Building a cluster of NLR genes conferring resistance to pests and pathogens: the story of the Vat gene cluster in cucurbits

Abstract

Most molecularly characterized plant resistance genes (R genes) belong to the nucleotide-binding-site-leucine-rich-repeat (NLR) receptor family and are prone to duplication and transposition with high sequence diversity. In this family, the Vat gene in melon is one of the few R genes known for conferring resistance to insect, i.e., Aphis gossypii, but it has been misassembled and/or mispredicted in the whole genomes of Cucurbits. We examined 14 genomic regions (about 400 kb) derived from long-read assemblies spanning Vat-related genes in Cucumis melo, Cucumis sativus, Citrullus lanatus, Benincasa hispida, Cucurbita argyrosperma, and Momordica charantia. We built the phylogeny of those genes. Investigating the paleohistory of the Vat gene cluster, we revealed a step by step process beginning from a common ancestry in cucurbits older than 50 my. We highlighted Vat exclusively in the Cucumis genera, which diverged about 20 my ago. We then focused on melon, evaluating a minimum duplication rate of Vat in 80 wild and cultivated melon lines using generalist primers; our results suggested that duplication started before melon domestication. The phylogeny of 44 Vat-CDS obtained from 21 melon lines revealed gain and loss of leucine-rich-repeat domains along diversification. Altogether, we revealed the high putative recognition scale offered in melon based on a combination of SNPs, number of leucine-rich-repeat domains within each homolog and number of homologs within each cluster that might jointly confer resistance to a large pest and pathogen spectrum. Based on our findings, we propose possible avenues for breeding programs.

Deciphering the Genetic Architecture of Plant Virus Resistance by GWAS, State of the Art and Potential Advances

“…On the contrary, the most significant ePAV was directly located in ZmTrxh, highlighting a more accurate mapping. Structural variant studies would be especially relevant for R genes since CNV of these genes are very common, e.g., in the Vat cluster in melon [90]. K-mers are contiguous small pieces of genomic sequences extracted from ILLUMINA sequences that could be used to reveal InDels [91] and should be considered in future GWAS focused on plant-virus resistance.…”

“…Virus resistance genes can be clustered in the plant genome, e.g., the Vat gene in melon [90], and unfortunately, LMMs are not able to distinguish colocalizing QTLs. Multiloci LMM (MLMM) and multi-loci random LMM (MRLMM) are designed to overcome this issue [112,113].…”

Comparative transcriptomics and genomic analyses reveal differential gene expression related to Colletotrichum brevisporum resistance in papaya (Carica papaya L.)

“…In plants, gene clusters play an important role in the synthesis of secondary metabolites and response to disease infection (Darma et al, 2019;Jeon et al, 2020), and resistance genes are also often present as gene clusters. Several studies have reported that resistance gene clusters function in resistance to pathogen infection (Barragan and Weigel, 2021;Chovelon et al, 2021). Anthracnose is a serious disease affecting plant growth and development.…”

E(gg)xit strategy of plant defense : Evolution and genetics of a butterfly egg-triggered cell death

“…This can complicate fine-mapping in absence of the exact genome assembly of the plant material being studied. Complex NLR loci formed by different tandem repeated genes are increasingly being resolved using long-read sequencing technologies (Read et al 2020, Chovelon et al 2021, Wang et al 2021a. Similar approaches will be certainly crucial to disentangle the genomic structure of the PEK locus.…”

“…Resolving the genomic structure of the PEK locus will be a fundamental step to enable further genetic and evolutionary studies. First, it will facilitate to pinpoint the causal variation through fine-mapping similarly to what it has been done on other NLR-containing loci (Read et al 2020, Chovelon et al 2021, Wang et al 2021a, Athiyannan et al 2022 benthamiana which are used as model to study the ability of PRRs and NLRs to induce HR (Wu et al 2017, Shangguan et al 2018. Finally, a correct assembly will make possible accurate genotyping of the locus that is required for population genetics studies aimed at characterizing the locus diversity in an ecological context (Stam et al 2016, Kourelis et al 2020.…”