Drought-induced root aerenchyma formation restricts water uptake in rice seedlings supplied with nitrate

Plant and Cell Physiology

Volumn 53, Issue 3, 2012, Pages 495-504

  Yang, Xiuxia ^a,b   Li, Yong ^a   Ren, Binbin ^a   Ding, Lei ^a   Gao, Cuimin ^a   Shen, Qirong ^a   Guo, Shiwei ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b JIANGXI AGRICULTURAL UNIVERSITY   (China)

Author keywords

Aerenchyma; Hydraulic conductivity; Rice (Oryza sativa L.); Root water uptake; Water stress

Indexed keywords

NITRATE; NITROGEN; WATER;

ARTICLE; BIOMASS; DEHYDRATION; DROUGHT; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; PHYSIOLOGY; PLANT; PLANT EXUDATE; PLANT ROOT; POROSITY; RICE; SEEDLING; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE; XYLEM;

BIOLOGICAL TRANSPORT; BIOMASS; DEHYDRATION; DROUGHTS; NITRATES; NITROGEN; ORYZA SATIVA; PLANT EXUDATES; PLANT ROOTS; PLANT SHOOTS; POROSITY; SEEDLING; WATER; XYLEM;

ORYZA SATIVA;

EID: 84863245602     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs003     Document Type: Article

References (55)

1. Britto, D.T., Siddiqi, M.Y., Glass, A.D.M. and Kronzucker, H.J. (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc. Natl Acad. Sci. USA 98: 4255-4258. (Pubitemid 32249931)
2. Cabuslay, G.S., Ito, O. and Alejar, A.A. (2002) Physiological evaluation of responses of rice (Oryza sativa L.) to water deficit. Plant Sci. 163: 815-827. (Pubitemid 35280851)
3. Carvajal, M., Cooke, D.T. and Clarkson, D.T. (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199: 372-381. (Pubitemid 26263194)
4. Chrispeels, M.J. and Maurel, C. (1994) Aquaporins: the molecular basis of facilitated water movement through living plant cells? Plant Physiol. 105: 9-13.
5. Clarkson, D.T., Carvajal, M., Henzler, T., Waterhouse, R.N., Smyth, A.J., Cooke, D.T. et al. (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J. Exp. Bot. 51: 61-70. (Pubitemid 30065412)
6. Cramer, M.D. and Lewis, O.A.M. (1993) The influence of nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) plants. Ann. Bot. 72: 359-365.
7. Drew, M.C., He, C.J. and Morgan, P.W. (1989) Decreased ethylene biosynthesis and induction of aerenchyma by nitrogen-starvation or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiol. 91: 266-271.
8. Eshel, A., Nielsen, K. and Lynch, J. (1995) Response of bean root systems to low level of P. In: Plant Roots-From Cells to Systems. 63; 14th Long Ashton International Symposium. IACR Bristol.
9. Evans, D.E. (2003) Aerenchyma formation. New Phytol. 161: 35-49. (Pubitemid 38050990)
10. Fan, M.S., Bai, R.Q., Zhao, X.F. and Zhang, J.H. (2007) Aerenchyma formed under phosphorus deficiency contributes to the reduced root hydraulic conductivity in maize roots. J. Integr. Plant. Biol. 49: 598-604.
11. Fan, M.S., Zhu, J.M., Richards, C., Brown, K.M. and Lynch, J.P. (2003) Physiological roles for aerenchyma in phosphorus-stressed roots. Funct. Plant Biol. 30: 493-506. (Pubitemid 36821212)
12. Frensch, J. and Steudle, E. (1989) Axial and radial hydraulic resistance to roots of maize (Zea mays L.). Plant Physiol. 91: 719-726.
13. Gao, Y.X., Li, Y., Yang, X.X., Li, H.J., Shen, Q.R. and Guo, S.W. (2010) Ammonium nutrition increases water absorption in rice seedlings (Oryza sativa L.) under water stress. Plant Soil 331: 193-201.
14. Guo, S.W., Brück, H. and Sattelmacher, B. (2002) Effect of supplied nitrogen form on growth and water uptake of French bean (Phaseolus vulgaris L.) plants. Plant Soil 239: 267-275. (Pubitemid 34465953)
15. Guo, S.W., Chen, G., Zhou, Y. and Shen, Q.R. (2007a) Ammonium nutrition increases photosynthesis rate under water stress at early development stage of rice (Oryza sativa L.). Plant Soil 296: 115-124. (Pubitemid 47052066)
16. Guo, S.W., Kaldenhoff, R., Uehlein, N., Sattelmacher, B. and Brueck, H. (2007b) Relationship between water and nitrogen uptake in nitrateand ammonium-supplied Phaseolus vulgaris L. plants. J. Plant Nutr. Soil Sci. 170: 73-80. (Pubitemid 46374195)
17. Guo, S.W., Shen, Q. and Brueck, H. (2007c) Effects of local nitrogen supply on water uptake of bean plants in a split root system. J. Integr. Plant Biol. 49: 472-480. (Pubitemid 46563552)
18. Guo, S.W., Zhou, Y., Li, Y., Gao, Y.X. and Shen, Q.R. (2008) Effects of different nitrogen form and water stress on water use efficiency of rice plants. Ann. Appl. Biol. 153: 127-134.
19. Guo, S.W., Zhou, Y., Shen, Q.R. and Zhang, F.S. (2007d) Effect of ammonium and nitrate nutrition on some physiological processes in higher plants-growth, photosynthesis, photorespiration, and water relations. Plant Biol. 9: 21-29. (Pubitemid 46225769)
20. He, C.J., Morgan, P.W. and Drew, M.C. (1992) Enhanced sensitivity to ethylene in nitrogen-or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiol. 98: 137-142.
21. Hose, E., Clarkson, D.T., Steudle, E., Schreiber, L. and Hartung, W. (2001) The exodermis: a variable apoplastic barrier. J. Exp. Bot. 52: 2245-2264. (Pubitemid 33145724)
22. Jackson, M.B. and Armstrong, W. (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol. 1: 274-287. (Pubitemid 29257167)
23. Jackson, M.B., Fenning, T.M. and Jenkins, W. (1985) Aerenchyma (gas-space) formation in adventitious roots of rice (Oryza sativa L.) is not controlled by ethylene or small partial pressures of oxygen. J. Exp. Bot. 36: 1566-1572.
24. Javot, H. and Maurel, C. (2002) The role of aquaporins in root water uptake. Ann. Bot. 90: 301-303.
25. Kim, J.D., Jugsujinda, A., Carbonell-Barrachina, A.A., DeLaune, R.D. and Patrick, W.H. (1999) Physiological functions and methane and oxygen exchange in Korean rice cultivars grown under controlled soil redox potential. Bot. Bull. Acad. Sin. 40: 185-191. (Pubitemid 29375308)
26. Kludze, H.K., DeLaune, R.D. and Patrick, W.H. (1993) Aerenchyma formation and methane and oxygen exchange in rice. Soil Sci. Soc. Amer. J. 57: 386-391.
27. Kramer, P.J. and Boyer, J.S. (1995) In Water Relations of Plants and Soil. Academic Press, Orlando, FL. Lawlor, D.W. (2002) Limitation to photosynthesis in water stressed leaves: stomata vs. metabolism and the role of ATP. Ann. Bot. 89: 1-15.
28. Li, Y., Gao, Y.X., Ding, L., Shen, Q.R. and Guo, S.W. (2009) Ammonium enhances the tolerance of rice seedlings (Oryza sativa L.) to drought condition. Agric. Water Manage. 96: 1746-1750.
29. Lu, Y., Wassmann, R., Neue, H.U. and Huang, C. (1999) Impact of phosphorus supply on root exudation, aerenchyma formation and methane emission of rice plants. Biogeochemistry 47: 203-218. (Pubitemid 29478106)
30. Lu, Z.J. and Neumann, P.M. (1999) Water stress inhibits hydraulic conductance and leaf growth in rice seedlings but not the transport of water via mercury-sensitive water channels in the root. Plant Physiol. 120: 143-151. (Pubitemid 29375417)
31. Lynch, J.P. and Ho, M.D. (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269: 45-56. (Pubitemid 40876597)
32. Maurel, C. (1997) Aquaporins and water permeability of plant membranes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 399-429.
33. Melchior, W. and Steudle, E. (1993) Water transport in onion Allium cepa L. roots: changes of axial and radial hydraulic conductivity during development. Plant Physiol. 101: 1305-1315.
34. Michel, B.E. and Kaulmann, M. (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiol. 51: 914-916.
35. Miyamoto, N., Steudle, E., Hirasawa, T. and Lafitte, R. (2001) Hydraulic conductivity of rice roots. J. Exp. Bot. 52: 1835-1846. (Pubitemid 32827965)
36. Mu, Z., Zhang, S., Zhang, L., Liang, A. and Liang, Z. (2006) Hydraulic conductivity of whole root system is better than hydraulic conductivity of single root in correlation with the leaf water status of maize. Bot. Stud. (Taipei Taiwan) 47: 145-151. (Pubitemid 43828878)
37. North, G.B. and Nobel, P.S. (2000) Heterogeneity in water availability alters cellular development and hydraulic conductivity along roots of Desert Succulent. Ann. Bot. 85: 247-255.
38. Ranathunge, K., Kotula, L., Steudle, E. and Lafitte, R. (2004) Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. J. Exp. Bot. 396: 433-447. (Pubitemid 38204123)
39. Ranathunge, K., Steudle, E. and Lafitte, R. (2003) Control of water uptake by rice (Oryza sativa L.): role of the outer part of the root. Planta 217: 193-205. (Pubitemid 36796714)
40. Raskin, I. (1983) A method for measuring leaf volume, density, thickness, and internal gas volume. Hortscience 18: 698-699.
41. Rieger, M. and Litvin, P. (1999) Root system hydraulic conductivity in species with contrasting root anatomy. J. Exp. Bot. 50: 201-220.
42. Saneoka, H., Moghaieb, R.E.A., Premachandra, G.S. and Fujita, K. (2004) Nitrogen nutrition and water stress effects on cell membrane stability and leaf water relations in Agrostis palustris Huds. Environ. Exp. Bot. 52: 131-138. (Pubitemid 39197371)
43. Shangguan, Z.P., Shao, M.A. and Dyckmans, J. (2000) Nitrogen nutrition and water stress effects on leaf photosynthetic gas exchange and water use efficiency in winter wheat. Environ. Exp. Bot. 44: 141-149.
44. Soejima, H., Sugiyama, T. and Ishihara, K. (1992) Changes in cytokinin activities and mass spectrometric analysis of cytokinins in root exudates of rice plant (Oryza sativa L.). Plant Physiol. 100: 1724-1729.
45. Steudle, E. (2000a) Water uptake by roots: effects of water deficit. J. Exp. Bot. 51: 1531-1542.
46. Steudle, E. (2000b) Water uptake by roots: an integration of views. Plant Soil 226: 45-56. (Pubitemid 32100696)
47. Steudle, E. (2001) The cohesion-tension mechanism and the acquisition of water by plant roots. Annu. Rev. Plant Physiol. Mol. Biol. 52: 847-875. (Pubitemid 33720057)
48. Steudle, E. and Henzler, T. (1995) Water channels in plants: do basic concepts of water transport change? J. Exp. Bot. 46: 1067-1076.
49. Steudle, E. and Peterson, C.A. (1998) How does water get through roots? J. Exp. Bot. 49: 775-778.
50. Thomson, C.J., Armstrong, W., Waters, I. and Greenway, H. (1990) Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat. Plant Cell Environ. 13: 395-403.
51. Tuberosa, R., Salvi, S., Giuliani, S., Sanguineti, M.C., Bellotti, M., Conti, S. et al. (2007) Genome-wide approaches to investigate and improve maize response to drought. Crop Sci. 47: S120-S141. (Pubitemid 351299946)
52. Wan, X.C., Steudle, E. and Hartung, W. (2004) Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. J. Exp. Bot. 55: 411-422. (Pubitemid 38204121)
53. Walch-Liu, P., Neumann, G., Bangerth, F. and Engels, C. (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J. Exp. Bot. 51: 227-237. (Pubitemid 30097611)
54. Weatherley, P.E. (1982) Water uptake and flow into roots. In Encyclopedia of Plant Physiology, Vol 12B: Physiological Plant Ecology, Water Relations and Carbon Assimilation. Edited by Lange, O.L., Nobel, P.S., Osmond, C.B. and Zeigler, H. pp. 79-109. Springer Berlin.
55. Zhu, J.M., Brown, K.M. and Lynch, J.P. (2010) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant Cell Environ. 33: 740-749.