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

Authors: THOMAS, SHAWN - University Of Missouri; VANDEN HOEK, KATHRYN - University Of Missouri; OGOTI, TASHA - University Of Missouri; DUONG, HA - University Of Missouri; ANGELOVICI, RUTHIE - University Of Missouri; PIRES, CHRIS - Colorado State University; MENDOZA-COZATL, DAVID - University Of Missouri; Washburn, Jacob; SCHENCK, CRAIG - University Of Missouri

Submitted to: American Journal of Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/19/2024
Publication Date: 4/10/2024
Citation: Thomas, S.K., Vanden Hoek, K., Ogoti, T., Duong, H., Angelovici, R., Pires, C.J., Mendoza-Cozatl, D., Washburn, J.D., Schenck, C.A. 2024. Halophytes and heavy metals: a multi-omics approach to understand the role of gene and genome duplication in abiotic stress tolerance of Cakile maritima. American Journal of Botany. 111. Article e16310. https://doi.org/10.1002/ajb2.16310.
DOI: https://doi.org/10.1002/ajb2.16310

Interpretive Summary: Salt and heavy metal tolerance allow some plants to thrive in environments where most plants would die. Understanding the genetics, physiology, and biochemistry of these stress tolerant plants could enable their application to improve agricultural productivity and sustainability. This study used artificially created high and low stress environment experiments along with know relationships between salt/heavy metal tolerant and intolerant species to show that gene duplication is likely at least partially responsible for tolerance in one of these species and that key transport genes are likely involved.

Technical Abstract: 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.