Long-distance transport of signals during symbiosis are nodule formation and mycorrhization autoregulated in a similar way?

Plant Signaling and Behavior

Volumn 6, Issue 3, 2011, Pages 372-377

  Staehelin, Christian ^a   Xie, Zhi Ping ^a   Illana, Antonio ^a   Vierheilig, Horst ^a  

^a CSIC   (Spain)

Author keywords

Arbuscular mycorrhiza; Autoregulation; CLE peptides; Mutant; Nodulation; Split root system

Indexed keywords

BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; LEGUME; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SYMBIOSIS;

FABACEAE; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; MODELS, BIOLOGICAL; MYCORRHIZAE; SIGNAL TRANSDUCTION; SYMBIOSIS;

ARBUSCULAR; FUNGI; MAGNOLIOPHYTA;

EID: 79956195068     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.6.3.13881     Document Type: Review

References (69)

1. Perret X, Staehelin C, Broughton WJ. Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 2000; 64:180-201.
2. Gibson KE, Kobayashi H, Walker GC. Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 2008; 42:413-441.
3. Reinhardt D. Programming good relations-development of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 2007; 10:98-105.
4. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 2008; 6:763-775.
5. Caetano-Anolés G, Gresshoff PM. Plant genetic control of nodulation. Annu Rev Microbiol 1991; 45:345-382.
6. Kinkema M, Scott PT, Gresshoff PM. Legume nodulation: successful symbiosis through short- and longdistance signalling. Funct Plant Biol 2006; 33:707-721.
7. Oka-Kira E, Kawaguchi M. Long-distance signaling to control root nodule number. Curr Opin Plant Biol 2006; 9:496-502.
8. Magori S, Kawaguchi M. Long-distance control of nodulation: molecules and models. Mol Cells 2009; 27:129-134.
9. Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, et al. Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 2010; 52:61-76.
10. Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y. Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem 2000; 32:589-595.
11. Vierheilig H, Maier W, Wyss U, Samson J, Strack D, Piché Y. Cyclohexenone derivative- and phosphate-levels in split-root systems and their role in the systemic suppression of mycorrhization in precolonized barley plants. J Plant Physiol 2000; 157:593-599.
12. Catford JG, Staehelin C, Lerat S, Piché Y, Vierheilig H. Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 2003; 54:1481-1487.
13. Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H. Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 2005; 222:709-715.
14. Shrihari PC, Sakamoto K, Inubushi K, Akao S. Interaction between supernodulating or non-nodulat-ing mutants of soybean and two arbuscular mycorrhizal fungi. Mycorrhiza 2000; 10:101-106.
15. Morandi D, Sagan M, Prado-Vivant E, Duc G. Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza 2000; 10:37-42.
16. Solaiman MZ, Senoo K, Kawaguchi M, lmaizumi-Anraku H, Akao S, Tanaka A, et al. Characterization of mycorrhizas formed by Glomus sp. on roots of hypernodulating mutants of Lotus japonicus. J Plant Res 2000; 113:443-448.
17. Oelkers K, Goffard N, Weiller GF, Gresshoff PM, Mathesius U, Frickey T. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol 2008; 8:1-15.
18. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, et al. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 2009; 50:67-77.
19. Mortier V, Den Herder G, Whitford R, Van de velde W, Rombauts S, D'haeseleer K, et al. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 2010; 153:222-237.
20. Jun JH, Fiume E, Fletcher JC. The CLE family of plant polypeptide signaling molecules. Cell Mol Life Sci 2008; 65:743-755.
21. Mitchum MG, Wang XH, Davis EL. Diverse and conserved roles of CLE peptides. Curr Opin Plant Biol 2008; 11:75-81.
22. Miwa H, Kinoshita A, Fukuda H, Sawa S. Plant meri-stems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. J Plant Res 2009; 122:31-39.
23. Wang G, Fiers M. CLE peptide signaling during plant development. Protoplasma 2010; 240:33-43.
24. van Brussel AAN, Tak T, Boot KJM, Kijne JW. 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 2002; 15:341-349.
25. Li DX, Kinkema M, Gresshoff PM. Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation. J Plant Physiol 2009; 166:955-967.
26. Novák K Early action of pea symbiotic gene NOD3 is confirmed by adventitious root phenotype. Plant Sci 2010; 179:472-478.
27. Combier JP, Küster H, Journet EP, Hohnjec N, Gamas P, Niebel A. Evidence for the involvement in nodulation of the two small putative regulatory peptide-encoding genes MtRALFL1 and MtDVL1. Mol Plant Microbe Interact 2008; 21:1118-1127.
28. Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM. Plant peptides in signalling: looking for new partners. Trends Plant Sci 2009; 14:255-263.
29. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, et al. Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 2002; 420:422-426.
30. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, et al. HAR1 mediates systemic regulation of symbiotic organ development. Nature 2002; 420:426-429.
31. Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, et al. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 2003; 299:109-112.
32. Penmetsa RV, Frugoli JA, Smith LS, Long SR, Cook DR. Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol 2003; 131:998-1008.
33. Schnabel E, Journet EP, Carvalho-Niebel F, Duc G, Frugoli J. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 2005; 58:809-822.
34. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y Arabidopsis CLV3 peptide directly binds CLV1 ectodo-main. Science 2008; 319:294.
35. Miyahara A, Hirani TA, Oakes M, Kereszt A, Kobe B, Djordjevic MA, et al. Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro. J Biol Chem 2008; 283:25381-25391.
36. Oka-Kira E, Tateno K, Miura Ki, Haga T, Hayashi M, Harada K, et al. klavier (klv), a novel hypernodula-tion mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant J 2005; 44:505-515.
37. Lin YH, Ferguson BJ, Kereszt A, Gresshoff PM. Suppression of hypernodulation in soybean by a leaf-extracted, NARK- and Nod factor-dependent, low molecular mass fraction. New Phytol 2010; 185:1074-1086.
38. Yamaya H, Arima Y. Evidence that a shoot-derived substance is involved in regulation of the super-nodulation trait in soybean. Soil Sci Plant Nutr 2010; 56:115-122.
39. Yamaya H, Arima Y. Shoot-synthesized nodulation-restricting substances are present in the medium-polarity fraction of shoot extracts from wild-type soybean plants. Soil Sci Plant Nutr 2010; 56:418-421.
40. Kenjo T, Yamaya H, Arima Y Shoot-synthesized nodu-lation-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 2010; 56:399-406.
41. Magori S, Oka-Kira E, Shibata S, Umehara Y, Kouchi H, Hase Y, et al. TOO MUCH LOVE, a root regulator associated with the long-distance control of nodulation in Lotus japonicus. Mol Plant Microbe Interact 2009; 22:259-268.
42. Magori S, Kawaguch M. Analysis of two potential long-distance signaling molecules, LjCLE-RS1/2 and jasmonic acid, in a hypernodulating mutant too much love. Plant Signal Behav 2010; 5:403-405.
43. Caba JM, Luz centeno M, Fernández B, Gresshoff PM, Ligero F. Inoculation and nitrate alter phyto-hormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 2000; 211:98-104.
44. Nakagawa T, Kawaguchi M. Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol 2006; 47:176-180.
45. van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U. Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol 2006; 140:1494-1506.
46. Kinkema M, Gresshoff PM. Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol Plant Microbe Interact 2008; 21:1337-1348.
47. Gresshoff PM, Lohar D, Chan PK, Biswas B, Jiang Q, Reid D, et al. Genetic analysis of ethylene regulation of legume nodulation. Plant Signal Behav 2009; 4:818-823.
48. Seo HS, Li J, Lee SY, Yu JW, Kim KH, Lee SH, et al. The hypernodulating nts mutation induces jasmonate synthetic pathway in soybean leaves. Mol Cells 2007; 24:185-193.
49. Catford J, Staehelin C, Larose G, Piché Y, Vierheilig H. Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 2006; 285:257-266.
50. Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM, De Bruijn FJ, et al. Short root mutant of Lotus japonicus with a dramatically altered symbiotic pheno-type. Plant J 2000; 23:97-114.
51. Nishimura R, Ohmori M, Kawaguchi M. The novel symbiotic phenotype of enhanced-nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone. Plant Cell Physiol j 2002; 43:853-859.
52. Nishimura R, Ohmori M, Fujita H, Kawaguchi M. A Lotus basic leucine zipper protein with a ring-finger motif negatively regulates the developmental program of nodulation. Proc Natl Acad Sci USA 2002; 99:15206-15210.
53. Morandi D, Le Signor C, Gianinazzi-Pearson V, Duc G. A Medicago truncatula mutant hyper-responsive to mycorrhiza and defective for nodulation. Mycorrhiza 2009; 19:435-441.
54. Vierheilig H. Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J Plant Physiol 2004; 161:339-341.
55. Vierheilig H. Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 2004; 82:1166-1176.
56. Meixner C, Vegvari G, Ludwig-Müller J, Gagnon H, Steinkellner S, Staehelin C, et al. Two defined alleles of the LRR receptor kinase GmNARK in supernodulating soybean govern differing autoregulation of mycorrhization. Physiol Plant 2007; 130:261-270.
57. Sakamoto K, Nohara Y Soybean (Glycine max [L.] Merr.) shoots systemically control arbuscule formation in mycorrhizal symbiosis. Soil Sci Plant Nutr 2009; 55:252-257.
58. Amiour N, Recorbet G, Robert F, Gianinazzi S, Dumas-Gaudot E. Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Mol Plant Microbe Interact 2006; 19:988-997.
59. Germain H, Chevalier E, Matton DP. Plant bioactive peptides: an expanding class of signaling molecules. Can J Bot 2006; 84:1-19.
60. Khaosaad T, Staehelin C, Steinkellner S, Hage-Ahmed K, Ocampo JA, Garcia-Garrido JM, et al. The Rhizobium sp. strain NGR234 systemically suppresses arbuscular mycorrhizal root colonization in a split-root system of barley (Hordeum vulgare). Physiol Plant 2010; 140:238-245.
61. Vierheilig H, Lerat S, Piché Y.Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 2003; 13:167-170.
62. Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 2009; 60:379-406.
63. Khaosaad T, Garcia-Garrido JM, Steinkellner S, Vierheilig H. Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 2007; 39:727-734.
64. Vierheilig H, Steinkellner S, Khaosaad T, Garcia-Garrido JM. The biocontrol effect of mycorrhization on soil-borne fungal pathogens and the autoregulation of the AM symbiosis: one mechanism, two effects? In: Varma A, Ed. Mycorrhiza: Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics. Heidelberg: Springer, 2008; 307-320.
65. Heil- M, Ton J. Long-distance signalling in plant defence. Trends Plant Sci 2008; 13:264-272.
66. Lohar DP, Bird DM. Lotus japonicus: A new model to study root-parasitic nematodes. Plant Cell Physiol 2003; 44:1176-1184.
67. Tazawa J, Takahashi M, Usuki K, Yamamoto H. Nodulation during vegetative growth of soybean stage does not affect the susceptibility to red crown rot caused by Calonectria ilicicola. J Gen Plant Pathol 2007; 73:180-184.
68. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y.A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 2009; 5:578-580.
69. Funayama-Noguchi S, Noguchi K, Yoshida C, Kawaguchi M. Two CLE genes are induced by phosphate in roots of Lotus japonicus. J Plant Res 2010; 124:155-163.