Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus Infection

Candidatus Liberibacter asiaticus (CLas) is the causative agent of Huanglongbing (HLB), which has caused great economic losses to the citrus industry. The molecular mechanism of the host response to CLas in wild citrus germplasm has been reported less. Eighteen weeks after inoculation via grafting,...

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Main Authors: Ting Peng, Jing-Liang Kang, Xin-Ting Xiong, Fang-Ting Cheng, Xiao-Juan Zhou, Wen-Shan Dai, Min Wang, Zhong-Yang Li, Hua-Nan Su, Ba-Lian Zhong
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.748209/full
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author Ting Peng
Jing-Liang Kang
Jing-Liang Kang
Xin-Ting Xiong
Fang-Ting Cheng
Xiao-Juan Zhou
Wen-Shan Dai
Wen-Shan Dai
Min Wang
Min Wang
Zhong-Yang Li
Hua-Nan Su
Ba-Lian Zhong
author_facet Ting Peng
Jing-Liang Kang
Jing-Liang Kang
Xin-Ting Xiong
Fang-Ting Cheng
Xiao-Juan Zhou
Wen-Shan Dai
Wen-Shan Dai
Min Wang
Min Wang
Zhong-Yang Li
Hua-Nan Su
Ba-Lian Zhong
author_sort Ting Peng
collection DOAJ
description Candidatus Liberibacter asiaticus (CLas) is the causative agent of Huanglongbing (HLB), which has caused great economic losses to the citrus industry. The molecular mechanism of the host response to CLas in wild citrus germplasm has been reported less. Eighteen weeks after inoculation via grafting, all the CLas-inoculated Chongyi wild mandarin (Citrus reticulata) were positive and showed severe anatomical aberrations, suggesting its susceptibility to HLB. Transcriptomics and metabolomics analyses of leaves, barks, and roots from mock-inoculated (control) and CLas-inoculated seedlings were performed. Comparative transcriptomics identified 3,628, 3,770, and 1,716 differentially expressed genes (DEGs) between CLas-infected and healthy tissues in the leaves, barks, and roots, respectively. The CLas-infected tissues had higher transcripts per kilobase per million values and more genes that reached their maximal expression, suggesting that HLB might cause an overall increase in transcript accumulation. However, HLB-triggered transcriptional alteration showed tissue specificity. In the CLas-infected leaves, many DEGs encoding immune receptors were downregulated. In the CLas-infected barks, nearly all the DEGs involved in signaling and plant-pathogen interaction were upregulated. In the CLas-infected roots, DEGs encoding enzymes or transporters involved in carotenoid biosynthesis and nitrogen metabolism were downregulated. Metabolomics identified 71, 62, and 50 differentially accumulated metabolites (DAMs) in the CLas-infected leaves, barks and roots, respectively. By associating DEGs with DAMs, nitrogen metabolism was the only pathway shared by the three infected tissues and was depressed in the CLas-infected roots. In addition, 26 genes were determined as putative markers of CLas infection, and a hypothesized model for the HLB susceptibility mechanism in Chongyi was proposed. Our study may shed light on investigating the molecular mechanism of the host response to CLas infection in wild citrus germplasm.
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spelling doaj.art-8e17aa7c844448eb9115e8fbc724382a2022-12-21T20:14:53ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-10-011210.3389/fpls.2021.748209748209Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus InfectionTing Peng0Jing-Liang Kang1Jing-Liang Kang2Xin-Ting Xiong3Fang-Ting Cheng4Xiao-Juan Zhou5Wen-Shan Dai6Wen-Shan Dai7Min Wang8Min Wang9Zhong-Yang Li10Hua-Nan Su11Ba-Lian Zhong12National Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaChina-USA Citrus Huanglongbing Joint Laboratory, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaChina-USA Citrus Huanglongbing Joint Laboratory, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaChina-USA Citrus Huanglongbing Joint Laboratory, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaNational Navel Orange Engineering Research Center, College of Life Sciences, Gannan Normal University, Ganzhou, ChinaCandidatus Liberibacter asiaticus (CLas) is the causative agent of Huanglongbing (HLB), which has caused great economic losses to the citrus industry. The molecular mechanism of the host response to CLas in wild citrus germplasm has been reported less. Eighteen weeks after inoculation via grafting, all the CLas-inoculated Chongyi wild mandarin (Citrus reticulata) were positive and showed severe anatomical aberrations, suggesting its susceptibility to HLB. Transcriptomics and metabolomics analyses of leaves, barks, and roots from mock-inoculated (control) and CLas-inoculated seedlings were performed. Comparative transcriptomics identified 3,628, 3,770, and 1,716 differentially expressed genes (DEGs) between CLas-infected and healthy tissues in the leaves, barks, and roots, respectively. The CLas-infected tissues had higher transcripts per kilobase per million values and more genes that reached their maximal expression, suggesting that HLB might cause an overall increase in transcript accumulation. However, HLB-triggered transcriptional alteration showed tissue specificity. In the CLas-infected leaves, many DEGs encoding immune receptors were downregulated. In the CLas-infected barks, nearly all the DEGs involved in signaling and plant-pathogen interaction were upregulated. In the CLas-infected roots, DEGs encoding enzymes or transporters involved in carotenoid biosynthesis and nitrogen metabolism were downregulated. Metabolomics identified 71, 62, and 50 differentially accumulated metabolites (DAMs) in the CLas-infected leaves, barks and roots, respectively. By associating DEGs with DAMs, nitrogen metabolism was the only pathway shared by the three infected tissues and was depressed in the CLas-infected roots. In addition, 26 genes were determined as putative markers of CLas infection, and a hypothesized model for the HLB susceptibility mechanism in Chongyi was proposed. Our study may shed light on investigating the molecular mechanism of the host response to CLas infection in wild citrus germplasm.https://www.frontiersin.org/articles/10.3389/fpls.2021.748209/fullHuanglongbingwild citrus germplasmRNA-seqmetabolometissue specificityanatomical aberration
spellingShingle Ting Peng
Jing-Liang Kang
Jing-Liang Kang
Xin-Ting Xiong
Fang-Ting Cheng
Xiao-Juan Zhou
Wen-Shan Dai
Wen-Shan Dai
Min Wang
Min Wang
Zhong-Yang Li
Hua-Nan Su
Ba-Lian Zhong
Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus Infection
Frontiers in Plant Science
Huanglongbing
wild citrus germplasm
RNA-seq
metabolome
tissue specificity
anatomical aberration
title Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus Infection
title_full Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus Infection
title_fullStr Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus Infection
title_full_unstemmed Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus Infection
title_short Integrated Transcriptomics and Metabolomics Analyses Provide Insights Into the Response of Chongyi Wild Mandarin to Candidatus Liberibacter Asiaticus Infection
title_sort integrated transcriptomics and metabolomics analyses provide insights into the response of chongyi wild mandarin to candidatus liberibacter asiaticus infection
topic Huanglongbing
wild citrus germplasm
RNA-seq
metabolome
tissue specificity
anatomical aberration
url https://www.frontiersin.org/articles/10.3389/fpls.2021.748209/full
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