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Comparative Transcriptomic and Metabolomic Profiling of Grapevine Leaves (cv. Kyoho) upon Infestation of Grasshopper and Botrytis cinerea

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Abstract

Grapes (Vitis sp.) are susceptible to infection by grasshopper and fungus that lead to damaging productivity and economic losses. In this study, we infected the young and old leaf of grapevine by Acrida chinensis and Botrytis cinerea and combined the metabolomic and transcriptomic analysis to comprehend the infection-mediated molecular and metabolic responses. Results indicated that the metabolic reprogramming of lipid, proline, and carbohydrate metabolism is necessary for the biosynthesis of specialized metabolites, which are involved in grapevine defense response. Moreover, the resistance mechanisms of grapevine induced by grasshopper and Botrytis required the hormones crosstalk of abscisic acid (ABA), salicylic acid (SA), ethylene (ETH), brassinosteroid (BR), and jasmonic acid (JA). We also identified the different genes involved in resistance to pathogen and insect attack in transcriptional levels, which encoded pathogenesis-related proteins (PRs), disease resistance proteins (RPS), calcium-binding proteins (CMLs), WRKY transcription factor, abscisic acid-insensitive (ABI), brassinosteroid insensitive 1 (BAK1), ethylene-responsive transcription factor (ERF), leucine-rich repeat receptor-like protein kinases (LRRs), zinc finger protein (ZAT10), chitinase 5, and E3 ubiquitin-protein ligase PUB23 in infected leaves. Furthermore, we nominated various infection-related metabolic biomarkers, including glutathione, proline, aspartyl-L-proline, adenine, histidine, and arginine, that has major effects on the tolerance of leaf-damaging insects and pathogens. Taken together, our research results clarify that there are differences in the defense mechanisms of old leaves and young leaves that lead to different biological stress tolerance and provide deeper insights into grapevine regulatory network mediating defense response against infection caused by grasshopper and B. cinerea, and uncover the resistance mechanisms for functional genomic studies.

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Availability of Data and Materials

The data sets supporting the conclusions of this article are included in this article and in its additional files.

Abbreviations

ABA:

Abscisic acid

ABI:

Abscisic acid-insensitive

BAK1:

Brassinosteroid insensitive 1

BR:

Brassnisteroid

CMLs:

Calcium-binding proteins

DEGs:

Differentially expressed genes

ELISA:

Enzyme-linked immunosorbent assay

ERF:

Ethylene-responsive transcription factor

ETH:

Ethylene

ETI:

Effector triggered immunity

F3M:

Flavonoid 3-monooxygenase

FAO:

Food and Agriculture Organization

FPKM:

Fragments per kilobase of transcript per million mapped reads

GO:

Gene ontology

HAMPs:

Herbivory- and pathogen- or microbial-associated

JA:

Jasmonic acid

KEGG:

Kyoto Encyclopedia of Genes and Genomes

LCMS:

Liquid chromatography-mass spectrometry

LPO:

Peroxidation

LRRs:

Leucine-rich repeat receptor-like protein kinases

MDA:

Malondialdehyde

OCN:

Old leaf control

ODT:

Old leaf affected by pathogen

OIT:

Old leaf infected by insect

PCA:

Principal component analysis

PRRs:

Pattern recognition receptors

PRs:

Pathogenesis-related proteins

PTI:

PAMP-triggered immunity

qRT-PCR:

Quantitative real-time PCR

RPS:

Disease resistance proteins

SA:

Salicylic acid

SOD:

Superoxide dismutase

TF:

Transcription factor

YCN:

Young leaf control

YDT:

Young leaf affected by pathogen

YIT:

Young leaf infected by insect

ZAT10:

Zinc finger protein

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Acknowledgements

This work was supported by the funding of the National Natural Science Foundation of China (31872938, 31672131, 31872047) and the Foundation for Distinguished Young Talents in Jiangsu (BK20180076). We are grateful to Ms. Shaoyao Lin and Ms. Ruiping Tian for helping us collect data.

Funding

the funding of National Natural Science Foundation of China,31872938,Haifeng Jia,31672131,Haifeng Jia,31872047,Haifeng Jia,Foundation for distinguished Young Talents in Jiangsu,BK20180076,Haifeng Jia

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Authors and Affiliations

  1. Key Laboratory of Genetics and Fruit Development, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Haoran Jia, Teng Li, Muhammad Salman Haider, Ehsan Sadeghnezhad, Qianqian Pang, Jian Han, Peian Zhang, Lingyun Su, Haifeng Jia & Jinggui Fang

  2. NJAU (Suqian) Academy of Protected Horticultures, Suqian, China

    Haoran Jia, Teng Li & Haifeng Jia

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  1. Haoran Jia
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  2. Teng Li
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  3. Muhammad Salman Haider
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Contributions

JHR conducted sample treatment, data analysis, and drafted the manuscript. LT and MS helped with data analysis. ES, PQQ, and HJ helped to draft the manuscript. ZPA and SLY participated in the design of the study. ES, JHF, and FJG designed and coordinated this study and revised the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Haifeng Jia.

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Key Message

• Transcriptome and metabolome analysis of old and young grape leaves revealed the regulatory network of the resistance to grasshopper and Botrytis cinerea.

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Jia, H., Li, T., Haider, M.S. et al. Comparative Transcriptomic and Metabolomic Profiling of Grapevine Leaves (cv. Kyoho) upon Infestation of Grasshopper and Botrytis cinerea. Plant Mol Biol Rep 40, 539–555 (2022). https://doi.org/10.1007/s11105-022-01336-8

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  • DOI: https://doi.org/10.1007/s11105-022-01336-8

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