Halophytes and heavy metals: A multi‐omics approach to understand the role of gene and genome duplication in the abiotic stress tolerance of Cakile maritima

• Published in: American journal of botany 2024-08, Vol.111 (8), p.e16310-n/a
• Main Authors: Thomas, Shawn K., Hoek, Kathryn Vanden, Ogoti, Tasha, Duong, Ha, Angelovici, Ruthie, Pires, J. Chris, Mendoza‐Cozatl, David, Washburn, Jacob, Schenck, Craig A.
• Format: Article
• Language: English
• Subjects: Abiotic stress; amino acid; Amino acids; Biological evolution; botany; Brassica; Cadmium; Cakile maritima; Cellular stress response; evolution; Evolutionary genetics; free amino acids; Gene duplication; Gene families; Genes; Genomes; Genomics; Halophytes; Heavy metals; ionomics; multiomics; Mustard; Polyploidy; Raw materials; Retention; salt stress; salt tolerance; Salts; species; stress response; stress tolerance; Transport processes
• ISSN: 0002-9122; 1537-2197; 1537-2197
• DOI: 10.1002/ajb2.16310

Premise The origin of diversity is a fundamental biological question. Gene duplications are one mechanism that provides raw material for the emergence of novel traits, but evolutionary outcomes depend on which genes are retained and how they become functionalized. Yet, following different duplication types (polyploidy and tandem duplication), the events driving gene retention and functionalization remain poorly understood. Here we used Cakile maritima, a species that is tolerant to salt and heavy metals and shares an ancient whole‐genome triplication with closely related salt‐sensitive mustard crops (Brassica), as a model to explore the evolution of abiotic stress tolerance following polyploidy. Methods Using a combination of ionomics, free amino acid profiling, and comparative genomics, we characterize aspects of salt stress response in C. maritima and identify retained duplicate genes that have likely enabled adaptation to salt and mild levels of cadmium. Results Cakile maritima is tolerant to both cadmium and salt treatments through uptake of cadmium in the roots. Proline constitutes greater than 30% of the free amino acid pool in C. maritima and likely contributes to abiotic stress tolerance. We find duplicated gene families are enriched in metabolic and transport processes and identify key transport genes that may be involved in C. maritima abiotic stress tolerance. Conclusions These findings identify pathways and genes that could be used to enhance plant resilience and provide a putative understanding of the roles of duplication types and retention on the evolution of abiotic stress response.