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GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion.

ABSTRACT: The non-protein amino acid ?-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to salinity. However, the physiological rationale for this elevation remains elusive. This study compared electrophysiological and whole-plant responses of salt-treated Arabidopsis mutants pop2-5 and gad1,2, which have different abilities to accumulate GABA. The pop2-5 mutant, which was able to overaccumulate GABA in its roots, showed a salt-tolerant phenotype. On the contrary, the gad1,2 mutant, lacking the ability to convert glutamate to GABA, showed oversensitivity to salinity. The greater salinity tolerance of the pop2-5 line was explained by: (i) the role of GABA in stress-induced activation of H+-ATPase, thus leading to better membrane potential maintenance and reduced stress-induced K+ leak from roots; (ii) reduced rates of net Na+ uptake; (iii) higher expression of SOS1 and NHX1 genes in the leaves, which contributed to reducing Na+ concentration in the cytoplasm by excluding Na+ to apoplast and sequestering Na+ in the vacuoles; (iv) a lower rate of H2O2 production and reduced reactive oxygen species-inducible K+ efflux from root epidermis; and (v) better K+ retention in the shoot associated with the lower expression level of GORK channels in plant leaves.

SUBMITTER: Su N

PROVIDER: S-EPMC6859739 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion.

Su Nana N Wu Qi Q Chen Jiahui J Shabala Lana L Mithöfer Axel A Wang Haiyang H Qu Mei M Yu Min M Cui Jin J Shabala Sergey S

Journal of experimental botany 20191101 21

The non-protein amino acid γ-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to salinity. However, the physiological rationale for this elevation remains elusive. This study compared electrophysiological and whole-plant responses of salt-treated Arabidopsis mutants pop2-5 and gad1,2, which have different abilities to accumulate GABA. The pop2-5 mutant, which was able to overaccumulate GABA in its roots, showed a salt-tolerant phenotype. On the contrary, the gad1,2 mutan ...[more]

PMID: 31420662

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Project description:BackgroundCultivated rice species (Oryza sativa L. and O. glaberrima Steud.) are generally considered among the crop species most sensitive to salt stress. A handful of lines are known to be tolerant, and a small number of these have been used extensively as donors in breeding programs. However, these donors use many of the same genes and physiological mechanisms to confer tolerance. Little information is available on the diversity of mechanisms used by these species to cope with salt stress, and there is a strong need to identify varieties displaying additional physiological and/or genetic mechanisms to confer higher tolerance.ResultsHere we present data on 103 accessions from O. sativa and 12 accessions from O. glaberrima, many of which are identified as salt tolerant for the first time, showing moderate to high tolerance of high salinity. The correlation of salinity-induced senescence (as judged by the Standard Evaluation System for Rice, or SES, score) with whole-plant and leaf blade Na+ concentrations was high across nearly all accessions, and was almost identical in both O. sativa and O. glaberrima. The association of leaf Na+ concentrations with cultivar-groups was very weak, but association with the OsHKT1;5 allele was generally strong. Seven major and three minor alleles of OsHKT1;5 were identified, and their comparisons with the leaf Na+ concentration showed that the Aromatic allele conferred the highest exclusion and the Japonica allele the least. A number of exceptions to this association with the Oryza HKT1;5 allele were identified; these probably indicate the existence of additional highly effective exclusion mechanisms. In addition, two landraces were identified, one from Thailand and the other from Senegal, that show high tissue tolerance.ConclusionsSignificant variation in salinity tolerance exists within both cultivated Oryza species, and this is the first report of significant tolerance in O. glaberrima. The majority of accessions display a strong quantitative relationship between tolerance and leaf blade Na+ concentration, and thus the major tolerance mechanisms found in these species are those contributing to limiting sodium uptake and accumulation in active leaves. However, there appears to be genetic variation for several mechanisms that affect leaf Na+ concentration, and rare cases of accessions displaying different mechanisms also occur. These mechanisms show great promise for improving salt tolerance in rice over that available from current donors.

Project description:BackgroundSalinity is a worldwide factor limiting the agricultural production. Cotton is an important cash crop; however, its yield and product quality are negatively affected by soil salinity. Use of nanomaterials such as cerium oxide nanoparticles (nanoceria) to improve plant tolerance to stress conditions, e.g. salinity, is an emerged approach in agricultural production. Nevertheless, to date, our knowledge about the role of nanoceria in cotton salt response and the behind mechanisms is still rare.ResultsWe found that PNC (poly acrylic acid coated nanoceria) helped to improve cotton tolerance to salinity, showing better phenotypic performance, higher chlorophyll content (up to 68% increase) and biomass (up to 38% increase), and better photosynthetic performance such as carbon assimilation rate (up to 144% increase) in PNC treated cotton plants than the NNP (non-nanoparticle control) group. Under salinity stress, in consistent to the results of the enhanced activities of antioxidant enzymes, PNC treated cotton plants showed significant lower MDA (malondialdehyde, up to 44% decrease) content and reactive oxygen species (ROS) level such as hydrogen peroxide (H2O2, up to 79% decrease) than the NNP control group, both in the first and second true leaves. Further experiments showed that under salinity stress, PNC treated cotton plants had significant higher cytosolic K+ (up to 84% increase) and lower cytosolic Na+ (up to 77% decrease) fluorescent intensity in both the first and second true leaves than the NNP control group. This is further confirmed by the leaf ion content analysis, showed that PNC treated cotton plants maintained significant higher leaf K+ (up to 84% increase) and lower leaf Na+ content (up to 63% decrease), and thus the higher K+/Na+ ratio than the NNP control plants under salinity stress. Whereas no significant increase of mesophyll cell vacuolar Na+ intensity was observed in PNC treated plants than the NNP control under salinity stress, suggesting that the enhanced leaf K+ retention and leaf Na+ exclusion, but not leaf vacuolar Na+ sequestration are the main mechanisms behind PNC improved cotton salt tolerance. qPCR results showed that under salinity stress, the modulation of HKT1 but not SOS1 refers more to the PNC improved cotton leaf Na+ exclusion than the NNP control.ConclusionsPNC enhanced leaf K+ retention and Na+ exclusion, but not vacuolar Na+ sequestration to enable better maintained cytosolic K+/Na+ homeostasis and thus to improve cotton salt tolerance. Our results add more knowledge for better understanding the complexity of plant-nanoceria interaction in terms of nano-enabled plant stress tolerance.

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Project description:The whole-cell voltage-clamp technique was used in rat cardiac myocytes to investigate the kinetics of ADP binding to phosphorylated states of Na,K-ATPase and its effects on presteady-state Na(+)-dependent charge movements by this enzyme. Ouabain-sensitive transient currents generated by Na,K-ATPase functioning in electroneutral Na(+)-Na(+) exchange mode were measured at 23 degrees C with pipette ADP concentrations ([ADP]) of up to 4.3 mM and extracellular Na(+) concentrations ([Na](o)) between 36 and 145 mM at membrane potentials (V(M)) from -160 to +80 mV. Analysis of charge-V(M) curves showed that the midpoint potential of charge distribution was shifted toward more positive V(M) both by increasing [ADP] at constant Na(+)(o) and by increasing [Na](o) at constant ADP. The total quantity of mobile charge, on the other hand, was found to be independent of changes in [ADP] or [Na](o). The presence of ADP increased the apparent rate constant for current relaxation at hyperpolarizing V(M) but decreased it at depolarizing V(M) as compared to control (no added ADP), an indication that ADP binding facilitates backward reaction steps during Na(+)-Na(+) exchange while slowing forward reactions. Data analysis using a pseudo three-state model yielded an apparent K(d) of approximately 6 mM for ADP binding to and release from the Na,K-ATPase phosphoenzyme; a value of 130 s(-1) for k(2), a rate constant that groups Na(+) deocclusion/release and the enzyme conformational transition E(1) approximately P --> E(2)-P; a value of 162 s(-1)M(-1) for k(-2), a lumped second-order V(M)-independent rate constant describing the reverse reactions; and a Hill coefficient of approximately 1 for Na(+)(o) binding to E(2)-P. The results are consistent with electroneutral release of ADP before Na(+) is deoccluded and released through an ion well. The same approach can be used to study additional charge-moving reactions and associated electrically silent steps of the Na,K-pump and other transporters.

Dataset Information

GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion.

Publications

GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion.

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