Type 2 Nep1-Like Proteins from the Biocontrol Oomycete Pythium oligandrum Suppress Phytophthora capsici Infection in Solanaceous Plants

Kun Yang; Xiaohua Dong; Jialu Li; Yi Wang; Yang Cheng; Ying Zhai; Xiaobo Li; Lihui Wei; Maofeng Jing; Daolong Dou

doi:10.3390/jof7070496

Type 2 Nep1-Like Proteins from the Biocontrol Oomycete Pythium oligandrum Suppress Phytophthora capsici Infection in Solanaceous Plants

J Fungi (Basel). 2021 Jun 22;7(7):496. doi: 10.3390/jof7070496.

Authors

Kun Yang¹, Xiaohua Dong¹, Jialu Li¹, Yi Wang¹, Yang Cheng¹, Ying Zhai², Xiaobo Li³, Lihui Wei⁴, Maofeng Jing¹, Daolong Dou¹

Affiliations

¹ The Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.
² Department of Plant Pathology, Washington State University, Pullman, WA 99164, USA.
³ Crops Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Crop Genetic Improvement, Guangdong, Guangzhou 510640, China.
⁴ Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China.

Abstract

As a non-pathogenic oomycete, the biocontrol agent Pythium oligandrum is able to control plant diseases through direct mycoparasite activity and boosting plant immune responses. Several P. oligandrum elicitors have been found to activate plant immunity as microbe-associated molecular patterns (MAMPs). Necrosis- and ethylene-inducing peptide 1 (Nep1)-like proteins (NLPs) are a group of MAMPs widely distributed in eukaryotic and prokaryotic plant pathogens. However, little is known about their distribution and functions in P. oligandrum and its sister species Pythium periplocum. Here, we identified a total of 25 NLPs from P. oligandrum (PyolNLPs) and P. periplocum (PypeNLPs). Meanwhile, we found that PyolNLPs/PypeNLPs genes cluster in two chromosomal segments, and our analysis suggests that they expand by duplication and share a common origin totally different from that of pathogenic oomycetes. Nine PyolNLPs/PypeNLPs induced necrosis in Nicotiana benthamiana by agroinfiltration. Eight partially purified PyolNLPs/PypeNLPs were tested for their potential biocontrol activity. PyolNLP5 and PyolNLP7 showed necrosis-inducing activity in N. benthamiana via direct protein infiltration. At sufficient concentrations, they both significantly reduced disease severity and suppressed the in planta growth of Phytophthora capsici in solanaceous plants including N. benthamiana (tobacco), Solanum lycopersicum (tomato) and Capsicum annuum (pepper). Our assays suggest that the Phytophthora suppression effect of PyolNLP5 and PyolNLP7 is irrelevant to reactive oxygen species (ROS) accumulation. Instead, they induce the expression of antimicrobial plant defensin genes, and the induction depends on their conserved nlp24-like peptide pattern. This work demonstrates the biocontrol role of two P. oligandrum NLPs for solanaceous plants, which uncovers a novel approach of utilizing NLPs to develop bioactive formulae for oomycete pathogen control with no ROS-caused injury to plants.

Keywords: Nep1-like proteins; Phytophthora capsici; Pythium oligandrum; oomycete resistance; solanaceous plants.

Abstract

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