The Fractionated Orthology of Bs2 and Rx/Gpa2 Supports Shared Synteny of Disease Resistance in the Solanaceae

Abstract

Comparative genomics provides a powerful tool for the identification of genes that encode traits shared between crop plants and model organisms. Pathogen resistance conferred by plant R genes of the nucleotide-binding-leucine-rich-repeat (NB-LRR) class is one such trait with great agricultural importance that occupies a critical position in understanding fundamental processes of pathogen detection and coevolution. The proposed rapid rearrangement of R genes in genome evolution would make comparative approaches tenuous. Here, we test the hypothesis that orthology is predictive of R-gene genomic location in the Solanaceae using the pepper R gene Bs2. Homologs of Bs2 were compared in terms of sequence and gene and protein architecture. Comparative mapping demonstrated that Bs2 shared macrosynteny with R genes that best fit criteria determined to be its orthologs. Analysis of the genomic sequence encompassing solanaceous R genes revealed the magnitude of transposon insertions and local duplications that resulted in the expansion of the Bs2 intron to 27 kb and the frequently detected duplications of the 59-end of R genes. However, these duplications did not impact protein expression or function in transient assays. Taken together, our results support a conservation of synteny for NB-LRR genes and further show that their distribution in the genome has been consistent with global rearrangements.

Isolation of an Rx homolog from C. annuum and the evolution of Rx genes in the Solanaceae family

“…This motif was present in all eight members of the B2 subgroup (the Rx-like genes), namely LaRGC from tomato; CapRGC from pepper, and Rx1, Rx2, Gpa2, RGC1 and two unigene sequences (SGN-U275797, SGN-U281895) with a disease resistance annotation in potato. However, this motif was not found in members of other groups in this study, even Bs2, which is considered to be an Rx homolog (Mazourek et al 2009). In this study, we also incorporated five representative Arabidopsis protein sequences into the motif analysis, and motif 14 was not found in these five sequences-not even RPP13, which is the Arabidopsis protein most closely related to Rx-like RGAs (data not shown).…”

Physical mapping of NBS-coding resistance genes to the Me-gene cluster on chromosome P9 reveals markers tightly linked to the N gene for root-knot nematode resistance in pepper

“…Physical mapping of CDS was problematic because most of the CDS (84 %) were positioned at both loci A and C. This may be due to evolutionary mechanisms such as recombination of the paralogous genes within the Me-gene cluster which caused in vivo DNA shuffling and duplications. Such rearrangements cause the dispersal of resistance genes (Song et al 2002;Mazourek et al 2009). Although it is known that R gene dispersal is associated with chromosome breakpoints, high-resolution comparative mapping studies between related genera need to be performed to estimate its effect on Me-gene cluster evolution (Ameline-Torregrosa et al 2008;Mazourek et al 2009).…”

“…Such rearrangements cause the dispersal of resistance genes (Song et al 2002;Mazourek et al 2009). Although it is known that R gene dispersal is associated with chromosome breakpoints, high-resolution comparative mapping studies between related genera need to be performed to estimate its effect on Me-gene cluster evolution (Ameline-Torregrosa et al 2008;Mazourek et al 2009). Precise location of the 2.12-Mb hotspots will be valuable information to develop markers for fine mapping resistance genes in the cluster.…”

“…To date, none of these resistance genes have been isolated; however, they were mapped to a 28 cM cluster on pepper chromosome 9 (Djian-Caporalino et al 2007;Fazari et al 2012;Uncu et al 2015). Comparative mapping studies showed that this cluster is syntenic to potato and tomato chromosome 12 which contains resistance genes such as Me(s), Bs2, Mi-3/Mi-5, Lv and Gpa2/Rx (Grube et al 2000;Mazourek et al 2009). Although the cluster was partially annotated in a study that identified the Bs2 gene conferring resistance to bacterial spot (Xanthomonas campestris pv.…”

A 1,681-locus consensus genetic map of cultivated cucumber including 67 NB-LRR resistance gene homolog and ten gene loci

“…In addition, nucleotide polymorphism analyses demonstrated extremely high level of inter- and intra-specific variations of NB-LRR genes, which presumably evolve rapidly in response to changes in pathogen populations [12,19]. Nevertheless, conservation of synteny for NB–LRR disease resistance genes among phylogenetically related species was also observed [20,21]. However, the extent of genome-wide conservation and synteny of NB-LRR RGHs between different species is not well documented.…”