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

As a non-pathogenic oomycete, the biocontrol agent <i>Pythium oligandrum</i> is able to control plant diseases through direct mycoparasite activity and boosting plant immune responses. Several <i>P. oligandrum</i> elicitors have been found to activate plant immunity as microb...

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Main Authors: Kun Yang, Xiaohua Dong, Jialu Li, Yi Wang, Yang Cheng, Ying Zhai, Xiaobo Li, Lihui Wei, Maofeng Jing, Daolong Dou
Format: Article
Language:English
Published: MDPI AG 2021-06-01
Series:Journal of Fungi
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Online Access:https://www.mdpi.com/2309-608X/7/7/496
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author Kun Yang
Xiaohua Dong
Jialu Li
Yi Wang
Yang Cheng
Ying Zhai
Xiaobo Li
Lihui Wei
Maofeng Jing
Daolong Dou
author_facet Kun Yang
Xiaohua Dong
Jialu Li
Yi Wang
Yang Cheng
Ying Zhai
Xiaobo Li
Lihui Wei
Maofeng Jing
Daolong Dou
author_sort Kun Yang
collection DOAJ
description As a non-pathogenic oomycete, the biocontrol agent <i>Pythium oligandrum</i> is able to control plant diseases through direct mycoparasite activity and boosting plant immune responses. Several <i>P. oligandrum</i> 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 <i>P. oligandrum</i> and its sister species <i>Pythium periplocum</i>. Here, we identified a total of 25 NLPs from <i>P. oligandrum</i> (PyolNLPs) and <i>P. periplocum</i> (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 <i>Nicotiana</i> <i>benthamiana</i> by agroinfiltration. Eight partially purified PyolNLPs/PypeNLPs were tested for their potential biocontrol activity. PyolNLP5 and PyolNLP7 showed necrosis-inducing activity in <i>N. benthamiana</i> via direct protein infiltration. At sufficient concentrations, they both significantly reduced disease severity and suppressed the in planta growth of <i>Phytophthora capsici</i> in solanaceous plants including <i>N. benthamiana</i> (tobacco), <i>Solanum lycopersicum</i> (tomato) and <i>Capsicum annuum</i> (pepper). Our assays suggest that the <i>Phytophthora</i> 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 <i>P. oligandrum</i> 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.
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spelling doaj.art-e4e9be424d4b422f842e0548f51897b02023-11-22T01:14:57ZengMDPI AGJournal of Fungi2309-608X2021-06-017749610.3390/jof7070496Type 2 Nep1-Like Proteins from the Biocontrol Oomycete <i>Pythium oligandrum</i> Suppress <i>Phytophthora capsici </i>Infection in Solanaceous PlantsKun Yang0Xiaohua Dong1Jialu Li2Yi Wang3Yang Cheng4Ying Zhai5Xiaobo Li6Lihui Wei7Maofeng Jing8Daolong Dou9The Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, ChinaThe Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, ChinaThe Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, ChinaThe Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, ChinaThe Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, Washington State University, Pullman, WA 99164, USACrops Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Crop Genetic Improvement, Guangdong, Guangzhou 510640, ChinaInstitute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, ChinaThe Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, ChinaThe Key Laboratory of Plant Immunity, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, ChinaAs a non-pathogenic oomycete, the biocontrol agent <i>Pythium oligandrum</i> is able to control plant diseases through direct mycoparasite activity and boosting plant immune responses. Several <i>P. oligandrum</i> 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 <i>P. oligandrum</i> and its sister species <i>Pythium periplocum</i>. Here, we identified a total of 25 NLPs from <i>P. oligandrum</i> (PyolNLPs) and <i>P. periplocum</i> (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 <i>Nicotiana</i> <i>benthamiana</i> by agroinfiltration. Eight partially purified PyolNLPs/PypeNLPs were tested for their potential biocontrol activity. PyolNLP5 and PyolNLP7 showed necrosis-inducing activity in <i>N. benthamiana</i> via direct protein infiltration. At sufficient concentrations, they both significantly reduced disease severity and suppressed the in planta growth of <i>Phytophthora capsici</i> in solanaceous plants including <i>N. benthamiana</i> (tobacco), <i>Solanum lycopersicum</i> (tomato) and <i>Capsicum annuum</i> (pepper). Our assays suggest that the <i>Phytophthora</i> 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 <i>P. oligandrum</i> 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.https://www.mdpi.com/2309-608X/7/7/496Nep1-like proteins<i>Pythium oligandrum</i><i>Phytophthora capsici</i>solanaceous plantsoomycete resistance
spellingShingle Kun Yang
Xiaohua Dong
Jialu Li
Yi Wang
Yang Cheng
Ying Zhai
Xiaobo Li
Lihui Wei
Maofeng Jing
Daolong Dou
Type 2 Nep1-Like Proteins from the Biocontrol Oomycete <i>Pythium oligandrum</i> Suppress <i>Phytophthora capsici </i>Infection in Solanaceous Plants
Journal of Fungi
Nep1-like proteins
<i>Pythium oligandrum</i>
<i>Phytophthora capsici</i>
solanaceous plants
oomycete resistance
title Type 2 Nep1-Like Proteins from the Biocontrol Oomycete <i>Pythium oligandrum</i> Suppress <i>Phytophthora capsici </i>Infection in Solanaceous Plants
title_full Type 2 Nep1-Like Proteins from the Biocontrol Oomycete <i>Pythium oligandrum</i> Suppress <i>Phytophthora capsici </i>Infection in Solanaceous Plants
title_fullStr Type 2 Nep1-Like Proteins from the Biocontrol Oomycete <i>Pythium oligandrum</i> Suppress <i>Phytophthora capsici </i>Infection in Solanaceous Plants
title_full_unstemmed Type 2 Nep1-Like Proteins from the Biocontrol Oomycete <i>Pythium oligandrum</i> Suppress <i>Phytophthora capsici </i>Infection in Solanaceous Plants
title_short Type 2 Nep1-Like Proteins from the Biocontrol Oomycete <i>Pythium oligandrum</i> Suppress <i>Phytophthora capsici </i>Infection in Solanaceous Plants
title_sort type 2 nep1 like proteins from the biocontrol oomycete i pythium oligandrum i suppress i phytophthora capsici i infection in solanaceous plants
topic Nep1-like proteins
<i>Pythium oligandrum</i>
<i>Phytophthora capsici</i>
solanaceous plants
oomycete resistance
url https://www.mdpi.com/2309-608X/7/7/496
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