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

  1. Carbonell-Bejerano, P. 1
  2. Royo, C. 1
  3. Torres-Pérez, R. 1
  4. Grimplet, J. 1
  5. Fernandez, L. 2
  6. Franco-Zorrilla, J.M. 3
  7. Lijavetzky, D. 4
  8. Baroja, E. 1
  9. Martínez, J. 1
  10. García-Escudero, E. 1
  11. Ibáñez, J. 1
  12. Martínez-Zapater, J.M. 1
  1. 1 Instituto de Ciencias de la Vid y del Vino
    info

    Instituto de Ciencias de la Vid y del Vino

    Logroño, España

    ROR https://ror.org/01rm2sw78

  2. 2 Unité Mixte de Recherche Biologie du Fruit et Pathologie, Institut National de la Recherche Agronomique, Villenave d’Ornon, France
  3. 3 Centro Nacional de Biotecnología
    info

    Centro Nacional de Biotecnología

    Madrid, España

    ROR https://ror.org/015w4v032

  4. 4 Instituto de Biología Agrícola de Mendoza, Consejo Nacional de Investigaciones Científicas y Técnicas- UNCuyo-FCA, Chacras de Coria, Argentina
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Revista:
Plant Physiology

ISSN: 0032-0889

Año de publicación: 2017

Volumen: 175

Número: 2

Páginas: 786-801

Tipo: Artículo

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DOI: 10.1104/PP.17.00715 SCOPUS: 2-s2.0-85030831163 WoS: WOS:000411813400017 GOOGLE SCHOLAR

Otras publicaciones en: Plant Physiology

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Resumen

Grape (Vitis vinifera) color somatic variants that can be used to develop new grapevine cultivars occasionally appear associated with 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 with its black berry ancestor, Tempranillo Tinto. Whole-genome sequencing 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 2 and 5. At least 11 validated clustered breakpoints involving intrachromosomal and interchromosomal translocations between three linkage groups 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 the order and orientation of the rearranged fragments, 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 arise spontaneously and stabilize during plant somatic growth. These dramatic rearrangements generate new interesting phenotypes that can be selected for the improvement of vegetatively propagated plant species. © 2017 American Society of Plant Biologists. All Rights Reserved.