Genes Encoding Recognition of theCladosporium fulvumEffector Protein Ecp5 Are Encoded at Several Loci in the Tomato Genome

Abstract

The molecular interactions between tomato and Cladosporium fulvum have been an important model for molecular plant pathology. Complex genetic loci on tomato chromosomes 1 and 6 harbor genes for resistance to Cladosporium fulvum, encoding receptor like-proteins that perceive distinct Cladosporium fulvum effectors and trigger plant defenses. Here, we report classical mapping strategies for loci in tomato accessions that respond to Cladosporium fulvum effector Ecp5, which is very sequence-monomorphic. We screened 139 wild tomato accessions for an Ecp5-induced hypersensitive response, and in five accessions, the Ecp5-induced hypersensitive response segregated as a monogenic trait, mapping to distinct loci in the tomato genome. We identified at least three loci on chromosomes 1, 7 and 12 that harbor distinct Cf-Ecp5 genes in four different accessions. Our mapping showed that the Cf-Ecp5 in Solanum pimpinellifolium G1.1161 is located at the Milky Way locus. The Cf-Ecp5 in Solanum pimpinellifolium LA0722 was mapped to the bottom arm of chromosome 7, while the Cf-Ecp5 genes in Solanum lycopersicum Ontario 7522 and Solanum pimpinellifolium LA2852 were mapped to the same locus on the top arm of chromosome 12. Bi-parental crosses between accessions carrying distinct Cf-Ecp5 genes revealed putative genetically unlinked suppressors of the Ecp5-induced hypersensitive response. Our mapping also showed that Cf-11 is located on chromosome 11, close to the Cf-3 locus. The Ecp5-induced hypersensitive response is widely distributed within tomato species and is variable in strength. This novel example of convergent evolution could be used for choosing different functional Cf-Ecp5 genes according to individual plant breeding needs.

Distinct Phyllosphere Microbiome of Wild Tomato Species in Central Peru upon Dysbiosis

“…Fungal core microbes were identified as Cladosporium , Filobasidium , Symmetrospora , and Erythrobasidium hasegawianum . The fungal genus Cladosporium includes commonly leaf mold pathogens (renamed to Passalora fulva ) found epiphytic and endophytic on tomato and other host species [ 49 , 89 ]. Multiple resistance genes have been described in wild tomatoes against Cladosporium fulvum .…”

Fulvia fulva [syn. Cladosporium fulvum, Passalora fulva] races in Argentina are evolving through genetic changes and carry polymorphic avr and ecp gene sequences

“…4 Alignment of the predicted Ecp5 protein sequence from strains CIDEFI 300 and CIDEFI 301 with the reference Ecp5 protein sequence, EF104527 (115 aa) elucidated (Stergiopoulos et al 2010). However, these proteins play an essential role in infection and colonization, since their deletion results in less virulent C. fulvum mutants (De Wit et al 2009a;De Wit et al 2012;Iakovidis et al 2020). Stergiopoulos et al (2007) stated that the frequency of loss of these genes within fungal populations is low, which might explain their presence in Argentinian isolates as well as their key role in pathogenesis.…”

“…Regarding the ECP5 protein, it has six cysteine residues and is the least polymorphic C. fulvum effector (Stergiopoulos et al 2007;De Wit et al 2009b). Iakovidis et al (2020) found that genes encoding ECPs that inducing an HR segregated as a monogenic trait, mapping to distinct loci in the tomato genome and identified at least three loci within chromosomes that might harbour distinct Cf-ecp5 genes. Based on an analysis of nucleotide and amino acid sequences, we can infer that the predicted change of Cys by Tyr as well as the premature stop codons that produce truncated ECP5 products and the frameshifts that change Nterminal or C-terminal regions might harm fitness of C. fulvum, to infect and colonize the apoplastic space.…”

“…A total of fourteen Ecps have been shown to trigger HR in wild species of tomato (Solanum spp.). These were Ecp1, Ecp2-1, Ecp4, Ecp5, Ecp6, Ecp8, Ecp9-1, Ecp10-1, Ecp11-1, Ecp12, Ecp13, Ecp14-1, Ecp15 and Ecp16 that carry the cognate Cf-ecp genes (Laugé et al 1998;Laugé et al 2000;Van der Hoorn et al 2001;Kruijt et al 2005;Thomma et al 2011;Mesarich et al 2018;Iakovidis et al 2020;Kahlon et al 2020). Recently, Iakovidis et al (2020) described the genes encoding recognition of the C. fulvum Ecp5 that are encoded by several loci within the genome of tomato.…”

Beyond the genomes of Fulvia fulva (syn. Cladosporium fulvum) and Dothistroma septosporum: New insights into how these fungal pathogens interact with their host plants

“…As broad‐spectrum resistance against leaf mould disease, to our knowledge, remains elusive in commercial tomato varieties, the last decade has seen significant efforts made in the mapping, identification, and characterization of additional Cf immune receptor genes (Chai et al, 2020 ; Iakovidis et al, 2020 ; Jiang et al, 2022 ; Liu et al, 2018 , 2019 , 2022 ; Xu et al, 2018 ; Xue et al, 2017 ; Zhang et al, 2020 ; Zhao et al, 2015 , 2016 , 2019 ). For example, the Cf ‐3 and Cf ‐11 immune receptor genes, which correspond to the yet‐unidentified CfAvr3 and CfAvr11 Avr genes of F. fulva , have recently been mapped to a narrow region on chromosome 11 and have been shown to be closely linked (Iakovidis et al, 2020 ). Interestingly, the target region seems to be devoid of genes encoding RLPs, which suggests that Cf ‐3 and Cf ‐11 mediate resistance using a different class of immune receptors.…”