Rhizobial and mycorrhizal symbioses in Lotus japonicus require Lectin Nucleotide Phosphohydrolase, which acts upstream of calcium signaling

Plant Physiology

Volumn 161, Issue 1, 2013, Pages 556-567

  Roberts, Nicholas J ^a,d   Morieri, Giulia ^b   Kalsi, Gurpreet ^a   Rose, Alan ^a   Stiller, Jiri ^c   Edwards, Anne ^b   Xie, Fang ^b   Gresshoff, Peter M ^c   Oldroyd, Giles E D ^b   Allan Downie, J ^b   Etzler, Marilynn E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHN INNES CENTRE   (United Kingdom)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d AGRESEARCH GRASSLANDS   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; GLOMUS INTRARADICES; LOTUS CORNICULATUS VAR. JAPONICUS;

EID: 84871728617     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.206110     Document Type: Article

References (75)

1. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, et al (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303: 1364-1367
2. Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé JC, Dénarié J, Truchet G (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6: 1357-1374
3. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Ghérardi M, Huguet T, et al (2006) The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279
4. Bek AS, Sauer J, Thygesen MB, Duus JØ, Petersen BO, Thirup S, James E, Jensen KJ, Stougaard J, Radutoiu S (2010) Improved characterization of nod factors and genetically based variation in LysM receptor domains identify amino acids expendable for nod factor recognition in Lotus spp. Mol Plant Microbe Interact 23: 58-66
5. Bevan M (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12: 8711-8721
6. 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
7. 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
8. Clark G, Fraley D, Steinebrunner I, Cervantes A, Onyirimba J, Liu A, Torres J, Tang W, Kim J, Roux SJ (2011) Extracellular nucleotides and apyrases regulate stomatal aperture in Arabidopsis. Plant Physiol 156: 1740-1753
9. Clark G, Roux SJ (2011) Apyrases, extracellular ATP and the regulation of growth. Curr Opin Plant Biol 14: 700-706
10. Cohn JR, Uhm T, Ramu S, Nam YW, Kim DJ, Penmetsa RV, Wood TC, Denny RL, Young ND, Cook DR, et al (2001) Differential regulation of a family of apyrase genes from Medicago truncatula. Plant Physiol 125: 2104-2119
11. Day RB, McAlvin CB, Loh JT, Denny RL, Wood TC, Young ND, Stacey G (2000) Differential expression of two soybean apyrases, one of which is an early nodulin. Mol Plant Microbe Interact 13: 1053-1070
12. Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K (2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytol 163: 381-392
13. Demidchik V, Nichols C, Oliynyk M, Dark A, Glover BJ, Davies JM (2003) Is ATP a signaling agent in plants? Plant Physiol 133: 456-461
14. Demidchik V, Shang Z, Shin R, Colaço R, Laohavisit A, Shabala S, Davies JM (2011) Receptor-like activity evoked by extracellular ADP in Arabidopsis root epidermal plasma membrane. Plant Physiol 156: 1375-1385
15. Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503-535
16. Doyle JJ (1998) Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3: 473-478
17. 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
18. Etzler ME, Kalsi G, Ewing NN, Roberts NJ, Day RB, Murphy JB (1999) A nod factor binding lectin with apyrase activity from legume roots. Proc Natl Acad Sci USA 96: 5856-5861
19. Etzler ME, Roberts NJ (2005). LNP, a protein involved in the initiation of mycorrhizal infection in plants. US Patent Application No. 6,849,777
20. Fahraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16: 374-381
21. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50: 151-158
22. Govindarajulu M, Kim SY, Libault M, Berg RH, Tanaka K, Stacey G, Taylor CG (2009) GS52 ecto-apyrase plays a critical role during soybean nodulation. Plant Physiol 149: 994-1004
23. 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 japonicus 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
24. Hoagland DR, Arnold DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347: 1-39
25. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, et al (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433: 527-531
26. 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
27. Kalsi G, Etzler ME (2000) Localization of a Nod factor-binding protein in legume roots and factors influencing its distribution and expression. Plant Physiol 124: 1039-1048
28. 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103: 359-364
29. Khakh BS, Burnstock G (2009) The double life of ATP. Sci Amer 301: 84-92
30. Kim SY, Sivaguru M, Stacey G (2006) Extracellular ATP in plants: visualization, localization, and analysis of physiological significance in growth and signaling. Plant Physiol 142: 984-992
31. Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, et al (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17: 2217-2229
32. Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131: 952-962
33. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GED (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105: 9823-9828
34. Lazo GR, Stein PA, Ludwig RA (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology (N Y) 9: 963-967
35. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364
36. Libault M, Joshi T, Benedito VA, Xu D, Udvardi MK, Stacey G (2009) Legume transcription factor genes: what makes legumes so special? Plant Physiol 151: 991-1001
37. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302: 630-633
38. Lombardo F, Heckmann AB, Miwa H, Perry JA, Yano K, Hayashi M, Parniske M, Wang TL, Downie JA (2006) Identification of symbiotically defective mutants of Lotus japonicus affected in infection thread growth. Mol Plant Microbe Interact 19: 1444-1450
39. 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
40. 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
41. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144: 324-335
42. McAlvin CB, Stacey G (2005) Transgenic expression of the soybean apyrase in Lotus japonicus enhances nodulation. Plant Physiol 137: 1456-1462
43. 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 calcium-and calmodulindependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20: 912-921
44. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kaló P, Prabhu R, Marsh JF, Mitra RM, Kereszt A, et al (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19: 1221-1234
45. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcriptbased cloning. Proc Natl Acad Sci USA 101: 4701-4705
46. Miwa H, Sun J, Oldroyd GE, Downie JA (2006a) Analysis of Nod-factorinduced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19: 914-923
47. Miwa H, Sun J, Oldroyd GE, Downie JA (2006b) 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
48. Navarro-Gochicoa MT, Camut S, Niebel A, Cullimore JV (2003) Expression of the apyrase-like APY1 genes in roots of Medicago truncatula is induced rapidly and transiently by stress and not by Sinorhizobium meliloti or Nod factors. Plant Physiol 131: 1124-1136
49. Nieuwkoop AJ, Banfalvi Z, Deshmane N, Gerhold D, Schell MG, Sirotkin KM, Stacey G (1987) A locus encoding host range is linked to the common nodulation genes of Bradyrhizobium japonicum. J Bacteriol 169: 2631-2638
50. Novero M, Faccio A, Genre A, Stougaard J, Webb KJ, Mulder L, Parniske M, Bonfante P (2002) Dual requirement of the LjSYM4 gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus roots. New Phytol 154: 741-749
51. Oláh B, Brière C, Bécard G, Dénarié J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44: 195-207
52. Oldroyd GED, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol 9: 351-357
53. Oldroyd GED, Harrison MJ, Paszkowski U (2009) Reprogramming plant cells for endosymbiosis. Science 324: 753-754
54. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6: 763-775
55. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201
56. Pietrzak M, Shillito RD, Hohn T, Potrykus I (1986) Expression in plants of two bacterial antibiotic resistance genes after protoplast transformation with a new plant expression vector. Nucleic Acids Res 14: 5857-5868
57. Quinn JM, Etzler ME (1987) Isolation and characterization of a lectin from the roots of Dolichos biflorus. Arch Biochem Biophys 258: 535-544
58. 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
59. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EMH, Albrektsen AS, James EK, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26: 3923-3935
60. Roberts NJ, Brigham J, Wu B, Murphy JB, Volpin H, Phillips DA, Etzler ME (1999) A Nod factor-binding lectin is a member of a distinct class of apyrases that may be unique to the legumes. Mol Gen Genet 262: 261-267
61. Rosenberg C, Boistard P, Dénarié J, Casse-Delbart F (1981) Genes controlling early and late functions in symbiosis are located on a megaplasmid in Rhizobium meliloti. Mol Gen Genet 184: 326-333
62. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, et al (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19: 610-624
63. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, et al (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15: 227-239
64. Shaw SL, Long SR (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol 131: 976-984
65. 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
66. Steinebrunner I, Wu J, Sun Y, Corbett A, Roux SJ (2003) Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiol 131: 1638-1647
67. Stiller J, Martirani L, Tuppale S, Chian RJ, Chiurazzi M, Gresshoff PM (1997) High frequency transformation and regeneration of transgenic plants in the model legume Lotus japonicus. J Exp Bot 48: 1357-1365
68. 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
69. Tanaka K, Nguyen CT, Libault M, Cheng J, Stacey G (2011) Enzymatic activity of the soybean ecto-apyrase GS52 is essential for stimulation of nodulation. Plant Physiol 155: 1988-1998
70. 2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441: 1153-1156
71. Wais RJ, Galera C, Oldroyd G, Catoira R, Penmetsa RV, Cook D, Gough C, Denarié J, Long SR (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Natl Acad Sci USA 97: 13407-13412
72. Walker SA, Downie JA (2000) Entry of Rhizobium leguminosarum bv. viciae into root hairs requires minimal Nod factor specificity, but subsequent infection thread growth requires nodO or nodE. Mol Plant Microbe Interact 13: 754-762
73. Walker SA, Viprey V, Downie JA (2000) Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by nod factors and chitin oligomers. Proc Natl Acad Sci USA 97: 13413-13418
74. Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, Oldroyd GED, Downie JA (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci USA 109: 633-638
75. 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