Time-Course Transcriptome Profiling Reveals Differential Resistance Responses of Tomato to a Phytotoxic Effector of the Pathogenic Oomycete Phytophthora cactorum

Author:

Zhou Xue1,Wen Ke1,Huang Shen-Xin1,Lu Yi1,Liu Yang12,Jin Jing-Hao12,Kale Shiv D.3,Chen Xiao-Ren12ORCID

Affiliation:

1. College of Plant Protection, Yangzhou University, 48 Eastern Wenhui Road, Yangzhou 225009, China

2. Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University, 48 Eastern Wenhui Road, Yangzhou 225009, China

3. Fralin Life Science Institute, Virginia Tech, Blacksburg, VA 24060, USA

Abstract

Blight caused by Phytophthora pathogens has a devastating impact on crop production. Phytophthora species secrete an array of effectors, such as Phytophthora cactorum-Fragaria (PcF)/small cysteine-rich (SCR) phytotoxic proteins, to facilitate their infections. Understanding host responses to such proteins is essential to developing next-generation crop resistance. Our previous work identified a small, 8.1 kDa protein, SCR96, as an important virulence factor in Phytophthora cactorum. Host responses to SCR96 remain obscure. Here, we analyzed the effect of SCR96 on the resistance of tomato treated with this recombinant protein purified from yeast cells. A temporal transcriptome analysis of tomato leaves infiltrated with 500 nM SCR96 for 0, 3, 6, and 12 h was performed using RNA-Seq. In total, 36,779 genes, including 2704 novel ones, were detected, of which 32,640 (88.7%) were annotated. As a whole, 5929 non-redundant genes were found to be significantly co-upregulated in SCR96-treated leaves (3, 6, 12 h) compared to the control (0 h). The combination of annotation, enrichment, and clustering analyses showed significant changes in expression beginning at 3 h after treatment in genes associated with defense and metabolism pathways, as well as temporal transcriptional accumulation patterns. Noticeably, the expression levels of resistance-related genes encoding receptor-like kinases/proteins, resistance proteins, mitogen-activated protein kinases (MAPKs), transcription factors, pathogenesis-related proteins, and transport proteins were significantly affected by SCR96. Quantitative reverse transcription PCR (qRT-PCR) validated the transcript changes in the 12 selected genes. Our analysis provides novel information that can help delineate the molecular mechanism and components of plant responses to effectors, which will be useful for the development of resistant crops.

Funder

National Natural Science Foundation of China

Jiangsu Agriculture Science and Technology Innovation Fund

Foundation of Guangdong Provincial Key Laboratory of High Technology for Plant Protection

Open Project of Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China

College Students’ Innovation and Entrepreneurship Training Program of Yangzhou University

Yangzhou University 2016 Project for Excellent Young Key Teachers; and the High-Level Talent Support Program of Yangzhou University

Publisher

MDPI AG

Subject

Plant Science,Ecology,Ecology, Evolution, Behavior and Systematics

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