A complex reciprocal translocation underlies reduced bunch compactness in a grapevine somatic variant

Background Because grapevine (Vitis vinifera L.) cultivars are highly heterozygous, they must be clonally propagated to preserve their varietal attributes. Over extended cultivar propagation histories, somatic mutations arise and can generate new phenotypes useful for intra-varietal improvement. Somatic variants with looser bunches – associated with more uniform berry ripening and reduced bunch rot incidence – are particularly valuable in compact-bunch cultivars. To understand the basis of this trait, we combined phenotyping, genomics, and genetic analyses to study VP11, a loose-bunch somatic variant clone of the wine grape cultivar ‘Tempranillo Tinto’. Results Pollen viability and the number of seeds per berry were reduced by ~50% in VP11 compared to a control clone of ‘Tempranillo Tinto’. Long-read whole-genome sequencing identified eleven large somatic structural variants (SVs) in VP11, including three inter-chromosomal events. These consisted of one fixed reciprocal translocation (Tra1-3), with duplications spanning tens of kilobases at the translocation breakpoints, and two segmental duplications (one fixed and one likely L2 meristem cell layer-restricted). All three SVs were molecularly validated, including the phasing and exchange of distal chromosome segments in Tra1-3. In VP11 self-cross progeny, pollen viability was significantly reduced among individuals carrying Tra1-3, and the two translocation chromosomes were always inherited together, indicating that gametes with an unbalanced chromosomal content are non-viable. Conclusions This study identifies reduced gamete viability caused by a heterozygous balanced reciprocal translocation as a mechanism underlying the loose-bunch trait in grapevine. We conclude that even if a genetic defect reduces gamete viability, it can still be useful to decrease seed and fruit set in vegetatively propagated crops where these traits are desirable.