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Two Groups of Thellungiella salsuginea RAVs Exhibit Distinct Responses and Sensitivity to Salt and ABA in Transgenic Arabidopsis.

Yang S, Luo C, Song Y, Wang J - PLoS ONE (2016)

Bottom Line: Under normal conditions, the germination process of all TsRAVs overexpressing transgenic seeds was inhibited with a stronger effect observed in 35S:A-TsRAVs seeds than in 35S:B-TsRAVs seeds.All 35S:TsRAVs transgenic plants showed a similar degree of reduction in root growth compared with untreated seedlings in the presence of ABA.Taken together, our results suggest that two groups of TsRAVs perform distinct regulating roles during plant growth and abiotic defense including drought and salt, and A-TsRAVs are more likely than B-TsRAVs to act as negative regulators in the above-mentioned biological processes.

View Article: PubMed Central - PubMed

Affiliation: School of Environmental Science and Engineering, Tianjin University, Tianjin, 300072, China.

ABSTRACT
Containing both AP2 domain and B3 domain, RAV (Related to ABI3/VP1) transcription factors are involved in diverse functions in higher plants. A total of eight TsRAV genes were isolated from the genome of Thellungiella salsuginea and could be divided into two groups (A- and B-group) based on their sequence similarity. The mRNA abundance of all Thellungiella salsuginea TsRAVs followed a gradual decline during seed germination. In Thellungiella salsuginea seedling, transcripts of TsRAVs in the group A (A-TsRAVs) were gradually and moderately reduced by salt treatment but rapidly and severely repressed by ABA treatment. In comparison, with a barely detectable constitutive expression, the transcriptional level of TsRAVs in the group B (B-TsRAVs) exhibited a moderate induction in cotyledons when confronted with ABA. We then produced the "gain-of-function" transgenic Arabidopsis plants for each TsRAV gene and found that only 35S:A-TsRAVs showed weak growth retardation including reduced root elongation, suggesting their roles in negatively controlling plant growth. Under normal conditions, the germination process of all TsRAVs overexpressing transgenic seeds was inhibited with a stronger effect observed in 35S:A-TsRAVs seeds than in 35S:B-TsRAVs seeds. With the presence of NaCl, seed germination and seedling root elongation of all plants including wild type and 35S:TsRAVs plants were retarded and a more severe inhibition occurred to the 35S:A-TsRAV transgenic plants. ABA treatment only negatively affected the germination rates of 35S:A-TsRAV transgenic seeds but not those of 35S:B-TsRAV transgenic seeds. All 35S:TsRAVs transgenic plants showed a similar degree of reduction in root growth compared with untreated seedlings in the presence of ABA. Furthermore, the cotyledon greening/expansion was more severely inhibited 35S:A-TsRAVs than in 35S:B-TsRAVs seedlings. Upon water deficiency, with a wider opening of stomata, 35S:A-TsRAVs plants experienced a faster transpirational water loss than wild type and 35S:B-TsRAVs lines. Taken together, our results suggest that two groups of TsRAVs perform distinct regulating roles during plant growth and abiotic defense including drought and salt, and A-TsRAVs are more likely than B-TsRAVs to act as negative regulators in the above-mentioned biological processes.

No MeSH data available.


Related in: MedlinePlus

Different water loss rates of wild-type and 35S:TsRAVs transgenic Arabidopsis plants.(A) Weight loss in fresh leaves under water deficit of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates. (B) Width/length ratio of the rosette leaf stomatal aperture of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates and different letters indicate significant differences among means (P<0.05 by Tukey’s test).
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pone.0153517.g007: Different water loss rates of wild-type and 35S:TsRAVs transgenic Arabidopsis plants.(A) Weight loss in fresh leaves under water deficit of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates. (B) Width/length ratio of the rosette leaf stomatal aperture of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates and different letters indicate significant differences among means (P<0.05 by Tukey’s test).

Mentions: Water stress can induce the synthesis of ABA within plants and ABA acts directly on guard cells to induce stomatal closure and minimize water loss through transpiration [47]. Previously, transgenic plants overexpressing pepper RAV1 have been shown to be more tolerant to water stress [10], whereas AtRAVs-overexpressing transgenic plants have been reported to exhibit higher transpirational water loss than wild type [4]. Thus, we cut leaves from the 4-week soil-grown 35S:TsRAVs transgenic plants, placed them on a filter paper in an ambient temperature and measured the transpirational water loss over a 3-hour period. Our results showed that 35S:A-TsRAVs experienced a significantly faster water loss than both wild type and 35S:B-TsRAVs plants (Fig 7A). Since water loss of leaves is associated with the ABA-regulated stomatal movement, which is one of the appropriate criteria to check the ABA sensitivity, we then analyzed the stomatal opening of TsRAVs-overexpressing transgenic plants in parallel with wild type plants. Under same conditions, a wider opening of stomata was detected in 35S:A-TsRAVs transgenic plants than both wild type and 35S:B-TsRAVs transgenic plants (Fig 7B), indicating that constitutive overexpression of A-TsRAVs, but not B-TsRAVs could result in a wider stomatal opening, an increased transpiration rate, and a comprised drought tolerance, which was consistent with the previous notion that a faster water loss in RAV1-overexpressing plants was caused by the incapacity of stomata of to respond to ABA [4].


Two Groups of Thellungiella salsuginea RAVs Exhibit Distinct Responses and Sensitivity to Salt and ABA in Transgenic Arabidopsis.

Yang S, Luo C, Song Y, Wang J - PLoS ONE (2016)

Different water loss rates of wild-type and 35S:TsRAVs transgenic Arabidopsis plants.(A) Weight loss in fresh leaves under water deficit of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates. (B) Width/length ratio of the rosette leaf stomatal aperture of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates and different letters indicate significant differences among means (P<0.05 by Tukey’s test).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4836749&req=5

pone.0153517.g007: Different water loss rates of wild-type and 35S:TsRAVs transgenic Arabidopsis plants.(A) Weight loss in fresh leaves under water deficit of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates. (B) Width/length ratio of the rosette leaf stomatal aperture of 4-week-old wild-type and 35S:TsRAVs transgenic Arabidopsis plants. Each data bar represents the mean ± SE of three replicates and different letters indicate significant differences among means (P<0.05 by Tukey’s test).
Mentions: Water stress can induce the synthesis of ABA within plants and ABA acts directly on guard cells to induce stomatal closure and minimize water loss through transpiration [47]. Previously, transgenic plants overexpressing pepper RAV1 have been shown to be more tolerant to water stress [10], whereas AtRAVs-overexpressing transgenic plants have been reported to exhibit higher transpirational water loss than wild type [4]. Thus, we cut leaves from the 4-week soil-grown 35S:TsRAVs transgenic plants, placed them on a filter paper in an ambient temperature and measured the transpirational water loss over a 3-hour period. Our results showed that 35S:A-TsRAVs experienced a significantly faster water loss than both wild type and 35S:B-TsRAVs plants (Fig 7A). Since water loss of leaves is associated with the ABA-regulated stomatal movement, which is one of the appropriate criteria to check the ABA sensitivity, we then analyzed the stomatal opening of TsRAVs-overexpressing transgenic plants in parallel with wild type plants. Under same conditions, a wider opening of stomata was detected in 35S:A-TsRAVs transgenic plants than both wild type and 35S:B-TsRAVs transgenic plants (Fig 7B), indicating that constitutive overexpression of A-TsRAVs, but not B-TsRAVs could result in a wider stomatal opening, an increased transpiration rate, and a comprised drought tolerance, which was consistent with the previous notion that a faster water loss in RAV1-overexpressing plants was caused by the incapacity of stomata of to respond to ABA [4].

Bottom Line: Under normal conditions, the germination process of all TsRAVs overexpressing transgenic seeds was inhibited with a stronger effect observed in 35S:A-TsRAVs seeds than in 35S:B-TsRAVs seeds.All 35S:TsRAVs transgenic plants showed a similar degree of reduction in root growth compared with untreated seedlings in the presence of ABA.Taken together, our results suggest that two groups of TsRAVs perform distinct regulating roles during plant growth and abiotic defense including drought and salt, and A-TsRAVs are more likely than B-TsRAVs to act as negative regulators in the above-mentioned biological processes.

View Article: PubMed Central - PubMed

Affiliation: School of Environmental Science and Engineering, Tianjin University, Tianjin, 300072, China.

ABSTRACT
Containing both AP2 domain and B3 domain, RAV (Related to ABI3/VP1) transcription factors are involved in diverse functions in higher plants. A total of eight TsRAV genes were isolated from the genome of Thellungiella salsuginea and could be divided into two groups (A- and B-group) based on their sequence similarity. The mRNA abundance of all Thellungiella salsuginea TsRAVs followed a gradual decline during seed germination. In Thellungiella salsuginea seedling, transcripts of TsRAVs in the group A (A-TsRAVs) were gradually and moderately reduced by salt treatment but rapidly and severely repressed by ABA treatment. In comparison, with a barely detectable constitutive expression, the transcriptional level of TsRAVs in the group B (B-TsRAVs) exhibited a moderate induction in cotyledons when confronted with ABA. We then produced the "gain-of-function" transgenic Arabidopsis plants for each TsRAV gene and found that only 35S:A-TsRAVs showed weak growth retardation including reduced root elongation, suggesting their roles in negatively controlling plant growth. Under normal conditions, the germination process of all TsRAVs overexpressing transgenic seeds was inhibited with a stronger effect observed in 35S:A-TsRAVs seeds than in 35S:B-TsRAVs seeds. With the presence of NaCl, seed germination and seedling root elongation of all plants including wild type and 35S:TsRAVs plants were retarded and a more severe inhibition occurred to the 35S:A-TsRAV transgenic plants. ABA treatment only negatively affected the germination rates of 35S:A-TsRAV transgenic seeds but not those of 35S:B-TsRAV transgenic seeds. All 35S:TsRAVs transgenic plants showed a similar degree of reduction in root growth compared with untreated seedlings in the presence of ABA. Furthermore, the cotyledon greening/expansion was more severely inhibited 35S:A-TsRAVs than in 35S:B-TsRAVs seedlings. Upon water deficiency, with a wider opening of stomata, 35S:A-TsRAVs plants experienced a faster transpirational water loss than wild type and 35S:B-TsRAVs lines. Taken together, our results suggest that two groups of TsRAVs perform distinct regulating roles during plant growth and abiotic defense including drought and salt, and A-TsRAVs are more likely than B-TsRAVs to act as negative regulators in the above-mentioned biological processes.

No MeSH data available.


Related in: MedlinePlus