Root nodulation: A developmental program involving cell fate conversion triggered by symbiotic bacterial infection

Current Opinion in Plant Biology

Volumn 21, Issue , 2014, Pages 16-22

  Suzaki, Takuya ^a,b   Kawaguchi, Masayoshi ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKININ; PHYTOHORMONE;

GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; NODULATION; PHYSIOLOGY; PLANT ROOT; RHIZOBIUM; SYMBIOSIS;

CYTOKININS; GENE EXPRESSION REGULATION, PLANT; PLANT GROWTH REGULATORS; PLANT ROOT NODULATION; PLANT ROOTS; RHIZOBIUM; ROOT NODULES, PLANT; SYMBIOSIS;

EID: 84903713564     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.06.002     Document Type: Review

References (55)

1. Kouchi H., Imaizumi-Anraku H., Hayashi M., Hakoyama T., Nakagawa T., Umehara Y., Suganuma N., Kawaguchi M. How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 2010, 51:1381-1397.
2. Oldroyd G.E., Murray J.D., Poole P.S., Downie J.A. The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 2011, 45:119-144.
3. Oldroyd G.E. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 2013, 11:252-263.
4. Szczyglowski K., Shaw R.S., Wopereis J., Copeland S., Hamburger D., Kasiborski Dazzo B.F.B., de Bruijn F.J. Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol Plant-Microbe Interact 1998, 11:684-697.
5. Gage D.J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 2004, 68:280-300.
6. Murray J.D. Invasion by invitation: rhizobial infection in legumes. Mol Plant-Microbe Interact 2011, 24:631-639.
7. Stracke S., Kistner C., Yoshida S., Mulder L., Sato S., Kaneko T., Tabata S., Sandal N., Stougaard J., Szczyglowski K., et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 2002, 417:959-962.
8. Madsen E.B., Madsen L.H., Radutoiu S., Olbryt M., Rakwalska M., Szczyglowski K., Sato S., Kaneko T., Tabata S., Sandal N., et al. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 2003, 425:637-640.
9. Radutoiu S., Madsen L.H., Madsen E.B., Felle H.H., Umehara Y., Grønlund M., Sato S., Nakamura Y., Tabata S., Sandal N., et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 2003, 425:585-592.
10. Imaizumi-Anraku H., Takeda N., Charpentier M., Perry J., Miwa H., Umehara Y., Kouchi H., Murakami Y., Mulder L., Vickers K., et al. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 2005, 433:527-531.
11. 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad of Sci U S A 2006, 103:359-364.
12. Saito K., Yoshikawa M., Yano K., Miwa H., Uchida H., Asamizu E., Sato S., Tabata S., Imaizumi-Anraku H., Umehara Y., et al. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 2007, 19:610-624.
13. Groth M., Takeda N., Perry J., Uchida H., Draxl S., Brachmann A., Sato S., Tabata S., Kawaguchi M., Wang T.L., et al. 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 2010, 22:2509-2526.
14. Gleason C., Chaudhuri S., Yang T., Munoz A., Poovaiah B.W., Oldroyd G.E. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 2006, 441:1149-1152.
15. 2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 2006, 441:1153-1156.
16. Shimoda Y., Han L., Yamazaki T., Suzuki R., Hayashi M., Imaizumi-Anraku H. Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulin-dependent protein kinase in Lotus japonicus. Plant Cell 2012, 24:304-321.
17. Miller J.B., Pratap A., Miyahara A., Zhou L., Bornemann S., Morris R.J., Oldroyd G.E. Calcium/calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling. Plant Cell 2013, 25:5053-5066.
18. Kaló P., Gleason C., Edwards A., Marsh J., Mitra R.M., Hirsch S., Jakab J., Sims S., Long S.R., Rogers J., et al. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 2005, 308:1786-1789.
19. Smit P., Raedts J., Portyanko V., Debell F., Gough C., Bisseling T., Geurts R. NSP1 of the GRAS protein family is essential for rhizobial nod factor-induced transcription. Science 2005, 308:1789-1791.
20. Heckmann A.B., Lombardo F., Miwa H., Perry J.A., Bunnewell S., Parniske M., Wang T.L., Downie J.A. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 2006, 142:1739-1750.
21. Murakami Y., Miwa H., Imaizumi-Anraku H., Kouchi H., Downie J.A., Kawaguchi M., Kawasaki S. Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation. DNA Res 2006, 13:255-265.
22. 2+ spiking. Plant J 2014, 77:146-159.
23. Rival P., de Billy F., Bono J.J., Gough C., Rosenberg C., Bensmihen S. Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula. Development 2012, 139:3383-3391.
24. Capoen W., Den Herder J., Sun J.J., Verplancke C., De Keyser A., De Rycke R., Goormachtig S., Oldroyd G., Holsters M. Calcium spiking patterns and the role of the calcium/calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell 2009, 21:1526-1540.
25. Madsen L.H., Tirichine L., Jurkiewicz A., Sullivan J.T., Heckmann A.B., Bek A.S., Ronson C.W., James E.K., Stougaard J. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 2010, 1:1-12.
26. Schauser L., Roussis A., Stiller J., Stougaard J. A plant regulator controlling development of symbiotic root nodules. Nature 1999, 402:191-195.
27. Soyano T., Kouchi H., Hirota A., Hayashi M. NODULE INCEPTION directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet 2013, 9:e1003352.
28. Yano K., Yoshida S., Muller J., Singh S., Banba M., Vickers K., Markmann K., White C., Schuller B., Sato S., et al. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad of Sci U S A 2008, 105:20540-20545.
29. Singh S., Katzer K., Lambert J., Cerri M., Parniske M. CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 2014, 15:139-152.
30. Tirichine L., James E.K., Sandal N., Stougaard J. Spontaneous root-nodule formation in the model legume Lotus japonicus: a novel class of mutants nodulates in the absence of rhizobia. Mol Plant-Microbe Interact 2006, 19:373-382.
31. Hayashi T., Banba M., Shimoda Y., Kouchi H., Hayashi M., Imaizumi-Anraku H. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J 2010, 63:141-154.
32. Cooper J.B., Long S.R. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 1994, 6:215-225.
33. Frugier F., Kosuta S., Murray J.D., Crespi M., Szczyglowski K. Cytokinin: secret agent of symbiosis. Trends Plant Sci 2008, 13:115-120.
34. Suzaki T., Ito M., Kawaguchi M. Genetic basis of cytokinin and auxin functions during root nodule development. Front Plant Sci 2013, 4:42.
35. Plet J., Wasson A., Ariel F., Le Signor C., Baker D., Mathesius U., Crespi M., Frugier F. MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J 2011, 65:622-633.
36. Murray J.D., Karas B.J., Sato S., Tabata S., Amyot L., Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 2007, 315:101-104.
37. Held M., Hou H., Miri M., Huynh C., Ross L., Hossain M.S., Sato S., Tabata S., Perry J., Wang T.L., et al. Lotus japonicus cytokinin receptors work partially redundantly to mediate nodule formation. Plant Cell 2014, 26:678-694.
38. Tirichine L., Sandal N., Madsen L.H., Radutoiu S., Albrektsen A.S., Sato S., Asamizu E., Tabata S., Stougaard J. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 2007, 315:104-107.
39. Heckmann A.B., Sandal N., Bek A.S., Madsen L.H., Jurkiewicz A., Nielsen M.W., Tirichine L., Stougaard J. Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol Plant-Microbe Interact 2011, 24:1385-1395.
40. Sturtevant D.B., Taller B.J. Cytokinin production by Bradyrhizobium japonicum. Plant Physiol 1989, 89:1247-1252.
41. Kisiala A., Laffont C., Emery R.J., Frugier F. Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. Mol Plant-Microbe Interact 2013, 26:1225-1231.
42. Chen Y., Chen W., Li X., Jiang H., Wu P., Xia K., Yang Y., Wu G. Knockdown of LjIPT3 influences nodule development in Lotus japonicus. Plant Cell Physiol 2014, 55:183-193.
43. Mortier V., Wasson A., Jaworek P., De Keyser A., Decroos M., Holsters M., Tarkowski P., Mathesius U., Goormachtig S. Role of LONELY GUY genes in indeterminate nodulation on Medicago truncatula. New Phytol 2014, 202:582-593.
44. Rightmyer A.P., Long S.R. Pseudonodule formation by wild-type and symbiotic mutant Medicago truncatula in response to auxin transport inhibitors. Mol Plant-Microbe Interact 2011, 24:1372-1384.
45. Suzaki T., Yano K., Ito M., Umehara Y., Suganuma N., Kawaguchi M. Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 2012, 139:3997-4006.
46. Heyl A., Schmulling T. Cytokinin signal perception and transduction. Curr Opin Plant Biol 2003, 6:480-488.
47. Ariel F., Brault-Hernandez M., Laffont C., Huault E., Brault M., Plet J., Moison M., Blanchet S., Ichante J.L., Chabaud M., et al. Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell 2012, 24:3838-3852.
48. Hirsch S., Kim J., Munoz A., Heckmann A.B., Downie J.A., Oldroyd G.E. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 2009, 21:545-557.
49. Suzaki T., Kim C.S., Takeda N., Szczyglowski K., Kawaguchi M. TRICOT encodes an AMP1-related carboxypeptidase that regulates root nodule development and shoot apical meristem maintenance in Lotus japonicus. Development 2013, 140:353-361.
50. Imin N., Mohd-Radzman N.A., Ogilvie H.A., Djordjevic M.A. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula. J Exp Bot 2013, 64:5395-5409.
51. Li S., Liu L., Zhuang X., Yu Y., Liu X., Cui X., Ji L., Pan Z., Cao X., Mo B., et al. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 2013, 153:562-574.
52. De Luis A., Markmann K., Cognat V., Holt D.B., Charpentier M., Parniske M., Stougaard J., Voinnet O. Two microRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiol 2012, 160:2137-2154.
53. Ikeuchi M., Sugimoto K., Iwase A. Plant callus: mechanisms of induction and repression. Plant Cell 2013, 25:3159-3173.
54. Kosuta S., Held M., Hossain M.S., Morieri G., Macgillivary A., Johansen C., Antolin-Llovera M., Parniske M., Oldroyd G.E., Downie A.J., et al. Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant J 2011, 67:929-940.
55. Karas B., Murray J., Gorzelak M., Smith A., Sato S., Tabata S., Szczyglowski K. Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti involves the nodulation factor-dependent induction of root hairs. Plant Physiol 2005, 137:1331-1344.