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Conserved Opposite Functions in Plant Resistance to Biotrophic and Necrotrophic Pathogens of the Immune Regulator SRFR1.

ABSTRACT: Plant immunity is mediated in large part by specific interactions between a host resistance protein and a pathogen effector protein, named effector-triggered immunity (ETI). ETI needs to be tightly controlled both positively and negatively to enable normal plant growth because constitutively activated defense responses are detrimental to the host. In previous work, we reported that mutations in SUPPRESSOR OF rps4-RLD1 (SRFR1), identified in a suppressor screen, reactivated EDS1-dependent ETI to Pseudomonas syringae pv. tomato (Pto) DC3000. Besides, mutations in SRFR1 boosted defense responses to the generalist chewing insect Spodoptera exigua and the sugar beet cyst nematode Heterodera schachtii. Here, we show that mutations in SRFR1 enhance susceptibility to the fungal necrotrophs Fusarium oxysporum f. sp. lycopersici (FOL) and Botrytis cinerea in Arabidopsis. To translate knowledge obtained in AtSRFR1 research to crops, we generated SlSRFR1 alleles in tomato using a CRISPR/Cas9 system. Interestingly, slsrfr1 mutants increased expression of SA-pathway defense genes and enhanced resistance to Pto DC3000. In contrast, slsrfr1 mutants elevated susceptibility to FOL. Together, these data suggest that SRFR1 is functionally conserved in both Arabidopsis and tomato and functions antagonistically as a negative regulator to (hemi-) biotrophic pathogens and a positive regulator to necrotrophic pathogens.

SUBMITTER: Son GH

PROVIDER: S-EPMC8233967 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Conserved Opposite Functions in Plant Resistance to Biotrophic and Necrotrophic Pathogens of the Immune Regulator SRFR1.

Son Geon Hui GH Moon Jiyun J Shelake Rahul Mahadev RM Vuong Uyen Thi UT Ingle Robert A RA Gassmann Walter W Kim Jae-Yean JY Kim Sang Hee SH

International journal of molecular sciences 20210615 12

Plant immunity is mediated in large part by specific interactions between a host resistance protein and a pathogen effector protein, named effector-triggered immunity (ETI). ETI needs to be tightly controlled both positively and negatively to enable normal plant growth because constitutively activated defense responses are detrimental to the host. In previous work, we reported that mutations in <i>SUPPRESSOR OF rps4-RLD1</i> (<i>SRFR1</i>), identified in a suppressor screen, reactivated EDS1-dep ...[more]

PMID: 34204013

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Project description:Autophagy is critical for plant defense against necrotrophic pathogens, which causes serious yield loss on crops. However, the post-translational regulatory mechanisms of autophagy pathway in plant resistance against necrotrophs remain poorly understood. In this study, we report that phosphorylation modification on ATG18a, a key regulator of autophagosome formation in Arabidopsis thaliana, constitutes a post-translation regulation of autophagy, which attenuates plant resistance against necrotrophic pathogens. We found that phosphorylation of ATG18a suppresses autophagosome formation and its subsequent delivery into the vacuole, which results in reduced autophagy activity and compromised plant resistance against Botrytis cinerea. In contrast, overexpression of ATG18a dephosphorylation-mimic form increases the accumulation of autophagosomes and complements the plant resistance of atg18a mutant against B. cinerea. Moreover, BAK1, a key regulator in plant resistance, was identified to physically interact with and phosphorylate ATG18a. Mutation of BAK1 blocks ATG18a phosphorylation at four of the five detected phosphorylation sites after B. cinerea infection and strongly activates autophagy, leading to enhanced resistance against B. cinerea. Collectively, the identification of functional phosphorylation sites on ATG18a and the corresponding kinase BAK1 unveiled how plant regulates autophagy during resistance against necrotrophic pathogens.Abbreviations: 35s: the cauliflower mosaic virus 35s promoter; A. thaliana: Arabidopsis thaliana; A. brassicicola: Alternaria brassicicola; ABA: abscisic acid; ATG: autophagy-related; ATG18a: autophagy-related protein 18a in A. thaliana; ATG8a: autophagy-related protein 8a in A. thaliana; ATG8-PE: ATG8 conjugated with PE; B. cinerea: Botrytis cinerea; BAK1: Brassinosteroid insensitive 1-associated receptor kinase1 in A. thaliana; BiFC: biomolecular fluorescence complementation; BIK1: Botrytis-insensitive kinase 1 in A. thaliana; BKK1: BAK1-like 1 in A. thaliana; BR: brassinosteroid; Co-IP: coimmunoprecipitation; dai: days after inoculation; DAMPs: damage-associated molecular patterns; E. coli: Escherochia coli; ER: endoplasmic reticulum; ETI: effector-triggered immunity; GFP: green fluorescent protein; HA: hemagglutinin; IP: immunoprecipitation; LC-MS/MS: liquid chromatography-tandem mass spectrometry; LCI: luciferase complementation imaging; MPK3: mitogen-activated protein kinase 3 in A. thaliana; MPK4: mitogen-activated protein kinase 4 in A. thaliana; MPK6: mitogen-activated protein kinase 6 in A. thaliana; N. benthamiana: Nicotiana benthamiana; NES: nuclear export sequence; PAMP: pathogen-associated molecular pattern; PCR: polymerase chain reaction; PE: phosphatidylethanolamine; PRR: pattern recognition receptor; PtdIns(3,5)P2: phosphatidylinositol (3,5)-biphosphate; PtdIns3P: phosphatidylinositol 3-biphosphate; PTI: PAMP-triggered immunity; qRT-PCR: quantitative reverse transcription PCR; SnRK2.6: SNF1-related protein kinase 2.6 in A. thaliana; TORC1: the rapamycin-sensitive Tor complex1; TRAF: tumor necrosis factor receptor-associated factor; WT: wild type plant; Yc: C-terminal fragment of YFP; YFP: yellow fluorescent protein; Yn: N-terminal fragment of YFP.

Project description:Fungi are an exceptional source of diverse and novel cytochrome P450 monooxygenases (P450s), heme-thiolate proteins, with catalytic versatility. Agaricomycotina saprophytes have yielded most of the available information on basidiomycete P450s. This resulted in observing similar P450 family types in basidiomycetes with few differences in P450 families among Agaricomycotina saprophytes. The present study demonstrated the presence of unique P450 family patterns in basidiomycete biotrophic plant pathogens that could possibly have originated from the adaptation of these species to different ecological niches (host influence). Systematic analysis of P450s in basidiomycete biotrophic plant pathogens belonging to three different orders, Agaricomycotina (Armillaria mellea), Pucciniomycotina (Melampsora laricis-populina, M. lini, Mixia osmundae and Puccinia graminis) and Ustilaginomycotina (Ustilago maydis, Sporisorium reilianum and Tilletiaria anomala), revealed the presence of numerous putative P450s ranging from 267 (A. mellea) to 14 (M. osmundae). Analysis of P450 families revealed the presence of 41 new P450 families and 27 new P450 subfamilies in these biotrophic plant pathogens. Order-level comparison of P450 families between biotrophic plant pathogens revealed the presence of unique P450 family patterns in these organisms, possibly reflecting the characteristics of their order. Further comparison of P450 families with basidiomycete non-pathogens confirmed that biotrophic plant pathogens harbour the unique P450 families in their genomes. The CYP63, CYP5037, CYP5136, CYP5137 and CYP5341 P450 families were expanded in A. mellea when compared to other Agaricomycotina saprophytes and the CYP5221 and CYP5233 P450 families in P. graminis and M. laricis-populina. The present study revealed that expansion of these P450 families is due to paralogous evolution of member P450s. The presence of unique P450 families in these organisms serves as evidence of how a host/ecological niche can influence shaping the P450 content of an organism. The present study initiates our understanding of P450 family patterns in basidiomycete biotrophic plant pathogens.

Dataset Information

Conserved Opposite Functions in Plant Resistance to Biotrophic and Necrotrophic Pathogens of the Immune Regulator SRFR1.

Publications

Conserved Opposite Functions in Plant Resistance to Biotrophic and Necrotrophic Pathogens of the Immune Regulator SRFR1.

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