A draft genome assembly for the heterozygous wild tomato Solanum habrochaites highlights haplotypic structural variations of intracellular immune receptors

Abstract

Solanum habrochaites LA1353 is a self-incompatible, highly heterozygous wild tomato that is a useful germplasm resource for the study of metabolism, reproduction and disease resistance. We generated a draft genome assembly with PacBio HiFi reads and genome annotations, which underscored the expansion of gene families associated with metabolite-production, self-incompatibility, DNA regulation and immunity. After manually curating intracellular nucleotide-binding leucine-rich repeat immune receptors (NLRs), we found that S. habrochaites LA1353 has a larger NLR inventory than other wild tomato species. A great number of heterozygous local copy number variations (CNVs) driven by haplotypic structural variations further expands the inventory, both enhancing NLR diversity and providing more opportunities for sequence evolution. The NLRs associated with local CNVs predominantly appear in the helper NLR (NRC)-related phylogenetic clades and are concentrated in a few physical NLR gene clusters. Synteny analysis points out that these genomic regions correspond to the known NLR clusters from which experimentally validated, functional NLRs, such as Hero, Mi-1.2 and Rpi-amr1, have been identified. Producing and incorporating Resistance Gene Enrichment Sequencing (RenSeq) data across wild tomato species, we reveal that the regions with local CNVs might have been shaped nearly equally by recent NLR gains and losses, along with enhanced sequence diversification that diminishes one-to-one orthology between heterozygous alleles. Our analysis suggests that these genomic regions may have accelerated evolutionary dynamics for NLR diversity generation in S. habrochaites LA1353.

Patterns of presence-absence variation of NLRs across populations ofSolanum chilenseare clade-dependent and mainly shaped by past demographic history

“…The new reference genome of S. chilense and refined annotation of coding regions allowed us to identify 278 NLRs, of which 170 are full length with NB-ARC domain, in line with previous reports of NLR numbers in wild tomatoes (204 to 265 across six self-compatible wild tomato species and the self-incompatible S. habrochaites 11,44 ). By sequencing this set of NLRs across 186 plants from 20 populations to study PAV at these loci , we reveal that only few NLRs clades exhibit PAV across geographic locations.…”

“…The new reference genome of S. chilense and refined annotation of coding regions allows us to identify 278 NLRs, of which 170 are full length with NB-ARC domain. Previous reports in wild tomatoes range between 204 and 265 across six self-compatible wild tomato species and the self-incompatible S. habrochaites (Seong et al, 2020(Seong et al, , 2022. We annotate about 18% more sensor NLRs than previously (Table S1).…”

Host resistance mechanisms and fungal infection strategies in the Botrytis cinerea-tomato interaction

“…The currently available assembly (NCBI accession GCA_000577655.1) has ~43,000 contigs and is not annotated. The recent availability of an annotated (partially manually curated) assembly from a different S. habrochaites accession may serve as a good starting point (Seong et al, 2022). Annotating the genome of LYC4 might help to define candidate resistance genes that are located within the QTL regions as was done for other wild tomato relatives.…”