key synthesis genes in the transcriptome data. Finally, exogenous application of an SA inhibitor [1-aminobenzotriazole (ABT)] rescued witches’ broom symptoms, while the contents of both JA and MeJA increased after ABT treatment compared to the control, demonstrating that exogenous application of an SA inhibitor rescued the symptoms of jujube after phytoplasma infection by decreasing the contents of SA and increasing the contents of JA and MeJA. Collectively, our study provides a new perspective on the transcriptional changes of Chinese jujube in response to JWB and novel insights that the crosstalk of JA and SA signaling communicated together to contribute to “T13” JWB resistance.
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spelling pubmed-89719942022-04-02 The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube Wang, Lixin Liu, Shiyan Gao, Mengjiao Wang, Lihu Wang, Linxia Wang, Yunjie Dai, Li Zhao, Jin Liu, Mengjun Liu, Zhiguo Front Microbiol Microbiology Jujube witches’ broom disease (JWB), one of the most serious phytoplasma diseases, usually results in the destruction of Chinese jujube (Ziziphus jujuba Mill.). Although most jujube cultivars are sensitive to JWB, we found a few genotypes that are highly resistant to JWB. However, the molecular mechanism of phytoplasma resistance has seldom been studied. Here, we used Chinese jujube “T13,” which has strong resistance to JWB, and a typical susceptible cultivar, “Pozao” (“PZ”), as materials to perform comparative transcriptome, hormone, and regulation analyses. After phytoplasma infection, the differential expression genes (DEGs) were detected at all three growth phases (S1, S2, and S3) in “PZ,” but DEGs were detected only at the first growth phase in “T13.” Meanwhile, no phytoplasma was detected, and the symptoms especially witches’ broom caused by JWB were not observed at the last two growth phases (S2 and S3) in “T13.” Protein–protein interaction analysis also showed that the key genes were mainly involved in hormone and reactive oxygen species (ROS) signaling. In addition, during the recovered growth phase in “T13” from S1 to S2, the level of hydrogen peroxide (H(2)O(2)) was significantly increased and then decreased from S2 to S3. Moreover, jasmonic acid (JA) was significantly accumulated in “PZ” diseased plants, especially at the S2 phase and at the S2 phase in “T13,” while the content of salicylic acid (SA) decreased significantly at the S2 phase of “T13” compared to that in “PZ.” The changes in H(2)O(2) and JA or SA were consistent with the changes in their key synthesis genes in the transcriptome data. Finally, exogenous application of an SA inhibitor [1-aminobenzotriazole (ABT)] rescued witches’ broom symptoms, while the contents of both JA and MeJA increased after ABT treatment compared to the control, demonstrating that exogenous application of an SA inhibitor rescued the symptoms of jujube after phytoplasma infection by decreasing the contents of SA and increasing the contents of JA and MeJA. Collectively, our study provides a new perspective on the transcriptional changes of Chinese jujube in response to JWB and novel insights that the crosstalk of JA and SA signaling communicated together to contribute to “T13” JWB resistance. Frontiers Media S.A. 2022-03-18 /pmc/articles/PMC8971994/ /pubmed/35369447 http://dx.doi.org/10.3389/fmicb.2022.800762 Text en Copyright © 2022 Wang, Liu, Gao, Wang, Wang, Wang, Dai, Zhao, Liu and Liu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wang, Lixin
Liu, Shiyan
Gao, Mengjiao
Wang, Lihu
Wang, Linxia
Wang, Yunjie
Dai, Li
Zhao, Jin
Liu, Mengjun
Liu, Zhiguo
The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube
title The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube
title_full The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube
title_fullStr The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube
title_full_unstemmed The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube
title_short The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube
title_sort crosstalk of the salicylic acid and jasmonic acid signaling pathways contributed to different resistance to phytoplasma infection between the two genotypes in chinese jujube
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8971994/
https://www.ncbi.nlm.nih.gov/pubmed/35369447
http://dx.doi.org/10.3389/fmicb.2022.800762
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