Nonadditive gene expression is correlated with nonadditive phenotypic expression in interspecific triploid hybrids of willow (Salix spp.)

Authors: Carlson, Craig; CHOI, YONGWOOK - Translational Genomics Research Institute; CHAN, AGNES - Translational Genomics Research Institute; TOWN, CHRISTOPHER - J Craig Venter Institute; SMART, LAWRENCE - Cornell University

Submitted to: G3, Genes/Genomes/Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/10/2021
Publication Date: 12/21/2021
Citation: Carlson, C.H., Choi, Y., Chan, A.P., Town, C.D., Smart, L. 2021. Nonadditive gene expression is correlated with nonadditive phenotypic expression in interspecific triploid hybrids of willow (Salix spp.). G3, Genes/Genomes/Genetics. https://doi.org/10.1093/g3journal/jkab436.
DOI: https://doi.org/10.1093/g3journal/jkab436

Interpretive Summary: Many studies have highlighted the complex basis where the hybrid outperforms both inbred parents (hybrid vigor). Despite the lack of a consensus, it is vital that we turn our attention to understanding this phenomena in more diverse crops, such as fast-growing, bioenergy willow. A consistent result in willow is the occurrence of hybrid vigor in crosses between different parent species and genome sizes. The genetic basis for this is unknown. Here, we examined how and why gene expression is different in the hybrid compared to its parents, and if those genes are responsible for hybrid vigor. Answers to these questions would help breeders better predict successful crosses. In diverse willow crosses, we found that genes in the hybrid that are expressed the same as one parent, but not the other, were most prominent, and importantly, genes that were differently expressed between parents were most indicative of hybrid vigor. This information not only facilitates a novel approach to plant breeding but further builds upon our understanding of the genetic basis of hybrid vigor.

Technical Abstract: Shrub willow is a dedicated energy crop bred to be fast-growing and high yielding on marginal land without competing with food crops. A trend in willow breeding is the consistent pattern of heterosis in triploids produced from crosses between diploid and tetraploid species. Here, we test whether differentially expressed genes are associated with heterosis in triploid families derived from diploid Salix purpurea, diploid Salix viminalis, and tetraploid Salix miyabeana parents. Three biological replicates of shoot tips from all family progeny and parents were collected after 12 weeks in the greenhouse and RNA extracted for RNA-Seq analysis. This study provides evidence that nonadditive patterns of gene expression are correlated with nonadditive phenotypic expression in interspecific triploid hybrids of willow. Expression-level dominance was most correlated with heterosis for biomass yield traits and was highly enriched for processes involved in starch and sucrose metabolism. In addition, there was a global dosage effect of parent alleles in triploid hybrids, with expression proportional to copy number variation. Importantly, differentially expressed genes between family parents were most predictive of heterosis for both field and greenhouse collected traits. Altogether, these data will be used to progress models of heterosis to complement the growing genomic resources available for the improvement of heterozygous perennial bioenergy crops.