Salinity Tolerance of Halophytic Grass Puccinellia nuttalliana Is Associated with Enhancement of Aquaporin-Mediated Water Transport by Sodium

Abstract

In salt-sensitive plants, root hydraulic conductivity is severely inhibited by NaCl, rapidly leading to the loss of water balance. However, halophytic plants appear to effectively control plant water flow under salinity conditions. In this study, we tested the hypothesis that Na+ is the principal salt factor responsible for the enhancement of aquaporin-mediated water transport in the roots of halophytic grasses, and this enhancement plays a significant role in the maintenance of water balance, gas exchange, and the growth of halophytic plants exposed to salinity. We examined the effects of treatments with 150 mM of NaCl, KCl, and Na2SO4 to separate the factors that affect water relations and, consequently, physiological and growth responses in three related grass species varying in salt tolerance. The grasses included relatively salt-sensitive Poa pratensis, moderately salt-tolerant Poa juncifolia, and the salt-loving halophytic grass Puccinellia nuttalliana. Our study demonstrated that sustained growth, chlorophyll concentrations, gas exchange, and water transport in Puccinellia nuttalliana were associated with the presence of Na in the applied salt treatments. Contrary to the other examined grasses, the root cell hydraulic conductivity in Puccinellia nuttalliana was enhanced by the 150 mM NaCl and 150 mM Na2SO4 treatments. This enhancement was abolished by the 50 µM HgCl2 treatment, demonstrating that Na was the factor responsible for the increase in mercury-sensitive, aquaporin-mediated water transport. The observed increases in root Ca and K concentrations likely played a role in the transcriptional and (or) posttranslational regulation of aquaporins that enhanced root water transport capacity in Puccinellia nuttalliana. The study demonstrates that Na plays a key role in the aquaporin-mediated root water transport of the halophytic grass Puccinellia nuttalliana, contributing to its salinity tolerance.

Analysis of aquaporins in northern grasses reveal functional importance of Puccinellia nuttalliana PIP2;2 in salt tolerance

“…We also demonstrated that NaCl treatments enhanced cell hydraulic conductivity (L pc ) in roots of Puccinellia nuttallianna and had relatively little effect on L pc in Poa juncifolia while, similarly to other glycophytes (Lee & Zwiazek, 2015;Carmen martínez-Ballesta et al, 2003), NaCl had a strong inhibitory effect on L pc in Poa pratensis (Vaziriyeganeh et al, 2018(Vaziriyeganeh et al, , 2022. Since in our earlier study (Vaziriyeganeh at al. 2022), we also determined that Puccinellia nuttalliana treated with 150 mM NaCl maintained leaf water potentials at the control level when measured after 6 days of treatment, we used this treatment duration to investigate the effects of NaCl on aquaporin expression in the present study.…”

“…However, L pc in roots of Arabidopsis plants overexpressing AtPIP2;5 was unaffected by the NaCl treatments, which caused several‐fold L pc reductions in the wild‐type plants (Lee & Zwiazek, 2015). The increased expression of PIP2;2 in Puccinellia nuttalliana and Poa juncifolia is likely linked to the enhanced water transport by NaCl (Vaziriyeganeh et al, 2018, 2022). The increase in PIP2;2 transcript levels in NaCl‐treated Puccinellia nuttalliana was also earlier confirmed by transcriptome analysis (Vaziriyeganeh et al, 2021).…”

“…The responses of indicate its possible important role in maintaining water status under salt stress and warrant further attention. enhanced L pc in this halophytic plant (Vaziriyeganeh et al, 2018(Vaziriyeganeh et al, , 2022, we examined whether the expression of Puccinellia nuttalliana aquaporins in yeast affects water transport in the absence and presence of NaCl. We carried out water transport measurements in yeast protoplasts using stopped-flow spectroscopy in response to changes in the incubation medium osmolarity (Koch, 1984).…”

“…We examined the expression levels of these genes in control and NaCl-treated plants and characterised their structural and functional properties that may have contributed to the reported differences in the responses of plant water relations to salinity (Vaziriyeganeh et al, 2018(Vaziriyeganeh et al, , 2022. We tested the hypothesis that the earlier reported differences in the responses of cell hydraulic conductivity to NaCl in the three grass species, including an enhancement of cell hydraulic conductivity in P. nuttalliana (Vaziriyeganeh et al, 2018(Vaziriyeganeh et al, , 2022, involve changes in the expression patterns of PIP and TIP aquaporins and direct effects of NaCl on gating properties. We also investigated whether PnuPIP2;2, the highly expressed aquaporin by NaCl in P. nuttalliana, possesses dual water and ion transport functionality when expressed in yeast and examined the pore properties of this aquaporin in the three grass species to shed light on its role in salt tolerance.…”

Biological and Agronomic Characterization of Improved Alkali Grass Genotypes (Puccinellia ciliata Bor) in the Aegean Region of Turkey

“…6). It was demonstrated the significant differences among Puccinellia species for chlorophyll a, b and a:b ratio and the supremacy of the P. pratensis [30]. Similarly, genotype X had a high performance for leaf thickness in all sowing times (Figs.…”