CsIVP functions in vasculature development and downy mildew resistance in cucumber

Shuangshuang Yan; Kang Ning; Zhongyi Wang; Xiaofeng Liu; Yanting Zhong; Lian Ding; Hailing Zi; Zhihua Cheng; Xuexian Li; Hongyan Shan; Qingyang Lv; Laixin Luo; Renyi Liu; Liying Yan; Zhaoyang Zhou; William John Lucas; Xiaolan Zhang

doi:10.1371/journal.pbio.3000671

CsIVP functions in vasculature development and downy mildew resistance in cucumber

PLoS Biol. 2020 Mar 23;18(3):e3000671. doi: 10.1371/journal.pbio.3000671. eCollection 2020 Mar.

Authors

Shuangshuang Yan^{1

2}, Kang Ning¹, Zhongyi Wang¹, Xiaofeng Liu¹, Yanting Zhong³, Lian Ding¹, Hailing Zi⁴, Zhihua Cheng¹, Xuexian Li³, Hongyan Shan⁵, Qingyang Lv⁶, Laixin Luo⁶, Renyi Liu⁷, Liying Yan⁸, Zhaoyang Zhou¹, William John Lucas⁹, Xiaolan Zhang¹

Affiliations

¹ State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China.
² Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (South China), Ministry of Agriculture and Rural Affairs, College of Horticulture, South China Agricultural University, Guangzhou, China.
³ Department of Plant Nutrition, the Key Laboratory of Plant-Soil Interactions, China Agricultural University, Beijing, China.
⁴ Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.
⁵ State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China.
⁶ Department of Plant Pathology, China Agricultural University, Beijing, China.
⁷ College of Horticulture, and FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China.
⁸ College of Horticulture Science and Technology, Hebei Normal University of Science & Technology, Qinhuangdao, China.
⁹ Department of Plant Biology, University of California, Davis, California, United States of America.

Abstract

Domesticated crops with high yield and quality are frequently susceptible to pathogen attack, whereas enhancement of disease resistance generally compromises crop yield. The underlying mechanisms of how plant development and disease resistance are coordinately programed remain elusive. Here, we showed that the basic Helix-Loop-Helix (bHLH) transcription factor Cucumis sativus Irregular Vasculature Patterning (CsIVP) was highly expressed in cucumber vascular tissues. Knockdown of CsIVP caused severe vasculature disorganization and abnormal organ morphogenesis. CsIVP directly binds to vascular-related regulators YABBY5 (CsYAB5), BREVIPEDICELLUS (CsBP), and AUXIN/INDOLEACETIC ACIDS4 (CsAUX4) and promotes their expression. Knockdown of CsYAB5 resulted in similar phenotypes as CsIVP-RNA interference (RNAi) plants, including disturbed vascular configuration and abnormal organ morphology. Meanwhile, CsIVP-RNAi plants were more resistant to downy mildew and accumulated more salicylic acid (SA). CsIVP physically interacts with NIM1-INTERACTING1 (CsNIMIN1), a negative regulator in the SA signaling pathway. Thus, CsIVP is a novel vasculature regulator functioning in CsYAB5-mediated organ morphogenesis and SA-mediated downy mildew resistance in cucumber.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Basic Helix-Loop-Helix Transcription Factors / genetics
Basic Helix-Loop-Helix Transcription Factors / metabolism*
Cucumis sativus / classification
Cucumis sativus / genetics
Cucumis sativus / growth & development*
Cucumis sativus / immunology*
Disease Resistance / genetics
Gene Expression
Gene Expression Regulation, Plant
Indoleacetic Acids / metabolism
Morphogenesis
Phylogeny
Plant Diseases / genetics
Plant Diseases / immunology
Plant Proteins / genetics
Plant Proteins / metabolism*
Plant Vascular Bundle / genetics
Plant Vascular Bundle / growth & development
Plants, Genetically Modified
Protein Binding
Salicylic Acid / metabolism
Signal Transduction / genetics

Substances

Basic Helix-Loop-Helix Transcription Factors
Indoleacetic Acids
Plant Proteins
Salicylic Acid

Grants and funding

This study was supported by the National Key Research and Development Program of China [2018YFD1000800], National Natural Science Foundation of China [31930097] and [31772315], 111 Project [B17043], the Construction of Beijing Science and Technology Innovation and Service Capacity in Top Subjects [CEFF-PXM2019_014207_000032] to XZ, the Project for Extramural Scientists of the State Key Laboratory of Agrobiotechnology [2020SKLAB6-22] to LY, and the Natural Science Foundation of Guangdong Province [2018A030313693] to SY. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.