A large-scale screening of quinoa accessions reveals an important role of epidermal bladder cells and stomatal patterning in salinity tolerance

The presence of epidermal bladder cells (EBCs) in halophytes allows considerable amount of Na⁺ being accumulated in these external structures, away from the metabolically active mesophile cells. Also, stomatal patterning may represent a primary mechanism by which plants can optimise its water-use efficiency under saline condition. This investigation was aimed to explore the varietal differences in a salinity tolerance of quinoa (Chenopodium quinoa) by evaluating a broad range of accessions and linking the overall salinity tolerance with changes in stomatal characteristics and EBC parameters. One hundred and fourteen accessions were grown under temperature-controlled glasshouse under non-saline and 400 mM NaCl conditions, and different physiological and anatomical characteristics were measured. Accessions were classified into three classes (sensitive, intermediate and tolerant) based on a relative dry weight defined as salinity tolerance index (STI). Results showed a large variability in STI indicating a strong genetic variation in salinity tolerance in quinoa. Bladders density was increased in a majority of accessions under saline condition while the bladder's diameter remained unchanged; this resulted in a large variability in a bladder's volume as a dependant variable. Stomata density remained unchanged between saline and non-saline conditions while the stomata length declined between 3% to 43% amongst accessions. Leaf Na⁺ concentration varied from 669 μmol/gDW to 3155 μmol/gDW under saline condition and, with an exception of a few accessions, leaf K⁺ concentration increased under saline conditions. Correlation analysis indicated a significant positive association between EBC diameter and STI on one hand and EBC volume and STI on the other hand, in a salt-tolerant group. These observations are consistent with the role of EBCs in sequestration of toxic Na⁺ in the external structures, away from the cytosol. A negative association was found between EBC density and diameter in salt-sensitive plants. A negative association between STI and stomata length was also found in a salt-tolerant group, suggesting that these plants were able to efficiently regulate stomatal patterning to balance water loss and CO₂ assimilation under saline conditions. Both salt-sensitive and salt-tolerant groups had the same Na⁺ concentration in the shoot under saline conditions; however, a negative association between leaf Na⁺ concentration and STI in salt-sensitive plants indicated a more efficient Na⁺ sequestration process into the EBCs in salt-tolerant plants.