Haem oxygenase modifies salinity tolerance in Arabidopsis by controlling K⁺ retention via regulation of the plasma membrane H⁺-ATPase and by altering SOS1 transcript levels in roots

Abstract

Reactive oxygen species (ROS) production is a common denominator in a variety of biotic and abiotic stresses, including salinity. In recent years, haem oxygenase (HO; EC 1.14.99.3) has been described as an important component of the antioxidant defence system in both mammalian and plant systems. Moreover, a recent report on Arabidopsis demonstrated that HO overexpression resulted in an enhanced salinity tolerance in this species. However, physiological mechanisms and downstream targets responsible for the observed salinity tolerance in these HO mutants remain elusive. To address this gap, ion transport characteristics (K⁺ and H⁺ fluxes and membrane potentials) and gene expression profiles in the roots of Arabidopsis thaliana HO-overexpressing (35S:HY1-1/2/3/4) and loss-of-function (hy-100, ho2, ho3, and ho4) mutants were compared during salinity stress. Upon acute salt stress, HO-overexpressing mutants retained more K⁺ (less efflux), and exhibited better membrane potential regulation (maintained more negative potential) and higher H⁺ efflux activity in root epidermis, compared with loss-of-function mutants. Pharmacological experiments suggested that high activity of the plasma membrane H⁺-ATPase in HO overexpressor mutants provided the proton-motive force required for membrane potential maintenance and, hence, better K⁺ retention. The gene expression analysis after 12h and 24h of salt stress revealed high expression levels of H⁺-ATPases (AHA1/2/3) and Na⁺/H⁺ antiporter [salt overly sensitive1 (SOS1)] transcripts in the plasma membrane of HO overexpressors. It is concluded that HO modifies salinity tolerance in Arabidopsis by controlling K⁺ retention via regulation of the plasma membrane H⁺-ATPase and by altering SOS1 transcript levels in roots.