Local cryptic diversity in salinity adaptation mechanisms in the wild outcrossing Brassica fruticulosa

Busoms, Silvia; da Silva, Ana C.; Escolà, Glòria; Abdilzadeh, Raziyeh; Curran, Emma; Bollmann-Giolai, Anita; Bray, Sian; Wilson, Michael; Poschenrieder, Charlotte; Yant, Levi

Abstract

It is normally supposed that populations of the same species should evolve shared mechanisms of adaptation to common stressors due to evolutionary constraint. Here, we describe a system of within-species local adaptation to coastal habitats, Brassica fruticulosa, and detail surprising strategic variability in adaptive responses to high salinity. These different adaptive responses in neighboring populations are evidenced by transcriptomes, diverse physiological outputs, and distinct genomic selective landscapes. In response to high salinity Northern Catalonian populations restrict root-to-shoot Na+ transport, favoring K+ uptake. Contrastingly, Central Catalonian populations accumulate Na+ in leaves and compensate for the osmotic imbalance with compatible solutes such as proline. Despite contrasting responses, both metapopulations were salinity tolerant relative to all inland accessions. To characterize the genomic basis of these divergent adaptive strategies in an otherwise non-saline-tolerant species, we generate a long-read-based genome and population sequencing of 18 populations (nine inland, nine coastal) across the B. fruticulosa species range. Results of genomic and transcriptomic approaches support the physiological observations of distinct underlying mechanisms of adaptation to high salinity and reveal potential genetic targets of these two very recently evolved salinity adaptations. We therefore provide a model of within-species salinity adaptation and reveal cryptic variation in neighboring plant populations in the mechanisms of adaptation to an important natural stressor highly relevant to agriculture.

Citation

Busoms, S., da Silva, A. C., Escolà, G., Abdilzadeh, R., Curran, E., Bollmann-Giolai, A., Bray, S., Wilson, M., Poschenrieder, C., & Yant, L. (2024). Local cryptic diversity in salinity adaptation mechanisms in the wild outcrossing Brassica fruticulosa. Proceedings of the National Academy of Sciences, 121(40), Article e2407821121. https://doi.org/10.1073/pnas.2407821121

• Journal Article Type: Article
• Acceptance Date: Aug 22, 2024
• Online Publication Date: Sep 24, 2024
• Publication Date: 2024-10
• Deposit Date: Sep 28, 2024
• Publicly Available Date: Oct 2, 2024
• Journal: Proceedings of the National Academy of Sciences
• Print ISSN: 0027-8424
• Electronic ISSN: 1091-6490
• Publisher: National Academy of Sciences
• Peer Reviewed: Peer Reviewed
• Volume: 121
• Issue: 40
• Article Number: e2407821121
• DOI: https://doi.org/10.1073/pnas.2407821121
• Public URL: https://nottingham-repository.worktribe.com/output/40000425
• Additional Information: Received: 2024-04-18; Accepted: 2024-08-22; Published: 2024-09-24