GABA operates upstream of H⁺-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K⁺ retention and Na⁺ exclusion
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 a...
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| Published in | Journal of experimental botany Vol. 70; no. 21; pp. 6349 - 6361 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
UK
Oxford University Press
18.11.2019
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| Abstract | 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 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. |
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| AbstractList | GABA has beneficial effects on salinity stress tolerance in Arabidopsis linked to increased activity of H+-ATPase, reduced ROS-induced K+ efflux from root epidermis, and increased SOS1 and NHX1 transcript levels in plant roots.
Abstract
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 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. 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 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. GABA has beneficial effects on salinity stress tolerance in Arabidopsis linked to increased activity of H+-ATPase, reduced ROS-induced K+ efflux from root epidermis, and increased SOS1 and NHX1 transcript levels in plant roots. GABA has beneficial effects on salinity stress tolerance in Arabidopsis linked to increased activity of H + -ATPase, reduced ROS-induced K + efflux from root epidermis, and increased SOS1 and NHX1 transcript levels in plant roots. 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 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 H 2 O 2 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. 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 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.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 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. The non-protein gamma-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to salinity. However, the physiological rationale beyond this elevation remains elusive. This study compared electrophysiological and whole-plant responses of salt-treated Arabidopsis thaliana mutants pop2-5 and gad1,2 that possess different abilities for GABA accumulation. The pop2-5 mutant that was capable to over-accumulate GABA in its roots showed a salt-tolerant phenotype. On the contrary, gad1,2 mutant lacking an ability for conversion of glutamate to GABA showed over-sensitivity to salinity. The differential salinity tolerance between two lines was explained by: (1) the role of GABA in the stress-induced activation of H+-ATPase thus leading to better membrane potential maintenance and reduced extent of stress-induced K+ leak from roots; (2) reduced rates of net Na+ uptake in pop2-5 roots; (3) higher expression of SOS1 and NHX1 genes in leaves of salt-tolerant pop2-5 plants, which contributed to reducing Na+ concentration in the cytoplasm by excluding Na+ to apoplast and sequestering Na+ in vacuole; (4) lower rate of H2O2 production and reduced ROS-inducible K+ efflux from root epidermis in the tolerant line; and (5) better K+ retention in the shoot associated with the lower expression level of GORK channels in plant leaves. |
| Author | Wu, Qi Qu, Mei Chen, Jiahui Cui, Jin Shabala, Sergey Mithöfer, Axel Su, Nana Shabala, Lana Wang, Haiyang Yu, Min |
| AuthorAffiliation | 5 Oklahoma State University , USA 1 College of Life Sciences, Nanjing Agricultural University , Nanjing 210095, China 4 Research Group of Plant Defense Physiology, Max Planck Institute for Chemical Ecology , D-07745 Jena, Germany 2 Tasmanian Institute for Agriculture, College of Science and Engineering, University of Tasmania , Hobart, Tasmania 7001, Australia 3 International Research Centre for Environmental Membrane Biology, Foshan University , Foshan 528000, China |
| AuthorAffiliation_xml | – name: 4 Research Group of Plant Defense Physiology, Max Planck Institute for Chemical Ecology , D-07745 Jena, Germany – name: 5 Oklahoma State University , USA – name: 3 International Research Centre for Environmental Membrane Biology, Foshan University , Foshan 528000, China – name: 2 Tasmanian Institute for Agriculture, College of Science and Engineering, University of Tasmania , Hobart, Tasmania 7001, Australia – name: 1 College of Life Sciences, Nanjing Agricultural University , Nanjing 210095, China |
| Author_xml | – sequence: 1 givenname: Nana surname: Su fullname: Su, Nana – sequence: 2 givenname: Qi surname: Wu fullname: Wu, Qi – sequence: 3 givenname: Jiahui surname: Chen fullname: Chen, Jiahui – sequence: 4 givenname: Lana surname: Shabala fullname: Shabala, Lana – sequence: 5 givenname: Axel surname: Mithöfer fullname: Mithöfer, Axel – sequence: 6 givenname: Haiyang surname: Wang fullname: Wang, Haiyang – sequence: 7 givenname: Mei surname: Qu fullname: Qu, Mei – sequence: 8 givenname: Min surname: Yu fullname: Yu, Min – sequence: 9 givenname: Jin surname: Cui fullname: Cui, Jin – sequence: 10 givenname: Sergey surname: Shabala fullname: Shabala, Sergey |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31420662$$D View this record in MEDLINE/PubMed |
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| Snippet | The non-protein amino acid γ-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to salinity. However, the physiological rationale for... GABA has beneficial effects on salinity stress tolerance in Arabidopsis linked to increased activity of H+-ATPase, reduced ROS-induced K+ efflux from root... The non-protein gamma-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to salinity. However, the physiological rationale beyond this... GABA has beneficial effects on salinity stress tolerance in Arabidopsis linked to increased activity of H + -ATPase, reduced ROS-induced K + efflux from root... |
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| Title | GABA operates upstream of H⁺-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K⁺ retention and Na⁺ exclusion |
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