Nuclear calcium signaling in plants

Plant Physiology

Volumn 163, Issue 2, 2013, Pages 496-503

  Charpentier, Myriam ^a   Oldroyd, Giles E D ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MODEL; CALCIUM SIGNALING; CELL NUCLEUS; METABOLISM; NOTE; PLANT;

CALCIUM SIGNALING; CELL NUCLEUS; MODELS, BIOLOGICAL; PLANTS;

EID: 84885206709     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.220863     Document Type: Note

References (94)

1. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, et al (2007) The molecular architecture of the nuclear pore complex. Nature 450: 695-701
2. Allen GJ, Kwak JM, Chu SP, Llopis J, Tsien RY, Harper JF, Schroeder JI (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J 19: 735-747
3. Amor BB, Shaw SL, Oldroyd GE, Maillet F, Penmetsa RV, Cook D, Long SR, Dénarié J, Gough C (2003) The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J 34: 495-506
4. Antolín-Llovera M, Ried MK, Binder A, Parniske M (2012) Receptor kinase signaling pathways in plant-microbe interactions. Annu Rev Phytopathol 50: 451-473
5. Batistic O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820: 1283-1293
6. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11-21
7. Biro RL, Daye S, Serlin BS, Terry ME, Datta N, Sopory SK, Roux SJ (1984) Characterization of oat calmodulin and radioimmunoassay of its subcellular distribution. Plant Physiol 75: 382-386
8. Bootman MD, Fearnley C, Smyrnias I, MacDonald F, Roderick HL (2009) An update on nuclear calcium signalling. J Cell Sci 122: 2337-2350
9. Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, Vinther M, Lorentzen A, Madsen EB, Jensen KJ, et al (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci USA 109: 13859-13864
10. Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, Hirsch S, Miwa H, Downie JA, Morris RJ, Ané JM, et al (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci USA 108: 14348-14353
11. 2+ spiking in the legume and nonlegume root epidermis. New Phytol 189: 347-355
12. Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20: 3467-3479
13. 2+ oscillations in legume symbioses. Plant Signal Behav 8: 1-3
14. 2+ spiking and specific ENOD gene expression. Plant Physiol 136: 3582-3593
15. Chen T, Zhu H, Ke D, Cai K, Wang C, Gou H, Hong Z, Zhang Z (2012) A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24: 823-838
16. Deng M, Hochstrasser M (2006) Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443: 827-831
17. 2+ oscillations through the spatial signature drives gene expression. Curr Biol 19: 853-858
18. 2+ response amplitude and duration. Nature 386: 855-858
19. Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933-936
20. Edwards A, Heckmann AB, Yousafzai F, Duc G, Downie JA (2007) Structural implications of mutations in the pea SYM8 symbiosis gene, the DMI1 ortholog, encoding a predicted ion channel. Mol Plant Microbe Interact 20: 1183-1191
21. Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673-681
22. Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966
23. Engstrom EM, Ehrhardt DW, Mitra RM, Long SR (2002) Pharmacological analysis of Nod factor-induced calcium spiking in Medicago truncatula: evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiol 128: 1390-1401
24. Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4: 415-420
25. Galon Y, Finkler A, Fromm H (2010) Calcium-regulated transcription in plants. Mol Plant 3: 653-669
26. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198: 190-202
27. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 3489-3499
28. Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346: 769-771
29. Gleason C, Chaudhuri S, Yang T, Muñoz A, Poovaiah BW, Oldroyd GE (2006) Nodulation independent of rhizobia induced by a calciumactivated kinase lacking autoinhibition. Nature 441: 1149-1152
30. Gobbato E, Marsh JF, Vernié T, Wang E, Maillet F, Kim J, Miller JB, Sun J, Bano SA, Ratet P, et al (2012) A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 22: 2236-2241
31. Granqvist E, Wysham D, Hazledine S, Kozlowski W, Sun J, Charpentier M, Martins TV, Haleux P, Tsaneva-Atanasova K, Downie JA, et al (2012) Buffering capacity explains signal variation in symbiotic calcium oscillations. Plant Physiol 160: 2300-2310
32. Groth M, Takeda N, Perry J, Uchida H, Dräxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, et al (2010) NENA, a Lotus japonicas homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22: 2509-2526
33. Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, Imaizumi-Anraku H (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J 63: 141-154
34. Hirsch S, Kim J, Muñoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21: 545-557
35. Horváth B, Yeun LH, Domonkos A, Halász G, Gobbato E, Ayaydin F, Miró K, Hirsch S, Sun J, Tadege M, et al (2011) Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant Microbe Interact 24: 1345-1358
36. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, et al (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132: 666-680
37. Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, et al (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 1786-1789
38. 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103: 359-364
39. 2+-responsive cis elements in Arabidopsis. Plant Cell 18: 2733-2748
40. Kevei Z, Lougnon G, Mergaert P, Horváth GV, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss GB, et al (2007) 3-Hydroxy3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19: 3974-3989
41. King MC, Lusk CP, Blobel G (2006) Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442: 1003-1007
42. Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352: 524-526
43. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105: 9823-9828
44. 2+ dynamics. Plant J 69: 181-192
45. Lachaud C, Da Silva D, Cotelle V, Thuleau P, Xiong TC, Jauneau A, Brière C, Graziana A, Bellec Y, Faure JD, et al (2010) Nuclear calcium controls the apoptotic-like cell death induced by D-erythro-sphinganine in tobacco cells. Cell Calcium 47: 92-100
46. Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, Ranjeva R, Pugin A (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38: 527-538
47. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781-784
48. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364
49. Liao J, Singh S, Hossain MS, Andersen SU, Ross L, Bonetta D, Zhou Y, Sato S, Tabata S, Stougaard J, et al (2012) Negative regulation of CCaMK is essential for symbiotic infection. Plant J 72: 572-584
50. Madsen EB, Antolín-Llovera M, Grossmann C, Ye J, Vieweg S, Broghammer A, Krusell L, Radutoiu S, Jensen ON, Stougaard J, et al (2011) Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J 65: 404-417
51. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, et al (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640
52. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1: 1-12
53. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, et al (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63
54. Mazars C, Bourque S, Mithöfer A, Pugin A, Ranjeva R (2009) Calcium homeostasis in plant cell nuclei. New Phytol 181: 261-274
55. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181: 275-294
56. Mehlmer N, Parvin N, Hurst CH, Knight MR, Teige M, Vothknecht UC (2012) A toolset of aequorin expression vectors for in planta studies of subcellular calcium concentrations in Arabidopsis thaliana. J Exp Bot 63: 1751-1761
57. Messinese E, Mun JH, Yeun LH, Jayaraman D, Rougé P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, et al (2007) A novel nuclear protein interacts with the symbiotic DMI3 calciumand calmodulindependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20: 912-921
58. 2+-signatures in plant cells. Biol Proced Online 4: 105-118
59. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcriptbased cloning. Proc Natl Acad Sci USA 101: 4701-4705
60. Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48: 883-894
61. Ng CK, McAinsh MR (2003) Encoding specificity in plant calcium signalling: hot-spotting the ups and downs and waves. Ann Bot (Lond) 92: 477-485
62. Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11: 252-263
63. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6: 763-775
64. Pauly N, Knight MR, Thuleau P, Graziana A, Muto S, Ranjeva R, Mazars C (2001) The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 30: 413-421
65. Pauly N, Knight MR, Thuleau P, van der Luit AH, Moreau M, Trewavas AJ, Ranjeva R, Mazars C (2000) Control of free calcium in plant cell nuclei. Nature 405: 754-755
66. Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riely BK, Otegui MS, Edwards A, Freshour G, Hahn MG, Cook DR, et al (2007) The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145: 192-203
67. Poovaiah BW, Du L, Wang H, Yang T (2013) Recent advances in calcium/ calmodulin-mediated signaling with an emphasis on plant:microbe interactions. Plant Phys 163: 531-542
68. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, et al (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585-592
69. Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium and calcium/calmodulin-regulated gene expression. Plant Cell 23: 2010-2032
70. Riely BK, Lougnon G, Ané JM, Cook DR (2007) The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49: 208-216
71. Rodríguez-Concepción M, Yalovsky S, Zik M, Fromm H, Gruissem W (1999) The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein. EMBO J 18: 1996-2007
72. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, et al (2007) NUCLEO-PORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19: 610-624
73. 2+/calmodulin-dependent protein kinase: role of the neural visininlike domain in regulating autophosphorylation and calmodulin affinity. J Biol Chem 275: 30417-30422
74. Shimoda Y, Han L, Yamazaki T, Suzuki R, Hayashi M, Imaizumi-Anraku H (2012) Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulin-dependent protein kinase in Lotus japonicus. Plant Cell 24: 304-321
75. 2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J 69: 822-830
76. 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151: 1197-1206
77. Singh S, Parniske M (2012) Activation of calcium and calmodulin dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr Opin Plant Biol 15: 444-453
78. Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, Gough C, Bisseling T (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145: 183-191
79. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789-1791
80. Stermer BA, Bianchini GM, Korth KL (1994) Regulation of HMG-CoA reductase activity in plants. J Lipid Res 35: 1133-1140
81. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, et al (2002) A plant receptor like kinase required for both bacterial and fungal symbiosis. Nature 417: 959-962
82. Sun J, Miwa H, Downie JA, Oldroyd GE (2007) Mastoparan activates calcium spiking analogous to Nod factor-induced responses in Medicago truncatula root hair cells. Plant Physiol 144: 695-702
83. Swainsbury DJ, Zhou L, Oldroyd GE, Bornemann S (2012) Calcium ion binding properties of Medicago truncatula calcium/calmodulin dependent protein kinase. Biochemistry 51: 6895-6907
84. Taj G, Agarwal P, Grant M, Kumar A (2010) MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 5: 1370-1378
85. Takeda N, Maekawa T, Hayashi M (2012) Nuclear-localized and deregulated calcium and calmodulin-dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 24: 810-822
86. 2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441: 1153-1156
87. van Brussel AA, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJ, Kijne JW (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257: 70-72
88. van Der Luit AH, Olivari C, Haley A, Knight MR, Trewavas AJ (1999) Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiol 121: 705-714
89. Venkateshwaran M, Cosme A, Han L, Banba M, Satyshur KA, Schleiff E, Parniske M, Imaizumi-Anraku H, Ané JM (2012) The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24: 2528-2545
90. 2+ signals in the nucleus and the cytosol of plant cells. Angew Chem Int Ed Engl 46: 4783-4785
91. Whalley HJ, Sargeant AW, Steele JF, Lacoere T, Lamb R, Saunders NJ, Knight H, Knight MR (2011) Transcriptomic analysis reveals calcium regulation of specific promoter motifs in Arabidopsis. Plant Cell 23: 4079-4095
92. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot (Lond) 92: 487-511
93. Yamashita M (2011) Fluctuations in nuclear envelope's potential mediate synchronization of early neural activity. Biochem Biophys Res Commun 406: 107-111
94. Yano K, Yoshida S, Müller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, et al (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105: 20540-20545