Guard cell transcriptome reveals membrane transport, stomatal development, and cell wall modifications as key traits involved in salinity tolerance in halophytic Chenopodium quinoa.

A comparative investigation was conducted to evaluate transcriptional changes in guard cells (GCs) of closely related halophytic (Chenopodium quinoa) and glycophytic (Spinacia oleracea) species. Plants were exposed to three weeks of 250 mM NaCl treatment and GC-enriched epidermal fragments were mechanically prepared. In both species salt-responsive genes were mainly related to categories of protein metabolism, secondary metabolites, signal transduction, and transport systems. Genes related to ABA signaling and ABA biosynthesis were strongly induced in quinoa but not in spinach GCs. Also, expression of the genes encoding transporters of amino acids, proline, sugars, sucrose, and potassium increased in quinoa GCs under salinity stress. Analysis of cell-wall-related genes suggests that genes involved in lignin synthesis (e.g., lignin biosynthesis LAC4) were highly upregulated by salt in spinach GCs. In contrast, transcripts related to cell wall plasticity (e.g., PM3) were highly induced in quinoa. Faster stomatal response to light and dark measured by observing kinetics of changes in stomatal conductance in quinoa might be associated with higher plasticity of the cell wall regulated by PME3. Furthermore, genes involving in inhibition of stomatal development and differentiation were highly expressed by salt in quinoa, but not in spinach. These changes correlated with reduced stomatal density and index in quinoa thus improving its water use efficiency. The fine modulation of transporters, cell wall modification and controlling stomatal development in GCs of quinoa may have resulted in high K+/Na+ ratio, lower stomatal conductance and higher stomatal speed for better adaptation to salinity stress in quinoa.