Genome-wide DNA methylation analysis and biochemical responses provide insights into the initial domestication of halophyte Puccinellia tenuiflora.

KEY MESSAGE: Puccinellia tenuiflora was domesticated for two years by growing it under non-saline conditions, providing epigenetic and biochemical insights into the initial domestication of extreme halophytes. Some halophytes have economic value as crop species. The domestication of halophytes may offer hope in solving the problem of soil salinization. We domesticated a wild halophyte, Puccinellia tenuiflora, for two years by growing it under non-saline conditions in a greenhouse and used re-sequencing, genome-wide DNA methylation, biochemical, and transcriptome analyses to uncover the mechanisms underlying alterations in the halophyte's tolerance to saline following domestication. Our results showed that non-saline domestication altered the methylation status for a number of genes and transposable elements, resulting in a much higher frequency of hypomethylation than hypermethylation. These modifications to DNA methylation were observed in many critical salinity-tolerance genes, particularly their promoter regions or transcriptional start sites. Twenty-nine potassium channel genes were hypomethylated and three were hypermethylated, suggesting that the DNA methylation status of potassium channel genes was influenced by domestication. The accelerated uptake of potassium is a major salinity tolerance characteristic of P. tenuiflora. We propose that modifications to the DNA methylation of potassium channel genes may be associated with the development of salinity tolerance in this species. By assessing whether non-saline domestication could change the salinity tolerance of P. tenuiflora, we demonstrated that non-saline domesticated plants are less tolerant to saline, which may be attributable to altered sucrose metabolism. DNA methylation and transposable elements may, therefore, be integrated into an environment-sensitive molecular engine that promotes the rapid domestication of P. tenuiflora to enable its use as a crop plant.