PvRbohB negatively regulates Rhizophagus irregularis colonization in Phaseolus vulgaris

Plant and Cell Physiology

Volumn 54, Issue 8, 2013, Pages 1391-1402

  Arthikala, Manoj Kumar ^a   Montiel, Jesús ^a   Nava, Noreide ^a   Santana, Olivia ^a   Sánchez López, Rosana ^a   Cárdenas, Luis ^a   Quinto, Carmen ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Arbuscular mycorrhiza; Common bean; Rbohs; ROS

Indexed keywords

ARBUSCULAR; FUNGI; MEDICAGO TRUNCATULA; PHASEOLUS VULGARIS; RHIZOPHAGUS;

REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VEGETABLE PROTEIN;

ARBUSCULAR MYCORRHIZA; ARTICLE; CYTOLOGY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; GLOMEROMYCOTA; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHASEOLUS; PHASEOLUS VULGARIS; PHYSIOLOGY; PLANT ROOT; RBOHS; REPORTER GENE; RNA INTERFERENCE; ROS; SYMBIOSIS;

ARBUSCULAR MYCORRHIZA; COMMON BEAN; RBOHS; ROS;

DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; GLOMEROMYCOTA; MYCORRHIZAE; NADPH OXIDASE; PHASEOLUS; PLANT PROTEINS; PLANT ROOTS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SYMBIOSIS;

EID: 84881440983     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct089     Document Type: Article

References (70)

1. Abbà, S., Khouja, H.R., Martino, E., Archer, D.B. and Perotto, S. (2009) SOD1-targeted gene disruption in the ericoid mycorrhizal fungus Oidiodendron maius reduces conidiation and the capacity for mycorrhization. Mol. Plant-Microbe Interact. 22: 1412-1421.
2. Akiyama, K., Matsuzaki, K. and Hayashi, H. (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827. (Pubitemid 40839733)
3. Bago, B., Pfeffer, P.E., Abubaker, J., Jun, J., Allen, J.W., Brouillette, J. et al. (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol. 131: 1496-1507. (Pubitemid 36400380)
4. Besserer, A., Puech-Pagès, V., Kiefer, P., Gómez- Roldán, V., Jauneau, A., Roy, S. et al. (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4: e226.
5. Blanco, F.A., Meschini, E.P., Zanetti, M.E. and Aguilar, O.M. (2009) A small GTPase of the Rab family is required for root hair formation and preinfection stages of the common bean-Rhizobium symbiotic association. Plant Cell 21: 2797-2810.
6. Borges, A., Tsai, S.M. and Caldas, D.G. (2012) Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep. 31: 827-838.
7. Bouvier, F., Backhaus, R.A. and Camara, B. (1998) Induction and control of chromoplast-specific carotenoid genes by oxidative stress. J. Biol. Chem. 273: 30651-30659. (Pubitemid 28545545)
8. Broughton, W.J. and Dilworth, M.J. (1971) Control of leghemoglobin synthesis in snake beans. Biochem J. 125: 1075-1080.
9. Brown, M.F. and King, E.J. (1982) Anatomy and cytology of vesicular-arbuscular mycorrhizae. In Methods and Principles of Mycorrhizal Research. Edited by Schenck, N.C. pp. 15-21. American Phytopathological Society, St Paul, MN.
10. 2+ spiking in the legume and nonlegume root epidermis. New Phytol. 189: 347-355.
11. David-Schwartz, R., Gadkar, V., Wininger, S., Bendov, R., Galili, G., Levy, A.A. et al. (2003) Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. Mol. Plant-Microbe Interact. 16: 382-388. (Pubitemid 36516846)
12. De Smet, I. (2012) Lateral root initiation: one step at a time. New Phytol. 193: 867-873.
13. Dubrovsky, J.G., Gambetta, G.A., Hernández-Barrera, A., Shishkova, S. and González, I. (2006) Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density and predictability. Ann. Bot. 97: 903-915.
14. Estrada-Navarrete, G., Alvarado-Affantranger, X., Olivares, J.E., Guillén, G., Díaz-Camino, C., Campos, F. et al. (2007) Fast, efficient and reproducible genetic transformation of Phaseolus spp. by Agrobacterium rhizogenes. Nat. Protoc. 2: 1819-1824.
15. Felten, J., Kohler, A., Morin, E., Bhalerao, R.P., Palme, K., Martin, F. et al. (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in Poplar and Arabidopsis through auxin transport and signaling. Plant Physiol. 151: 1991-2005.
16. Fester, T. and Hause, G. (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15: 373-379. (Pubitemid 40968300)
17. Fitter, A.H. (2005) Darkness visible: reflections on underground ecology. J. Ecol. 93: 231-243. (Pubitemid 40483088)
18. Gadkar, V., David-Schwartz, R., Nagahashi, G., Douds, D.D., Wininger, S. and Kapulnik, Y. (2003) Root exudate of pmi tomato mutant M161 reduces AM fungal proliferation in vitro. FEMS Microbiol Lett. 223: 193-198. (Pubitemid 36776323)
19. Genre, A., Chabaud, M., Faccio, A., Barker, D.G. and 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. (Pubitemid 352844191)
20. Gobbato, E., Marsh, J.F., Vernié, T., Wang, E., Maillet, F., Kim, J. et al. (2012) A GRAS-type transcription factor with a specific function in mycorrhizal signalling. Curr. Biol. 22: 2236-2241.
21. González-Guerrero, M., Oger, E., Benabdellah, K., Azcón-Aguilar, C., Lanfranco, L. and Ferrol, N. (2010) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr. Genet. 56: 265-274.
22. Govindarajulu, M., Pfeffer, P.E., Jin, H., Abubaker, J., Douds, D.D., Allen, J.W. et al. (2005) Nitrogen transfer in the arbuscular mycor-rhizal symbiosis. Nature 435: 819-823. (Pubitemid 40839732)
23. Grissa, I., Bidard, F., Grognet, P., Grossetete, S. and Silar, P. (2010) The Nox/ferric reductase/ferric reductase-like families of Eumycetes. Fungal Biol. 114: 766-777.
24. Harrison, M.J. (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu. Rev. Microbiol. 59: 19-42. (Pubitemid 41507422)
25. Harrison, M.J. (2013) Cellular programs for arbuscular mycorrhizal symbiosis. Curr. Opin Plant Biol. 15: 691-698.
26. Harrison, M.J., Dewbre, G.R. and Liu, J. (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 2413-2429. (Pubitemid 35235287)
27. Harley, J.L. and Smith, S.E. (1983) Mycorrhizal Symbiosis. pp. 36-39. Academic Press, NewYork.
28. Islas-Flores, T., Guillén, G., Alvarado-Affantranger, X., Lara-Flores, M., Sánchez, F. and Villanueva, M.A. (2011) PvRACK1 loss-of-function impairs cell expansion and morphogenesis in Phaseolus vulgaris L. root nodules. Mol. Plant-Microbe Interact. 24: 819-826.
29. Javot, H., Penmetsa, R.V., Terzaghi, N., Cook, D.R. and Harrison, M.J. (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. USA 104: 1720-1725. (Pubitemid 46214657)
30. Jefferson, R.A. (1987) Assaying chimeric genes in plants, the GUS gene fusion system. Plant Mol. Biol. Rep. 5: 387-405.
31. Karimi, M., Inzé, D. and Depicker, A. (2002) Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195. (Pubitemid 36725938)
32. Kiirika, L.M., Bergmann, H.F., Schikowsky, C., Wimmer, D., Korte, J., Schmitz, U. et al. (2012) Silencing of the Rac1 GTPase MtROP9 in Medicago truncatula stimulates early mycorrhizal and oomycete root colonizations but negatively affects rhizobial infection. Plant Physiol. 159: 501-516.
33. Kistner, C., Winzer, T., Pitzschke, A., Mulder, L., Sato, S., Kaneko, T. et al. (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17: 2217-2229. (Pubitemid 41672942)
34. Kobayashi, M., Ohura, I., Kawakita, K., Yokota, N., Fujiwara, M., Shimamoto, K. et al. (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19: 1065-1080. (Pubitemid 46953247)
35. Koske, R.E. and Gemma, J.N. (1989) A modified procedure for staining roots to detect V-A mycorrhizas. Mycol. Res. 92: 486-488.
36. Kosuta, S., Chabaud, M., Lougnon, G., Gough, C., Denarié, J., Barker, D.G. et al. (2003) A diffusible factor from arbuscular mycor-rhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol. 131: 952-962. (Pubitemid 36400335)
37. Kuhn, H., Küster, H. and Requena, N. (2010) Membrane steroid-binding protein induced by a diffusible fungal signal is critical for mycor-rhization in Medicago truncatula. New Phytol. 185: 716-733.
38. Lambais, M.R., Ríos-Ruiz, W.F. and Andrade, R.M. (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol. 160: 421-428. (Pubitemid 37298619)
39. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583-593. (Pubitemid 24363802)
40. Lin, F., Ding, H., Wang, J., Zhang, H., Zhang, A., Zhang, Y. et al. (2009) Positive feedback regulation of maize NADPH oxidase by mito-gen-activated protein kinase cascade in abscisic acid signalling. J. Exp. Bot. 60: 3221-3238.
41. Liu, J., Blaylock, L.A., Endre, G., Cho, J., Town, C.D., VandenBosch, K.A. et al. (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. (Pubitemid 37144064)
42. Liu, J., Maldonado-Mendoza, I., Lopez-Meyer, M., Cheung, F., Town, C.D. and Harrison, M.J. (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. (Pubitemid 46634492)
43. Maeda, D., Ashida, K., Iguchi, K., Chechetka, S.A., Hijikata, A., Okusako, Y. et al. (2006) Knockdown of an arbuscular mycor-rhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol. 47: 807-817. (Pubitemid 44286320)
44. Maillet, F., Poinsot, V., André, O., Puech-Pagés, V., Haouy, A., Gueunier, M. et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
45. Marino, D., Andrio, E., Danchin, E.G., Oger, E., Gucciardo, S., Lambert, A. et al. (2011) A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning. New Phytol. 189: 580-592.
46. McGonigle, T.P., Millers, M.H., Evans, D.G., Fairchild, G.L. and Swan, J.A. (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 115: 495-501.
47. Montiel, J., Arthikala, M. and Quinto, C. (2013) Phaseolus vulgaris RbohB functions in lateral root development. Plant Signal Behav. 8: 1-3.
48. Montiel, J., Nava, N., Cárdenas, L., Sánchez-López, R., Arthikala, M.K., Santana, O. et al. (2012) A Phaseolus vulgaris NADPH oxidase gene is required for root infection by Rhizobia. Plant Cell Physiol. 53: 1751-1767.
49. Navazio, L., Moscatiello, R., Genre, A., Novero, M., Baldan, B., Bonfante, P. et al. (2007) A diffusible signal from arbuscular mycor-rhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol. 144: 673-681. (Pubitemid 46944734)
50. Oláh, B., Brière, C., Bécard, G., Dénarié, J. and 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 J. 44: 195-207.
51. Parniske, M. (2008) Arbuscular mycorrhiza: the endosymbioses. Nat. Rev. Microbiol. 6: 763-775.
52. Paszkowski, U., Jakovleva, L. and Boller, T. (2006) Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. Plant J. 47: 165-173. (Pubitemid 43974627)
53. Pollard, M., Beisson, F., Li, Y. and Ohlrogge, J.B. (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 13: 236-246.
54. Proels, R.K., Oberhollenzer., K., Pathuri, I.P., Hensel, G., Kumlehn, J. and Hückelhoven, R. (2010) RBOHF2 of barley is required for normal development of penetration resistance to the parasitic fungus Blumeria graminis f. sp. hordei. Mol. Plant-Microbe Interact. 23: 1143-1150.
55. Ramel, F., Sulmon, C., Bogard, M., Couée, I. and Gouesbet, G. (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol. 13: 9-28.
56. Ramu, S.K., Peng, H.M. and Cook, D.R. (2002) Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Mol. Plant-Microbe Interact. 15: 522-528. (Pubitemid 34577380)
57. Salzer, P., Corbiere, H. and Boller, T. (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208: 319-325.
58. Shaw, S.L. and Long, S.R. (2003) Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol. 132: 2196-2204. (Pubitemid 37024179)
59. Smith, S.E. and Read, D.J. (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London.
60. Smith, S.E., Smith, F.A. and Jakobsen, I. (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133: 16-20. (Pubitemid 37144076)
61. Solaiman, M.D.Z. and Saito, M. (1997) Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirome-try. New Phytol. 136: 533-538. (Pubitemid 28016880)
62. Torres, M.A., Dangl, J.L. and Jones, J.D. (2002) Arabidopsis gp91 phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA 99: 517-522. (Pubitemid 34060393)
63. phox). Plant J. 14: 365-370. (Pubitemid 28236000)
64. Tsukagoshi, H., Busch, W. and Benfey, P.N. (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616.
65. Valdés-López, O., Arenas-Huertero, C., Ramírez, M., Girard, L., Sánchez, F., Vance, C.P. et al. (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus deficiency signalling in common bean roots. Plant Cell Environ. 31: 1834-1843.
66. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal reference genes. Genome Biol. 3: research0034.1-0034.11.
67. Wang, E., Schornack, S., Marsh, J.F., Gobbato, E., Schwessinger, B., Eastmond, P. et al. (2012) A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22: 2242-2246.
68. Wong, H.L., Pinontoan, R., Hayashi, K., Tabata, R., Yaeno, T., Hasegawa, K. et al. (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19: 4022-4034. (Pubitemid 351253117)
69. Zhang, J., Shao, F., Li, Y., Cui, H., Chen, L., Li, H. et al. (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe. 1: 175-185. (Pubitemid 46706361)
70. Zhang, R.Q., Zhu, H.H. and Yao, Q. (2013) Arbuscular mycorrhizal fungal inoculation increases phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signalling pathways. J. Plant Physiol. 170: 74-79.