Evolution and selection of Rhg1, a copy‐number variant nematode‐resistance locus

Abstract

The soybean cyst nematode (SCN) resistance locus Rhg1 is a tandem repeat of a 31.2 kb unit of the soybean genome. Each 31.2-kb unit contains four genes. One allele of Rhg1, Rhg1-b, is responsible for protecting most US soybean production from SCN. Whole-genome sequencing was performed, and PCR assays were developed to investigate allelic variation in sequence and copy number of the Rhg1 locus across a population of soybean germplasm accessions. Four distinct sequences of the 31.2-kb repeat unit were identified, and some Rhg1 alleles carry up to three different types of repeat unit. The total number of copies of the repeat varies from 1 to 10 per haploid genome. Both copy number and sequence of the repeat correlate with the resistance phenotype, and the Rhg1 locus shows strong signatures of selection. Significant linkage disequilibrium in the genome outside the boundaries of the repeat allowed the Rhg1 genotype to be inferred using high-density single nucleotide polymorphism genotyping of 15 996 accessions. Over 860 germplasm accessions were found likely to possess Rhg1 alleles. The regions surrounding the repeat show indications of non-neutral evolution and high genetic variability in populations from different geographic locations, but without evidence of fixation of the resistant genotype. A compelling explanation of these results is that balancing selection is in operation at Rhg1.

Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1

“…Up-regulation of the proportion of alternatively spliced α-SNAP Rhg1 LC transcript could provide a bypass that reduces disruptive α-SNAP production and promotes balance with regard to wild-type α-SNAPs. Other areas for future work are suggested by the positive correlation between the strength of SCN resistance and copy number of high-copy (α-SNAP Rhg1 HCencoding) Rhg1 repeats (9,21,47,48). Improved SCN resistance may be obtained if haplotypes can be identified or generated that carry more Rhg1 copies than the current mainstay 10-copy haplotype.…”

“…Most soybeans are susceptible to SCN, and their single-copy Rhg1 locus α-SNAP matches this consensus, but the SCN resistance-conferring highcopy or low-copy Rhg1 loci encode multiple copies of α-SNAPs that diverge at these sites and an upstream residue (Fig. 1A) (9,21). Because electrostatic contacts between the NSF N domain and the acidic residues at the α-SNAP C terminus are reported in animal systems (12) and α-SNAP Rhg1 LC, respectively, and the SCN-susceptible Williams 82 wild-type α-SNAP (α-SNAP Rhg1 WT).…”

“…Two distinct classes of resistanceencoding Rhg1 haplotypes have been identified: low-copy (three copies or fewer) and high-copy (more than four copies); the lowand high-copy Rhg1 haplotypes each encode distinct polymorphic α-SNAPs (Fig. 1A) (9,21). No amino acid polymorphisms are predicted in the Glyma.18G022400 or Glyma.18G022700 products from SCN-susceptible as opposed to SCN-resistant Rhg1 haplotypes, but Rhg1 copy-number expansion constitutively elevates the transcript levels of these genes in SCN-resistant plants (9).…”

The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode

“…This segment also includes partial gene sequences for Glyma18g02570 and Glyma18g02610 . Direct repeats (2–10) are present in SCN-resistant soybean lines, whereas only one copy is present in SCN-susceptible soybean lines789. Using the Glyma18g02590 gene sequences, two specific KASP (kompetitive allele-specific PCR) single-nucleotide polymorphism (SNP) markers were developed to select the rhg1 resistance alleles and the assay can be used to differentiate Peking-type and PI 88788-type resistance10.…”

Systematic Mutagenesis of Serine Hydroxymethyltransferase Reveals an Essential Role in Nematode Resistance

“…Thus, the high copy number of the repeat and the concerted action of these genes are the basis of resistance to SCN in PI 88788-type resistance. In sources with Peking-type resistance, only two to four copies of this repeat region are present (Cook et al, 2014;Lee et al, 2015). Furthermore, the a-SNAP gene (GmSNAP18) in the rhg1-a repeat of soybean cv Forrest (resistance from Peking) is sufficient for SCN resistance .…”