Nitric oxide reduces the stress effects of aluminum on the process of germination and early root growth of rice

Journal of Plant Nutrition and Soil Science

Volumn 173, Issue 6, 2010, Pages 885-891

  Peres Da Rocha Oliveiros Marciano, Danielle ^a   Toledo Ramos, Flávia ^b   Neiva Alvim, Marina ^a   Ronaldo Magalhaes, Jose ^c   Giovanni Costa França, Marcel ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEAD   (Brazil)

^c EMBRAPA CERRADOS   (Brazil)

Author keywords

Aluminum toxicity; Nitric oxide; Oryza sativa; Relative root elongation

Indexed keywords

ORYZA SATIVA;

EID: 78649784537     PISSN: 14368730     EISSN: 15222624     Source Type: Journal    
DOI: 10.1002/jpln.200900312     Document Type: Article

References (47)

1. Alvim, M. N., Ramos, F. T., França, M. G. C. (2007): Seed storage period reduces aluminum tolerance in rice (Oryza sativa L.). Seed Sci. Technol. 35, 688-697.
2. Anderson, L. S., Mansfield, T. A. (1979): Effects of nitric-oxide pollution on the growth of tomato. Environ. Poll. 20, 113-121.
3. Beligni, M. V., Lamattina, L. (1999): Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissue. Planta 208, 337-344.
4. Beligni, M. V., Lamattina, L. (2000): Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyls elongation, three light-inducible responses in plants. Planta 210, 215-221.
5. Bethke, P. C., Libourel, I. G. L., Aoyama, N., Chung, Y. Y., Still, D. W., Jones, R. L. (2007): The Arabidopsis aleurone layer responds to oxide nitric, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol. 143, 1173-1188.
6. Bewley, J. D. (1997): Seed germination and dormancy. Plant Cell 9, 1055-1066.
7. Britez, R. M., Watanabe, T., Jansen, S., Reissmann, C. B., Osaki, M. (2002): The relationship between aluminium and silicon accumulation in leaves of Faramea marginata (Rubiaceae). New Phytol. 156, 437-444.
8. Clune, T. S., Copeland, L. (1999): Effect of aluminum on canola roots. Plant Soil 216, 27-33.
9. Custódio, C. C., Bomfim, D. C., Saturnino, S. M., Machado-Neto, N. B. (2002): Estresse por alumínio e por acidez em cultivares de soja. Scientia Agricola 59, 145-153.
10. Eleftheriou, E. P., Moustakas, M., Fragiskos, N. (1993): Aluminate-induced changes in morphology and ultrastructure of Thinopyrum roots. J. Exp. Bot. 44, 427-436.
11. Gouvea, C. M. C. P., Souza, J. F., Magalhaes, A. C. N., Martins, I. S. (1997): NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Regul. 21, 183-187.
12. Gubler, F., Millar, A. A., Jacobsen, J. V. (2005): Dormancy release, ABA and pre-harvest sprouting. Curr. Opin. Plant Biol. 8, 183-187.
13. Hagenbeek, D., Quatrano, R. S., Rock, C. D. (2000): Trivalent ions activate abscisic acid-inducible promoters through an ABI1-dependent pathway in rice protoplasts. Plant Physiol. 123, 1553-1560.
14. Hsu, Y. T., Kao, C. H. (2004): Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Reg. 42, 227-238.
15. Kidd, P. S., Liugany, M., Poschenrieder, C., Gunse, B., Barcelo, J. (2001): The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize a (Zea mays L.). J. Exp. Bot. 52, 1339-1352.
16. Kinraide, T. B., Parker, D. R. (1989): Assessing the phytotoxicity of mononuclear hydroxy-aluminum. Plant Cell Environ. 12, 479-487.
17. Kochian, L. V. (1995): Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 237-260.
18. Kojima, H., Nakatsubo, N., Kikuch, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y., Nagano, T. (1998): Detection and imaging of nitric oxide with novel fluorescent indicators: Diaminofluoresceins. Anal. Chem. 70, 2446-2453.
19. Kollmeier, M., Felle, H. H., Horst, W. J. (2000): Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol. 122, 945-956.
20. Lanteri, M. L., Laxalt, A. M., Lamattina, L. (2008): Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol. 147, 188-198.
21. Laxalt, A. M., Raho, N., Have, A., Lamattina, L. (2007): Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J. Biol. Chem. 282, 21160-21168.
22. Ma, J. F., Shen, R. F., Zhao, Z. Q., Wissuwa, M., Takeuchi, Y., Ebitani, T., Yano, M. (2002): Responses of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol. 43, 652-659.
23. Ma, J. F., Nagao, S., Huang, C. F., Nishimura, M. (2005): Isolation and characterization of a rice mutant hypersensitive to Al. Plant Cell Physiol. 46, 1054-1061.
24. Magalhaes, J. R., Singh, R. P. (2004): Nitric oxide signaling in higher plants. Studium Press, Houston.
25. Magalhaes, J. R., Monte, D. C., Durzan, D. (2000): Nitric oxide and ethylene emission in Arabidopsis thaliana. Physiol. Mol. Biol. Plants 6, 117-127.
26. Marin, A., Santos, D. M. M., Banzatto, D. A., Ferraudo, A. S. (2004): Germinação de sementes de guandu sob efeito de disponibilidade hídrica e de doses subletais de alumínio. Bragantia 63, 13-24.
27. Morimura, S., Takahashi, E., Matsumoto, H. (1978): Association of aluminum with nuclei and inhibition of cell-division in onion (Allium-cepa) roots. Z. Pflanzenphysiol. 88, 395-401.
28. +-ATPase: structure, function and regulation. Biochim. Biophys. Acta-Biomem. 1465, 1-16.
29. Neill, S. J., Desikan, R., Clark, A., Hancock, J. T. (2002): Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128, 13-16.
30. Polle, E., Konzak, C. F., Kittrick, J. A. (1978): Visual detection of aluminum tolerance levels in wheat by hematoxylin staining of seedlings roots. Crop Sci. 18, 823-827.
31. Ramos, F. T. (2003): Avaliação da toxidez por alumínio sobre a ultraestrutura celular, composição e função de lipídios membranares em raízes de gramíneas. Tese de Doutorado (PhD thesis), Universidade Federal Rural do Rio de Janeiro, Brazil.
32. Ramos, F. T., Rossiello, R. O. P., França, M. G. C., Alvim, M. N., Olivares, F. L. (2007a): Aluminum hematoxylin complex indicates the contribution of mucilage to Al tolerance in the apex of rice roots. Physiol. Mol. Biol. Plants 13, 9-16.
33. Ramos, F. T., Rossiello, R. O. P., Lamas, M. E., Marciano, D. P. R. O., Façanha, A. R. (2007b): Fosfolipídios de membranas de raízes de arroz são alterados diferencialmente por estresse por alumínio. Rev. Bras. Biocien. 5, 117-119.
34. Rangel, A. F., Rao, I. M., Horst, W. J. (2009): Intracellular distribution and binding state of aluminum in root apices of two common bean (Phaseolus vulgaris) genotypes in relation to Al toxicity. Physiol. Plant. 135, 162-173.
35. Rengel, Z. (1996): Tansley review 89. Uptake of aluminium by plant cells. New Phytol. 134, 389-406.
36. Sivaguru, M., Paliwal, K. (1993): Differential aluminum tolerance in some tropical rice cultivars. 1. Growth-performance. J. Plant Nutr. 16, 1705-1716.
37. Song, J., Shi, G., Xing, S., Chen, M., Wang, B. (2009): Effects of nitric oxide and nitrogen on seedling emergence, ion accumulation, and seedling growth under salinity in the euhalophyte Suaeda salsa. J. Plant Nutr. Soil Sci. 172, 544-549.
38. Tian, Q. Y., Sun, D. H., Zhao, M. G., Zhang, W. H. (2007): Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol. 174, 322-331.
39. Vasconcelos, S. S., Rossiello, R. O. P., Jacob-Neto, J. (2002): Parâmetros morfológicos para estabelecer tolerância diferencial à toxidade de alumínio em cultivares de arroz. Pesq. Agropec. Bras. 37, 357-363.
40. Vicente, F. M. P., Rossiello, R. O. P., Pereira, M. B. (1998): Características indicativas de sensibilidade ao alumínio em arroz. I. Crescimento em solução nutritiva. Pesq. Agropec. Bras. 33, 9-15.
41. Wang, J. W., Kao, C. H. (2005): Effect of aluminium on endosperm reserve mobilization in germinating rice grains. Biol. Plant. 49, 405-409.
42. Wang, Y. S., Yang, Z. M. (2005): Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol. 46, 1915-1923.
43. Watanabe, T., Okada, K. (2005): Interactive effects of Al, Ca and other cations on root elongation of rice cultivars under low pH. Ann. Bot. 95, 379-385.
44. Yu, C. C., Hung, K. T., Kao, C. H. (2005): Nitric oxide reduces Cu toxicity and Cu-induced NH accumulation in rice leaves. J. Plant Physiol. 162, 1319-1330.
45. Yu, M., Shen, R., Liu, J., Chen, R., Xu, M., Yang, Y., Xiao, H., Wang, H., Wang, H., Wang, C. (2009): The role of root border cells in aluminum resistance of pea (Pisum sativum) grown in mist culture. J. Plant Nutr. Soil Sci. 172, 528-534.
46. Zhang, H., Shen, W. B., Zhang, W., Xu, L. L. (2005): A rapid response of beta-amylase to nitric oxide but not gibberellin in wheat seeds during the early stage of germination. Planta 220, 708-716.
47. + antiport in the tonoplast. Planta 224, 545-555.