Transient Nod factor-dependent gene expression in the nodulation-competent zone of soybean (Glycine max [L.] Merr.) roots

Plant Biotechnology Journal

Volumn 10, Issue 8, 2012, Pages 995-1010

  Hayashi, Satomi ^a   Reid, Dugald E ^a   Lorenc, Michał T ^a   Stiller, Jiri ^a   Edwards, David ^a   Gresshoff, Peter M ^a   Ferguson, Brett J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Legume; Nodule; Plant development; Signalling; Symbiosis; Transcriptome

Indexed keywords

GIBBERELLIC ACID; GIBBERELLIN; LIPOPOLYSACCHARIDE; MESSENGER RNA;

ARTICLE; BIOSYNTHESIS; BRADYRHIZOBIUM; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; NODULATION; PHYSIOLOGY; PLANT GENE; SOYBEAN; SYMBIOSIS;

BRADYRHIZOBIUM; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GIBBERELLINS; LIPOPOLYSACCHARIDES; PLANT ROOT NODULATION; RNA, MESSENGER; ROOT NODULES, PLANT; SOYBEANS; SYMBIOSIS;

BRADYRHIZOBIUM; BRADYRHIZOBIUM JAPONICUM; GLYCINE MAX; RHIZOBIACEAE;

EID: 84865733578     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2012.00729.x     Document Type: Article

References (74)

1. Beveridge, C.A., Mathesius, U., Rose, R.J. and Gresshoff, P.M. (2007) Common regulatory themes in meristem development and whole plant homeostasis. Curr. Opin. Plant Biol. 10, 44-51.
2. Bhuvaneswari, T.V., Turgeon, B.G. and Bauer, W.D. (1980) Early events in the infection of soybean (Glycine max L. Merr.) by Rhizobium japonicum: 1. Localization of infectible root cells. Plant Physiol. 66, 1027-1031.
3. Biswas, B., Chan, P.K. and Gresshoff, P.M. (2009) A novel ABA insensitive mutant of Lotus japonicus with a wilty phenotype but unaltered nodulation regulation. Mol. Plant, 2, 487-499.
4. Brechenmacher, L., Kim, M.Y., Benitez, M., Li, M., Joshi, T., Calla, B., Lee, M.P., Libault, M., Vodkin, L.O., Xu, D., Lee, S.H., Clough, S.J. and Stacey, G. (2008) Transcription profiling of soybean nodulation by Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 21, 631-645.
5. Caetano-Anollés, G. and Gresshoff, P.M. (1991) Plant genetic-control of nodulation. Annu. Rev. Microbiol. 45, 345-382.
6. Calvert, H.E., Pence, M.K., Pierce, M., Malik, N.S.A. and Bauer, W.D. (1984) Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots. Can. J. Bot. 62, 2375-2384.
7. Carroll, B.J., McNeil, D.L. and Gresshoff, P.M. (1985) Isolation and properties of soybean mutants which nodulate in the presence of high nitrate concentrations. Proc. Natl Acad. Sci. USA, 82, 4162-4166.
8. Colebatch, G., Desbrosses, G., Ott, T., Krusell, L., Montanari, O., Kloska, S., Kopka, J. and Udvardi, M.K. (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39, 487-512.
9. Cosgrove, D.J. (2000) Loosening of plant cell walls by expansins. Nature, 407, 321-326.
10. Crespi, M. and Frugier, F. (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Sci. Signal. 1, 1-8.
11. Delves, A.C., Mathews, A., Day, D.A., Carter, A.S., Carroll, B.J. and Gresshoff, P.M. (1986) Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol. 82, 588-590.
12. Dénarié, J., Debelle, F. and Prome, J.C. (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503-535.
13. Desbrosses, G.J. and Stougaard, J. (2011) Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe, 10, 348-358.
14. Dinesh-Kumar, S.P., Tham, W.H. and Baker, B.J. (2000) Structure-function analysis of the tobacco mosaic virus resistance gene N. Proc. Natl Acad. Sci. USA, 97, 14789-14794.
15. El Yahyaoui, F., Küster, H., Ben Amor, B., Hohnjec, N., Pühler, A., Becker, A., Gouzy, J., Vernié, T., Gough, C., Niebel, A., Godiard, L. and Gamas, P. (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol. 136, 3159-3176.
16. Ferguson, B.J. (2012) Rhizobia and legume nodulation genes. In Brenner's Online Encyclopedia of Genetics, 2nd edn (Maloy, S. and Hughes, K., eds). Oxford, UK: Elsevier, In press.
17. Ferguson, B.J. and Gresshoff, P.M. (2009) Soybean as a model legume. Grain Legumes, 53, 7.
18. Ferguson, B.J. and Mathesius, U. (2003) Signaling interactions during nodule development. J. Plant Growth Regul. 22, 47-72.
19. Ferguson, B.J., Ross, J.J. and Reid, J.B. (2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiol. 138, 2396-2405.
20. Ferguson, B.J., Indrasumunar, A., Hayashi, S., Lin, M.-H., Lin, Y.-H., Reid, D.E. and Gresshoff, P.M. (2010) Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52, 61-76.
21. Ferguson, B.J., Foo, E., Ross, J.J. and Reid, J.B. (2011) Relationship between gibberellin, ethylene and nodulation in Pisum sativum. New Phytol. 189, 829-842.
22. Franssen, H.J., Thompson, D.V., Idler, K., Kormelink, R., Vankammen, A. and Bisseling, T. (1990) Nucleotide-sequence of two soybean ENOD2 early nodulin genes encoding Ngm-75. Plant Mol. Biol. 14, 103-106.
23. Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.C., Jaubert, M., Simon, D., Cartieaux, F., Prin, Y., Bena, G., Hannibal, L., Fardoux, J., Kojadinovic, M., Vuillet, L., Lajus, A., Cruveiller, S., Rouy, Z., Mangenot, S., Segurens, B., Dossat, C., Franck, W.L., Chang, W.S., Saunders, E., Bruce, D., Richardson, P., Normand, P., Dreyfus, B., Pignol, D., Stacey, G., Emerich, D., Verméglio, A., Médigue, C. and Sadowsky, M. (2007) Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science, 316, 1307-1312.
24. Gresshoff, P.M. (2012) Glycine max (Soybean). In Brenner's Online Encyclopedia of Genetics, 2nd edn (Maloy, S. and Hughes, K., eds). Oxford, UK: Elsevier, In press.
25. Gresshoff, P.M. and Delves, A.C. (1986) Plant genetic approaches to symbiotic nodulation and nitrogen fixation in legumes. In Plant Gene Research. III. A Genetical Approach to Plant Biochemistry (Blonstein, A.D. and King, P.J., eds), pp. 156-206. Vienna, Austria: Springer-Verlag.
26. Han, L., Hanan, J. and Gresshoff, P.M. (2010) Computational Complementation: a modelling approach to study signalling mechanisms during legume autoregulation of nodulation. PLoS Comput. Biol. 6, e1000685.
27. Hayashi, S., Gresshoff, P.M. and Kinkema, M. (2008) Molecular analysis of lipoxygenases associated with nodule development in soybean. Mol. Plant-Microbe Interact. 21, 843-853.
28. Herridge, D.F. (1977) Carbon and nitrogen nutrition of two annual legumes. PhD dissertation. Perth, WA, Australia: University of Western Australia.
29. Indrasumunar, A., Kereszt, A., Searle, I., Miyagi, M., Li, D., Nguyen, C.D.T., Men, A., Carroll, B.J. and Gresshoff, P.M. (2010) Inactivation of duplicated Nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol. 51, 201-214.
30. Indrasumunar, A., Searle, I., Lin, M.-H., Kereszt, A., Men, A., Carroll, B.J. and Gresshoff, P.M. (2011) Nodulation factor receptor kinase 1a controls nodule organ number in soybean (Glycine max L. Merr.). Plant J. 65, 39-50.
31. Jones, K.M., Sharopova, N., Lohar, D.P., Zhang, J.Q., VandenBosch, K.A. and Walker, G.C. (2008) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc. Natl Acad. Sci. USA, 105, 704-709.
32. Kinkema, M. and Gresshoff, P.M. (2008) Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol. Plant-Microbe Interact. 21, 1337-1348.
33. Kosslak, R.M., Bookland, R., Barkei, J., Paaren, H.E. and Applebaum, E.R. (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc. Natl Acad. Sci. USA, 84, 7428-7432.
34. Kouchi, M. and Hata, S. (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol. Gen. Genet. 238, 106-119.
35. Krusell, L., Madsen, L.H., Sato, S., Aubert, G., Genua, A., Szczyglowski, K., Duc, G., Kaneko, T., Tabata, S., de Bruijn, F., Pajuelo, E., Sandal, N. and Stougaard, J. (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature, 420, 422-426.
36. Lam, H.M., Xu, X., Liu, X., Chen, W., Yang, G., Wong, F.L., Li, M.-W., He, W., Qin, N., Wang, B., Li, J., Jian, M., Wang, J., Shao, G., Wang, J., Sun, S.S. and Zhang, G. (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42, 1053-1059.
37. Leigh, J.A., Signer, E.R. and Walker, G.C. (1985) Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl Acad. Sci. USA, 82, 6231-6235.
38. Li, R.Q., Li, Y.R., Kristiansen, K. and Wang, J. (2008) SOAP: short oligonucleotide alignment program. Bioinformatics, 24, 713-714.
39. Li, D., Kinkema, M. and Gresshoff, P.M. (2009) Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation. J. Plant Physiol. 166, 955-967.
40. Libault, M., Farmer, A., Brechenmacher, L., Drnevich, J., Langley, R.J., Bilgin, D.D., Radwan, O., Neece, D.J., Clough, S.J., May, G.D. and Stacey, G. (2010a) Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol. 152, 541-552.
41. Libault, M., Farmer, A., Joshi, T., Takahashi, K., Langley, R.J., Franklin, L.D., He, J., Xu, D., May, G. and Stacey, G. (2010b) An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J. 63, 86-99.
42. Lievens, S., Goormachtig, S. and Holsters, M. (2001) A critical evaluation of differential display as a tool to identify genes involved in legume nodulation: looking back and looking forward. Nucleic Acids Res. 29, 3459-3468.
43. Lievens, S., Goormachtig, S., Den Herder, J., Capoen, W., Mathis, R., Hedden, P. and Holsters, M. (2005) Gibberellins are involved in nodulation of Sesbania rostrata. Plant Physiol. 139, 1366-1379.
44. Lim, C.W., Lee, Y.W. and Hwang, C.H. (2011) Soybean nodule-enhanced CLE peptides in roots act as signals in GmNARK-mediated nodulation suppression. Plant Cell Physiol. 52, 1613-1627.
45. Lin, Y.-H., Ferguson, B.J., Kereszt, A. and Gresshoff, P.M. (2010) Suppression of hypernodulation in soybean by a leaf-extracted, NARK- and Nod factor-dependent small molecular fraction. New Phytol. 185, 1074-1086.
46. Lin, M.-H., Gresshoff, P.M., Indrasumunar, A. and Ferguson, B.J. (2011a) pHairyRed: a novel binary vector containing the DsRed2 reporter gene for visual selection of transgenic hairy roots. Mol. Plant, 4, 537-545.
47. Lin, Y.-H., Lin, M.-H., Gresshoff, P.M. and Ferguson, B.J. (2011b) An efficient petiole-feeding bioassay for introducing aqueous solutions into dicotyledonous plants. Nat. Protoc. 6, 36-45.
48. Lohar, D.P., Sharopova, N., Endre, G., Penuela, S., Samac, D., Town, C., Silverstein, K.A.T. and VandenBosch, K.A. (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol. 140, 221-234.
49. Maguire, T.L., Grimmond, S., Forrest, A., Iturbe-Ormaetxe, I., Meksem, K. and Gresshoff, P.M. (2002) Tissue-specific gene expression in soybean (Glycine max) detected by cDNA microarray analysis. J. Plant Physiol. 159, 1361-1374.
50. Mathesius, U., Mulers, S., Gao, M., Teplitski, M., Caetano-Anollés, G., Rolfe, B.G. and Bauer, W.D. (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl Acad. Sci. USA, 100, 1444-1449.
51. Mathews, A., Carroll, B.J. and Gresshoff, P.M. (1989) Development of Bradyrhizobium infection in supernodulating and non-nodulating mutants of soybean (Glycine max [L.] Merrill). Protoplasma, 150, 40-47.
52. Mortier, V., Den Herder, G., Whitford, R., Van de Velde, W., Rombauts, S., D'Haeseleer, K., Holsters, M. and Goormachtig, S. (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol. 153, 222-237.
53. Munné-Bosch, S. (2005) The role of α-tocopherol in plant stress tolerance. J. Plant Physiol. 162, 743-748.
54. Nieuwkoop, A.J., Banfalvi, Z., Deshmane, N., Gerhold, D., Schell, M.G., Sirotkin, K.M. and Stacey, G. (1987) A locus encoding host range is linked to the common nodulation gene of Bradyrhizobium japonicum. J. Bacteriol. 169, 2631-2638.
55. Nishimura, R., Hayashi, M., Wu, G.J., Kouchi, H., Imaizumi-Anraku, H., Murakami, Y., Kawasaki, S., Akao, S., Ohmori, M., Nagasawa, M., Harada, K. and Kawaguchi, M. (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature, 420, 426-429.
56. Okamoto, S., Ohnishi, E., Sato, S., Takahashi, H., Nakazono, M., Tabata, S. and Kawaguchi, M. (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 50, 67-77.
57. Oldroyd, G.E.D. and Downie, J.M. (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546.
58. Peters, N.K., Frost, J.W. and Long, S.R. (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science, 233, 977-980.
59. Ramakers, C., Ruijter, J.M., Deprez, R.H.L. and Moorman, A.F.M. (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-66.
60. Redmond, J.W., Batley, M., Djordjevic, M.A., Innes, R.W., Kuempel, P.L. and Rolfe, B.G. (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature, 323, 632-635.
61. Reid, D.E., Ferguson, B.J., Hayashi, S., Lin, Y.-H. and Gresshoff, P.M. (2011a) Molecular mechanisms controlling legume autoregulation of nodulation. Ann. Bot. 108, 789-795.
62. Reid, D.E., Ferguson, B.J. and Gresshoff, P.M. (2011b) NARK-dependent nodule regulation is activated in the shoot and root in response to inoculation and nitrate induced CLE peptides of soybean. Mol. Plant-Microbe Interact. 24, 606-618.
63. Reid, D.E., Hayashi, S., Lorenc, M., Stiller, J., Edwards, D., Gresshoff, P.M. and Ferguson, B.J. (2012) Identification of systemic responses in soybean nodulation by xylem sap feeding and complete transcriptome sequencing reveal a novel component of the autoregulation pathway. Plant Biotechnol. J. 10, 680-689.
64. Robinson, M.D. and Oshlack, A. (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25.
65. Sanjuan, J., Carlson, R.W., Spaink, H.P., Bhat, U.R., Barbour, W.M., Glushka, J. and Stacey, G. (1992) A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc. Natl Acad. Sci. USA, 89, 8789-8793.
66. Sato, T., Onoma, N., Fujikake, H., Ohtake, N., Sueyoshi, K. and Ohyama, T. (2001) Changes in four leghemoglobin components in nodules of hypernodulating soybean (Glycine max L. Merr.) mutant and its parent in the early nodule developmental stage. Plant Soil, 237, 129-135.
67. Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., Xu, D., Hellsten, U., May, G.D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, M.K., Sandhu, D., Valliyodan, B., Lindquist, E., Peto, M., Grant, D., Shu, S., Goodstein, D., Barry, K., Futrell-Griggs, M., Abernathy, B., Du, J., Tian, Z., Zhu, L., Gill, N., Joshi, T., Libault, M., Sethuraman, A., Zhang, X.C., Shinozaki, K., Nguyen, H.T., Wing, R.A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D., Stacey, G., Shoemaker, R.C. and Jackson, S.A. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178-183.
68. Schnabel, E., Journet, E.P., de Carvalho-Niebel, F., Duc, G. and 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.
69. Searle, I.R., Men, A.E., Laniya, T.S., Buzas, D.M., Iturbe-Ormaetxe, I., Carroll, B.J. and Gresshoff, P.M. (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science, 299, 109-112.
70. Severin, A.J., Woody, J.L., Bolon, Y.T., Joseph, B., Diers, B.W., Farmer, A.D., Muehlbauer, G.J., Nelson, R.T., Grant, D., Specht, J.E., Graham, M.A., Cannon, S.B., May, G.D., Vance, C.P. and Shoemaker, R.C. (2010) RNA-seq atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10, 160.
71. Spaink, H.P. (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54, 257-288.
72. Thimm, O., Blasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, L.A., Rhee, S.Y. and Stitt, M. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939.
73. Usadel, B., Nagel, A., Steinhauser, D., Gibon, Y., Bläsing, O.E., Redestig, H., Sreenivasulu, N., Krall, L., Hannah, M.A., Poree, F., Fernie, A.R. and Stitt, M. (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics, 7, 535.
74. Wiborg, O., Hyldignielsen, J.J., Jensen, E.O., Paludan, K. and Marcker, K.A. (1982) The nucleotide sequence of two leghemoglobin genes from soybean. Nucleic Acids Res. 10, 3487-3494.