Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> Decne

<i>Camptotheca acuminata</i> Witches’-broom disease (CaWB) is the most destructive disease affecting <i>C. acuminata</i> in China. Previous studies on CaWB have failed to clarify the incidence pattern in <i>C. acuminata</i> after infection with phytoplasma. The ti...

Full description

Bibliographic Details
Main Authors: Kai Qiao, Weiyi Huang, Xuemei Li, Jiahui Liang, Hong Cai
Format: Article
Language:English
Published: MDPI AG 2023-10-01
Series:Agriculture
Subjects:
Online Access:https://www.mdpi.com/2077-0472/13/10/1943
_version_ 1827722159032631296
author Kai Qiao
Weiyi Huang
Xuemei Li
Jiahui Liang
Hong Cai
author_facet Kai Qiao
Weiyi Huang
Xuemei Li
Jiahui Liang
Hong Cai
author_sort Kai Qiao
collection DOAJ
description <i>Camptotheca acuminata</i> Witches’-broom disease (CaWB) is the most destructive disease affecting <i>C. acuminata</i> in China. Previous studies on CaWB have failed to clarify the incidence pattern in <i>C. acuminata</i> after infection with phytoplasma. The time interval between phytoplasma infection of <i>C. acuminata</i> and the onset of Witches’-broom symptoms in <i>C. acuminata</i> was very long. <i>C. acuminata</i> inoculated with CaWB showed leaf margin scorching symptoms at 4 weeks in inoculated leaves. At 16 weeks after infection (WAI), old leaves were shed, while new leaves showed a mild leaf margin scorch; at 28 WAI, typical symptoms appeared. Transcriptomic and metabolomic analyses of the three sampling periods revealed 194 differentially expressed genes, mainly enriched in MAPK signaling, plant–pathogen interaction, phenylpropanoid biosynthesis, starch and phenylpropanoid biosynthesis, and phenylpropanoid biosynthesis pathways. The expression of calcium-dependent protein kinase (CDPK), β Ketoacyl-CoA Synthase1/10 (KCS1/10), and WRKY22/29 genes in the plant–pathogen interaction pathway significantly increased, indicating that they may be key genes in the CaWB phytoplasma-mediated maintenance of ROS homeostasis. Moreover, isochlorogenic acid B, atractylenolide II, and 3-methoxybenzoic acid were found, which might serve as signaling or functional substances in the defense response. Our results provide novel insights into the pathogenesis of CaWB and the defense response of <i>C. acuminata</i> under the influence of phytoplasma. Additionally, we identified potential candidate genes related to the defense response of <i>C. acuminata</i>, laying the foundation for further research.
first_indexed 2024-03-10T21:31:40Z
format Article
id doaj.art-c42cd497e2e0488e8f5fd46fc4a5ec5b
institution Directory Open Access Journal
issn 2077-0472
language English
last_indexed 2024-03-10T21:31:40Z
publishDate 2023-10-01
publisher MDPI AG
record_format Article
series Agriculture
spelling doaj.art-c42cd497e2e0488e8f5fd46fc4a5ec5b2023-11-19T15:18:57ZengMDPI AGAgriculture2077-04722023-10-011310194310.3390/agriculture13101943Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> DecneKai Qiao0Weiyi Huang1Xuemei Li2Jiahui Liang3Hong Cai4Phytopathology Laboratory of Yunnan Province, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaPhytopathology Laboratory of Yunnan Province, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaPhytopathology Laboratory of Yunnan Province, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaPhytopathology Laboratory of Yunnan Province, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaPhytopathology Laboratory of Yunnan Province, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, China<i>Camptotheca acuminata</i> Witches’-broom disease (CaWB) is the most destructive disease affecting <i>C. acuminata</i> in China. Previous studies on CaWB have failed to clarify the incidence pattern in <i>C. acuminata</i> after infection with phytoplasma. The time interval between phytoplasma infection of <i>C. acuminata</i> and the onset of Witches’-broom symptoms in <i>C. acuminata</i> was very long. <i>C. acuminata</i> inoculated with CaWB showed leaf margin scorching symptoms at 4 weeks in inoculated leaves. At 16 weeks after infection (WAI), old leaves were shed, while new leaves showed a mild leaf margin scorch; at 28 WAI, typical symptoms appeared. Transcriptomic and metabolomic analyses of the three sampling periods revealed 194 differentially expressed genes, mainly enriched in MAPK signaling, plant–pathogen interaction, phenylpropanoid biosynthesis, starch and phenylpropanoid biosynthesis, and phenylpropanoid biosynthesis pathways. The expression of calcium-dependent protein kinase (CDPK), β Ketoacyl-CoA Synthase1/10 (KCS1/10), and WRKY22/29 genes in the plant–pathogen interaction pathway significantly increased, indicating that they may be key genes in the CaWB phytoplasma-mediated maintenance of ROS homeostasis. Moreover, isochlorogenic acid B, atractylenolide II, and 3-methoxybenzoic acid were found, which might serve as signaling or functional substances in the defense response. Our results provide novel insights into the pathogenesis of CaWB and the defense response of <i>C. acuminata</i> under the influence of phytoplasma. Additionally, we identified potential candidate genes related to the defense response of <i>C. acuminata</i>, laying the foundation for further research.https://www.mdpi.com/2077-0472/13/10/1943transcriptomemetabolomephytoplasma<i>Camptotheca acuminata</i> Decnedefensive response
spellingShingle Kai Qiao
Weiyi Huang
Xuemei Li
Jiahui Liang
Hong Cai
Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> Decne
Agriculture
transcriptome
metabolome
phytoplasma
<i>Camptotheca acuminata</i> Decne
defensive response
title Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> Decne
title_full Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> Decne
title_fullStr Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> Decne
title_full_unstemmed Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> Decne
title_short Combined Transcriptomic and Metabolomic Analyses of Defense Mechanisms against Phytoplasma Infection in <i>Camptotheca acuminata</i> Decne
title_sort combined transcriptomic and metabolomic analyses of defense mechanisms against phytoplasma infection in i camptotheca acuminata i decne
topic transcriptome
metabolome
phytoplasma
<i>Camptotheca acuminata</i> Decne
defensive response
url https://www.mdpi.com/2077-0472/13/10/1943
work_keys_str_mv AT kaiqiao combinedtranscriptomicandmetabolomicanalysesofdefensemechanismsagainstphytoplasmainfectioninicamptothecaacuminataidecne
AT weiyihuang combinedtranscriptomicandmetabolomicanalysesofdefensemechanismsagainstphytoplasmainfectioninicamptothecaacuminataidecne
AT xuemeili combinedtranscriptomicandmetabolomicanalysesofdefensemechanismsagainstphytoplasmainfectioninicamptothecaacuminataidecne
AT jiahuiliang combinedtranscriptomicandmetabolomicanalysesofdefensemechanismsagainstphytoplasmainfectioninicamptothecaacuminataidecne
AT hongcai combinedtranscriptomicandmetabolomicanalysesofdefensemechanismsagainstphytoplasmainfectioninicamptothecaacuminataidecne