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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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rsa1-1 plants are hypersensitive to NaCl, and RSA1 is involved in Na+ homeostasis under salt stress.(A)–(C) Five-d-old wild-type and rsa1-1 seedlings grown on MS medium were transferred to MS medium supplemented with different levels of NaCl and allowed to grow for an additional 8 d. Root elongation or shoot fresh weight was measured and is shown as a percentage relative to growth on normal MS medium. (D) Two-week-old wild-type and rsa1-1 plants grown in soil were irrigated with 300 mM NaCl for 0 or 14 d. (E) Survival rate of wild-type and rsa1-1 plants as shown in (D). (F) Seed germination of wild type and rsa1-1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. Seeds in which the radical had emerged through the seed coat were considered germinated. (G) Na+ content in soil-grown wild-type and rsa1-1 plants. DW, dry weight. (H) K+ content in soil-grown wild-type and rsa1-1 plants. (I) Ratio of Na+ to K+ accumulation in soil-grown wild-type and rsa1-1 plants. WT, wild type. Error bars indicate the standard deviation (n = 30–40). The experiments in Figure 1 were repeated at least five times with similar results, and data from one representative experiment are presented.
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pgen-1003755-g001: rsa1-1 plants are hypersensitive to NaCl, and RSA1 is involved in Na+ homeostasis under salt stress.(A)–(C) Five-d-old wild-type and rsa1-1 seedlings grown on MS medium were transferred to MS medium supplemented with different levels of NaCl and allowed to grow for an additional 8 d. Root elongation or shoot fresh weight was measured and is shown as a percentage relative to growth on normal MS medium. (D) Two-week-old wild-type and rsa1-1 plants grown in soil were irrigated with 300 mM NaCl for 0 or 14 d. (E) Survival rate of wild-type and rsa1-1 plants as shown in (D). (F) Seed germination of wild type and rsa1-1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. Seeds in which the radical had emerged through the seed coat were considered germinated. (G) Na+ content in soil-grown wild-type and rsa1-1 plants. DW, dry weight. (H) K+ content in soil-grown wild-type and rsa1-1 plants. (I) Ratio of Na+ to K+ accumulation in soil-grown wild-type and rsa1-1 plants. WT, wild type. Error bars indicate the standard deviation (n = 30–40). The experiments in Figure 1 were repeated at least five times with similar results, and data from one representative experiment are presented.

Mentions: To isolate genes that play essential roles in salt stress tolerance, we used a modified root-bending assay [13], [14] and screened an ethyl methanesulfonate (EMS)-mutagenized Arabidopsis M2 population for mutants with hypersensitivity to 100 mM NaCl. These mutants were designated as short root in salt medium (rsa). One of these mutants, rsa1-1, was chosen for detailed characterization. The shoot development of rsa1-1 is normal under control conditions, but the primary root of rsa1-1 is slightly shorter than that of the wild type (Figure 1A). Both roots and shoots of rsa1-1 seedlings display a hypersensitive phenotype in response to supplemental NaCl in the growth medium (Figure 1A–1C). The roots of rsa1-1 seedlings have more root hairs than the wild type under control and salt-treated conditions (Figure S1A). The soil-grown rsa1-1 plants are more sensitive than the wild type when treated with 300 mM NaCl (Figure 1D and 1E), and germination of rsa1-1 seeds is more inhibited by NaCl than is germination of wild-type seeds (Figure 1F), suggesting that salt hypersensitivity of rsa1-1 plants does not depend on developmental stage. We then determined whether the salt hypersensitive phenotype of rsa1-1 is specific to Na+. We found that rsa1-1 mutant plants are not more sensitive to LiCl or CsCl than the wild type (Figure S1B and S1C), even though Li and Cs are in the same column of the periodic table of the elements as Na and are generally considered more toxic. The response of rsa1-1 plants to mannitol, which induces general osmotic stress, was similar to that of wild-type plants (Figure S1D). Thus, rsa1-1 is only hypersensitive to NaCl.


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)

rsa1-1 plants are hypersensitive to NaCl, and RSA1 is involved in Na+ homeostasis under salt stress.(A)–(C) Five-d-old wild-type and rsa1-1 seedlings grown on MS medium were transferred to MS medium supplemented with different levels of NaCl and allowed to grow for an additional 8 d. Root elongation or shoot fresh weight was measured and is shown as a percentage relative to growth on normal MS medium. (D) Two-week-old wild-type and rsa1-1 plants grown in soil were irrigated with 300 mM NaCl for 0 or 14 d. (E) Survival rate of wild-type and rsa1-1 plants as shown in (D). (F) Seed germination of wild type and rsa1-1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. Seeds in which the radical had emerged through the seed coat were considered germinated. (G) Na+ content in soil-grown wild-type and rsa1-1 plants. DW, dry weight. (H) K+ content in soil-grown wild-type and rsa1-1 plants. (I) Ratio of Na+ to K+ accumulation in soil-grown wild-type and rsa1-1 plants. WT, wild type. Error bars indicate the standard deviation (n = 30–40). The experiments in Figure 1 were repeated at least five times with similar results, and data from one representative experiment are presented.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3757082&req=5

pgen-1003755-g001: rsa1-1 plants are hypersensitive to NaCl, and RSA1 is involved in Na+ homeostasis under salt stress.(A)–(C) Five-d-old wild-type and rsa1-1 seedlings grown on MS medium were transferred to MS medium supplemented with different levels of NaCl and allowed to grow for an additional 8 d. Root elongation or shoot fresh weight was measured and is shown as a percentage relative to growth on normal MS medium. (D) Two-week-old wild-type and rsa1-1 plants grown in soil were irrigated with 300 mM NaCl for 0 or 14 d. (E) Survival rate of wild-type and rsa1-1 plants as shown in (D). (F) Seed germination of wild type and rsa1-1 in response to various NaCl levels. There were 80–150 seeds per genotype per biological replicate. Seeds in which the radical had emerged through the seed coat were considered germinated. (G) Na+ content in soil-grown wild-type and rsa1-1 plants. DW, dry weight. (H) K+ content in soil-grown wild-type and rsa1-1 plants. (I) Ratio of Na+ to K+ accumulation in soil-grown wild-type and rsa1-1 plants. WT, wild type. Error bars indicate the standard deviation (n = 30–40). The experiments in Figure 1 were repeated at least five times with similar results, and data from one representative experiment are presented.
Mentions: To isolate genes that play essential roles in salt stress tolerance, we used a modified root-bending assay [13], [14] and screened an ethyl methanesulfonate (EMS)-mutagenized Arabidopsis M2 population for mutants with hypersensitivity to 100 mM NaCl. These mutants were designated as short root in salt medium (rsa). One of these mutants, rsa1-1, was chosen for detailed characterization. The shoot development of rsa1-1 is normal under control conditions, but the primary root of rsa1-1 is slightly shorter than that of the wild type (Figure 1A). Both roots and shoots of rsa1-1 seedlings display a hypersensitive phenotype in response to supplemental NaCl in the growth medium (Figure 1A–1C). The roots of rsa1-1 seedlings have more root hairs than the wild type under control and salt-treated conditions (Figure S1A). The soil-grown rsa1-1 plants are more sensitive than the wild type when treated with 300 mM NaCl (Figure 1D and 1E), and germination of rsa1-1 seeds is more inhibited by NaCl than is germination of wild-type seeds (Figure 1F), suggesting that salt hypersensitivity of rsa1-1 plants does not depend on developmental stage. We then determined whether the salt hypersensitive phenotype of rsa1-1 is specific to Na+. We found that rsa1-1 mutant plants are not more sensitive to LiCl or CsCl than the wild type (Figure S1B and S1C), even though Li and Cs are in the same column of the periodic table of the elements as Na and are generally considered more toxic. The response of rsa1-1 plants to mannitol, which induces general osmotic stress, was similar to that of wild-type plants (Figure S1D). Thus, rsa1-1 is only hypersensitive to NaCl.

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