Halophytism: What Have We Learnt From Arabidopsis thaliana Relative Model Systems?

Abstract

Halophytes are able to thrive in salt concentrations that would kill 99% of other plant species, and identifying their salt-adaptive mechanisms has great potential for improving the tolerance of crop plants to salinized soils. Much research has focused on the physiological basis of halophyte salt tolerance, whereas the elucidation of molecular mechanisms has traditionally lagged behind due to the absence of a model halophyte system. However, over the last decade and a half, two Arabidopsis (Arabidopsis thaliana) relatives, Eutrema salsugineum and Schrenkiella parvula, have been established as transformation-competent models with various genetic resources including high-quality genome assemblies. These models have facilitated powerful comparative analyses with salt-sensitive Arabidopsis to unravel the genetic adaptations that enable a halophytic lifestyle. The aim of this review is to explore what has been learned about halophytism using E. salsugineum and S. parvula We consider evidence from physiological and molecular studies suggesting that differences in salt tolerance between related halophytes and salt-sensitive plants are associated with alterations in the regulation of basic physiological, biochemical, and molecular processes. Furthermore, we discuss how salt tolerance mechanisms of the halophytic models are reflected at the level of their genomes, where evolutionary processes such as subfunctionalization and/or neofunctionalization have altered the expression and/or functions of genes to facilitate adaptation to saline conditions. Lastly, we summarize the many areas of research still to be addressed with E. salsugineum and S. parvula as well as obstacles hindering further progress in understanding halophytism.

Figure 1.

Growth of Arabidopsis, S. parvula, and E. salsugineum on increasing levels of soil NaCl. A, Seven-day-old Arabidopsis plants were treated with various concentrations of NaCl incrementally until final salt concentrations (0, 100, 250, and 500 mm) were reached 1 week later. Plants were imaged after another 1 week. B, E. salsugineum plants treated in the same manner as in A. C, Forty-five-day-old S. parvula plants were treated with various concentrations of NaCl (0, 50, 100, 400, and 600 mm) for 21 d and imaged on day 70. S. parvula plants were able to complete their life cycle and yield seeds even at extreme salt levels. D, E. salsugineum in the salt-crust soils of the Yukon, Canada. Note the presence of cauline leaves while rosette leaves are absent. (Photograph by Jeff Dedrick.)

Figure 2.

CNV in the HKT1 gene family indicating subfunctionalization and neofunctionalization following tandem duplication in S. parvula and E. salsugineum. A, The single copy of HKT1 in Arabidopsis (At) is tandemly duplicated in S. parvula (Sp) and E. salsugineum (Es). Collinear genomic regions are shown in At, Sp, and Es, with blue and green histograms indicating normalized RNA coverage (RPM) for shoots and roots under stress-neutral conditions. Orthologous genes are connected with arrows. The tissue-specific expression among halophyte HKT1 paralogs suggests gene subfunctionalization. B, Amino acid alignment and tree structure of the HKT1 proteins. ScTRK1, a yeast K⁺ transporter, was used as an outgroup. The sequences selected are a subset of those published by Ali et al. (2012). The alignment includes Es- and Sp-specific HKT1 copies, with the amino acid substitution from Asn (N) to Asp (D) in the second pore-loop domain (depicted in the red boxes for EsHKT1;2, SpHKT1;2, and ScTRK1 copies, with red letters for the substituted D). This N→D substitution was shown to confer the unique K⁺ transport activity (Ali et al., 2012, 2018; Ali and Yun, 2016) indicating neofunctionalization in the HKT1;2 copies compared with the Arabidopsis ortholog. The maximum likelihood tree based on sequence alignment was generated using MEGA7 with a consensus tree based on 100 bootstrap values (Kumar et al., 2016).

Figure 3.

Summary of physiological and molecular adaptations that facilitate a halophytic lifestyle. Only those mechanisms demonstrated so far to exhibit differences in E. salsugineum and S. parvula compared with Arabidopsis are depicted. CNV, copy number variation; EsSOS1, E. salsugineum ortholog of the AtSOS1 Na⁺/H⁺ antiporter; EsHKT1, E. salsugineum ortholog of the AtHKT1 Na⁺/K⁺ co-transporter. The genes encoding these transporters have undergone subfunctionalization, neofunctionalization, or both.