Cross-Tolerance to Salinity and Osmotic Stress in Chenopodium quinoa

Under natural conditions, halophytes are simultaneously exposed to multiple abiotic stresses and develop cross-tolerance as they adapt to changing environments. We studied cross-tolerance in the halophyte Chenopodium quinoa by acclimating plants to different salinity levels (0, 100, 200, and 300 mM NaCl) to activate plant tolerance mechanisms, and then additionally exposing them to osmotic stress (ψs = –0.3 MPa). This allowed us to assess the role of various photosystem (PS) protection mechanisms in energy balance maintenance in chloroplasts. Acclimation of C. quinoa plants to salinity (100–300 mM NaCl) did not affect the maximum quantum yield of PSII (Fv/Fm), but induced activation of the malate valve and suppression of photorespiration. Increased cyclic electron transport (CET) around PSI and induction of non-photochemical quenching (NPQ) of PSII were observed at 200 and 300 mM NaCl, similarly to non-saline conditions. At 300 mM NaCl, stress-induced accumulation of proline was also observed. The additional action of osmotic stress decreased water content in all plants, and reduced biomass at 300 mM NaCl. Stable Rubisco content at 200–300 mM NaCl was maintained via regulation of rbcL expression. In plants acclimated to 100 mM NaCl, additional osmotic stress 2-fold increased NPQ, activated photorespiration and the P5C-Pro cycle of proline metabolism, and downregulated expression of the PnsB5 gene, encoding a subunit of the NDH complex involved in CET PSI. Additional osmotic stress in plants grown at 200 mM NaCl also increased NPQ and proline synthesis. In plants at 300 mM NaCl, these parameters did not change significantly, as protective mechanisms were already activated by high salinity. Thereby, the mechanisms of photosystem protection and energy balance maintenance in C. quinoa involve the malate valve, CET PSI, NPQ and proline metabolism, which were differentially activated under all stress combinations. Our results suggest that malate valve activation is primarily driven by the ionic component of salinity, whereas changes in NPQ and proline metabolism are associated with osmotic stress. Both salinity and osmotic stress can shift the balance between the PGR5/PGRL1 and NDH pathways of CET PSI in C. quinoa.