TOO MUCH LOVE, a novel kelch repeat-containing F-box protein, functions in the long-distance regulation of the LEGUME-rhizobium symbiosis

Plant and Cell Physiology

Volumn 54, Issue 4, 2013, Pages 433-447

  Takahara, Masahiro ^a,b   Magori, Shimpei ^c   Soyano, Takashi ^b   Okamoto, Satoru ^b   Yoshida, Chie ^d   Yano, Koji ^b   Sato, Shusei ^e   Tabata, Satoshi ^e   Yamaguchi, Katsushi ^b   Shigenobu, Shuji ^a,b   Takeda, Naoya ^a,b   Suzaki, Takuya ^a,b   Kawaguchi, Masayoshi ^a,b  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^c STONY BROOK UNIVERSITY   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

^e KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Autoregulation of nodulation; CLE; HAR1; Lotus japonicus; Systemic regulation; TOO MUCH LOVE

Indexed keywords

F BOX PROTEIN; VEGETABLE PROTEIN;

ARTICLE; FABACEAE; GENETICS; LOTUS; METABOLISM; MICROBIOLOGY; NODULATION; PHYSIOLOGY; RHIZOBIUM; SYMBIOSIS;

F-BOX PROTEINS; FABACEAE; LOTUS; PLANT PROTEINS; PLANT ROOT NODULATION; RHIZOBIUM; ROOT NODULES, PLANT; SYMBIOSIS;

LOTUS CORNICULATUS VAR. JAPONICUS; RHIZOBIUM;

EID: 84875980016     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct022     Document Type: Article

References (76)

1. Akashi, K., Yamaya, H. and Arima, Y. (2010) Shoot-synthesized nodulation-restricting substances of wild type soybean present in two different high-performance liquid chromatography peaks of the ethanol-soluble medium-polarity fraction. Soil Sci. Plant Nutr. 56: 399-406.
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: I. Localization of infectible root cells. Plant Physiol. 66: 1027-1031.
3. Bishopp, A., Help, H. and Helariutta, Y. (2009) Cytokinin signaling during root development. Int. Rev. Cell Mol. Biol. 276: 1-48.
4. Broughton, W.J. and Dilworth, M.J. (1971) Control of leghaemoglobin synthesis in snake beans. Biochem. J. 125: 1075-1080.
5. Caetano-Anollés, G. and Gresshoff, P.M. (1991) Plant genetic control of nodulation. Annu. Rev. Microbiol. 45: 345-382.
6. Catford, J.G., Staehelin, C., Lerat, S., Piche, Y. and Vierheilig, H. (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J. Exp. Bot. 54: 1481-1487.
7. Chu, H., Qian, Q., Liang, W., Yin, C., Tan, H., Yao, X. et al. (2006) The FLORAL ORGAN NUMBER4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiol. 142: 1039-1052.
8. Colebatch, G., Desbrosses, G., Ott, T., Krusell, L., Montanari, O., Kloska, S. et al. (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39: 487-512.
9. 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.
10. Ehrhardt, D.W., Wais, R. and Long, S.R. (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673-681.
11. Ferguson, B.J., Indrasumunar, A., Hayashi, S., Lin, M.H., Lin, Y.H., Reid, D.E. et al. (2010) Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52: 61-76.
12. Foo, E., Yoneyama, K., Hugill, C.J., Quittenden, L.J. and Reid, J.B. (2012) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol. Plant 6: 76-87.
13. Fu, Z.Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N. et al. (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486: 228-232.
14. George, M.L.C. (1992) Nodulation suppression by Rhizobium leguminosarum bv. phaseoli in bean split-root systems. Symbiosis 12: 95-105.
15. Gomi, K., Sasaki, A., Itoh, H., Ueguchi-Tanaka, M., Ashikari, M., Kitano, H. et al. (2004) GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice. Plant J. 37: 626-634.
16. Gonzalez-Rizzo, S., Crespi, M. and 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.
17. Harmon, F.G. and Kay, S.A. (2003) The F box protein AFR is a positive regulator of phytochrome A-mediated light signaling. Curr. Biol. 13: 2091-2096.
18. Imaizumi, T., Schultz, T.F., Harmon, F.G., Ho, L.A. and Kay, S.A. (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309: 293-297.
19. Ito, S., Song, Y.H. and Imaizumi, T. (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol. Plant 5: 573-582.
20. Jeudy, C., Ruffel, S., Freixes, S., Tillard, P., Santoni, A.L., Morel, S. et al. (2010) Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses. New Phytol. 185: 817-828.
21. Kim, H.S. and Delaney, T.P. (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell 14: 1469-1482.
22. Kosslak, R.M. and Bohlool, B.B. (1984) Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiol. 75: 125-130.
23. Krusell, L., Madsen, L.H., Sato, S., Aubert, G., Genua, A., Szczyglowski, K. et al. (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420: 422-426.
24. Krusell, L., Sato, N., Fukuhara, I., Koch, B.E., Grossmann, C., Okamoto, S. et al. (2011) The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation. Plant J. 65: 861-871.
25. Kuppusamy, K.T., Ivashuta, S., Bucciarelli, B., Vance, C.P., Gantt, J.S. and Vandenbosch, K.A. (2009) Knockdown of CELL DIVISION CYCLE16 reveals an inverse relationship between lateral root and nodule numbers and a link to auxin in Medicago truncatula. Plant Physiol. 151: 1155-1166.
26. 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.
27. 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, low molecular mass fraction. New Phytol. 185: 1074-1086.
28. Lin, Y.H., Lin, M.H., Gresshoff, P.M. and Ferguson, B.J. (2011) An efficient petiole-feeding bioassay for introducing aqueous solutions into dicotyledonous plants. Nat. Protoc. 6: 36-45.
29. Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B., Bek, A.S. et al. (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun. 1: 10.
30. Maekawa, T., Kusakabe, M., Shimoda, Y., Sato, S., Tabata, S., Murooka, Y. et al. (2008) Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol. Plant-Microbe Interact. 21: 375-382.
31. Magori, S., Oka-Kira, E., Shibata, S., Umehara, Y., Kouchi, H., Hase, Y. et al. (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.
32. Mathesius, U., Weinman, J.J., Rolfe, B.G. and Djordjevic, M.A. (2000) Rhizobia can induce nodules in white clover by hijacking mature cortical cells activated during lateral root development. Mol. Plant-Microbe Interact. 13: 170-182.
33. Miwa, H., Sun, J., Oldroyd, G.E. and Downie, J.A. (2006) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol. Plant-Microbe Interact. 19: 914-923.
34. Miyazawa, H., Oka-Kira, E., Sato, N., Takahashi, H., Wu, G.J., Sato, S. et al. (2010) The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 137: 4317-4325.
35. Mortier, V., Den Herder, G., Whitford, R., Van de Velde, W., Rombauts, S., DHaeseleer, K. et al. (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol. 153: 222-237.
36. Mortier, V., Fenta, B.A., Martens, C., Rombauts, S., Holsters, M., Kunert, K. et al. (2011) Search for nodulation-related CLE genes in the genome of Glycine max. J. Exp. Bot. 62: 2571-2583.
37. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y. et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104: 34-41.
38. Nishimura, R., Hayashi, M., Wu, G.J., Kouchi, H., Imaizumi-Anraku, H., Murakami, Y. et al. (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420: 426-429.
39. Nutman, P.S. (1952) Studies on the physiology of nodule formation. Ann. Bot. 16: 79-103.
40. Ogawa, M., Shinohara, H., Sakagami, Y. and Matsubayashi, Y. (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294.
41. Oka-Kira, E., Tateno, K., Miura, K., Haga, T., Hayashi, M., Harada, K. 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.
42. Okamoto, S., Ohnishi, E., Sato, S., Takahashi, H., Nakazono, M., Tabata, S. et al. (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 50: 67-77.
43. Oldroyd, G.E., Engstrom, E.M. and Long, S.R. (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13: 1835-1849.
44. Oldroyd, G.E., Murray, J.D., Poole, P.S. and Downie, J.A. (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet 45: 119-144.
45. Olsson, J.E., Nakao, P., Bohlool, B.B. and Gresshoff, P.M. (1989) Lack of systemic suppression of nodulation in split root systems of supernodulating soybean (Glycine max [L.] Merr.) mutants. Plant Physiol. 90: 1347-1352.
46. Pant, B.D., Musialak-Lange, M., Nuc, P., May, P., Buhtz, A., Kehr, J. et al. (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 150: 1541-1555.
47. Penmetsa, R.V., Frugoli, J.A., Smith, L.S., Long, S.R. and Cook, D.R. (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol. 131: 998-1008.
48. Pierce, M. and Bauer, W.D. (1983) A rapid regulatory response governing nodulation in soybean. Plant Physiol. 73: 286-290.
49. Reid, D.E., Ferguson, B.J. and Gresshoff, P.M. (2011) Inoculation-and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol. Plant-Microbe Interact. 24: 606-618.
50. Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl Acad. Sci. USA 108: 18524-18529.
51. Sagan, M. and Duc, G. (1996) Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L.). Symbiosis 20: 229-245.
52. Sargent, L., Huang, S.Z., Rolfe, B.G. and Djordjevic, M.A. (1987) Split-root assays using Trifolium subterraneum show that Rhizobium infection induces a systemic response that can inhibit nodulation of another invasive Rhizobium strain. Appl. Environ. Microbiol. 53: 1611-1619.
53. 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.
54. Schnabel, E., Mukherjee, A., Smith, L., Kassaw, T., Long, S. and Frugoli, J. (2010) The lss supernodulation mutant of Medicago truncatula reduces expression of the SUNN gene. Plant Physiol. 154: 1390-1402.
55. Schumann, N., Navarro-Quezada, A., Ullrich, K., Kuhl, C. and Quint, M. (2011) Molecular evolution and selection patterns of plant F-box proteins with C-terminal kelch repeats. Plant Physiol. 155: 835-850.
56. Searle, I.R., Men, A.E., Laniya, T.S., Buzas, D.M., Iturbe-Ormaetxe, I., Carroll, B.J. et al. (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299: 109-112.
57. Sheng, C. and Harper, J.E. (1997) Shoot versus root signal involvement in nodulation and vegetative growth in wild type and hypernodulating soybean genotypes. Plant Physiol. 113: 825-831.
58. Singleton, P.W. (1983) A split-root growth system for evaluating the effect of salinity on components of the soybean Rhizobium japonicum symbiosis. Crop Sci. 23: 259-262.
59. Sun, J., Cardoza, V., Mitchell, D.M., Bright, L., Oldroyd, G. and Harris, J.M. (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J. 46: 961-970.
60. Sun, L., Shi, W., Li, L., Yu, W., Liang, J., Zhang, H. et al. (2009) JFK, a Kelch domain-containing F-box protein, links the SCF complex to p53 regulation. Proc. Natl Acad. Sci. USA 106: 10195-10200.
61. Suzaki, T., Ohneda, M., Toriba, T., Yoshida, A. and Hirano, H.Y. (2009) FON2 SPARE1 redundantly regulates floral meristem maintenance with FLORAL ORGAN NUMBER2 in rice. PLoS Genet. 5: e1000693.
62. Suzaki, T., Yano, K., Ito, M., Umehara, Y., Suganuma, N. and 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.
63. Suzaki, T., Yoshida, A. and Hirano, H.Y. (2008) Functional diversification of CLAVATA3-related CLE proteins in meristem maintenance in rice. Plant Cell 20: 2049-2058.
64. Suzuki, A., Hara, H., Kinoue, T., Abe, M., Uchiumi, T., Kucho, K. et al. (2008) Split-root study of autoregulation of nodulation in the model legume Lotus japonicus. J. Plant Res. 121: 245-249.
65. Szczyglowski, K., Shaw, R.S., Wopereis, J., Copeland, S., Hamburger, D., Kasiborski, B. et al. (1998) Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant-Microbe Interact. 11: 684-697.
66. Takase, T., Nishiyama, Y., Tanihigashi, H., Ogura, Y., Miyazaki, Y., Yamada, Y. et al. (2011) LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1. Plant J. 67: 608-621.
67. Tirichine, L., Sandal, N., Madsen, L.H., Radutoiu, S., Albrektsen, A.S., Sato, S. et al. (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315: 104-107.
68. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N. et al. (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200.
69. Wais, R.J., Galera, C., Oldroyd, G., Catoira, R., Penmetsa, R.V., Cook, D. et al. (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc. Natl Acad. Sci. USA 97: 13407-13412.
70. Walker, S.A., Viprey, V. and Downie, J.A. (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.
71. Wopereis, J., Pajuelo, E., Dazzo, F.B., Jiang, Q., Gresshoff, P.M., de Bruijn, F.J. et al. (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J. 23: 97-114.
72. Yamaya, H. and Arima, Y. (2010a) Evidence that a shoot-derived substance is involved in regulation of the super-nodulation trait in soybean. Soil Sci. Plant Nutr. 56: 115-122.
73. Yamaya, H. and Arima, Y. (2010a) Shoot-synthesized nodulationrestricting substances are present in the medium-polarity fraction of shoot extracts from wild-type soybean plants. Soil Sci. Plant Nutr. 56: 418-421.
74. Yendrek, C.R., Lee, Y.C., Morris, V., Liang, Y., Pislariu, C.I., Burkart, G. et al. (2010) A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. Plant J. 62: 100-112.
75. Yokota, K., Li, Y.Y., Hisatomi, M., Wang, Y., Ishikawa, K., Liu, C.T. et al. (2009) Root-determined hypernodulation mutant of Lotus japonicus shows high-yielding characteristics. Biosci. Biotechnol. Biochem. 73: 1690-1692.
76. Yoshida, S., Kameoka, H., Tempo, M., Akiyama, K., Umehara, M., Yamaguchi, S. et al. (2012) The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytol. 196: 1208-1216.