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.
Highlights
Oomycetes are a large and diverse group of Stramenopiles, which display fungallike morphology
A unique “GHxFAYYFxKDQ” motif occurs in the N-terminal regions of PyolNLPs/PypeNLPs, whereas pathogenic Pythium novel type (NLP) contain an “AIMYSWYFPKDSP” motif typically found in other type 1 and type 2 NLPs [38] (Figure 2A)
We further examined transcript accumulation changes of key plant defense responses upon P. capsici infection, including Cyp71D20 and PTI5 as involved in PTI [43] (Supplementary Figure S4A), Enhanced disease susceptibility 1 (EDS1) and protein 1 (PR1) involved in salicylic acid signaling pathway [44] (Supplementary Figure S4B, Figure 6E), and Ethylene Insensitive 3 (EIN3), plant defensin 1.2 (PDF1.2), LOX, PR2, PR3 and PR4 involved in jasmonic acid and ethylene signaling pathways [45] (Supplementary Figure S4C, Figure 6E,F)
Summary
Oomycetes are a large and diverse group of Stramenopiles, which display fungallike morphology. Most oomycetes are devastating pathogens of plants or animals [1,2,3]. Oomycete disease incidence and severity have increased significantly in recent decades and caused substantial losses in agriculture throughout the world [4]. P. oligandrum colonizes the root ecosystem of diverse plants to induce defense responses [6]. It produces antimicrobial compounds, competes for nutrients and space with pathogens, and promotes plant growth via producing the auxin precursor tryptamine [6,9,10]. P. oligandrum has been successfully used in agriculture for plant disease control [6,11,12]
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