Biologia Plantarum

, Volume 61, Issue 1, pp 127–137 | Cite as

Water use efficiency in the drought-stressed sorghum and maize in relation to expression of aquaporin genes

  • S. A. Hasan
  • S. H. Rabei
  • R. M. Nada
  • G. M. Abogadallah
Original Paper


Zea mays L. is less tolerant to drought than Sorghum bicolor L. In the present study, we investigated the response of both plants to drought stress applied under field conditions by withholding water for 10 d. The plant growth in terms of shoot fresh and dry masses was more severely reduced in maize than in sorghum, consistently with reduction of leaf relative water content. Gas exchange was also more inhibited by drought in maize than in sorghum. The water use efficiency (WUE) of maize fluctuated during the day and in response to the drought stress. In contrast, sorghum was able to maintain a largely constant WUE during the day in the well-watered plants as well as in the stressed ones. Studying the expression of four aquaporin genes (PIP1;5, PIP1;6, PIP2;3, and TIP1;2) revealed that PIP1;5 in leaves and PIP2;3 in roots were highly responsive to drought in sorghum but not in maize, where they might have supported a greater water transport. The expression pattern of PIP1;6 suggests its possible role in CO2 transport in control but not droughty leaves of both the plants. TIP1;2 seemed to contribute to water transport in leaves of the control but not droughty plants. We conclude that PIP1;5 and PIP2;3 may have a prominent role in drought tolerance and maintenance of WUE in sorghum plants.

Additional key words

gas exchange plasma membrane intrinsic proteins relative water content Sorghum bicolor tonoplast intrinsic proteins Zea mays 





crassulacean acid metabolism


sub-stomatal CO2 concentration


transpiration rate


field capacity of soil


stomatal conductance


net photosynthetic rate


reverse transcriptase polymerase chain reaction


relative water content


water use efficiency


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

10535_2016_656_MOESM1_ESM.pdf (851 kb)
Supplementary material, approximately 852 KB.


  1. Bassett, C.L.: Water use and drought response in cultivated and wild apples. - In: Kourosh, V. (ed.): Abiotic Stress - Plant Responses and Applications in Agriculture. Pp. 249–275, 2013. Scholar
  2. Bienert, G.P., Moller, A.L., Kristiansen, K.A., Schulz, A., Moller, I.M., Schjoerring, J.K., Jahn, T.P.: Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. - J. biol. Chem. 282: 1183–1192, 2007.CrossRefPubMedGoogle Scholar
  3. Belder, P., Spiertz, J.H.J., Bouman, B.A.M., Lu, G., Tuong, T.P.: Nitrogen economy and water productivity of lowland rice under water saving irrigation. - Field Crops Res. 93: 169–185, 2005.CrossRefGoogle Scholar
  4. Bouman, B.A.M.: A conceptual framework for the improvement of crop water productivity at different spatial scales. - Agr. Syst. 93: 43–60, 2007.CrossRefGoogle Scholar
  5. Chaumont, F., Barrieu, F., Wojcik, E., Chrispeels, M.J., Jung, R.: Aquaporins constitute a large and highly divergent protein family in maize. - Plant Physiol. 125: 1206–1215, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Erdei, L., Taleisnik, E.: Changes in water relation parameters under osmotic and salt stresses in maize and sorghum. - Physiol. Plant. 89: 381–387, 1993.CrossRefGoogle Scholar
  7. Farre, I., Faci, J.M.: Comparative response of maize (Zea mays L.) and sorghum (Sorghum bicolor L. Moench) to deficit irrigation in a Mediterranean environment. - Agr. Water Manage. 83: 135–143, 2006.CrossRefGoogle Scholar
  8. Fetter, K., Wilder, V.V., Moshelion, M., Chaumont, F.: Interactions between plasma membrane aquaporins modulate their water channel activity. - Plant Cell 16: 215–228, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fischer, R.A., Turner, N.C.: Plant productivity in the arid and semiarid zones. - Annu. Rev. Plant. Physiol. 29: 277–317, 1978.CrossRefGoogle Scholar
  10. Flexas, J., Bota, J., Escalona, J.M., Sampol, B., Medrano, H.: Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. - Funct. Plant Biol. 29: 461–471, 2002.CrossRefGoogle Scholar
  11. Flexas, J., Medrano, H.: Drought inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitation revisited. - Ann. Bot. 89: 183–189, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Foyer, C.H., Valadier, M.H., Migge, A., Becker, T.W.: Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. - Plant Physiol. 117: 283–292, 1998.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Franks, P.J., Drake, P.L., Froend, R.H.: Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. - Plant Cell Environ. 30: 19–30, 2007.CrossRefPubMedGoogle Scholar
  14. Ghannoum, O., Von Caemmerer, S., Conroy, J.P.: Effect of drought on plant water use efficiency of nine NAD-ME and nine NADP-ME Australian C4 grasses. - Funct. Plant Biol. 29: 1337–1348, 2002.CrossRefGoogle Scholar
  15. Hachez, C., Moshelion, M, Zelazny, E., Cavez, D., Chaumont, F.: Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. - Plant mol. Biol. 62: 305–323, 2006.CrossRefPubMedGoogle Scholar
  16. Hachez, C., Heinen, R.B., Draye, X., Chaumont, F.: The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. - Plant mol. Biol. 68: 337–353, 2008.CrossRefPubMedGoogle Scholar
  17. Hachez, C., Veselov, D., Ye, Q., Reinhardt, H., Knipfer, T., Fricke, W., Chaumont, F.: Short-term control of maize cell and root water permeability through plasma membrane aquaporin isoforms. - Plant Cell Environ. 35: 185–198, 2012.CrossRefPubMedGoogle Scholar
  18. Heinen, R.B., Bienert, G.P., Cohen, D., Chevalier, A.S., Uehlein, N., Hachez, C., Kaldenhoff, R., Thiec, D.L., Chaumont, F.: Expression and characterization of plasma membrane aquaporins in stomatal complexes of Zea mays. - Plant mol. Biol. 86: 335–350, 2014.CrossRefPubMedGoogle Scholar
  19. Hsiao, T.C., Acevedo, E.: Plant responses to water deficits, water use efficiency, and drought resistance. - Agr. Meteorol. 14: 59–84, 1974.CrossRefGoogle Scholar
  20. Jones, H.G.: Moderate-term water stresses and associated changes in some photosynthetic parameters in cotton. - New Phytol. 72: 1095–1105, 1973.CrossRefGoogle Scholar
  21. Jones, M.M., Rawson, H.M.: Influence of rate of development of leaf water deficits upon photosynthesis, leaf conductance, water use efficiency and osmotic potential in sorghum. - Physiol. Plant. 45: 103–111, 1979.CrossRefGoogle Scholar
  22. Kakani, V.G., Vu, J.C., Allen, L.H., Boote, K.J.: Leaf photosynthesis and carbohydrates of CO2-enriched maize and grain sorghum exposed to a short period of soil water deficit during vegetative development. - J. Plant Physiol. 168: 2169–2176, 2011.CrossRefPubMedGoogle Scholar
  23. Kaldenhoff, R., Bertl, A., Otto, B., Moshelion, M., Uehlein, N.: Characterization of plant aquaporins. - Method. Enzymol. 428: 505–531, 2007.CrossRefGoogle Scholar
  24. Lal, A., Edwards, G.E.: Analysis of inhibition of photosynthesis under water stress in the C4 species Amaranthus cruentus and Zea mays: electron transport, CO2 fixation and carboxylation capacity. - Aust. J. Plant Physiol. 23: 403–412, 1996.CrossRefGoogle Scholar
  25. Liu, P., Yin, L., Deng, X., Wang, S., Tanaka, K., Zhang, S.: Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. - J. exp. Bot. 65: 4747–4756, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Liu, P., Yin, L., Wang, S., Zhang, M., Deng, X., Zhang, S., Tanaka, K.: Enhanced root hydraulic conductance by aquaporin regulation accounts for silicon alleviated saltinduced osmotic stress in Sorghum bicolor L. - Environ. exp. Bot. 111: 42–51, 2015.CrossRefGoogle Scholar
  27. Lu, Z.J., Neumann, P.M.: 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, 1999.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Maroco, J.P., Pereira, J.S., Chaves, M.M.: Growth, photosynthesis and water-use efficiency of two C4 Sahelian grasses subjected to water deficits. - J. Arid Environ. 45: 119–137, 2000.CrossRefGoogle Scholar
  29. Maurel, C.: Plant aquaporins: novel functions and regulation properties. - FEBS Lett. 581: 2227–2236, 2007.CrossRefPubMedGoogle Scholar
  30. Maurel, C., Verdoucq, L., Luu, D-T., Santoni, V.: Plant Aquaporins: membrane channels with multiple integrated functions. - Ann. Rev. Plant Biol. 59: 595–624, 2008.CrossRefGoogle Scholar
  31. Merrill, S.D., Tanaka, D.L., Krupinsky, J.M., Liebig, M.A., Hanson, D.: Soil water depletion and recharge under ten crop species and applications to the principles of dynamic cropping systems. - Agron. J. 99: 931–938, 2007.CrossRefGoogle Scholar
  32. Reddy, P.S., Rao, T.S.R.B., Sharma, K.K., Vadez, V.: Genomewide identification and characterization of the aquaporin gene family in Sorghum bicolor (L.). - Plant Gene 1: 8–28, 2015.CrossRefGoogle Scholar
  33. Ripley, B.S., Gilbert, M.E., Ibrahim, D.G., Osborne, C.P.: Drought constraints on C4 photosynthesis: stomatal and metabolic limitations in C3 and C4 subspecies of Alloteropsis semialata. - J. exp. Bot. 58: 1351–1363, 2007.CrossRefPubMedGoogle Scholar
  34. Saccardy, K., Cornic, G., Brulfert, J., Reyss, A.: Effect of drought on net CO2 uptake by Zea leaves. - Planta 199: 589–595, 1996.CrossRefGoogle Scholar
  35. Sakurai-Ishikawa, J., Murai-Hatano, M., Hayashi, H., Ahamed, A., Fukushi, F., Matsumoto, T., Kitagawa, Y.: Transpiration from shoots triggers diurnal changes in root aquaporin expression. - Plant Cell Environ. 34: 1150–1163, 2011.CrossRefPubMedGoogle Scholar
  36. Sanchez-Diaz, M.F., Kramer, P.J.: Turgor differences and water stress in maize and sorghum leaves during drought and recovery. - J. exp. Bot. 24: 511–515, 1973.CrossRefGoogle Scholar
  37. Schittenhelm, S., Schroetter, S.: Comparison of drought tolerance of maize, sweet sorghum and sorghum-sudangrass hybrids. - J. Agr. Crop Sci. 200: 46–53, 2014.CrossRefGoogle Scholar
  38. Singh, B.R., Singh, D.P.: Agronomic and physiological responses of sorghum, maize and pearl millet to irrigation. - Field Crops Res. 42: 57–67, 1995.CrossRefGoogle Scholar
  39. Singh, V., Van Oosterom, E.J., Jordan, D.R., Messina, C.D., Cooper, M., Hammer, G.L.: Morphological and architectural development of root systems in sorghum and maize. - Plant Soil 333: 287–299, 2010.CrossRefGoogle Scholar
  40. Steudle, E., Peterson, C.A.: How does water get through roots? J. exp. Bot. 49: 775–788, 1998.Google Scholar
  41. Tardieu, F.: Drought perception by plants: do cells of droughted plants experience water stress? - Plant Growth Regul. 20: 93–104, 1996.CrossRefGoogle Scholar
  42. Tardieu, F., Simonneau, T.: Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. - J. exp. Bot. 49: 419–432, 1998.CrossRefGoogle Scholar
  43. Taylor, S.H., Ripley, B.S., Woodward, F.I., Osborne, C.P.: Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment. - Plant Cell Environ. 34: 65–75, 2011.CrossRefPubMedGoogle Scholar
  44. Vandeleur, R., Niemietz, C., Tilbrook, J., Tyerman, S.D.: Roles of aquaporins in root responses to irrigation. - Plant Soil 274: 141–161, 2005.CrossRefGoogle Scholar
  45. Way, D.A., Katul, G.G., Manzoni, S., Vico, G.: Increasing water use efficiency along the C3 to C4 evolutionary pathway: a stomatal optimization perspective. - J. exp. Bot. 65: 3683–3693, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Winter, K., Aranda, J., Holtum, J.A.M.: Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism. - Funct. Plant. Biol. 32: 381–388, 2005.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • S. A. Hasan
    • 1
  • S. H. Rabei
    • 1
  • R. M. Nada
    • 1
  • G. M. Abogadallah
    • 1
  1. 1.Department of Botany, Faculty of ScienceDamietta UniversityNew DamiettaEgypt

Personalised recommendations