Naturally Occurring Disruptive Genetic Variants Affect Expression of Populus trichocarpa Secondary Cell Wall Deposition Genes and Associated Wood Traits

Disruptive variants within coding DNA can lead to defective gene products. Some of these rare naturally occurring genetic mutations may be targets for molecular breeding. Literature review yielded 156 genes currently known to be involved in the formation of the secondary cell wall in Populus trichocarpa. Using a genomic dataset for 1014 individuals, we identified 58 disruptive genetic variants within these genes, despite their known conservation in the wood formation process across woody angiosperms. We then examined the expression patterns of genes harboring disruptive variants using two transcriptomic datasets comprising a total of 598 individuals. Transcript expression differed significantly between individuals with disruptive variants and those without for 13% of gene transcripts in which disruptive variants had been found. Disruptive variants mostly occurred in a heterozygous state where their allele-specific expression was significantly different from the reference allele in c.50% of our observations. The allele-specific expression of disruptive variants also varied significantly between genotypes and clonemates. Gene expression variation between different cultivation sites did not always agree, highlighting the importance of environmental influences on transcript expression. Multiple regulatory mechanisms may affect the expression of genes with disruptive variants in different environments. We demonstrated the effect of two disruptive variants in two hemicellulose genes, GUX and GT8D2, on wood traits to evaluate their potential for tree breeding. Overall, our results show complex expression regulation of secondary cell wall deposition genes with disruptive variants during the wood formation process, and call for further evaluation of the usefulness of such variants for improving wood properties.