Residual heterozygosity and epistatic interactions underlie the complex genetic architecture of yield in diploid potato

Authors: MARAND, ALEXANDRE - University Of Wisconsin; Jansky, Shelley; GAGE, JOSEPH - University Of Wisconsin; Hamernik, Andy; DE LEON, NATALIA - University Of Wisconsin; JIANG, JIMING - Michigan State University

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2019
Publication Date: 3/18/2019
Citation: Marand, A.P., Jansky, S.H., Gage, J.L., Hamernik, A.J., de Leon, N., Jiang, J. 2019. Residual heterozygosity and epistatic interactions underlie the complex genetic architecture of yield in diploid potato. Genetics. 212(1):317-332. https://doi.org/10.1534/genetics.119.302036.
DOI: https://doi.org/10.1534/genetics.119.302036

Interpretive Summary: Although yield is the most important trait for potato breeders, the genes that influence yield are not known. In this study, 1.5 million genetic markers were evaluated in a diploid population comprised of 90 clones segregating for tuber number, average tuber weight, and total tuber yield. Several of these clones produced yields equivalent to tetraploid cultivars. Genetic analysis revealed 14 genomic locations associated with yield variability. Interactions among these genomic regions were important in determining yield traits. Several candidate genes for yield were identified. This is a significant paper, as it documents high yield in diploid potato, in a rigorous four-year data set. Genetic analysis also revealed that tuber number and tuber size are independent traits, so breeders can make progress for both yield components simultaneously. Finally, the identification of QTL for high yield provides the first opportunity for breeders to select for yield. All of these findings are critical to improve genetic gains from selection in potato breeding programs.

Technical Abstract: Deconvolution of the genetic and transcriptional architecture underlying yield is critical for understanding bases of genetic gain in species of agronomic importance. To dissect the genetic components of yield in potato, we developed a reference-based haplotype bin map composed of four segregating alleles from a pseudo-testcross F1 potato population. Approximately 1.5 million short nucleotide variants were utilized during map construction, resulting in unprecedented resolution for an F1 population; estimated by a median bin length of 146-kb, and roughly 11 genes per bin. Regression models uncovered 14 quantitative trait loci (QTLs) underpinning yield and its components, average tuber weight and tubers produced per plant, that collectively result in a striking 332% average mid-parent value heterosis. Nearly 80% of yield-associated QTLs were epistatic, with each QTL interval containing between 0 and 44 annotated genes. We found that approximately half of epistatic QTLs overlap regions of residual heterozygosity identified in the inbred parental parent. Remarkably, genomic regions recalcitrant to inbreeding were associated with elevated gene density, genes under selection, floral tissue-specificity, and constitutive genes expressed predominantly in tuber and stolon tissues. Dissection of the genome-wide additive and dominance values for yield and its components indicated a widespread prevalence of dominance contributions in this population, enriched at QTLs and regions of residual heterozygosity. Finally, the effects of short nucleotide variants and patterns of gene expression were determined for all genes underlying yield-associated QTLs, exposing several promising candidate genes that we speculate may influence yield in potato.