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A nuclear calcium-sensing pathway is critical for gene regulation and salt stress tolerance in Arabidopsis.

Guan Q, Wu J, Yue X, Zhang Y, Zhu J - PLoS Genet. (2013)

Bottom Line: Through a forward genetic screen, we found a nuclear-localized calcium-binding protein, RSA1 (SHORT ROOT IN SALT MEDIUM 1), which is required for salt tolerance, and identified its interacting partner, RITF1, a bHLH transcription factor.We show that RSA1 and RITF1 regulate the transcription of several genes involved in the detoxification of reactive oxygen species generated by salt stress and that they also regulate the SOS1 gene that encodes a plasma membrane Na(+)/H(+) antiporter essential for salt tolerance.Together, our results suggest the existence of a novel nuclear calcium-sensing and -signaling pathway that is important for gene regulation and salt stress tolerance.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland, United States of America.

ABSTRACT
Salt stress is an important environmental factor that significantly limits crop productivity worldwide. Studies on responses of plants to salt stress in recent years have identified novel signaling pathways and have been at the forefront of plant stress biology and plant biology in general. Thus far, research on salt stress in plants has been focused on cytoplasmic signaling pathways. In this study, we discovered a nuclear calcium-sensing and signaling pathway that is critical for salt stress tolerance in the reference plant Arabidopsis. Through a forward genetic screen, we found a nuclear-localized calcium-binding protein, RSA1 (SHORT ROOT IN SALT MEDIUM 1), which is required for salt tolerance, and identified its interacting partner, RITF1, a bHLH transcription factor. We show that RSA1 and RITF1 regulate the transcription of several genes involved in the detoxification of reactive oxygen species generated by salt stress and that they also regulate the SOS1 gene that encodes a plasma membrane Na(+)/H(+) antiporter essential for salt tolerance. Together, our results suggest the existence of a novel nuclear calcium-sensing and -signaling pathway that is important for gene regulation and salt stress tolerance.

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ritf1 mutant plants are sensitive to salt and oxidative stresses, and overexpression of RITF1 increases plant tolerance to salt and oxidative stresses.(A) Seed germination of wild type and ritf1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. (B) Fresh weight of wild-type and ritf1 seedlings under salt stress. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 7 d. (C) Growth responses of wild-type and ritf1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). (D) and (E) Fresh weight of seedlings grown on MS medium containing various levels of H2O2 (D) or MV (E) as shown in (C). (F) Salt tolerance of RITF1 overexpression plants. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 10 d. (G) and (H) Fresh weight of wild-type and RITF1 overexpression plants grown on MS medium containing various levels of H2O2 (G) or MV (H). In (C)–(E), (G), and (H), seeds were sown directly on MS medium supplemented with various levels of H2O2 or MV and allowed to grow for an additional 10 d. Error bars represent the standard deviation (n = 8 in [A], 40 in [B], [D]–[H]). One-way ANOVA (Tukey-Kramer test) was performed, and statistically significant differences are indicated by different lowercase letters (p<0.05). The experiments in Figure 5 were repeated at least four times with similar results, and data from one representative experiment are presented.
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pgen-1003755-g005: ritf1 mutant plants are sensitive to salt and oxidative stresses, and overexpression of RITF1 increases plant tolerance to salt and oxidative stresses.(A) Seed germination of wild type and ritf1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. (B) Fresh weight of wild-type and ritf1 seedlings under salt stress. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 7 d. (C) Growth responses of wild-type and ritf1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). (D) and (E) Fresh weight of seedlings grown on MS medium containing various levels of H2O2 (D) or MV (E) as shown in (C). (F) Salt tolerance of RITF1 overexpression plants. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 10 d. (G) and (H) Fresh weight of wild-type and RITF1 overexpression plants grown on MS medium containing various levels of H2O2 (G) or MV (H). In (C)–(E), (G), and (H), seeds were sown directly on MS medium supplemented with various levels of H2O2 or MV and allowed to grow for an additional 10 d. Error bars represent the standard deviation (n = 8 in [A], 40 in [B], [D]–[H]). One-way ANOVA (Tukey-Kramer test) was performed, and statistically significant differences are indicated by different lowercase letters (p<0.05). The experiments in Figure 5 were repeated at least four times with similar results, and data from one representative experiment are presented.

Mentions: qRT-PCR analysis indicated that RITF1 is slightly inducible by salt stress (Figure 4F). We obtained the T-DNA knockdown plants of RITF1 (ritf1) (Figure S4B). The ritf1 plants are substantially more sensitive to salt stress than wild-type plants during seed germination and during seedling growth and development (Figure 5A and 5B). We further observed that ritf1 plants are more sensitive to oxidative stress imposed by H2O2 or MV than the wild type (Figure 5C–5E). We overexpressed RITF1 in Arabidopsis (Figure S4C), and all of the RITF1 overexpression plants displayed increased tolerance to NaCl and the oxidative stress-inducing reagents H2O2 and MV (Figure 5F–5H). These results suggest that the RSA1 interacting transcription factor, RITF1, is required for plant tolerance to salt and oxidative stresses.


A nuclear calcium-sensing pathway is critical for gene regulation and salt stress tolerance in Arabidopsis.

Guan Q, Wu J, Yue X, Zhang Y, Zhu J - PLoS Genet. (2013)

ritf1 mutant plants are sensitive to salt and oxidative stresses, and overexpression of RITF1 increases plant tolerance to salt and oxidative stresses.(A) Seed germination of wild type and ritf1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. (B) Fresh weight of wild-type and ritf1 seedlings under salt stress. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 7 d. (C) Growth responses of wild-type and ritf1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). (D) and (E) Fresh weight of seedlings grown on MS medium containing various levels of H2O2 (D) or MV (E) as shown in (C). (F) Salt tolerance of RITF1 overexpression plants. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 10 d. (G) and (H) Fresh weight of wild-type and RITF1 overexpression plants grown on MS medium containing various levels of H2O2 (G) or MV (H). In (C)–(E), (G), and (H), seeds were sown directly on MS medium supplemented with various levels of H2O2 or MV and allowed to grow for an additional 10 d. Error bars represent the standard deviation (n = 8 in [A], 40 in [B], [D]–[H]). One-way ANOVA (Tukey-Kramer test) was performed, and statistically significant differences are indicated by different lowercase letters (p<0.05). The experiments in Figure 5 were repeated at least four times with similar results, and data from one representative experiment are presented.
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Related In: Results  -  Collection

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pgen-1003755-g005: ritf1 mutant plants are sensitive to salt and oxidative stresses, and overexpression of RITF1 increases plant tolerance to salt and oxidative stresses.(A) Seed germination of wild type and ritf1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. (B) Fresh weight of wild-type and ritf1 seedlings under salt stress. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 7 d. (C) Growth responses of wild-type and ritf1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). (D) and (E) Fresh weight of seedlings grown on MS medium containing various levels of H2O2 (D) or MV (E) as shown in (C). (F) Salt tolerance of RITF1 overexpression plants. Five-d-old seedlings grown on MS medium were transferred to MS medium containing 0 or 100 mM NaCl and allowed to grow for an additional 10 d. (G) and (H) Fresh weight of wild-type and RITF1 overexpression plants grown on MS medium containing various levels of H2O2 (G) or MV (H). In (C)–(E), (G), and (H), seeds were sown directly on MS medium supplemented with various levels of H2O2 or MV and allowed to grow for an additional 10 d. Error bars represent the standard deviation (n = 8 in [A], 40 in [B], [D]–[H]). One-way ANOVA (Tukey-Kramer test) was performed, and statistically significant differences are indicated by different lowercase letters (p<0.05). The experiments in Figure 5 were repeated at least four times with similar results, and data from one representative experiment are presented.
Mentions: qRT-PCR analysis indicated that RITF1 is slightly inducible by salt stress (Figure 4F). We obtained the T-DNA knockdown plants of RITF1 (ritf1) (Figure S4B). The ritf1 plants are substantially more sensitive to salt stress than wild-type plants during seed germination and during seedling growth and development (Figure 5A and 5B). We further observed that ritf1 plants are more sensitive to oxidative stress imposed by H2O2 or MV than the wild type (Figure 5C–5E). We overexpressed RITF1 in Arabidopsis (Figure S4C), and all of the RITF1 overexpression plants displayed increased tolerance to NaCl and the oxidative stress-inducing reagents H2O2 and MV (Figure 5F–5H). These results suggest that the RSA1 interacting transcription factor, RITF1, is required for plant tolerance to salt and oxidative stresses.

Bottom Line: Through a forward genetic screen, we found a nuclear-localized calcium-binding protein, RSA1 (SHORT ROOT IN SALT MEDIUM 1), which is required for salt tolerance, and identified its interacting partner, RITF1, a bHLH transcription factor.We show that RSA1 and RITF1 regulate the transcription of several genes involved in the detoxification of reactive oxygen species generated by salt stress and that they also regulate the SOS1 gene that encodes a plasma membrane Na(+)/H(+) antiporter essential for salt tolerance.Together, our results suggest the existence of a novel nuclear calcium-sensing and -signaling pathway that is important for gene regulation and salt stress tolerance.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland, United States of America.

ABSTRACT
Salt stress is an important environmental factor that significantly limits crop productivity worldwide. Studies on responses of plants to salt stress in recent years have identified novel signaling pathways and have been at the forefront of plant stress biology and plant biology in general. Thus far, research on salt stress in plants has been focused on cytoplasmic signaling pathways. In this study, we discovered a nuclear calcium-sensing and signaling pathway that is critical for salt stress tolerance in the reference plant Arabidopsis. Through a forward genetic screen, we found a nuclear-localized calcium-binding protein, RSA1 (SHORT ROOT IN SALT MEDIUM 1), which is required for salt tolerance, and identified its interacting partner, RITF1, a bHLH transcription factor. We show that RSA1 and RITF1 regulate the transcription of several genes involved in the detoxification of reactive oxygen species generated by salt stress and that they also regulate the SOS1 gene that encodes a plasma membrane Na(+)/H(+) antiporter essential for salt tolerance. Together, our results suggest the existence of a novel nuclear calcium-sensing and -signaling pathway that is important for gene regulation and salt stress tolerance.

Show MeSH