A new avirulence gene of Leptosphaeria maculans, AvrLm14, identifies a resistance source in American broccoli (Brassica oleracea) genotypes

Degrave, Alexandre; Wagner, Marine; George, Pierre; Coudard, Laurent; Pinochet, Xavier; Ermel, Magali; Gay, Elise; Fudal, Isabelle; Moreno-Rico, Onésimo; Rouxel, Thierry; Balesdent, Marie‐Hélène

doi:10.1111/mpp.13131

Cited by 23 publications

(19 citation statements)

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“…L. maculans can be controlled by combining qualitative and quantitative resistance of the host plant [12]. To date, ten AVR genes (called AvrLm ) recognized by the products of R genes (called Rlm ) from Brassica napus or other Brassica species have been identified [13–17] and share common characteristics: they encode small secreted proteins with no or low homologies in sequence databases, are located in repeat-rich regions of the genome, and are specifically expressed during the early stages of leaf infection. Among them, AvrLm4-7 suppresses Rlm3-mediated resistance triggered by AvrLm3 and Rlm9-mediated resistance triggered by AvrLm5-9 [9,14].…”

Section: Introductionmentioning

confidence: 99%

A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

Lazar

Mesarich

Petit

et al. 2020

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Recognition of a pathogen avirulence (AVR) effector protein by a cognate plant resistance (R) protein triggers a set of immune responses that render the plant resistant. Pathogens can escape this so-called Effector-Triggered Immunity (ETI) by different mechanisms including the deletion or loss-of-function mutation of the AVR gene, the incorporation of point mutations that allow recognition to be evaded while maintaining virulence function, and the acquisition of new effectors that suppress AVR recognition. The Dothideomycete Leptosphaeria maculans, causal agent of oilseed rape stem canker, is one of the few fungal pathogens where suppression of ETI by an AVR effector has been demonstrated. Indeed, AvrLm4-7 suppresses the recognition of AvrLm3 and AvrLm5-9 by the R proteins Rlm3 and Rlm9, respectively. The presence of AvrLm4-7 does not impede AvrLm3 and AvrLm5-9 expression, and the three AVR proteins do not appear to physically interact. To decipher the epistatic interaction between these L. maculans AVR effectors, we determined the crystal structure of AvrLm5-9 and obtained a 3D model of AvrLm3, based on the crystal structure of Ecp11-1, a homologous avirulence effector candidate from Fulvia fulva. Despite a lack of sequence similarity, AvrLm5-9 and AvrLm3 are structural analogues of AvrLm4-7 (structure previously characterized). Structure-informed sequence database searches identified a larger number of putative structural analogues among L. maculans effector candidates, including the avirulence effector AvrLmS-Lep2, all produced during the early stages of oilseed rape infection, as well as among effector candidates from other phytopathogenic fungi. These structural analogues were called LARS (for Leptosphaeria AviRulence-Suppressing) effectors. Remarkably, transformants of L. maculans expressing one of these structural analogues, Ecp11-1, triggered Rlm3-mediated immunity. Furthermore, this recognition could be suppressed by AvrLm4-7. These results suggest that Ecp11-1 has the same function as AvrLm3, or that the Ecp11-1 structure is sufficiently close to that of AvrLm3 to be recognized by Rlm3.Author summaryAn efficient strategy to control fungal diseases in the field is genetic control using resistant crop cultivars. Crop resistance mainly relies on gene-for-gene relationships between plant resistance (R) genes and pathogen avirulence (AVR) genes, as defined by Flor in the 1940s. However, gene-for-gene relationships diversify to increased complexity in the course of plant-pathogen co-evolution. Resistance against the plant-pathogenic fungus Leptosphaeria maculans by Brassica napus and other Brassica species relies on recognition of effector (AVR) proteins by R proteins; however, L. maculans is able to produce an effector that suppresses a subset of these specific recognitions. Using a protein structure approach, we revealed structural analogy between different effectors within L. maculans and other plant-pathogenic species in the Dothideomycetes and Sordariomycetes classes, defining a new family of effectors called LARS, and providing a clue to the mechanisms behind recognition suppression. Cross-species expression of one LARS effector from Fulvia fulva, a pathogen of tomato, in L. maculans triggers recognition by an oilseed rape resistant cultivar. These results highlight the need to integrate knowledge on effector structures to improve resistance management and to develop broad-spectrum resistances for multi-pathogen control of diseases.

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Section: Introductionmentioning

confidence: 99%

A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

Lazar

Mesarich

Petit

et al. 2020

Preprint

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“…Map-based cloning of the first AvrLm genes (AvrLm1, AvrLm6, and AvrLm4-7; Fudal et al, 2007;Gout et al, 2006;Parlange et al, 2009) took many years due to the lack of a L. maculans genome sequence and their location in repeat-rich, gene-poor regions of the genome (Rouxel et al, 2011). The availability of a reference genome and a repertoire of effector genes facilitated rapid identification of several further AVR genes, including AvrLm11, AvrLm2, AvrLm5-9, and AvrLm14 (Balesdent et al, 2013;Degrave et al, 2021;Ghanbarnia et al, 2015Ghanbarnia et al, , 2018.…”

Section: Introductionmentioning

confidence: 99%

“…To date, 18 R genes to L. maculans have been described, with only three cloned to date: LepR3, Rlm2 , and Rlm9 (Delourme et al, 2004, 2006; Larkan et al, 2013, 2015, 2020; Long et al, 2011; Rimmer, 2006; Van de Wouw et al, 2009; Yu et al, 2005, 2008). Meanwhile, nine L. maculans avirulence genes have already been cloned: AvrLm1, AvrLm2, AvrLm3, AvrLm4‐7, AvrLm5‐9, AvrLm6, AvrLm10, AvrLm11 , and AvrLm14 (Balesdent et al, 2013; Degrave et al, 2021; Fudal et al, 2007; Ghanbarnia et al, 2015, 2018; Gout et al, 2006; Parlange et al, 2009; Petit‐Houdenot et al, 2019; Plissonneau et al, 2016; Van de Wouw et al, 2014). Map‐based cloning of the first AvrLm genes ( AvrLm1 , AvrLm6 , and AvrLm4‐7 ; Fudal et al, 2007; Gout et al, 2006; Parlange et al, 2009) took many years due to the lack of a L. maculans genome sequence and their location in repeat‐rich, gene‐poor regions of the genome (Rouxel et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Two independent approaches converge to the cloning of a new Leptosphaeria maculans avirulence effector gene, AvrLmS‐Lep2

Neik

Ghanbarnia

Ollivier

et al. 2022

Molecular Plant Pathology

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Brassica napus (oilseed rape, canola) seedling resistance to Leptosphaeria maculans, the causal agent of blackleg (stem canker) disease, follows a gene-for-gene relationship.The avirulence genes AvrLmS and AvrLep2 were described to be perceived by the resistance genes RlmS and LepR2, respectively, present in B. napus 'Surpass 400'. Here we report cloning of AvrLmS and AvrLep2 using two independent methods. AvrLmS was cloned using combined in vitro crossing between avirulent and virulent isolates with sequencing of DNA bulks from avirulent or virulent progeny (bulked segregant sequencing). AvrLep2 was cloned using a biparental cross of avirulent and virulent L. maculans isolates and a classical map-based cloning approach. Taking these two approaches independently, we found that AvrLmS and AvrLep2 are the same gene.Complementation of virulent isolates with this gene confirmed its role in inducing resistance on Surpass 400, Topas-LepR2, and an RlmS-line. The gene, renamed AvrLmS-Lep2, encodes a small cysteine-rich protein of unknown function with an N-terminal secretory signal peptide, which is a common feature of the majority of effectors from extracellular fungal plant pathogens. The AvrLmS-Lep2/LepR2 interaction phenotype was found to vary from a typical hypersensitive response through intermediate resistance sometimes towards susceptibility, depending on the inoculation conditions.AvrLmS-Lep2 was nevertheless sufficient to significantly slow the systemic growth of the pathogen and reduce the stem lesion size on plant genotypes with LepR2, indicating the potential efficiency of this resistance to control the disease in the field.

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“…One of these waves, Wave2, includes effector genes expressed during the asymptomatic stages of leaf, petiole and stem colonization ('biotrophy'-effectors). These include the twelve AVR genes which have been identified so far in L. maculans, referred to hereafter as AvrLm genes (Balesdent et al, 2002;Gout et al, 2006;Fudal et al, 2007;Parlange et al, 2009;Balesdent et al, 2013;Ghanbarnia et al, 2015;Plissonneau et al, 2016;Ghanbarnia et al, 2018;Petit-Houdenot et al, 2019;Neik et al, 2020;Degrave et al, 2021). The genes in this wave display a peak of expression at 7 days post inoculation (DPI) on cotyledons, and are also strongly expressed during petiole and then stem colonization, being switched on and off multiple times during plant colonization (Gay et al 2021).…”

Section: Introductionmentioning

confidence: 99%

The neighboring genes AvrLm10A and AvrLm10B are part of a large multigene family of cooperating effector genes conserved in Dothideomycetes and Sordariomycetes

Talbi

Fokkens

Audran

et al. 2022

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With only a few exceptions, fungal effectors (small secreted proteins) have long been considered as species- or even isolate-specific. With the increasing availability of high-quality fungal genomes and annotations, trans-species or trans-genera families of effectors are being uncovered. Two avirulence effectors, AvrLm10A and AvrLm10B, of Leptosphaeria maculans, the fungus responsible for stem canker of oilseed rape, are members of such a large family of effectors. AvrLm10A and AvrLm10B are neighboring genes, organized in divergent transcriptional orientation. Sequence searches within the L. maculans genome show that AvrLm10A/AvrLm10B belong to a multigene family comprising five pairs of genes with a similar tail-to-tail organization. The two genes in a pair always had the same expression pattern and two expression profiles were distinguished, associated with the biotrophic colonization of cotyledons and / or petioles and stems. Of the two protein pairs further investigated Lmb_jn3_08094/Lmb_jn3_08095 and Lmb_jn3_09745 / Lmb_jn3_09746, one (Lmb_jn3_09745 / Lmb_jn3_09746) had the ability to physically interact, similarly to what was previously described for the AvrLm10A/AvrLm10B pair. AvrLm10A homologues are present in more than 30 Dothideomycete and Sordariomycete plant-pathogenic fungi whereas fewer AvrLm10B homologues were identified. One of the AvrLm10A homologues, SIX5, is an effector from Fusarium oxysporum f.sp. lycopersici physically interacting with the avirulence effector Avr2. We found that AvrLm10A homologues were associated with at least eight distinct putative effector families, suggesting an ability of AvrLm10A/SIX5 to cooperate with diverse effectors. These results point to a general role of the AvrLm10A/SIX5 protein as a ‘cooperator protein’, able to interact with diverse families of effectors whose encoding gene is co-regulated with the neighboring AvrLm10A homologue.

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A new avirulence gene of Leptosphaeria maculans, AvrLm14, identifies a resistance source in American broccoli (Brassica oleracea) genotypes

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri butio n-NonCo mmerc ial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Cited by 23 publications

References 53 publications

A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

Two independent approaches converge to the cloning of a new Leptosphaeria maculans avirulence effector gene, AvrLmS‐Lep2

The neighboring genes AvrLm10A and AvrLm10B are part of a large multigene family of cooperating effector genes conserved in Dothideomycetes and Sordariomycetes

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