Catastrophic unbalanced genome rearrangements cause somatic loss of berry color in grapevine

Abstract

Grape color somatic variants that can be used to develop new grapevine cultivars occasionally appear associated to deletion events of uncertain origin. To understand the mutational mechanisms generating somatic structural variation in grapevine, we compared the Tempranillo Blanco (TB) white berry somatic variant to its black berry ancestor, Tempranillo Tinto. Whole-genome sequencing (WGS) uncovered a catastrophic genome rearrangement in TB that caused the hemizygous deletion of 313 genes, including the loss of the functional copy for the MYB transcription factors required for anthocyanin pigmentation in the berry skin. Loss of heterozygosity and decreased copy number delimited interspersed monosomic and disomic regions in the right arm of linkage groups (LG) 2 and 5. At least eleven validated clustered breakpoints involving intra- and inter-chromosomal translocations between three LGs flanked the deleted fragments, which, according to segregation analyses, are phased in a single copy of each of the affected chromosomes. These hallmarks along with the lack of homology between breakpoint joins and the randomness of rearranged fragments order and orientation are all consistent with a chromothripsis-like pattern generated after chromosome breakage and illegitimate rejoining. This unbalanced genome reshuffling has additional consequences in reproductive development. In TB, lack of sexual transmission of rearranged chromosomes associates with low gamete viability, which compromises fruit set and decreases fruit production. Our findings show that catastrophic genome rearrangements spontaneously arise and stabilize during plant somatic growth. Despite these dramatic changes may compromise sexual fitness, they generate new interesting phenotypes that can be perpetuated in vegetatively propagated plants.