Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice Species

Soil salinity is a major constraint that affects plant growth and development. Rice is a staple food for more than half of the human population but is extremely sensitive to salinity. Among the several known mechanisms, the ability of the plant to exclude cytosolic Na<sup>+</sup> is stro...

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Main Authors: Babar Shahzad, Lana Shabala, Meixue Zhou, Gayatri Venkataraman, Celymar Angela Solis, David Page, Zhong-Hua Chen, Sergey Shabala
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/17/9900
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author Babar Shahzad
Lana Shabala
Meixue Zhou
Gayatri Venkataraman
Celymar Angela Solis
David Page
Zhong-Hua Chen
Sergey Shabala
author_facet Babar Shahzad
Lana Shabala
Meixue Zhou
Gayatri Venkataraman
Celymar Angela Solis
David Page
Zhong-Hua Chen
Sergey Shabala
author_sort Babar Shahzad
collection DOAJ
description Soil salinity is a major constraint that affects plant growth and development. Rice is a staple food for more than half of the human population but is extremely sensitive to salinity. Among the several known mechanisms, the ability of the plant to exclude cytosolic Na<sup>+</sup> is strongly correlated with salinity stress tolerance in different plant species. This exclusion is mediated by the plasma membrane (PM) Na<sup>+</sup>/H<sup>+</sup> antiporter encoded by <i>Salt Overly Sensitive</i> (<i>SOS1</i>) gene and driven by a PM H<sup>+</sup>-ATPase generated proton gradient. However, it is not clear to what extent this mechanism is operational in wild and cultivated rice species, given the unique rice root anatomy and the existence of the bypass flow for Na<sup>+</sup>. As wild rice species provide a rich source of genetic diversity for possible introgression of abiotic stress tolerance, we investigated physiological and molecular basis of salinity stress tolerance in <i>Oryza</i> species by using two contrasting pairs of cultivated (<i>Oryza sativa</i>) and wild rice species (<i>Oryza alta</i> and <i>Oryza punctata</i>). Accordingly, dose- and age-dependent Na<sup>+</sup> and H<sup>+</sup> fluxes were measured using a non-invasive ion selective vibrating microelectrode (the MIFE technique) to measure potential activity of <i>SOS1</i>-encoded Na<sup>+</sup>/H<sup>+</sup> antiporter genes. Consistent with GUS staining data reported in the literature, rice accessions had (~4–6-fold) greater net Na<sup>+</sup> efflux in the root elongation zone (EZ) compared to the mature root zone (MZ). Pharmacological experiments showed that Na<sup>+</sup> efflux in root EZ is suppressed by more than 90% by amiloride, indicating the possible involvement of Na<sup>+</sup>/H<sup>+</sup> exchanger activity in root EZ. Within each group (cultivated vs. wild) the magnitude of amiloride-sensitive Na<sup>+</sup> efflux was higher in tolerant genotypes; however, the activity of Na<sup>+</sup>/H<sup>+</sup> exchanger was 2–3-fold higher in the cultivated rice compared with their wild counterparts. Gene expression levels of <i>SOS1</i>, <i>SOS2</i> and <i>SOS3</i> were upregulated under 24 h salinity treatment in all the tested genotypes, with the highest level of <i>SOS1</i> transcript detected in salt-tolerant wild rice genotype <i>O. alta</i> (~5–6-fold increased transcript level) followed by another wild rice, <i>O. punctata</i>. There was no significant difference in <i>SOS1</i> expression observed for cultivated rice (IR1-tolerant and IR29-sensitive) under both 0 and 24 h salinity exposure. Our findings suggest that salt-tolerant cultivated rice relies on the cytosolic Na<sup>+</sup> exclusion mechanism to deal with salt stress to a greater extent than wild rice, but its operation seems to be regulated at a post-translational rather than transcriptional level.
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spelling doaj.art-0ceb37a079ca44e3a83a33886f1bc3872023-11-23T13:19:03ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-08-012317990010.3390/ijms23179900Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice SpeciesBabar Shahzad0Lana Shabala1Meixue Zhou2Gayatri Venkataraman3Celymar Angela Solis4David Page5Zhong-Hua Chen6Sergey Shabala7Tasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS 7001, AustraliaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS 7001, AustraliaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS 7001, AustraliaPlant Molecular Biology Laboratory, M. S. Swaminathan Research Foundation, III Cross Street, Taramani Institutional Area, Chennai 600113, IndiaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS 7001, AustraliaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS 7001, AustraliaSchool of Science, Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, AustraliaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS 7001, AustraliaSoil salinity is a major constraint that affects plant growth and development. Rice is a staple food for more than half of the human population but is extremely sensitive to salinity. Among the several known mechanisms, the ability of the plant to exclude cytosolic Na<sup>+</sup> is strongly correlated with salinity stress tolerance in different plant species. This exclusion is mediated by the plasma membrane (PM) Na<sup>+</sup>/H<sup>+</sup> antiporter encoded by <i>Salt Overly Sensitive</i> (<i>SOS1</i>) gene and driven by a PM H<sup>+</sup>-ATPase generated proton gradient. However, it is not clear to what extent this mechanism is operational in wild and cultivated rice species, given the unique rice root anatomy and the existence of the bypass flow for Na<sup>+</sup>. As wild rice species provide a rich source of genetic diversity for possible introgression of abiotic stress tolerance, we investigated physiological and molecular basis of salinity stress tolerance in <i>Oryza</i> species by using two contrasting pairs of cultivated (<i>Oryza sativa</i>) and wild rice species (<i>Oryza alta</i> and <i>Oryza punctata</i>). Accordingly, dose- and age-dependent Na<sup>+</sup> and H<sup>+</sup> fluxes were measured using a non-invasive ion selective vibrating microelectrode (the MIFE technique) to measure potential activity of <i>SOS1</i>-encoded Na<sup>+</sup>/H<sup>+</sup> antiporter genes. Consistent with GUS staining data reported in the literature, rice accessions had (~4–6-fold) greater net Na<sup>+</sup> efflux in the root elongation zone (EZ) compared to the mature root zone (MZ). Pharmacological experiments showed that Na<sup>+</sup> efflux in root EZ is suppressed by more than 90% by amiloride, indicating the possible involvement of Na<sup>+</sup>/H<sup>+</sup> exchanger activity in root EZ. Within each group (cultivated vs. wild) the magnitude of amiloride-sensitive Na<sup>+</sup> efflux was higher in tolerant genotypes; however, the activity of Na<sup>+</sup>/H<sup>+</sup> exchanger was 2–3-fold higher in the cultivated rice compared with their wild counterparts. Gene expression levels of <i>SOS1</i>, <i>SOS2</i> and <i>SOS3</i> were upregulated under 24 h salinity treatment in all the tested genotypes, with the highest level of <i>SOS1</i> transcript detected in salt-tolerant wild rice genotype <i>O. alta</i> (~5–6-fold increased transcript level) followed by another wild rice, <i>O. punctata</i>. There was no significant difference in <i>SOS1</i> expression observed for cultivated rice (IR1-tolerant and IR29-sensitive) under both 0 and 24 h salinity exposure. Our findings suggest that salt-tolerant cultivated rice relies on the cytosolic Na<sup>+</sup> exclusion mechanism to deal with salt stress to a greater extent than wild rice, but its operation seems to be regulated at a post-translational rather than transcriptional level.https://www.mdpi.com/1422-0067/23/17/9900Na<sup>+</sup> exclusion<i>Salt Overly Sensitive (SOS1)</i>salinity stress toleranceNa<sup>+</sup> sequestrationwild rice
spellingShingle Babar Shahzad
Lana Shabala
Meixue Zhou
Gayatri Venkataraman
Celymar Angela Solis
David Page
Zhong-Hua Chen
Sergey Shabala
Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice Species
International Journal of Molecular Sciences
Na<sup>+</sup> exclusion
<i>Salt Overly Sensitive (SOS1)</i>
salinity stress tolerance
Na<sup>+</sup> sequestration
wild rice
title Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice Species
title_full Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice Species
title_fullStr Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice Species
title_full_unstemmed Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice Species
title_short Comparing Essentiality of <i>SOS1</i>-Mediated Na<sup>+</sup> Exclusion in Salinity Tolerance between Cultivated and Wild Rice Species
title_sort comparing essentiality of i sos1 i mediated na sup sup exclusion in salinity tolerance between cultivated and wild rice species
topic Na<sup>+</sup> exclusion
<i>Salt Overly Sensitive (SOS1)</i>
salinity stress tolerance
Na<sup>+</sup> sequestration
wild rice
url https://www.mdpi.com/1422-0067/23/17/9900
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