The Tomato Interspecific NB-LRR Gene Arsenal and Its Impact on Breeding Strategies

Abstract

Tomato (Solanum lycopersicum L.) is a model system for studying the molecular basis of resistance in plants. The investigation of evolutionary dynamics of tomato resistance (R)-loci provides unique opportunities for identifying factors that promote or constrain genome evolution. Nucleotide-binding domain and leucine-rich repeat (NB-LRR) receptors belong to one of the most plastic and diversified families. The vast amount of genomic data available for Solanaceae and wild tomato relatives provides unprecedented insights into the patterns and mechanisms of evolution of NB-LRR genes. Comparative analysis remarked a reshuffling of R-islands on chromosomes and a high degree of adaptive diversification in key R-loci induced by species-specific pathogen pressure. Unveiling NB-LRR natural variation in tomato and in other Solanaceae species offers the opportunity to effectively exploit genetic diversity in genomic-driven breeding programs with the aim of identifying and introducing new resistances in tomato cultivars. Within this motivating context, we reviewed the repertoire of NB-LRR genes available for tomato improvement with a special focus on signatures of adaptive processes. This issue is still relevant and not thoroughly investigated. We believe that the discovery of mechanisms involved in the generation of a gene with new resistance functions will bring great benefits to future breeding strategies.

Domestication Shapes Recombination Patterns in Tomato

“…In detecting association, we included the 2-kb regions flanking both sides of the genes. First, we compared hotspots against R genes, which are known to reside in recombination hotspots ( Nieri et al 2017 ; Andolfo et al 2021 ), and observed a significant overlap (Fisher’s exact test; P = 3.38×10 −17 ). Afterward, we computed the overlap between hotspots and the selective sweeps or regions with reduced nucleotide diversity previously reported by Lin et al (2014) .…”

Large-scale gene gains and losses molded the NLR defense arsenal during the Cucurbita evolution

“…On average, a slightly higher number of CNLs compared to TNLs was identified in most Cucurbita assemblies. A similar CNL\TNL ratio was found in Solanaceae (Di Donato et al 2017;Andolfo et al 2021), while the Brassicaceae and Fabaceae contain from twofold to sixfold more TNL than CNL genes (Guo et al 2011;Kang et al 2012). Surprisingly, the Cucurbita RNL (also known as helper) genes varied from ~ 18 to ~ 6% of the full NLR gene complement (Suppl.…”

Genome-wide identification, characterization, and comparative analysis of NLR resistance genes in Coffea spp

“…Our results showed that of the 17 reference NLRs that have been cloned and characterized in species of the genus Solanum and that were also used in this study, 8 of them are present in shared orthogroups with coffee (Supplementary Table 2 and Supplementary Table 8), being 1 TNL ( Gro1-4 ) and 7 CNL ( Hero, Prf, Rpi-blb1, Rx2, Sw-5, Tm-2a, Tm-2 ). These genes have been found to be involved in resistance to a diverse group of pathogens including viruses, oomycetes, bacteria and nematodes (Bendahmane et al, 2000; Van Der Vossen et al, 2003; Paal et al, 2004; Andolfo et al, 2021). In total, 46 orthogroups were shared between coffee and solanum indicating that these orthologs were probably present before the speciation of these two groups.…”

“…In all three coffee species, a set of orphan genes and orthogroups that share NLRs within the same species were detected. In tomato, 45 of ~320 NLRs sequences are more similar to each other than to any other sequences compared (Andolfo et al, 2021) and orthogroups that share NLRs within the same species of Solanum are attributed to duplication events that generate different gene repertoires and result in species-specific subfamilies (Seo et al, 2016).…”

“…In these clusters it is possible to find tandem gene duplications, recombination hotspots or active transposon elements functioning as a reservoir of genetic variation to generate specificity for new pathogen variants (Michelmore and Meyers, 1998;Zhang et al, 2014). Within plant genomes many R genes have been found to reside in clusters (Jupe et al, 2012;Andolfo et al, 2014Andolfo et al, , 2021Seo et al, 2016;Zheng et al, 2016;Read et al, 2020). The S H 3 locus in coffee, for example, corresponds to a complex cluster of multiple genes, including CNL-like NLR genes (Ribas et al, 2011;Cenci et al, 2012).…”