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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 mutant plants accumulate more ROS and are hypersensitive to oxidative stress.(A) Total ROS accumulation in roots of 5-d-old wild-type and rsa1-1 seedlings subjected to 0 or 50 mM NaCl for 12 h. Bars = 200 µm. (B) Fluorescence intensity in plants shown in (A). (C) H2O2 content of wild-type and rsa1-1 plants subjected to 0 or 50 mM NaCl for 12 h. (D) Growth responses of wild-type and rsa1-1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). Seeds of the wild type and rsa1-1 were sown directly on MS medium containing 0 or 1 mM H2O2 (upper panel) and 0 or 0.2 µM MV (lower panel) and allowed to grow for an additional 14 d. (E) and (F) Shoot fresh weight and chlorophyll content in wild-type and rsa1-1 plants under treatment conditions shown in (D). Error bars indicate the standard deviation (n = 24). The experiments in Figure 2 were repeated at least four times with similar results, and data from one representative experiment are presented.
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pgen-1003755-g002: rsa1-1 mutant plants accumulate more ROS and are hypersensitive to oxidative stress.(A) Total ROS accumulation in roots of 5-d-old wild-type and rsa1-1 seedlings subjected to 0 or 50 mM NaCl for 12 h. Bars = 200 µm. (B) Fluorescence intensity in plants shown in (A). (C) H2O2 content of wild-type and rsa1-1 plants subjected to 0 or 50 mM NaCl for 12 h. (D) Growth responses of wild-type and rsa1-1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). Seeds of the wild type and rsa1-1 were sown directly on MS medium containing 0 or 1 mM H2O2 (upper panel) and 0 or 0.2 µM MV (lower panel) and allowed to grow for an additional 14 d. (E) and (F) Shoot fresh weight and chlorophyll content in wild-type and rsa1-1 plants under treatment conditions shown in (D). Error bars indicate the standard deviation (n = 24). The experiments in Figure 2 were repeated at least four times with similar results, and data from one representative experiment are presented.

Mentions: Abiotic stresses including salt stress can cause production of ROS [7], [15]. We determined the effect of the rsa1-1 mutation on ROS levels and on the response to oxidative stress. The fluorescent dye 5-(and 6)-chloromethyl-2′7′-dichlorodihydrofluorescein diacetate acetyl ester (CM-H2DCFDA) was used to visualize and quantify total ROS in the root tissues. The rsa1-1 plants accumulated slightly more ROS than the wild type under control conditions but accumulated substantially more ROS than the wild type when treated with 50 mM NaCl (Figure 2A and 2B). Similar results were obtained for the levels of hydrogen peroxide (H2O2), which was quantified with the Amplex red reagent, 10-acetyl-3,7-dihydrophenoxazine (Figure 2C). These results suggest that RSA1 is an important regulator of ROS accumulation in plants under salt stress. Furthermore, we found that rsa1-1 plants are hypersensitive to exogenous application of H2O2 or methyl viologen (MV) (Figure 2D–2F). MV can lead to an increase in the generation of toxic superoxide free radicals in chloroplasts [16].


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 mutant plants accumulate more ROS and are hypersensitive to oxidative stress.(A) Total ROS accumulation in roots of 5-d-old wild-type and rsa1-1 seedlings subjected to 0 or 50 mM NaCl for 12 h. Bars = 200 µm. (B) Fluorescence intensity in plants shown in (A). (C) H2O2 content of wild-type and rsa1-1 plants subjected to 0 or 50 mM NaCl for 12 h. (D) Growth responses of wild-type and rsa1-1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). Seeds of the wild type and rsa1-1 were sown directly on MS medium containing 0 or 1 mM H2O2 (upper panel) and 0 or 0.2 µM MV (lower panel) and allowed to grow for an additional 14 d. (E) and (F) Shoot fresh weight and chlorophyll content in wild-type and rsa1-1 plants under treatment conditions shown in (D). Error bars indicate the standard deviation (n = 24). The experiments in Figure 2 were repeated at least four times with similar results, and data from one representative experiment are presented.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3757082&req=5

pgen-1003755-g002: rsa1-1 mutant plants accumulate more ROS and are hypersensitive to oxidative stress.(A) Total ROS accumulation in roots of 5-d-old wild-type and rsa1-1 seedlings subjected to 0 or 50 mM NaCl for 12 h. Bars = 200 µm. (B) Fluorescence intensity in plants shown in (A). (C) H2O2 content of wild-type and rsa1-1 plants subjected to 0 or 50 mM NaCl for 12 h. (D) Growth responses of wild-type and rsa1-1 seedlings to oxidative stress-inducing reagents H2O2 and methyl viologen (MV). Seeds of the wild type and rsa1-1 were sown directly on MS medium containing 0 or 1 mM H2O2 (upper panel) and 0 or 0.2 µM MV (lower panel) and allowed to grow for an additional 14 d. (E) and (F) Shoot fresh weight and chlorophyll content in wild-type and rsa1-1 plants under treatment conditions shown in (D). Error bars indicate the standard deviation (n = 24). The experiments in Figure 2 were repeated at least four times with similar results, and data from one representative experiment are presented.
Mentions: Abiotic stresses including salt stress can cause production of ROS [7], [15]. We determined the effect of the rsa1-1 mutation on ROS levels and on the response to oxidative stress. The fluorescent dye 5-(and 6)-chloromethyl-2′7′-dichlorodihydrofluorescein diacetate acetyl ester (CM-H2DCFDA) was used to visualize and quantify total ROS in the root tissues. The rsa1-1 plants accumulated slightly more ROS than the wild type under control conditions but accumulated substantially more ROS than the wild type when treated with 50 mM NaCl (Figure 2A and 2B). Similar results were obtained for the levels of hydrogen peroxide (H2O2), which was quantified with the Amplex red reagent, 10-acetyl-3,7-dihydrophenoxazine (Figure 2C). These results suggest that RSA1 is an important regulator of ROS accumulation in plants under salt stress. Furthermore, we found that rsa1-1 plants are hypersensitive to exogenous application of H2O2 or methyl viologen (MV) (Figure 2D–2F). MV can lead to an increase in the generation of toxic superoxide free radicals in chloroplasts [16].

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
Related in: MedlinePlus