Abstract
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.
Similar content being viewed by others
Abbreviations
- AQPs:
-
aquaporins
- CAM:
-
crassulacean acid metabolism
- ci :
-
sub-stomatal CO2 concentration
- E:
-
transpiration rate
- FC:
-
field capacity of soil
- gs :
-
stomatal conductance
- PN:
-
net photosynthetic rate
- RT-PCR:
-
reverse transcriptase polymerase chain reaction
- RWC:
-
relative water content
- WUE:
-
water use efficiency
References
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. http://www.intechopen.com/books/abiotic-stressplant-responses-and-applications-in-agriculture.
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.
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.
Bouman, B.A.M.: A conceptual framework for the improvement of crop water productivity at different spatial scales. - Agr. Syst. 93: 43–60, 2007.
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.
Erdei, L., Taleisnik, E.: Changes in water relation parameters under osmotic and salt stresses in maize and sorghum. - Physiol. Plant. 89: 381–387, 1993.
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.
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.
Fischer, R.A., Turner, N.C.: Plant productivity in the arid and semiarid zones. - Annu. Rev. Plant. Physiol. 29: 277–317, 1978.
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.
Flexas, J., Medrano, H.: Drought inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitation revisited. - Ann. Bot. 89: 183–189, 2002.
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.
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.
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.
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.
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.
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.
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.
Hsiao, T.C., Acevedo, E.: Plant responses to water deficits, water use efficiency, and drought resistance. - Agr. Meteorol. 14: 59–84, 1974.
Jones, H.G.: Moderate-term water stresses and associated changes in some photosynthetic parameters in cotton. - New Phytol. 72: 1095–1105, 1973.
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.
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.
Kaldenhoff, R., Bertl, A., Otto, B., Moshelion, M., Uehlein, N.: Characterization of plant aquaporins. - Method. Enzymol. 428: 505–531, 2007.
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.
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.
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.
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.
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.
Maurel, C.: Plant aquaporins: novel functions and regulation properties. - FEBS Lett. 581: 2227–2236, 2007.
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.
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.
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.
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.
Saccardy, K., Cornic, G., Brulfert, J., Reyss, A.: Effect of drought on net CO2 uptake by Zea leaves. - Planta 199: 589–595, 1996.
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.
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.
Schittenhelm, S., Schroetter, S.: Comparison of drought tolerance of maize, sweet sorghum and sorghum-sudangrass hybrids. - J. Agr. Crop Sci. 200: 46–53, 2014.
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.
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.
Steudle, E., Peterson, C.A.: How does water get through roots? J. exp. Bot. 49: 775–788, 1998.
Tardieu, F.: Drought perception by plants: do cells of droughted plants experience water stress? - Plant Growth Regul. 20: 93–104, 1996.
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.
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.
Vandeleur, R., Niemietz, C., Tilbrook, J., Tyerman, S.D.: Roles of aquaporins in root responses to irrigation. - Plant Soil 274: 141–161, 2005.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: The authors would like to thank the University of Damietta for funding this work.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Hasan, S.A., Rabei, S.H., Nada, R.M. et al. Water use efficiency in the drought-stressed sorghum and maize in relation to expression of aquaporin genes. Biol Plant 61, 127–137 (2017). https://doi.org/10.1007/s10535-016-0656-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-016-0656-9