A Nuclear Calcium-Sensing Pathway Is Critical for Gene Regulation and Salt Stress Tolerance in

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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.

Vyšlo v časopise: A Nuclear Calcium-Sensing Pathway Is Critical for Gene Regulation and Salt Stress Tolerance in. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003755
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003755

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Zdroje

1. HasegawaPM, BressanRA, ZhuJ-K, BohnertHJ (2000) Plant Cellular and Molecular Responses to High Salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463–499.

2. ZhuJ-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6: 441–445.

3. YangQ, ChenZZ, ZhouXF, YinHB, LiX, et al. (2009) Overexpression of SOS (Salt Overly Sensitive) Genes Increases Salt Tolerance in Transgenic Arabidopsis. Mol Plant 2: 22–31.

4. ChengNH, PittmanJK, ZhuJ-K, HirsschiKD (2004) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279: 2922–2926.

5. QiuQS, GuoY, QuinteroFJ, PardoJM, SchumakerKS, et al. (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279: 207–215.

6. Katiyar-AgarwalS, ZhuJ, KimK, AgarwalM, FuX, et al. (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 103: 18816–18821.

7. ApelK, HirtH (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373–399.

8. GillSS, TutejaN (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48: 909–930.

9. NandaAK, AndrioE, MarinoD, PaulyN, DunandC (2010) Reactive oxygen species during plant-microorganism early interactions. J Integr Plant Biol 52: 195–204.

10. MøllerIM, JensenPE, HanssonA (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58: 459–481.

11. JonakC, ÖkreszL, BögreL, HirtH (2002) Complexity, cross talk and integration of plant MAP kinase signaling. Curr Opin Plant Biol 5(5): 415–424.

12. KovtunY, ChiuW-L, TenaG, SheenJ (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97: 2940–2945.

13. WuS-J, LeiD, ZhuJ-K (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8: 617–627.

14. ZhuJ, GongZ, ZhangC, SongCP, DamszB, et al. (2002) OSM1/SYP61: A syntaxin protein in Arabidopsis controls abscisic acid–mediated and non-abscisic acid–mediated responses to abiotic stress. Plant Cell 14: 3009–3028.

15. BorsaniO, ValpuestaV, BotellaMA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126: 1024–1030.

16. FujibeT, SajiH, ArakawaK, YabeN, TakeuchiY, et al. (2004) A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol 134: 275–285.

17. DayIS, ReddyVS, Shad AliG, ReddyAS (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol 3 (10): research0056.1–0056.24.

18. HeimMA, JakobyM, WerberM, MartinC, WeisshaarB, et al. (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20: 735–747.

19. Toledo-OrtizG, HuqE, QuailPH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15: 1749–1770.

20. EhrhardtDW, WaisR, LongSR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673–681.

21. KosutaS, HazledineS, SunJ, MiwaH, MorrisRJ, et al. (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105: 9823–9828.

22. Sieberer BJ ChabaudM, TimmersAC, MoninA, FournierJ, et al. (2009) A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151: 1197–1206.

23. van der LuitAH, OlivariC, HaleyA, KnightM, TrewavasA (1999) Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiol 121: 705–714.

24. PaulyN, KnightMR, ThuleauP, GrazianaA, MutoS, et al. (2001) The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 30: 413–421.

25. WatahikiMK, TrewavasAJ, PartonRM (2004) Fluctuations in the pollen tube tip-focused calcium gradient are not reflected in nuclear calcium level: a comparative analysis using recombinant yellow cameleon reporter. Sex Plant Reprod 17: 125–130.

26. LecourieuxD, LamotteO, BourqueS, WendehenneD, MazarsC, et al. (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38: 527–538.

27. WalterA, MazarsC, MaitrejeanM, HopkeJ, RanjevaR, et al. (2007) Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. Angew Chem Int Ed Engl 46: 4783–4785.

28. MazarsC, BourqueS, MithöferA, PuginA, RanjevaR (2009) Calcium homeostasis in plant cell nuclei. New Phytol 181: 261–274.

29. HirschS, KimJ, MuñozA, HeckmannAB (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21: 545–557.

30. CapoenW, SunJ, WyshamD, OteguiMS, VenkateshwaranM, et al. (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci USA 108: 14348–14353.

31. KalóP, GleasonC, EdwardsA, MarshJ, MitraRM, et al. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 1786–1789.

32. LévyJ, BresC, GeurtsR, ChalhoubB, KulikovaO, et al. (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361–1364.

33. SmitP, RaedtsJ, PortyankoV, DebelléF, GoughC, et al. (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789–1791.

34. HeckmannAB, LombardoF, MiwaH, PerryJA, BunnewellS, et al. (2006) Lotus japonicus nodulation requires two GRAS-domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142: 1739–1750.

35. TirichineL, Imaizumi-AnrakuH, YoshidaS, MurakamiY, MadsenLH, et al. (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441: 1153–1156.

36. PopescuSC, PopescuGV, BachanS, ZhangZ, GersteinM (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23: 80–92.

37. ZhuJ-K, LiuJ, XiongL (1998) Genetic analysis of salt tolerance in arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell 10: 1181–1191.

38. ShiH, XiongL, StevensonB, LuT, ZhuJ-K (2002) The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. Plant Cell 14: 575–588.

39. ShiH, KimYS, GuoY, StevensonB, ZhuJ-K (2003) The Arabidopsis SOS5 locus encodes a cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15: 19–32.

40. ZhuJ, LeeBH, DellingerM, CuiX, ZhangC, et al. (2010) A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J 63: 128–140.

41. IshitaniM, XiongL, StevensonB, ZhuJ-K (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9: 1935–1949.

42. LiW, GuanQ, WangZY, WangY, ZhuJ (2013) A Bi-Functional Xyloglucan Galactosyltransferase Is an Indispensable Salt Stress Tolerance Determinant in Arabidopsis. Mol Plant 6: 1344–54 DOI: 10.1093/mp/sst062

43. GuanQ, WenC, ZengH, ZhuJ (2012) A KH Domain-Containing Putative RNA-Binding Protein Is Critical for Heat Stress-Responsive Gene Regulation and Thermotolerance in Arabidopsis. Mol Plant 6: 386–395.

44. WangZY, XiongL, LiW, ZhuJK, ZhuJ (2011) The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. Plant Cell 23: 1971–1984.

45. GuanQ, WuJ, ZhangY, JiangC, LiuR, et al. (2013) A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25: 342–356.

46. EdgarR, DomrachevM, LashAE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207–210.

47. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–745.

48. GendrelA-V, LippmanZ, YordanC, ColotV, MartienssenRA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297: 1871–1873.

49. GuanQ, LuX, ZengH, ZhangY, ZhuJ (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74: 840–851.

50. MaruyamaK, MikawaT, EbashiS (1984) Detection of calcium binding proteins by 45Ca autoradiography on nitrocellulose membrane after sodium dodecyl sulfate gel electrophoresis. J Biochem 95: 511–519.

51. IshitaniM, LiuJ, HalfterU, KimCS, ShiW, et al. (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12: 1667–1678.

52. KimJ, HarterK, TheologisA (1997) Protein-protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci USA 94: 11786–11791.

53. TsengT-S, SaloméPA, McClungCR, OlszewskiNE (2004) SPINDLY and GIGANTEA interact and act in Arabidopsis thaliana pathways involved in light responses, flowering, and rhythms in cotyledon movements. Plant Cell 16: 1550–1563.

54. WalterM, ChabanC, SchützeK, BatisticO, WeckermannK (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428–438.

55. VoinnetO, RivasS, MestreP, BaulcombeD (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949–956.

56. ChenH, ZouY, ShangY, LinH, WangY, et al. (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146: 368–376.

57. LeisterRT, DahlbeckD, DayB, LiY, ChesnokovaO, et al. (2005) Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell 17: 1268–1278.

58. Choi duS, HwangIS, HwangBK (2012) Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper. Plant Cell 24: 1675–1690.

59. HellensRP, AllanAC, FrielEN, BolithoK, GraftonK, et al. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Method 1: 13.

60. CodlingEE, MulchiCL, ChaneyRL (2007) Grain yield and mineral element composition of maize grown on high phosphorus soils amended with water treatment residual. J Plant Nutr 30: 225–240.

61. LichtenthalerHK, WellburnAR (1983) Determinations of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem Soc Trans 11: 591–592.

62. MancinelliA, WalshL (1979) Photocontrol of anthocyanin synthesis. Plant Physiol 63: 841–846.

63. HallTA (1999) BioEdit: a user-friendly biological sequence alignment editor and analyses program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.

64. HruzT, LauleO, SzaboG, WessendorpF, BleulerS, et al. (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 420747.

65. DereeperA, GuignonV, BlancG, AudicS, BuffetS, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36 (Web Server issue) W465–469.