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Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex.

Colaneri AC, Tunc-Ozdemir M, Huang JP, Jones AM - BMC Plant Biol. (2014)

Bottom Line: Glucose in the growth media improved the survival under salt stress in Col but not in agb1-2 or rgs1-2 mutants.These results demonstrate a direct role for G-protein signaling in the plant growth response to salt stress.The phenotypes of the loss-of-function mutations prompted the model that during salt stress, G activation promotes growth and attenuates senescence probably by releasing ER stress.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill NC, 27599, USA. alan_jones@unc.edu.

ABSTRACT

Background: Plant growth is plastic, able to rapidly adjust to fluctuation in environmental conditions such as drought and salinity. Due to long-term irrigation use in agricultural systems, soil salinity is increasing; consequently crop yield is adversely affected. It is known that salt tolerance is a quantitative trait supported by genes affecting ion homeostasis, ion transport, ion compartmentalization and ion selectivity. Less is known about pathways connecting NaCl and cell proliferation and cell death. Plant growth and cell proliferation is, in part, controlled by the concerted activity of the heterotrimeric G-protein complex with glucose. Prompted by the abundance of stress-related, functional annotations of genes encoding proteins that interact with core components of the Arabidopsis heterotrimeric G protein complex (AtRGS1, AtGPA1, AGB1, and AGG), we tested the hypothesis that G proteins modulate plant growth under salt stress.

Results: Na+ activates G signaling as quantitated by internalization of Arabidopsis Regulator of G Signaling protein 1 (AtRGS1). Despite being components of a singular signaling complex loss of the Gβ subunit (agb1-2 mutant) conferred accelerated senescence and aborted development in the presence of Na+, whereas loss of AtRGS1 (rgs1-2 mutant) conferred Na+ tolerance evident as less attenuated shoot growth and senescence. Site-directed changes in the Gα and Gβγ protein-protein interface were made to disrupt the interaction between the Gα and Gβγ subunits in order to elevate free activated Gα subunit and free Gβγ dimer at the plasma membrane. These mutations conferred sodium tolerance. Glucose in the growth media improved the survival under salt stress in Col but not in agb1-2 or rgs1-2 mutants.

Conclusions: These results demonstrate a direct role for G-protein signaling in the plant growth response to salt stress. The contrasting phenotypes of agb1-2 and rgs1-2 mutants suggest that G-proteins balance growth and death under salt stress. The phenotypes of the loss-of-function mutations prompted the model that during salt stress, G activation promotes growth and attenuates senescence probably by releasing ER stress.

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Genetic characterization of G-protein signaling under hypersaline/hyperosmotic stress. Arabidopsis seeds from each genotype were germinated and seedlings grown on ¼ MS agar media supplemented with 100 mM NaCl. Green seedlings were counted 10 d after germination. Error bars represent the standard deviation calculated from triplicates. Pair wise comparisons between the means were done with t-tests at a confidence level (CL) of 90% and 95%. “a” indicates that the mean for rgs1-2 differs from Col-0 or rgs1-2/agb1-2 double mutant (CL 95%, p-values = 0.002 and 0.005 respectively). “b” indicates gpa1-4 and Col 0 have different means (CL 95%, p-value = 0.02). Results are representative of three different experiments. “c” indicates that the means of these genotypes were compared with all the other genotypes and always resulted in statistical significant differences between them and all other genotypes not denoted with “c” at a CL of 95% (p value < 0.05). “d” indicates that agg1-1 and agg2-1 have different means (CL 90%, p-value = 0.051).
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Figure 3: Genetic characterization of G-protein signaling under hypersaline/hyperosmotic stress. Arabidopsis seeds from each genotype were germinated and seedlings grown on ¼ MS agar media supplemented with 100 mM NaCl. Green seedlings were counted 10 d after germination. Error bars represent the standard deviation calculated from triplicates. Pair wise comparisons between the means were done with t-tests at a confidence level (CL) of 90% and 95%. “a” indicates that the mean for rgs1-2 differs from Col-0 or rgs1-2/agb1-2 double mutant (CL 95%, p-values = 0.002 and 0.005 respectively). “b” indicates gpa1-4 and Col 0 have different means (CL 95%, p-value = 0.02). Results are representative of three different experiments. “c” indicates that the means of these genotypes were compared with all the other genotypes and always resulted in statistical significant differences between them and all other genotypes not denoted with “c” at a CL of 95% (p value < 0.05). “d” indicates that agg1-1 and agg2-1 have different means (CL 90%, p-value = 0.051).

Mentions: Seedlings lacking the Gα subunit (gpa1-4) behaved similarly to rgs1 mutants (Figure 3) consistent with AtRGS1 signaling operating through its cognate Gα subunit (t-test, p-value = 0.02, CL 95%). It also suggests that the primary signaling element is the Gβγ dimer since loss of either AtRGS1 or AtGPA1 increases the pool size of freed Gβγ dimer at the plasma membrane. As expected, when all three of the Gγ subunits are genetically deleted thus removing AGB1 from the plasma membrane, plants had the agb1-2 phenotype. Loss of either AGG1 or AGG2 had little or no effect suggesting functional redundancy or that AGB1 dimers comprised with AGG1 or AGG2 are not involved in the Na+ response. The agb1-2 allele was epistatic to the rgs1-2 allele consistent with AGB1 acting downstream of AtRGS1 (Figure 3). Like rgs1-2 mutants, fewer gpa1-4 seedlings were arrested on 100 mM NaCl compared to Col-0, however they were 30% smaller than rgs1-2 (t-test, p-value = 0.0005, confidence level = 95%), thus the gpa1 “salt” phenotype is not exactly like the rgs1 phenotype.


Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex.

Colaneri AC, Tunc-Ozdemir M, Huang JP, Jones AM - BMC Plant Biol. (2014)

Genetic characterization of G-protein signaling under hypersaline/hyperosmotic stress. Arabidopsis seeds from each genotype were germinated and seedlings grown on ¼ MS agar media supplemented with 100 mM NaCl. Green seedlings were counted 10 d after germination. Error bars represent the standard deviation calculated from triplicates. Pair wise comparisons between the means were done with t-tests at a confidence level (CL) of 90% and 95%. “a” indicates that the mean for rgs1-2 differs from Col-0 or rgs1-2/agb1-2 double mutant (CL 95%, p-values = 0.002 and 0.005 respectively). “b” indicates gpa1-4 and Col 0 have different means (CL 95%, p-value = 0.02). Results are representative of three different experiments. “c” indicates that the means of these genotypes were compared with all the other genotypes and always resulted in statistical significant differences between them and all other genotypes not denoted with “c” at a CL of 95% (p value < 0.05). “d” indicates that agg1-1 and agg2-1 have different means (CL 90%, p-value = 0.051).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4061919&req=5

Figure 3: Genetic characterization of G-protein signaling under hypersaline/hyperosmotic stress. Arabidopsis seeds from each genotype were germinated and seedlings grown on ¼ MS agar media supplemented with 100 mM NaCl. Green seedlings were counted 10 d after germination. Error bars represent the standard deviation calculated from triplicates. Pair wise comparisons between the means were done with t-tests at a confidence level (CL) of 90% and 95%. “a” indicates that the mean for rgs1-2 differs from Col-0 or rgs1-2/agb1-2 double mutant (CL 95%, p-values = 0.002 and 0.005 respectively). “b” indicates gpa1-4 and Col 0 have different means (CL 95%, p-value = 0.02). Results are representative of three different experiments. “c” indicates that the means of these genotypes were compared with all the other genotypes and always resulted in statistical significant differences between them and all other genotypes not denoted with “c” at a CL of 95% (p value < 0.05). “d” indicates that agg1-1 and agg2-1 have different means (CL 90%, p-value = 0.051).
Mentions: Seedlings lacking the Gα subunit (gpa1-4) behaved similarly to rgs1 mutants (Figure 3) consistent with AtRGS1 signaling operating through its cognate Gα subunit (t-test, p-value = 0.02, CL 95%). It also suggests that the primary signaling element is the Gβγ dimer since loss of either AtRGS1 or AtGPA1 increases the pool size of freed Gβγ dimer at the plasma membrane. As expected, when all three of the Gγ subunits are genetically deleted thus removing AGB1 from the plasma membrane, plants had the agb1-2 phenotype. Loss of either AGG1 or AGG2 had little or no effect suggesting functional redundancy or that AGB1 dimers comprised with AGG1 or AGG2 are not involved in the Na+ response. The agb1-2 allele was epistatic to the rgs1-2 allele consistent with AGB1 acting downstream of AtRGS1 (Figure 3). Like rgs1-2 mutants, fewer gpa1-4 seedlings were arrested on 100 mM NaCl compared to Col-0, however they were 30% smaller than rgs1-2 (t-test, p-value = 0.0005, confidence level = 95%), thus the gpa1 “salt” phenotype is not exactly like the rgs1 phenotype.

Bottom Line: Glucose in the growth media improved the survival under salt stress in Col but not in agb1-2 or rgs1-2 mutants.These results demonstrate a direct role for G-protein signaling in the plant growth response to salt stress.The phenotypes of the loss-of-function mutations prompted the model that during salt stress, G activation promotes growth and attenuates senescence probably by releasing ER stress.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill NC, 27599, USA. alan_jones@unc.edu.

ABSTRACT

Background: Plant growth is plastic, able to rapidly adjust to fluctuation in environmental conditions such as drought and salinity. Due to long-term irrigation use in agricultural systems, soil salinity is increasing; consequently crop yield is adversely affected. It is known that salt tolerance is a quantitative trait supported by genes affecting ion homeostasis, ion transport, ion compartmentalization and ion selectivity. Less is known about pathways connecting NaCl and cell proliferation and cell death. Plant growth and cell proliferation is, in part, controlled by the concerted activity of the heterotrimeric G-protein complex with glucose. Prompted by the abundance of stress-related, functional annotations of genes encoding proteins that interact with core components of the Arabidopsis heterotrimeric G protein complex (AtRGS1, AtGPA1, AGB1, and AGG), we tested the hypothesis that G proteins modulate plant growth under salt stress.

Results: Na+ activates G signaling as quantitated by internalization of Arabidopsis Regulator of G Signaling protein 1 (AtRGS1). Despite being components of a singular signaling complex loss of the Gβ subunit (agb1-2 mutant) conferred accelerated senescence and aborted development in the presence of Na+, whereas loss of AtRGS1 (rgs1-2 mutant) conferred Na+ tolerance evident as less attenuated shoot growth and senescence. Site-directed changes in the Gα and Gβγ protein-protein interface were made to disrupt the interaction between the Gα and Gβγ subunits in order to elevate free activated Gα subunit and free Gβγ dimer at the plasma membrane. These mutations conferred sodium tolerance. Glucose in the growth media improved the survival under salt stress in Col but not in agb1-2 or rgs1-2 mutants.

Conclusions: These results demonstrate a direct role for G-protein signaling in the plant growth response to salt stress. The contrasting phenotypes of agb1-2 and rgs1-2 mutants suggest that G-proteins balance growth and death under salt stress. The phenotypes of the loss-of-function mutations prompted the model that during salt stress, G activation promotes growth and attenuates senescence probably by releasing ER stress.

Show MeSH
Related in: MedlinePlus