Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis

New Phytologist

Volumn 189, Issue 1, 2011, Pages 347-355

  Chabaud, Mireille ^a   Genre, Andrea ^b   Sieberer, Björn J ^a   Faccio, Antonella ^b   Fournier, Joëlle ^a   Novero, Mara ^b   Barker, David G ^a   Bonfante, Paola ^b  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Arbuscular mycorrhiza; Calcium spiking; Common SYM pathway; Fungal plant signalling; Gigaspora spp.; Medicago truncatula; Nuclear localized cameleon; Spore exudates

Indexed keywords

ARBUSCULAR MYCORRHIZA; BIOASSAY; CALCIUM; ENDOSYMBIONT; EXUDATION; GENE EXPRESSION; GERMINATION; ION EXCHANGE; LEGUME;

ARTICLE; BARREL MEDIC; CALCIUM SIGNALING; CARROT; FUNGUS SPORE; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT;

CALCIUM SIGNALING; DAUCUS CAROTA; MEDICAGO TRUNCATULA; MYCORRHIZAE; PLANT ROOTS; SPORES, FUNGAL;

ARBUSCULAR; ASTERIDS; BACTERIA (MICROORGANISMS); DAUCUS CAROTA; FUNGI; GIGASPORA; MEDICAGO TRUNCATULA; ROSIDAE;

EID: 78649751639     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03464.x     Document Type: Article

References (44)

1. Akashi R, Kawano T, Hashiguchi M, Kutsuna Y, Hoffmann-Tsay SS, Hoffmann F. 2003. Super roots in Lotus corniculatus: a unique tissue culture and regeneration system in a legume species. Plant and Soil 255: 27-33.
2. Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827.
3. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Levy J, Debellé F, Baek JM, Kalo P et al. 2004. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303: 1364-1367.
4. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, De Carvalho-Niebel F, Journet EP, Ghérardi M, Huguet T et al. 2006. The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiology 142: 265-279.
5. Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, Imaizumi-Anraku H. 2008. Divergence of evolutionary ways among common Sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant and Cell Physiology 49: 1659-1671.
6. Bécard G, Fortin JA. 1988. Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytologist 108: 211-218.
7. Ben Amor B, Shaw SL, Oldroyd GED, Maillet F, Penmetsa RV, Cook D, Long SR, Dénarié J, Gough C. 2003. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant Journal 34: 495-506.
8. Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C, Barker DG. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14: 695-700.
9. Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G. 2000. The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Molecular Plant-Microbe Interactions 13: 693-698.
10. Capoen W, Oldroyd G, Goormachtig S, Holsters M. 2010. Sesbania rostrata: a case study of natural variation in legume nodulation. New Phytologist 186: 340-345.
11. Catoira R, Galéra C, De Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J. 2000. Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647-1665.
12. Chabaud M, Venard C, Defaux-Petras A, Bécard G, Barker DG. 2002. Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytologist 156: 265-273.
13. 2+ spiking and specific ENOD gene expression. Plant Physiology 136: 3582-3593.
14. Chen CY, Fan C, Gao MQ, Zhu HY. 2009. Antiquity and function of CASTOR and POLLUX, the twin ion channel-encoding genes key to the evolution of root symbioses in plants. Plant Physiology 149: 306-317.
15. 2+/calmodulin-dependent protein kinase. Plant Physiology 145: 1619-1628.
16. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB. 2002. A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966.
17. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P. 2008. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20: 1407-1420.
18. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG. 2005. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 3489-3499.
19. Gleason C, Chaudhuri S, Yang TB, Munoz A, Poovaiah BW, Oldroyd GED. 2006. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441: 1149-1152.
20. Gutjahr C, Novero M, Guether M, Montanari O, Udvardi M, Bonfante P. 2009. Presymbiotic factors released by the arbuscular mycorrhizal fungus Gigaspora margarita induce starch accumulation in Lotus japonicus roots. New Phytologist 183: 53-61.
21. Harrison MJ. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59: 19-42.
22. Kistner C, Parniske M. 2002. Evolution of signal transduction in intracellular symbiosis. Trends in Plant Science 7: 511-518.
23. Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G. 2003. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiology 131: 952-962.
24. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GED. 2008. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proceedings of the National Academy of Sciences, USA 105: 9823-9828.
25. Kuhn H, Küster H, Requena N. 2010. Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytologist 185: 716-733.
26. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
27. Markmann K, Giczey G, Parniske M. 2008. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biology 6: e68.
28. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proceedings of the National Academy of Sciences, USA 101: 4701-4705.
29. Miwa H, Sun J, Oldroyd GED, Downie JA. 2006. Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant Journal 48: 883-894.
30. 2+ measurements using improved cameleons. Proceedings of the National Academy of Sciences, USA 96: 2135-2140.
31. 2+ based on green fluorescent proteins and calmodulin. Nature 388: 882-887.
32. Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P. 2007. A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiology 144: 673-681.
33. Olah B, Brière C, Bécard G, Dénarié J, Gough C. 2005. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant Journal 44: 195-207.
34. Oldroyd GED, Downie JA. 2006. Nuclear calcium changes at the core of symbiosis signalling. Current Opinion in Plant Biology 9: 351-357.
35. Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews. Microbiology 6: 763-775.
36. Riely BK, Lougnon G, Ané JM, Cook DR. 2007. The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant Journal 49: 208-216.
37. Séjalon-Delmas N, Magnier A, Douds DD, Bécard G. 1998. Cytoplasmic autofluorescence of an arbuscular mycorrhizal fungus Gigaspora gigantea and nondestructive fungal observations in planta. Mycologia 90: 921-926.
38. 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiology 151: 1197-1206.
39. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R. 2005. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789-1791.
40. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. London, UK: Elsevier.
41. Wais RJ, Galera C, Oldroyd G, Catoira R, Penmetsa RV, Cook D, Gough C, Dénarié J, Long SR. 2000. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proceedings of the National Academy of Sciences, USA 97: 13407-13412.
42. Wang B, Yeun L, Xue JY, Liu Y, Ané JM, Qiu YL. 2010. Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonisation of land by plants. New Phytologist 186: 514-525.
43. Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE. 2009. Rosid radiation and the rapid rise of angiosperm-dominated forests. Proceedings of the National Academy of Sciences, USA 106: 3853-3858.
44. Zhu HY, Riely BK, Burns NJ, Ane JM. 2006. Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses. Genetics 172: 2491-2499.