The <i>Brassica napus</i> wall‐associated kinase‐like (WAKL) gene <i>Rlm9</i> provides race‐specific blackleg resistance

Larkan, Nicholas J.; Ma, Lisong; Haddadi, Parham; Buchwaldt, Miles; Parkin, Isobel A. P.; Djavaheri, Mohammad; Borhan, M. Hossein

doi:10.1111/tpj.14966

Cited by 63 publications

(49 citation statements)

References 52 publications

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“…CC-BY-NC-ND 4.0 International license perpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted December 17, 2020. ; https://doi.org/10.1101/2020.12.17.423041 doi: bioRxiv preprint cloned and found to encode a wall-associated kinase-like (WAKL) protein, a newly described class of Receptor-Like Kinase (RLK) R protein (Larkan et al, 2020). Using a yeast two-hybrid (Y2H) assay, no direct interaction between the extracellular region of Rlm9 and AvrLm5-9 could be detected.…”

Section: Discussionmentioning

confidence: 99%

“…Rlm9, Rlm4, Rlm7 and Rlm3 are located in the same genetic cluster and could possibly be allelic (Delourme et al, 2004). Rlm9 was recently cloned and found to encode a wall-associated kinase-like (WAKL) protein, a newly described class of Receptor-Like Kinase (RLK) R protein (Larkan et al, 2020). Using a yeast two-hybrid (Y2H) assay, no direct interaction between the extracellular region of Rlm9 and AvrLm5-9 could be detected.…”

Section: Discussionmentioning

confidence: 99%

“…However, a direct interaction between AvrLm5-9 and Rlm9 cannot be excluded since Y2H is not an optimal technique to test interaction with a membrane protein. Larkan et al [42] identified at the Rlm9 locus, in other resistant accessions of oilseed rape, three WALK genes that could potentially correspond to Rlm3, Rlm4 and Rlm7, suggesting they could be variants or duplications of the same WAKL locus. Based on the zig-zag model [6], we hypothesize that…”

Section: Discussionmentioning

confidence: 99%

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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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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: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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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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“…Congruently as cGMP is involved in plant responses to pathogens [ 53 , 54 , 55 ], transcript expression and functional genomic studies positively implicate WAKL10 in basal and R-gene mediated resistance [ 52 , 56 ]. Intriguingly, the guanylate cyclase activity of Rlm9 protein, a Brassica napus homolog of AtWAKL10, appears to be a key component of the hypersensitive response to infection caused by fungal pathogen Leptosphaeria maculans carrying the corresponding avirulence gene AvrLm5-9 [ 57 ]. In accordance with this notion, the wheat Stb6 protein lacks the guanylate cyclase in its kinase domain and fails to trigger a hypersensitive response [ 58 ].…”

Section: Moonlighting Kinasesmentioning

confidence: 99%

Moonlighting Proteins Shine New Light on Molecular Signaling Niches

Turek

Irving

2021

IJMS

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Plants as sessile organisms face daily environmental challenges and have developed highly nuanced signaling systems to enable suitable growth, development, defense, or stalling responses. Moonlighting proteins have multiple tasks and contribute to cellular signaling cascades where they produce additional variables adding to the complexity or fuzziness of biological systems. Here we examine roles of moonlighting kinases that also generate 3′,5′-cyclic guanosine monophosphate (cGMP) in plants. These proteins include receptor like kinases and lipid kinases. Their guanylate cyclase activity potentiates the development of localized cGMP-enriched nanodomains or niches surrounding the kinase and its interactome. These nanodomains contribute to allosteric regulation of kinase and other molecules in the immediate complex directly or indirectly modulating signal cascades. Effects include downregulation of kinase activity, modulation of other members of the protein complexes such as cyclic nucleotide gated channels and potential triggering of cGMP-dependent degradation cascades terminating signaling. The additional layers of information provided by the moonlighting kinases are discussed in terms of how they may be used to provide a layer of fuzziness to effectively modulate cellular signaling cascades.

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“…Researchers have suggested that the rotation of R genes could be an efficient strategy to control blackleg ( Marcroft et al, 2012 ), and the foundation of this is to validate the presence of R genes in plants and to specify them. So far, at least 18 R genes in Brassica species have been identified ( Zhang et al, 2016a ); however, only three of them, i.e., Rlm2 ( Larkan et al, 2015 ), LepR3 ( Larkan et al, 2013 ), and Rlm9 ( Larkan et al, 2020 ), were cloned. Rlm1 is a single dominant R gene ( Fu et al, 2019 ), and its interaction with corresponding avirulence gene AvrLm1 in L. maculans provided the first genetic evidence for the “gene-to-gene” interactions ( Ansan-Melayah et al, 1998 ).…”

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confidence: 99%

Detection of Blackleg Resistance Gene Rlm1 in Double-Low Rapeseed Accessions from Sichuan Province, by Kompetitive Allele-Specific PCR

et al. 2021

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Blackleg is a serious disease in Brassica plants, causing moderate to severe yield losses in rapeseed worldwide. Although China has not suffered from this disease yet (more aggressive Leptosphaeria maculans is not present yet), it is crucial to take provisions in breeding for disease resistance to have excellent blackleg-resistant cultivars already in the fields or in the breeding pipeline. The most efficient strategy for controlling this disease is breeding plants with identified resistance genes. We selected 135 rapeseed accessions in Sichuan, including 30 parental materials and 105 hybrids, and we determined their glucosinolate and erucic acid content and confirmed 17 double-low materials. A recently developed single-nucleotide polymorphism (SNP) marker, SNP_208, was used to genotype allelic Rlm1/rlm1 on chromosome A07, and 87 AvrLm1 -resistant materials. Combined with the above-mentioned seed quality data, we identified 11 AvrLm1 -resistant double-low rapeseed accessions, including nine parental materials and two hybrids. This study lays the foundation of specific R gene-oriented breeding, in the case that the aggressive Leptosphaeria maculans invades and establishes in China in the future and a robust and less labor consuming method to identify resistance in canola germplasm.

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The Brassica napus wall‐associated kinase‐like (WAKL) gene Rlm9 provides race‐specific blackleg resistance

Cited by 63 publications

References 52 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

Moonlighting Proteins Shine New Light on Molecular Signaling Niches

Detection of Blackleg Resistance Gene Rlm1 in Double-Low Rapeseed Accessions from Sichuan Province, by Kompetitive Allele-Specific PCR

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