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A stratagem for primary root elongation under moderate salt stress in the halophyte Schrenkiella parvula

Halophytes are salt-tolerant plants that grow in soil or waters of high salinity. Schrenkiella parvula is one of the halophyte plants that grow around Tuz (Salt) Lake, TURKEY that can survive at 600 mM NaCl. Intriguingly, S. parvula belongs to the same Brassicaceae family as the model plant Arabidopsis thaliana, and its genome is 90% homologous to the Arabidopsis genome. Here, we performed proteomic analysis and physiological studies on the roots of S. parvula seedlings cultivated under a moderate salt condition at 100 mM NaCl. Surprisingly, under 100 mM NaCl conditions, the primary roots elongated much faster than under NaCl-free conditions, although up to 200 mM those were reduced. On the other hand, iso-osmotic mannitol did not promote primary root elongation, suggesting a specific response to NaCl. Epidermal cell elongation was promoted in the elongation zone, but meristem size and DNA replication were decreased. In addition, root hair formation and lateral root elongation were suppressed at moderate salinity. Compared with A. thaliana, the cell death and ROS increase of root tip meristem cells under 100 mM NaCl condition were significantly lower in S. parvula seedlings. The size and starch content of sedimentary amyloplasts/statoliths in columella cells decreased, and gravitropism of primary roots was partially reduced. Gene expression analyses showed that the expression of auxin response and biosynthesis genes IAA1, IAA2, TAA1 and YUC8 were repressed and the SOS1 gene was upregulated two-fold in roots grown under moderate salt conditions. Proteomic analysis showed that co-chaperone and activator of HSPs such as Hop2 and Aha1 domain-containing protein orthologs were upregulated. Moreover, several secondary metabolic process-related proteins, antioxidant proteins, stress response proteins and proline catabolic process-related proteins were also increased. In contrast, enzymes associated with root hair elongation and nucleotide and protein syntheses were downregulated. These changes in auxin-related physiological responses, root architecture, lower ROS signaling, and stress-related protein expression promote primary root penetration into lower-salinity deeper soils as an adaptation of S. parvula.