Target enrichment sequencing coupled with GWAS identifies MdPRX10 as a candidate gene in the control of budbreak in apple

Amy E Watson; Baptiste Guitton; Alexandre Soriano; Ronan Rivallan; Hélène Vignes; Isabelle Farrera; Bruno Huettel; Catalina Arnaiz; Vítor da Silveira Falavigna; Aude Coupel-Ledru; Vincent Segura; Gautier Sarah; Jean-François Dufayard; Stéphanie Sidibe-Bocs; Evelyne Costes; Fernando Andrés

doi:10.3389/fpls.2024.1352757

Target enrichment sequencing coupled with GWAS identifies MdPRX10 as a candidate gene in the control of budbreak in apple

Front Plant Sci. 2024 Feb 21:15:1352757. doi: 10.3389/fpls.2024.1352757. eCollection 2024.

Authors

Amy E Watson¹, Baptiste Guitton¹, Alexandre Soriano^{1

2

3}, Ronan Rivallan^{1

2}, Hélène Vignes^{1

2}, Isabelle Farrera¹, Bruno Huettel⁴, Catalina Arnaiz⁵, Vítor da Silveira Falavigna¹, Aude Coupel-Ledru¹, Vincent Segura¹, Gautier Sarah¹, Jean-François Dufayard^{1

2

3}, Stéphanie Sidibe-Bocs^{1

2

3}, Evelyne Costes^#¹, Fernando Andrés^#¹

Affiliations

¹ UMR AGAP Institut, Univ Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.
² CIRAD, UMR AGAP Institut, Montpellier, France.
³ French Institute of Bioinformatics (IFB) - South Green Bioinformatics Platform, Bioversity, CIRAD, INRAE, IRD, Montpellier, France.
⁴ Genome Centre, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
⁵ Centro de Biotecnología y Genómica de Plantas, Instituto de Investigación y Tecnología Agraria y Alimentaria, Universidad Politécnica de Madrid, Madrid, Spain.

^# Contributed equally.

Abstract

The timing of floral budbreak in apple has a significant effect on fruit production and quality. Budbreak occurs as a result of a complex molecular mechanism that relies on accurate integration of external environmental cues, principally temperature. In the pursuit of understanding this mechanism, especially with respect to aiding adaptation to climate change, a QTL at the top of linkage group (LG) 9 has been identified by many studies on budbreak, but the genes underlying it remain elusive. Here, together with a dessert apple core collection of 239 cultivars, we used a targeted capture sequencing approach to increase SNP resolution in apple orthologues of known or suspected A. thaliana flowering time-related genes, as well as approximately 200 genes within the LG9 QTL interval. This increased the 275 223 SNP Axiom^® Apple 480 K array dataset by an additional 40 857 markers. Robust GWAS analyses identified MdPRX10, a peroxidase superfamily gene, as a strong candidate that demonstrated a dormancy-related expression pattern and down-regulation in response to chilling. In-silico analyses also predicted the residue change resulting from the SNP allele associated with late budbreak could alter protein conformation and likely function. Late budbreak cultivars homozygous for this SNP allele also showed significantly up-regulated expression of C-REPEAT BINDING FACTOR (CBF) genes, which are involved in cold tolerance and perception, compared to reference cultivars, such as Gala. Taken together, these results indicate a role for MdPRX10 in budbreak, potentially via redox-mediated signaling and CBF gene regulation. Moving forward, this provides a focus for developing our understanding of the effects of temperature on flowering time and how redox processes may influence integration of external cues in dormancy pathways.

Keywords: CBF; budbreak; capture; cold-perception; dormancy; flowering; peroxidase; redox.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This project received funding from ERA-NET SusCrop2 (FruitFlow, ANR-21-SUSC-0002) to support the postdoctoral post of AEW and from the Agropolis Foundation (ID 1503-008) through the Investissements d’Avenir program (Labex Agro: ANR-10-LABX-0001-01) for capture sequencing.