A Positive regulator of nodule organogenesis, NODULE INCEPTION, acts as a negative regulator of rhizobial infection in Lotus japonicus

Plant Physiology

Volumn 165, Issue 2, 2014, Pages 747-758

  Yoro, Emiko ^a,b   Suzaki, Takuya ^a,b   Toyokura, Koichi ^c   Miyazawa, Hikota ^d   Fukaki, Hidehiro ^c   Kawaguchi, Masayoshi ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c KOBE UNIVERSITY   (Japan)

^d HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84901744358     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.233379     Document Type: Article

References (52)

1. Borisov AY, Madsen LH, Tsyganov VE, Umehara Y, Voroshilova VA, Batagov AO, Sandal N, Mortensen A, Schauser L, Ellis N, et al (2003) The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol 131: 1009-1017
2. Bozsó Z, Maunoury N, Szatmari A, Mergaert P, Ott PG, Zsíros LR, Szabó E, Kondorosi E, Klement Z (2009) Transcriptome analysis of a bacterially induced basal and hypersensitive response of Medicago truncatula. Plant Mol Biol 70: 627-646
3. Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125: 1075-1080
4. Crespi M, Frugier F (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Sci Signal 1: re11
5. Fournier J, Timmers ACJ, 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
6. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogenfixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68: 280-300
7. Gao QM, Venugopal S, Navarre D, Kachroo A (2011) Low oleic acidderived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins. Plant Physiol 155: 464-476
8. Goh T, Joi S, Mimura T, Fukaki H (2012) The establishment of asymmetry in Arabidopsis lateral root founder cells is regulated by LBD16/ASL18 and related LBD/ASL proteins. Development 139: 883-893
9. Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18: 2680-2693
10. Gregis V, Sessa A, Colombo L, Kater MM (2008) AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. Plant J 56: 891-902
11. 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
12. Ikeda M, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21: 3493-3505
13. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: betaglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907
14. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5: 619-633
15. Kosuta S, Held M, Hossain MS, Morieri G, Macgillivary A, Johansen C, Antolín-Llovera M, Parniske M, Oldroyd GED, Downie AJ, et al (2011) Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant J 67: 929-940
16. Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, Kawaguchi M (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 51: 1381-1397
17. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, et al (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420: 422-426
18. Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16: 319-331
19. Liu ZC, Mara C (2010) Regulatory mechanisms for floral homeotic gene expression. Semin Cell Dev Biol 21: 80-86
20. 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: 10
21. Maekawa T, Kusakabe M, Shimoda Y, Sato S, Tabata S, Murooka Y, Hayashi M (2008) Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol Plant Microbe Interact 21: 375-382
22. Magori S, Oka-Kira E, Shibata S, Umehara Y, Kouchi H, Hase Y, Tanaka A, Sato S, Tabata S, Kawaguchi M (2009) Too much love, a root regulator associated with the long-distance control of nodulation in Lotus japonicus. Mol Plant Microbe Interact 22: 259-268
23. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GED (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144: 324-335
24. Miyashima S, Koi S, Hashimoto T, Nakajima K (2011) Non-cellautonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138: 2303-2313
25. Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D'Haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153: 222-237
26. Murray JD (2011) Invasion by invitation: rhizobial infection in legumes. Mol Plant Microbe Interact 24: 631-639
27. Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315: 101-104
28. Nakagawa T, Kaku H, Shimoda Y, Sugiyama A, Shimamura M, Takanashi K, Yazaki K, Aoki T, Shibuya N, Kouchi H (2011) From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume-Rhizobium symbiosis. Plant J 65: 169-180
29. Oka-Kira E, Kawaguchi M (2006) Long-distance signaling to control root nodule number. Curr Opin Plant Biol 9: 496-502
30. Oka-Kira E, Tateno K, Miura K, Haga T, Hayashi M, Harada K, Sato S, Tabata S, Shikazono N, Tanaka A, et al (2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant J 44: 505-515
31. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50: 67-77
32. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11: 252-263
33. Op den Camp RH, De Mita S, Lillo A, Cao Q, Limpens E, Bisseling T, Geurts R (2011) A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol 157: 2013-2022
34. Oshima Y, Mitsuda N, Nakata M, Nakagawa T, Nagaya S, Kato K, Ohme-Takagi M (2011) Novel vector systems to accelerate functional analysis of transcription factors using chimeric repressor gene-silencing technology (CRES-T). Plant Biotechnol 28: 201-210
35. Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527-530
36. Popp C, Ott T (2011) Regulation of signal transduction and bacterial infection during root nodule symbiosis. Curr Opin Plant Biol 14: 458-467
37. 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
38. Rival P, de Billy F, Bono JJ, Gough C, Rosenberg C, Bensmihen S (2012) Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula. Development 139: 3383-3391
39. Sakaue-Sawano A, Ohtawa K, Hama H, Kawano M, Ogawa M, Miyawaki A (2008) Tracing the silhouette of individual cells in S/G2/M phases with fluorescence. Chem Biol 15: 1243-1248
40. Sandal N, Petersen TR, Murray J, Umehara Y, Karas B, Yano K, Kumagai H, Yoshikawa M, Saito K, Hayashi M, et al (2006) Genetics of symbiosis in Lotus japonicus: recombinant inbred lines, comparative genetic maps, and map position of 35 symbiotic loci. Mol Plant Microbe Interact 19: 80-91
41. Saur IML, Oakes M, Djordjevic MA, Imin N (2011) Crosstalk between the nodulation signaling pathway and the autoregulation of nodulation in Medicago truncatula. New Phytol 190: 865-874
42. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402: 191-195
43. Soto MJ, Domínguez-Ferreras A, Pérez-Mendoza D, Sanjuán J, Olivares J (2009) Mutualism versus pathogenesis: the give-and-take in plantbacteria interactions. Cell Microbiol 11: 381-388
44. Soyano T, Kouchi H, Hirota A, Hayashi M (2013) Nodule inception directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet 9: e1003352
45. Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139: 3997-4006
46. 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
47. van Brussel AAN, Tak T, Boot KJM, Kijne JW (2002) Autoregulation of root nodule formation: signals of both symbiotic partners studied in a split-root system of Vicia sativa subsp. nigra. Mol Plant Microbe Interact 15: 341-349
48. COI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25: 744-761
49. Vasse J, Debilly F, Truchet G (1993) Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J 4: 555-566
50. Vasse JM, Truchet GL (1984) The Rhizobium-legume symbiosis: observation of root infection by bright-field microscopy after staining with methylene blue. Planta 161: 487-489
51. 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
52. Yoshida C, Funayama-Noguchi S, Kawaguchi M (2010) plenty, a novel hypernodulation mutant in Lotus japonicus. Plant Cell Physiol 51: 1425-1435