Medicago truncatula ERN transcription factors: Regulatory interplay with NSP1/NSP2 GRAS factors and expression dynamics throughout rhizobial infection

Plant Physiology

Volumn 160, Issue 4, 2012, Pages 2155-2172

  Cerri, Marion R ^a   Frances, Lisa ^a   Laloum, Tom ^a   Auriac, Marie Christine ^a   Niebel, Andreas ^a   Oldroyd, Giles E D ^b   Barker, David G ^a   Fournier, Joëlle ^a   de Carvalho Niebel, Fernanda ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84870856057     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.203190     Document Type: Article

References (60)

1. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvalho-Niebel F (2007) AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19: 2866-2885.
2. 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.
3. 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.
4. 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 motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279.
5. Ben 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.
6. Boisson-Dernier A, Andriankaja A, Chabaud M, Niebel A, Journet EP, Barker DG, de Carvalho-Niebel F (2005) MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol Plant Microbe Interact 18: 1269-1276.
7. 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.
8. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647-1666.
9. Chabaud M, de Carvalho-Niebel F, Barker DG (2003) Efficient transformation of Medicago truncatula cv. Jemalong using the hypervirulent Agrobacterium tumefaciens strain AGL1. Plant Cell Rep 22: 46-51.
10. Chandler JW, Cole M, Flier A, Grewe B, Werr W (2007) The AP2 transcription factors DORNROSCHEN and DORNROSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development 134: 1653-1662.
11. 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.
12. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316: 421-425.
13. de Carvalho-Niebel F, Timmers AC, Chabaud M, Defaux-Petras A, Barker DG (2002) The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula. Plant J 32: 343-352.
14. Den Herder G, Parniske M (2009) The unbearable naivety of legumes in symbiosis. Curr Opin Plant Biol 12: 491-499.
15. 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.
16. Fournier J, Timmers AC, Sieberer BJ, Jauneau A, Chabaud M, Barker DG (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol 148: 1985-1995.
17. Gallego-Bartolomé J, Alabadí D, Blázquez MA (2011) DELLA-induced early transcriptional changes during etiolated development in Arabidopsis thaliana. PLoS ONE 6: e23918.
18. 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.
19. Heckmann AB, Sandal N, Bek AS, Madsen LH, Jurkiewicz A, Nielsen MW, Tirichine L, Stougaard J (2011) Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol Plant Microbe Interact 24: 1385-1395.
20. 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.
21. Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Küster H (2011) Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 157: 2023-2043.
22. Indrasumunar A, Gresshoff PM (2010) Duplicated nod-factor receptor 5 (NFR5) genes are mutated in soybean (Glycine max L. Merr.). Plant Signal Behav 5: 535-536.
23. Indrasumunar A, Searle I, Lin MH, Kereszt A, Men A, Carroll BJ, Gresshoff PM (2011) Nodulation factor receptor kinase 1a controls nodule organ number in soybean (Glycine max L. Merr). Plant J 65: 39-50.
24. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14: 737-748.
25. 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103: 359-364.
26. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
27. 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.
28. 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.
29. 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.
30. Mbengue M, Camut S, de Carvalho-Niebel F, Deslandes L, Froidure S, Klaus-Heisen D, Moreau S, Rivas S, Timmers T, Hervé C, et al (2010) The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22: 3474-3488.
31. 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 calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20: 912-921.
32. 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.
33. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcriptbased cloning. Proc Natl Acad Sci USA 101: 4701-4705.
34. Mitsuda N, Ohme-Takagi M (2008) NAC transcription factors NST1 and NST3 regulate pod shattering in a partially redundant manner by promoting secondary wall formation after the establishment of tissue identity. Plant J 56: 768-778.
35. 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.
36. Morohashi K, Minami M, Takase H, Hotta Y, Hiratsuka K (2003) Isolation and characterization of a novel GRAS gene that regulates meiosisassociated gene expression. J Biol Chem 278: 20865-20873.
37. Murray JD (2011) Invasion by invitation: rhizobial infection in legumes. Mol Plant Microbe Interact 24: 631-639.
38. Ogasawara H, Kaimi R, Colasanti J, Kozaki A (2011) Activity of transcription factor JACKDAW is essential for SHR/SCR-dependent activation of SCARECROW and MAGPIE and is modulated by reciprocal interactions with MAGPIE, SCARECROW and SHORT ROOT. Plant Mol Biol 77: 489-499.
39. Oldroyd GE, Long SR (2003) Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling. Plant Physiol 131: 1027-1032.
40. Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45: 119-144.
41. Plet J, Wasson A, Ariel F, Le Signor C, Baker D, Mathesius U, Crespi M, Frugier F (2011) MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J 65: 622-633.
42. Quandt HJ, Puhler A, Broer I (1993) Transgenic root nodules of Vicia hirsuta: a fast and efficient system for the study of gene expression in indeterminate-type nodules. Mol Plant Microbe Interact 6: 699-706.
43. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, 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.
44. Rae L, Lao NT, Kavanagh TA (2011) Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta 234: 429-444.
45. 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.
46. Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58: 809-822.
47. Shimizu R, Ji J, Kelsey E, Ohtsu K, Schnable PS, Scanlon MJ (2009) Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol 149: 841-850.
48. 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151: 1197-1206.
49. Singh LN, Hannenhalli S (2008) Functional diversification of paralogous transcription factors via divergence in DNA binding site motif and in expression. PLoS ONE 3: e2345.
50. Song YH, Yoo CM, Hong AP, Kim SH, Jeong HJ, Shin SY, Kim HJ, Yun DJ, Lim CO, Bahk JD, et al (2008) DNA-binding study identifies C-box and hybrid C/G-box or C/A-box motifs as high-affinity binding sites for STF1 and LONG HYPOCOTYL5 proteins. Plant Physiol 146: 1862-1877.
51. 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 receptorlike kinase required for both bacterial and fungal symbiosis. Nature 417: 959-962.
52. Sun X, Jones WT, Rikkerink EHA (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. Biochem J 442: 1-12.
53. Szabados L, Charrier B, Kondorosi A, Debruijn FJ, Ratet P (1995) New plant promoter and enhancer testing vectors. Mol Breed 1: 419-423.
54. Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315: 104-107.
55. Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latché A, Pech JC, Bouzayen M (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett 550: 149-154.
56. 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.
57. Vernié T, Moreau S, de Billy F, Plet J, Combier JP, Rogers C, Oldroyd G, Frugier F, Niebel A, Gamas P (2008) EFD is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20: 2696-2713.
58. 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.
59. Young ND, Debellé F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H, et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524.
60. Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, et al (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057.