Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi

Plant Physiology

Volumn 149, Issue 3, 2009, Pages 1424-1434

  Genre, Andrea ^a   Ortu, Giuseppe ^a   Bertoldo, Chiara ^a   Martino, Elena ^a   Bonfante, Paola ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARBUSCULAR; FUNGI; MEDICAGO TRUNCATULA;

EID: 63549097299     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.132225     Document Type: Article

References (54)

1. Bécard G, Fortin A (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol 108: 211-218
2. Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13: 492-498
3. Bonfante P, Gianinazzi-Pearson V, Martinengo L (1980) Ultrastructural aspects of endomycorrhiza in the Ericaceae. IV. Comparison of infection by Pezizella ericae in host and non-host plants. New Phytol 98: 329-333
4. Castell-Miller CV, Zeyen RJ, Samac DA (2007) Infection and development of Phoma medicaginis on moderately resistant and susceptible alfalfa genotypes. Can J Plant Pathol 29: 290-298
5. Chabaud M, Venard C, Defaux-Petras A, Be'card 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 Phytol 156: 265-273
6. Dangl JL, Jones JD (2001) Plant pathogens and integrated defense responses to infection. Nature 411: 826-833
7. Esseling JJ, Lhuissier FG, Emons AM (2004) A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16: 933-944
8. Fournier J, Timmers ACJ, Sieberer BJ, Jauneau A, ChabaudM, Barker DG (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol 148: 1985-1995
9. Gal TZ, Aussenberg ER, Burdman S, Kapulnik Y, Koltai H (2006) Expression of a plant expansin is involved in the establishment of root knot nematode parasitism in tomato. Planta 224: 155-162
10. Geldner N, Robatzek S (2008) Plant receptors go endosomal: a moving view on signal transduction. Plant Physiol 147: 1565-1574
11. Genre A, Bonfante P (2007) Check-in procedures for plant cell entry by biotrophic microbes. Mol Plant Microbe Interact 9: 1023-1030
12. 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
13. 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
14. GiordanoW, Hirsch AM (2004) The expression of MaEXP1, a Melilotus alba expansin gene, is upregulated during the sweetclover-Sinorhizobium meliloti interaction. Mol Plant Microbe Interact 17: 613-622
15. Goodbody K, Lloyd CW (1990) Actin filaments line-up across Tradescantia epidermal cells, anticipating wound-induced division planes. Protoplasma 157: 92-101
16. Gross P, Julius C, Schmelzer E, Hahlbrock K (1993) Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defense gene activation in infected, cultured parsley cells. EMBO J 12: 1735-1744
17. Guimil S, Chang H, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, et al (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102: 8066-8070
18. Gus-Mayer S, Naton B, Hahlbrock K, Schmelzer E (1998) Local mechanical stimulation induces components of the pathogen defense response in parsley. Proc Natl Acad Sci USA 95: 8398-8403
19. Hardham AR, Jones DA, Takemoto D (2007) Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10: 342-348
20. Hardham AR, Takemoto D, White RG (2008) Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8: 63
21. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59: 19-42
22. Haswell ES, Peyronnet R, Barbier-Brygoo H, Meyerowitz EM, Frachisse J (2008) Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr Biol 18: 730-734
23. Heath MC, Nimchuk ZL, Xu H (1997) Plant nuclear migrations as indicators of critical interactions between resistant or susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus. New Phytol 135: 689-700
24. Jaffe MJ, Leopold AC, Staples RC (2002) Thigmo responses in plants and fungi. Am J Bot 89: 375-382
25. Journet EP, van Tuinen D, Gouzy J, Crespeau H, Carreau V, Farmer M, Niebel A, Schiex T, Jaillon O, Chatagnier O, et al (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res 30: 5579-5592
26. Kenneth JL, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCt method. Methods 25: 402-408
27. Koh S, Andre A, Edwards H, Ehrhardt D, Somerville S (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44: 516-529
28. Kosuta S, Chabaud M, Lougnon G, Gough C, De'narie J, Barker DG, Be'card G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131: 1-11
29. Kwon C, Bednarek P, Schultze-Lefert P (2008) Secretory pathways in plant immune responses. Plant Physiol 147: 1575-1583
30. Le'vy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane' J, Lauber E, Bisseling T, et al (2004) A putative Ca2+ and calmodulin-dependant protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364
31. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Lantag J, Brandt W, Rosahl S, Scheel D, et al (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183
32. Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15: 2106-2123
33. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50: 529-544
34. Martino E, Coisson JD, Lacourt I, Favaron F, Bonfante P, Perotto S (2000) Influence of heavy metals on production and activity of pectinolytic enzymes in ericoid mycorrhizal fungi. Mycol Res 104: 825-833
35. Mellersh D, Parniske M (2006) Common symbiosis genes of Lotus japonicus are not required for intracellular accommodation of the rust fungus Uromyces loti. New Phytol 170: 641-644
36. O'Connell RJ, Panstruga R (2006) Teĉte-á-teĉte inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171: 699-718
37. O'Neill NR, Bauchan GR, Samac DA (2003) Reactions in the annual Medicago spp. core germ plasm collection to Phoma medicaginis. Plant Dis 87: 557-562
38. Pappelis AJ, Pappelis GA, Kulfinski FB (1974) Nuclear orientation in onion epidermal cells in relation to wounding and infection. Phytopathology 64: 1010-1012
39. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6: 763-775
40. Paszkowski U (2006) Mutualism and parasitism: the yin and yang of plant symbioses. Curr Opin Plant Biol 9: 364-370
41. Perotto S, Peretto R, Faccio A, Schubert A, Varma A, Bonfante P (1995) Ericoid mycorrhyzal fungi: cellular and molecular bases of their interactions with the host plant. Can J Bot 73: S557-S568
42. Rowland O, Ludwig AA, Merrick CJ, Baillieul F, Tracy FE, Durrant WE, Fritz-Laylin L, Nekrasov V, Sjölander K, Yoshioka H, et al (2005) Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. Plant Cell 17: 295-310
43. Sagan M, de Larambergue H, Morandi D (1998) Genetic analysis of symbiosis mutants in Medicago truncatula. In C Elmerich, A Kondorosi, WE Newton, eds, Biological Nitrogen Fixation for the 21st Century, Vol 31. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 317-318
44. Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6: 242-250
45. Sanchez L, Weidmann S, Arnould C, Bernard AR, Gianinazzi S, Gianinazzi-Pearson V (2005) Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol 139: 1065-1077
46. Siciliano V, Genre A, Balestrini R, Cappellazzo G, DeWitt P, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144: 1455-1466
47. Sukno SA, Garcia VM, Shaw BD, Thon MR (2008) Root infection and systemic colonization of maize by Colletotrichum graminicola. Appl Environ Microbiol 4: 823-832
48. Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136: 3864-3876
49. Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33: 775-792
50. Torregrosa C, Cluzet S, Fournier J, Huguet T, Gamas P, Prosperi JM, Esquerre'-Thugaye' M, Dumas B, Jaquet C (2004) Cytological, genetic, and molecular analysis to characterize compatible and incompatible interactions between Medicago truncatula and Colletotrichum trifolii. Mol Plant Microbe Interact 17: 909-920
51. Vieweg MF, Hohnjec N, Küster H (2005) Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220: 757-766
52. Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, Durachko DM, CosgroveDJ, KreilDP, Puzio PS,BohlmanH, et al (2006) Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J 48: 98-112
53. Weidmann S, Sanchez-Calderon L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction related plant genes precedes mycorrhiza establishment and requires the DMI3 gene in Medicago truncatula. Mol Plant Microbe Interact 17: 1385-1393
54. Yang SM, Gao MQ, Xu CW, Gao J, Deshpande S, Lin S, Roe BA, Zhu H (2008) Alfalfa benefits from Medicago truncatula: the RCT1 gene from M. truncatula confers broad-spectrum resistance to anthracnose in alfalfa. Proc Natl Acad Sci USA 105: 12164-12169