Aldehyde oxidase (AO) in the root nodules of Lupinus albus and Medicago truncatula: Identification of AO in meristematic and infection zones

Molecular Plant-Microbe Interactions

Volumn 18, Issue 5, 2005, Pages 405-413

  Fedorova, Elena ^a,b   Redondo, Francisco J ^a   Koshiba, Tomokazu ^c   Pueyo, José J ^a   De Felipe, M Rosario ^a   Lucas, M Mercedes ^a  

^a INSTITUTO DE CIENCIAS AGRARIAS   (Spain)

^b TIMIRYAZEV INSTITUTE OF PLANT PHYSIOLOGY   (Russian Federation)

^c TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

ABA; Bradyrhizobium; Immunofluorescence; Mesorhizobium loti

Indexed keywords

ABSCISIC ACID; ALDEHYDE OXIDASE; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; ISOENZYME;

ARTICLE; BARREL MEDIC; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION; LUPIN; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT;

ABSCISIC ACID; ALDEHYDE OXIDASE; GENE EXPRESSION; INDOLEACETIC ACIDS; ISOENZYMES; LUPINUS; MEDICAGO TRUNCATULA; MYCORRHIZAE; PLANT ROOTS;

BRADYRHIZOBIUM; LUPINUS; LUPINUS ALBUS; MEDICAGO TRUNCATULA; MESORHIZOBIUM; MESORHIZOBIUM LOTI;

EID: 17644408065     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-18-0405     Document Type: Article

References (57)

1. Akaba, S., Seo, M., Dohmae, N., Takio, K., Sekimoto, H., Kamiya, Y., Furuya, N., Komano, T., and Koshiba, T. 1999. Production of homo- and hetero-dimeric isozymes from two aldehyde oxidase genes of Arabidopsis thaliana. Plant Cell Physiol. 39:433-442.
2. Aloni, R., Schwalm, K., Langhans, M., and Ullrich, C. I. 2003. Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841-853.
3. Bartel, B. 1997. Auxin biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol.48:51-66.
4. Boot, K. J. M., van Brussel, A. A. N., Tak, T., Spaink, H. P., and Kijne, J. W. 1999. Lipochitin oligosaccarides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp. nigra roots. Mol. Plant-Microbe Interact. 12:839-844.
5. Cooper, J. B., and Long, S. R. 1994. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6:215-225.
6. de Billy, F., Grosjean, C., May, S., Bennett, M., and Cullimore, J. V. 2001. Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol. Plant-Microbe Interact. 14:267-277.
7. DeLong, A., Mockaitis, K., and Christensen, S. 2002. Protein phosphorylation in the delivery of and response to auxin signals. Pages 285-303 in: Auxin Molecular Biology. C. Perrot-Rechenmann and G. Hagen. eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
8. Fang, Y., and Hirsch, A. M. 1998. Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in alfalfa. Plant Physiol. 116:53-68.
9. Fedorova, E. E., Greenwood, J. S., and G. S. Oaks A. 1994. In situ localization of nitrate reductase in maize root. Planta 194:279-286.
10. Fedorova, E. E., Zhiznevskaya, G. Y., Kalibernaya, Z. V., Artemenko, E. N., Izmailow, S. F., and Gus'kov, A. 2000. IAA metabolism during the development of symbiosis between Phaseolus vulgaris and Rhizobium phaseoli. Russ. J. Plant Physiol. 47:203-206.
11. Ferguson, B. J., and Mathesius, U. 2003. Signaling interactions during nodule development. J. Plant Growth Regul. 22:47-72.
12. Fukuhara, H., Minakawa, Y., Akao, S., and Minamisawa, K. 1994. The involvement of indole-3-acetic acid produced by Bradyrhizobium elkanii in nodule formation. Plant Cell Physiol. 35:1261-1265.
13. González-Guzmán, M., Abia, D., Salinas, J., Serrano, R., and Rodríguez, P. L. 2004. Two new alleles of abcisic aldehyde oxidase 3 gene reveal its role in abcisic acid biosynthesis in seeds. Plant Physiol. 135:325-333.
14. González-Sama, A., Lucas, M. M., de Felipe, M. R., and Pueyo, J. J. 2004. An unusual mechanism of infection and nodule morphogenesis in lupin (Lupinus albus) lead to a unique nodule type. New Phytol. 163:371-380.
15. Heidstra, R., Yang, W. C., Yacin, Y., Peck, S., Emons, A., vanKammen, A., and Bisseling, T. 1997. Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124:1781-1787.
16. Hirsch, A. 1992. Developmental biology of legume nodulation. New Phytol. 122:211-237.
17. Hirsch, A. M., Bhuvaneswari, T. V., Torrey, J. G., and Bisseling, T. 1989. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc. Natl. Acad. Sci. U.S.A. 86:1244-1248.
18. Hirsch, A. M., Fang, Y., Asad, S., and Kapulnik, Y. 1997. The role of phytohormones in plant-microbe symbioses. Plant Soil 194:171-184.
19. Hoagland, D. R., and Arnon, D. I. 1938. The water culture method for growing plants without soil. University of California. Agricultural Experimental Station Circle. no. 347. Berkley, CA, U.S.A.
20. Jelenska, J., Deckert, J., Kondorosi, E., and Legocki, A. 2000. Mitotic B-type cyclins are differentially regulated by phytohormones and during yellow lupin nodule development. Plant Sci. 150:29-39.
21. Kawaguchi, M., and Syono, K. 1996. The excessive production of indole-3-acetic acid and its significance in studies of the biosynthesis of this regulator of plant growth and development. Plant Cell Physiol. 3:1043-1048.
22. Kiers, T. E., Rousseau, R. A., West, S. A., and Denison, R. F. 2003. Host sanctions and the legume-Rhizobium mutualism. Nature 425:78-81.
23. Koiwai, H., Nakminami, K., Seo, M., Mitsuhashi, W., Toyomasu, T. and Koshiba, T. 2004. Tissue-specific localization of an abcisic acid biosynthetic enzyme. AAO3. in Arabidopsis. Plant Physiol. 134:1-11.
24. Koshiba, T., Saito, E., Ono, N., Yamamoto, N., and Sato, M. 1996. Purification and properties of flaying- and molybdenum-containing aldehyde oxidase from coleoptiles of maize. Plant Physiol. 110:781-789.
25. Lambrecht, M., Okon, Y., Vande Broek, A., and Vanderleyden, J. 2000. Indole-3-acetic acid: A reciprocal signaling molecule in bacteria-plant interactions. Trends Microbiol. 8:298-300.
26. Ljung, K., Hull, A. K., Kowalczyk, M., Marchant, A., Celenza, J., Cohen, J. D., and Sandberg, G. 2002. Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Pages 249-272 in: Auxin Molecular Biology. C. Perrot-Rechenmann and G. Hagen, eds. Kluwer Academic Publishers, Dordrecht. The Netherlands.
27. Lohar, D. P., Schaff, J. E., Laskey, J. G., Kieber, J. J., Bilyeu, K. D., and Bird, D. M. 2004. Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J. 38:203-214.
28. Long, S. R. 1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885-1898.
29. Mathesius, U. 2001. Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J. Exp. Bot, 52:419-426.
30. Mathesius, U., Schlaman, H. M., Spaink, H. P., Sautter, C., Rolfe, B. G., and Djordjevic, M. A. 1998. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivates of chitin oligosaccarides. Plant J. 14:23-34.
31. Mathesius, U., Charon, C., Rolfe, B. G., Kondorosi, A., and Crespi, M. 2000. Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Mol. Plant-Microbe Interact. 13:617-628.
32. Miyata, S., Suzuki, Y., Kamisaka, S., and Masuda, Y. 1981. Indole -3-acetaldehyde oxidase of pea seedlings. Physiol. Plantarum. 51:402-406.
33. Normanly, J., and Bartel, B. 1999. Redundancy as a way of life - IAA metabolism. Curr. Opin. Plant Biol. 2:207-213.
34. Ohmiya, A., Haayashi, T., and Kakiuchi, N. 1990. Immuno-gold localization of indole-3-acetic acid in peach seedlings. Plant Cell Physiol. 31:711-715.
35. Oldroyd, G. E. D., Engstrom, E. M., and Long, S. R. 2001. Ethylene inhibits the Nod Factor signal transduction pathway of Medicago truncatula. Plant Cell 13:1835-1849.
36. Omarov, R., Dräger, D., Tischner, R., and Lips, H. 2003. Adlehyde oxidase isoforms and subunit composition in roots of barley as affected by ammonium and nitrate. Physiol Plantarum 117:337-342.
37. Pastor, A., López-Carbonell, M. and Alegre, L. 1999. Abcisic acid immunolocalization and ultrastructural changes in water-stressed lavender (Lavandula stoechas L.) plants. Physiol. Plant. 105:272-279.
38. Roudier, F., Fedorova, E., Lebris, M., Lecomte, P., Györgiev, J., Vaubert, D., Horvath, G., Abad, P., Kondorosi, A., and Kondorosi, E. 2003. The Medicago species A2-type cyclin is auxin regulated and involved in meristem formation but dispensable for endoreduplication-associated developmental programs. Plant Physiol. 131:1091-1103.
39. Scheres, B., van Engelen, F., van der Knaap, E., van de Wiel, C., van Kammen, A., and Bisseling, T. 1990. Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell. 2:687-700.
40. Schultze, M., and Kondorosi, A. 1998. Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32:33-57.
41. Sekimoto, H., Seo, M., Dohmaei, N., Takioi, K., Kamiya, Y., and Koshiba, T. 1997.Cloning and molecular characterization of plant aldehyde oxidase. J. Biol. Chem. 272:15280-15285.
42. Sekimoto, H. Seo, M. Kawakami, N. Komano, T. Desloire, S. Liotenberg, S. Marion-Poll, A. Caboche, M. Kamiya, Y. and Koshiba, T. 1998. Molecular cloning and characterization of aldehyde oxidases in Arabidopsis thaliana. Plant Cell Physiol. 39:33-42.
43. Seo, M., and Koshiba, T. 2002. Complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 7:41-48.
44. Seo, M., Akaba, S., Oritani, T., Delarue, M., Bellini, C., Caboche, M., and T. Koshiba. 1998. Higher activity of an aldehyde oxidase in the auxin-overproducing superroot I mutant of Arabidopsis thaliana. Plant Physiol. 116:687-693.
45. Seo, M., Koiwai, H., Akaba, S., Komano, T., Oritani, T., Kamiya, Y. and Koshiba, T. 2000a. Abscisic aldehyde oxidase in leaves of Ambidapsis thaliana. Plant J. 23:481-488.
46. Seo, M., Peeters, A. J .M., Koiwai, H., Oritani, T., Marion-Poll, A., Zeevaart, J. A. D., Koornneef, M., Kamiya, Y. and Koshiba, T. 2000b. The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abcisic acid biosynthesis in leaves. Proc. Natl. Acad. Sci. U.S.A. 97:12908-12913.
47. Shi, L., Miller, I., and Moore, R. 1993. Immunocytochemical localisation of indole-3-acetic acid in primary roots of Zea mays. Plant Cell Environ. 16:967-973.
48. Stals, H., and Inze, D. 2001. When plant cells decide to divide. Trends Plant Sci. 6:359-364.
49. Stougaard, J. 2000. Regulators and regulation of legume root nodule development. Plant Physiol. 124:531-540.
50. Thomas, C., Bronner, R., Molinier, J., Prinsen, E., van Onckelen, H., and Hahne, G. 2002. Immuno-cytochemical localisation of indole-3-acetic acid during induction of somatic embryogenesis in cultured sunflower embryos. Planta 215:577-583.
51. Vanna, R., Penmetsa, J. A., Frugoli, L., Smith, S., Long, S. R., and Cook, D. R., 2003. Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol. 131:998-1008.
52. Vasse, J., de Billy, F., Camut, S., and Truchet, G. 1990. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J. Bacteriol. 172:4295-4306.
53. Vincent, J. M. 1970. A manual for the practical study of root-nodule bacteria. I.B.P. Handbook no. 15. Blackwell Scientific Publications, Oxford.
54. Welbaum, G. E., Bian, D., Hill, D. R., Grayson, R. L., and Gunatilaka, M. K. 1997. Freezing tolerance, protein composition, and abscisic acid localisation and content of pea epicotyl, shoot, and root tissue in response to temperature and water stress. J. Exp. Bot. 48:643-654.
55. Zdunek E., and Lips, S. H. 2001. Transport and accumulation rates of abcisic acid and aldehyde oxidase activity in Pisum sativum L. in response to suboptimal growth conditions. J. Exp. Bot. 52:1-8.
56. Zdunek-Zastocka, E., Omarov, R. T., Koshiba, T. and Lips, S. H. 2004. Activity and protein level of AO isoforms in pea plants (Pisum sativum L.) during vegetative development and in response to stress conditions. J. Exp. Bot. DOI: 10.1093/jxb/erhl34, 1-9.
57. Zhu, J., Oger, P. M., Schrammeijer, B., Hooykaas, P. J. J., Farrand, S. K., and Winans, S. C. 2000. The bases of crown gall tumorigenesis. J. Bacteriol. 182:3885-3895.