Proteomic and metabolomic analyses uncover integrative mechanisms in Sesuvium portulacastrum tolerance to salt stress

Dingding Cao; Wenbin Zhang; Nan Yang; Ziling Li; Chaoyue Zhang; Dan Wang; Guiping Ye; Jianjun Chen; Xiangying Wei

doi:10.3389/fpls.2023.1277762

Proteomic and metabolomic analyses uncover integrative mechanisms in Sesuvium portulacastrum tolerance to salt stress

Front Plant Sci. 2023 Nov 28:14:1277762. doi: 10.3389/fpls.2023.1277762. eCollection 2023.

Authors

Dingding Cao¹, Wenbin Zhang¹, Nan Yang¹, Ziling Li¹, Chaoyue Zhang¹, Dan Wang¹, Guiping Ye¹, Jianjun Chen², Xiangying Wei¹

Affiliations

¹ Fujian Key Laboratory on Conservation and Sustainable Utilization of Marine Biodiversity, Fuzhou Institute of Oceanography, College of Geography and Oceanography, Minjiang University, Fuzhou, China.
² Mid-Florida Research and Education Center, Department of Environmental Horticulture, Institute of Food and Agricultural Sciences, University of Florida, Apopka, FL, United States.

Abstract

Introduction: Salt stress is a major constraint affecting crop productivity worldwide. Investigation of halophytes could provide valuable information for improving economically important crops to tolerate salt stress and for more effectively using halophytes to remediate saline environments. Sesuvium portulacastrum L. is a halophyte species widely distributed in tropical and subtropical coastal regions and can absorb a large amount of sodium (Na). This study was to analyze S. portulacastrum responses to salt stress at morphological, physiological, proteomic, and metabolomic levels and pursue a better understanding of mechanisms behind its salt tolerance.

Methods: The initial experiment evaluated morphological responses of S. portulacastrum to different concentrations of NaCl in a hydroponic system, and subsequent experiments compared physiological, proteomic, and metabolomic changes in S. portulacastrum after being exposed to 0.4 M NaCl for 24 h as immediate salt stress (IS) to 14 days as adaptive salt stress (AS). Through these analyses, a working model to illustrate the integrative responses of S. portulacastrum to salt stress was proposed.

Results: Plants grown in 0.4 M NaCl were morphologically comparable to those grown in the control treatment. Physiological changes varied in control, IS, and AS plants based on the measured parameters. Proteomic analysis identified a total of 47 and 248 differentially expressed proteins (DEPs) in leaves and roots, respectively. KEGG analysis showed that DEPs, especially those occurring in roots, were largely related to metabolic pathways. Root metabolomic analysis showed that 292 differentially expressed metabolites (DEMs) occurred in IS plants and 371 in AS plants. Among them, 20.63% of upregulated DEMs were related to phenolic acid metabolism.

Discussion: Based on the integrative analysis of proteomics and metabolomics, signal transduction and phenolic acid metabolism appeared to be crucial for S. portulacastrum to tolerate salt stress. Specifically, Ca2+, ABA, and JA signalings coordinately regulated salt tolerance in S. portulacastrum. The stress initially activated phenylpropanoid biosynthesis pathway through Ca2+ signal transduction and increased the content of metabolites, such as coniferin. Meanwhile, the stress inhibited MAPK signaling pathway through ABA and JA signal transduction, which promoted Na sequestration into the vacuole to maintain ROS homeostasis and enhanced S. portulacastrum tolerance to salt stress.

Keywords: Sesuvium portulacastrum; mechanism; metabolomics; proteomics; salt tolerance.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported in part by the Natural Science Foundation of Fujian Province (2022J011135), Fujian Provincial Department of Education (JAT200399), and Minjiang University talent introduction funds.