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Initiation of organ maturation and fruit ripening in grapevine is controlled by the CARPO-NAC transcription factor

Erica D’Incà, Chiara Foresti, Luis Orduña, Alessandra Amato, Elodie Vandelle, Antonio Santiago, Alessandro Botton, Stefano Cazzaniga, Edoardo Bertini, Mario Pezzotti, James Giovannoni, Julia Vrebalov, View ORCID ProfileJosé Tomás Matus, View ORCID ProfileGiovanni Battista Tornielli, View ORCID ProfileSara Zenoni
doi: https://doi.org/10.1101/2021.11.13.468481
Erica D’Incà
1Department of Biotechnology, University of Verona, Italy
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Chiara Foresti
1Department of Biotechnology, University of Verona, Italy
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Luis Orduña
2Institute for Integrative Systems Biology (I2SysBio), Universitat de València-CSIC, Paterna, 46908, Valencia, Spain
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Alessandra Amato
1Department of Biotechnology, University of Verona, Italy
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Elodie Vandelle
1Department of Biotechnology, University of Verona, Italy
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Antonio Santiago
2Institute for Integrative Systems Biology (I2SysBio), Universitat de València-CSIC, Paterna, 46908, Valencia, Spain
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Alessandro Botton
3Department of Agronomy, Food, Natural resources, Animals and Environment, University of Padova, Italy
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Stefano Cazzaniga
1Department of Biotechnology, University of Verona, Italy
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Edoardo Bertini
1Department of Biotechnology, University of Verona, Italy
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Mario Pezzotti
1Department of Biotechnology, University of Verona, Italy
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James Giovannoni
4USDA-ARS Robert W. Holley Center and Boyce Thompson Institute for Plant Research, Tower Road, Cornell Campus, Ithaca, NY 14853, USA
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Julia Vrebalov
4USDA-ARS Robert W. Holley Center and Boyce Thompson Institute for Plant Research, Tower Road, Cornell Campus, Ithaca, NY 14853, USA
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José Tomás Matus
2Institute for Integrative Systems Biology (I2SysBio), Universitat de València-CSIC, Paterna, 46908, Valencia, Spain
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  • ORCID record for José Tomás Matus
  • For correspondence: sara.zenoni@univr.it
Giovanni Battista Tornielli
1Department of Biotechnology, University of Verona, Italy
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  • For correspondence: sara.zenoni@univr.it
Sara Zenoni
1Department of Biotechnology, University of Verona, Italy
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  • ORCID record for Sara Zenoni
  • For correspondence: sara.zenoni@univr.it
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ABSTRACT

Grapevine is a woody temperate perennial plant and one of the most important fruit crops with global relevance in both the fresh fruit and winemaking industries. Unfortunately, global warming is affecting viticulture by altering developmental transitions and fruit maturation processes. In this context, uncovering the molecular mechanisms controlling the onset and progression of ripening could prove essential to maintain high-quality grapes and wines. Through a deep inspection of previously published transcriptomic data we identified the NAC family member VviCARPO (Controlled Adjustment of Ripening and maturation of Plant Organs) as a key regulator of grapevine maturation whose induction precedes the expression of well-known ripening associated genes. We explored VviCARPO binding landscapes through DAP-seq and overlapped its bound genes with transcriptomics datasets from stable and transient VviCARPO overexpressing grapevine plants to define a set of high-confidence targets. Among these, we identified key molecular ripening markers. Physiological, metabolic and promoter activation analyses showed that VviCARPO induces chlorophyll degradation and anthocyanin accumulation through the up-regulation of VviSGR1 and VviMYBA1, respectively, with the latter being up-regulated through a VviCARPO-VviNAC03 regulatory complex. Despite showing a closer phylogenetic relationship to senescent-related AtNAP homologues, VviCARPO complemented the nor mutant phenotype in tomato, suggesting it may have acquired a dual role as an orchestrator of both ripening- and senescence-related processes. Our data supports CARPO as a master regulator of the grapevine vegetative-to-mature phase organ transition and therefore an essential target for insuring fruit quality and environmental resilience.

SIGNIFICANT STATEMENT CARPO is a grape NAC transcription factor central to fruit ripening and tissue senescence. This regulator influences multiple biological pathways common to both processes including cell wall metabolism, chlorophyll degradation, pigment production and hormone synthesis/signaling through regulation of their key genes. As various external stresses and changing climatic conditions influence vegetative growth and berry ripening, CARPO could prove a useful genetic and breeding target towards maintaining necessary crop performance and fruit-quality characteristics.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 14, 2021.
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Initiation of organ maturation and fruit ripening in grapevine is controlled by the CARPO-NAC transcription factor
Erica D’Incà, Chiara Foresti, Luis Orduña, Alessandra Amato, Elodie Vandelle, Antonio Santiago, Alessandro Botton, Stefano Cazzaniga, Edoardo Bertini, Mario Pezzotti, James Giovannoni, Julia Vrebalov, José Tomás Matus, Giovanni Battista Tornielli, Sara Zenoni
bioRxiv 2021.11.13.468481; doi: https://doi.org/10.1101/2021.11.13.468481
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Initiation of organ maturation and fruit ripening in grapevine is controlled by the CARPO-NAC transcription factor
Erica D’Incà, Chiara Foresti, Luis Orduña, Alessandra Amato, Elodie Vandelle, Antonio Santiago, Alessandro Botton, Stefano Cazzaniga, Edoardo Bertini, Mario Pezzotti, James Giovannoni, Julia Vrebalov, José Tomás Matus, Giovanni Battista Tornielli, Sara Zenoni
bioRxiv 2021.11.13.468481; doi: https://doi.org/10.1101/2021.11.13.468481

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