Structural Analysis of an Avr4 Effector Ortholog Offers Insight into Chitin Binding and Recognition by the Cf-4 Receptor

Kohler, Amanda C.; Chen, Li-Hung; Hurlburt, Nicholas K.; Salvucci, Anthony E.; Schwessinger, Benjamin; Fisher, A.J.; Stergiopoulos, Ioannis

doi:10.1105/tpc.15.00893

Cited by 38 publications

(71 citation statements)

References 67 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…In support of this possibility, the Cf-4 immune receptor has been shown to recognize homologs of Avr4 from D. septosporum, P. fijiensis, and Pseudocercospora fuligena (black leaf mold disease of tomato) Kohler et al 2016;Stergiopoulos et al 2010), while the CfEcp2-1 immune receptor has been shown to recognize homologs of Ecp2-1 from D. septosporum and P. fijiensis Stergiopoulos et al 2010). It must be pointed out, however, that the Cf-4 immune receptor does not recognize homologs of Avr4 from Cercospora apii, Cercospora beticola, and Cercospora nicotianae (leaf spot disease of celery, beet, and tobacco, respectively) Stergiopoulos et al 2010).…”

Section: Discussionmentioning

confidence: 98%

Specific Hypersensitive Response–Associated Recognition of New Apoplastic Effectors from Cladosporium fulvum in Wild Tomato

Mesarich

Ökmen

Rövenich

et al. 2018

MPMI

View full text Add to dashboard Cite

Tomato leaf mold disease is caused by the biotrophic fungus Cladosporium fulvum. During infection, C. fulvum produces extracellular small secreted protein (SSP) effectors that function to promote colonization of the leaf apoplast. Resistance to the disease is governed by Cf immune receptor genes that encode receptor-like proteins (RLPs). These RLPs recognize specific SSP effectors to initiate a hypersensitive response (HR) that renders the pathogen avirulent. C. fulvum strains capable of overcoming one or more of all cloned Cf genes have now emerged. To combat these strains, new Cf genes are required. An effectoromics approach was employed to identify wild tomato accessions carrying new Cf genes. Proteomics and transcriptome sequencing were first used to identify 70 apoplastic in planta-induced C. fulvum SSPs. Based on sequence homology, 61 of these SSPs were novel or lacked known functional domains. Seven, however, had predicted structural homology to antimicrobial proteins, suggesting a possible role in mediating antagonistic microbe-microbe interactions in planta. Wild tomato accessions were then screened for HR-associated recognition of 41 SSPs, using the Potato virus X-based transient expression system. Nine SSPs were recognized by one or more accessions, suggesting that these plants carry new Cf genes available for incorporation into cultivated tomato.Leaf mold disease of tomato (Solanum lycopersicum) is caused by the biotrophic Dothideomycete fungal pathogen Cladosporium fulvum (syn. Passalora fulva and Fulvia fulva) (Thomma et al. 2005). The fungus likely originated in South America, the center of origin for tomato (Jenkins 1948), with Nucleotide sequence data is available in the GenBank database under the following accession numbers: Ecp6, KX943112; Ecp7, KX943113; Ecp8, KX943038; Ecp9-1, KX943041; Ecp9-2, KX943114; Ecp9-3, KX943115; Ecp9-4, KX943116; Ecp9-5, KX943117; Ecp9-6, KX943118; Ecp9-7, KX943119; Ecp9-8, KX943120; Ecp9-9, KX943081; Ecp10-1, KX943046; Ecp10-2, KX943063; Ecp10-3, KX943121; Ecp11-1, KX943050; Ecp12, KX943058; Ecp13, KX943065; Ecp14-1, KX943087; Ecp14-2, KX943122; Ecp15, KX943091; Ecp16, KX943080; Ecp17, KX943051; Ecp18, KX943035; Ecp19-1, KX943036; Ecp19-2, KX943048; Ecp20-1, KX943037; Ecp20-2, KX943057; Ecp20-3, KX943096; Ecp21-1, KX943039; Ecp22, KX943040; Ecp23, KX943044; Ecp24-1, KX943045; Ecp24-2, KX943094; Ecp25, KX943047; Ecp26, KX943052; Ecp27, KX943054; Ecp28-1, KX943056; Ecp28-2, KX943088; Ecp28-3, KX943090; Ecp29, KX943103; Ecp30, KX943076; Ecp31, KX943059; Ecp32-1, KX943062; Ecp32-2, KX943101; Ecp33, KX943066; Ecp34, KX943067; Ecp35, KX943068; Ecp36-1, KX943069; Ecp37, KX943072; Ecp38, KX943073; Ecp39, KX943074; Ecp40, KX943079; Ecp41, KX943082; Ecp42, KX943083; Ecp43-1, KX943089; Ecp44, KX943092; Ecp45, KX943093; Ecp46, KX943095; Ecp47, KX943097; Ecp48, KX943098; Ecp49-1, KX943099; Ecp50-1, KX943100; Ecp51, KX943102; Ecp52, KX943104; Ecp53-1, KX943105; Ecp54-1, KX943107; Ecp55, KX943108; Ecp56, KX943110; Ecp57-1,

show abstract

Section: Discussionmentioning

confidence: 98%

Specific Hypersensitive Response–Associated Recognition of New Apoplastic Effectors from Cladosporium fulvum in Wild Tomato

Mesarich

Ökmen

Rövenich

et al. 2018

MPMI

View full text Add to dashboard Cite

show abstract

“…Recent studies showed that hybridization and introgression enabling pathogens to expand their host ranges is more common than previously thought (Lemaire et al, 2015;Depotter et al, 2016;Menardo et al, 2016). In comparison to a large number of evolutionarily young effectors, relatively few effectors are conserved across fungal taxa (Kohler et al, 2016;Franceschetti et al, 2017). Coevolution between hosts and pathogens led to the diversification of specific fungal effectors across pathogen lineages (Jiang et al, 2008;Huang et al, 2014;Sperschneider et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

The emergence of the multi‐species NIP1 effector in Rhynchosporium was accompanied by high rates of gene duplications and losses

Mohd‐Assaad

McDonald

Croll

2019

Environmental Microbiology

View full text Add to dashboard Cite

Summary Plant pathogens secrete effector proteins to manipulate the host and facilitate infection. Cognate hosts trigger strong defence responses upon detection of these effectors. Consequently, pathogens and hosts undergo rapid coevolutionary arms races driven by adaptive evolution of effectors and receptors. Because of their high rate of turnover, most effectors are thought to be species‐specific and the evolutionary trajectories are poorly understood. Here, we investigate the necrosis‐inducing protein 1 (NIP1) effector in the multihost pathogen genus Rhynchosporium. We retraced the evolutionary history of the NIP1 locus using whole‐genome assemblies of 146 strains covering four closely related species. NIP1 orthologues were present in all species but the locus consistently segregated presence–absence polymorphisms suggesting long‐term balancing selection. We also identified previously unknown paralogues of NIP1 that were shared among multiple species and showed substantial copy‐number variation within R. commune. The NIP1A paralogue was under significant positive selection suggesting that NIP1A is the dominant effector variant coevolving with host immune receptors. Consistent with this prediction, we found that copy number variation at NIP1A had a stronger effect on virulence than NIP1B. Our analyses unravelled the origins and diversification mechanisms of a pathogen effector family shedding light on how pathogens gain adaptive genetic variation.

show abstract

“…The finding that most new HR-eliciting Ecps have homologs in other plant-pathogenic fungal species raises the possibility of cross-species resistance. In support of this possibility, the Cf-4 immune receptor has been shown to recognize homologs of Avr4 from D. septosporum , P. fijiensis and Pseudocercospora fuligena (black leaf mould disease of tomato) (de Wit et al, 2012; Kohler et al, 2016; Stergiopoulos et al, 2010), while the Cf-Ecp2-1 immune receptor has been shown to recognize homologs of Ecp2-1 from D. septosporum and P. fijiensis (de Wit et al, 2012; Stergiopoulos et al, 2012). It must be pointed out, however, that the Cf-4 immune receptor does not recognize homologs of Avr4 from Cercospora apii , Cercospora beticola and Cercospora nicotianae (leaf spot disease of celery, beet and tobacco, respectively) (Mesarich et al, 2016; Stergiopoulos et al, 2012).…”

Section: Discussionmentioning

confidence: 97%

Specific hypersensitive response-associated recognition of new apoplastic effectors fromCladosporium fulvumin wild tomato

Mesarich

Ökmen

Rövenich

et al. 2017

Preprint

View full text Add to dashboard Cite

Structural Analysis of an Avr4 Effector Ortholog Offers Insight into Chitin Binding and Recognition by the Cf-4 Receptor

Cited by 38 publications

References 67 publications

Specific Hypersensitive Response–Associated Recognition of New Apoplastic Effectors from Cladosporium fulvum in Wild Tomato

Specific Hypersensitive Response–Associated Recognition of New Apoplastic Effectors from Cladosporium fulvum in Wild Tomato

The emergence of the multi‐species NIP1 effector in Rhynchosporium was accompanied by high rates of gene duplications and losses

Specific hypersensitive response-associated recognition of new apoplastic effectors fromCladosporium fulvumin wild tomato

Contact Info

Product

Resources

About