A complex reciprocal translocation is linked to reduced gamete viability in a loose-bunch grapevine somatic variant

Because grapevine (Vitis vinifera L.) cultivars are highly heterozygous, they must be clonally propagated to preserve their varietal attributes. Over extended cultivar propagation, 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 with reduced fruit set of the wine grape cultivar 'Tempranillo Tinto'.

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 heterozygous 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. 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.

This study identifies a heterozygous balanced reciprocal translocation linked to reduced gamete viability in a loose-bunch grapevine somatic variant with low fruit set. This finding suggests that genetic defects that reduce gamete viability might be selected in vegetatively propagated crops when decreased seed and fruit set confer agronomic benefits.