AJPS  Vol.8 No.4 , March 2017
Hypoxia-Responsive Root Hydraulic Conductivity Influences Soybean Cultivar-Specific Waterlogging Tolerance
Abstract: Excess soil moisture induces hypoxic conditions and causes waterlogging injury in soybean [Glycine max (L.) Merr.]. This study investigated the mechanism underlying the development of waterlogging injury. Nine Japanese soybean cultivars with varying degrees of waterlogging tolerance were grown in a hydroponic system for 14 days under hypoxic conditions. Shoot and root biomasses and root hydraulic conductivity were measured at an early vegetative stage for plants under control and hypoxic conditions. Root morphological traits and intramembrane aquaporin proteins were also analyzed. The tolerance of each cultivar to field waterlogging was based on biomass changes induced by the hypoxia treatment. Root hydraulic conductivity responses to hypoxia were associated with changes in total dry weight, leaf dry weight, and leaf area. The effects of hypoxic conditions on root hydraulic conductivity were also represented by the changes in root morphology, such as total root length, thick-root length, and number of root tips. Additionally, a 32.3 kDa aquaporin-like protein seemed to regulate root hydraulic conductivity. Our results from a hydroponic culture suggest that the soybean cultivar-specific responses to hypoxic conditions in the rhizosphere reflect fluctuations in hydraulic conductivity related to root morphological or qualitative changes.
Cite this paper: Jitsuyama, Y. (2017) Hypoxia-Responsive Root Hydraulic Conductivity Influences Soybean Cultivar-Specific Waterlogging Tolerance. American Journal of Plant Sciences, 8, 770-790. doi: 10.4236/ajps.2017.84054.

[1]   Ahmed, F., Rafii, M.Y., Ismail, M.R., Juraimi, A.S., Rahim, H.A., Asfaliza, R. and Latif, M.A. (2013) Waterlogging Tolerance of Crops: Breeding, Mechanism of Tolerance, Molecular Approaches, and Future Prospects. BioMed Research International, 2013, Article ID: 963525.

[2]   E-STAT (2016) Portal Site of Official Statistics of Japan.

[3]   Takahashi, M., Hosokawa, H. and Matsuzaki, M. (2006) N2 Fixation of Nodules and N Absorption by Soybean Roots Associated with Ridge Tillage on Poorly Drained Upland Fields Converted from Rice Paddy Fields. Soil Science and Plant Nutrition, 52, 291-299.

[4]   Yoshinaga, S. (2012) Improvement of Soybean Growth and Yield (Glycine max L.) by Inter-Row Stripe Tillage in Upland Fields Converted from Paddy Fields. Japan Agricultural Research Quarterly, 46, 115-121.

[5]   Shimada, S., Hamaguchi, H., Kim, Y., Matsuura, K., Kato, M., Kokuryu, T., Tazawa, J. and Fujimori, S. (2012) Effects of Water Table Control by Farm-Oriented Enhancing Aquatic System on Photosynthesis, Nodule Nitrogen Fixation and Yield of Soybeans. Plant Production Science, 15, 132-143.

[6]   Kokubun, M. (2013) Genetic and Cultural Improvement of Soybean for Waterlogged Conditions in Asia. Field Crops Research, 152, 3-7.

[7]   Tian, X.-H., Nakamura, T. and Kokubun, M. (2005) The Role of Seed Structure and Oxygen Responsiveness in Pre-Germination Flooding Tolerance of Soybean Cultivars. Plant Production Science, 8, 157-165.

[8]   Jitsuyama, Y., Hagihara, Y. and Konno, Y. (2014) Two Imbibition Properties Independently Influence the Cultivar-Specific Flooding Tolerance of Dried Soybean Seeds. Seed Science Research, 24, 37-48.

[9]   Oosterhuis, D.M., Scott, H.D., Hampton, R.E. and Wullschleger, S.D. (1990) Physiological Responses of Two Soybean (Glycine max (L.) Merr.) Cultivars to Short-Term Flooding. Environmental and Experimental Botany, 30, 85-92.

[10]   Sung, F.J.M. (1993) Waterlogging Effect on Nodule Nitrogenase and Leaf Nitrate Reductase Activities in Soybean. Field Crops Research, 35, 183-189.

[11]   Board, J.E. (2008) Waterlogging Effects on Plant Nutrient Concentrations in Soybean. Journal of Plant Nutrition, 31, 828-838.

[12]   Bacanamwo, M. and Purcell, L.C. (1999) Soybean Dry Matter and N Accumulation Responses to Flooding Stress, N Sources and Hypoxia. Journal of Experimental Botany, 50, 689-696.

[13]   Sauter, M. (2013) Root Responses in Flooding. Current Opinion in Plant Biology, 16, 282-286.

[14]   Shimamura, S., Yamamoto, R., Nakamura, T., Shimada, S. and Komatsu, S. (2010) Stem Hypertrophic Lenticels and Secondary Aerenchyma Enable Oxygen Transport to Roots of Soybean in Flooded Soil. Annals of Botany, 106, 277-284.

[15]   Matsukawa, I., Tanimura, Y., Teranishi, R. and Banba, H. (1983) Varietal Difference of Resistance to Excess Wet Injury of Soybean in Dry Field Converted from Paddy Rice Field. Research Bulletin of Hokkaido Prefecture Agricultural Experimental Station, 49, 32-40. (In Japanese, with Summary in English)

[16]   Thomas, A.L., Guerreiro, S.M.C. and Sodek, L. (2005) Aerenchyma Formation and Recovery from Hypoxia of the Flooded Root System of Nodulated Soybean. Annals of Botany, 96, 1191-1198.

[17]   Jitsuyama, Y. (2013) Responses of Japanese Soybeans to Hypoxic Condition at Rhizosphere Were Different Depending Upon Cultivars and Ambient Temperatures. American Journal of Plant Science, 4, 1297-1308.

[18]   Jitsuyama, Y. (2015) Morphological Root Responses of Soybean to Rhizosphere Hypoxia Reflect Waterlogging Tolerance. Canadian Journal of Plant Science, 95, 999-1005.

[19]   Kousaka, F., Ohnishi, S., Nakamura, T., Hiraga, S., Maekawa, T., Shimada, S. and Fujita, S. (2013) Response of Soybean (Glycine max) Waterlogging-Tolerant Variety Shoku-kei32 to Short-Term Soil Flooding. 11th Conference of the International Society for Plant Anaerobiosis, Los Bacos, 6-11 October 2013, 121.

[20]   Hokkaido Research Organization, Agriculture Research Department Central Agricultural Experiment Station (HCAES) (2009) Results Outline in 2009. General Topic. Field Survey for Soybean Waterlogging Tolerance after the Blooming Stage. (In Japanese)

[21]   Fehr, W.R., Caviness, C.E., Burmood, D.T. and Pennington, J.S. (1971) Stage of Development Descriptions for Soybeans, Glycine max (L.) Merrill. Crop Science, 11, 929-931.

[22]   Kaneko, T., Horie, T., Nakahara, Y., Tsuji, N., Shibasaka, M. and Katsuhara, M. (2015) Dynamic Regulation of the Root Hydraulic Conductivity of Barley Plants in Response to Salinity/Osmotic Stress. Plant and Cell Physiology, 56, 875-882.

[23]   Emery, R.J.N. and Salon, C. (2002) Water Entry into Detached Root Systems Saturates with Increasing Externally Applied Pressure: A Result Inconsistent with Models of Simple Passive Diffusion. Physiologia Plantarum, 115, 406-416.

[24]   Hanba, T.Y., Shibasaka, M., Hayashi, Y., Hayakawa, T., Kasamo, K., Terashima, I. and Katsuhara, M. (2004) Overexpression of the Barley Aquaporin HvPIP2. 1 Increases Internal CO2 Conductance and CO2 Assimilation in the Leaves of Transgenic Rice Plants. Plant and Cell Physiology, 45, 521-529.

[25]   Bradford, M.M. (1976) A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Analytical Biochemistry, 72, 248-254.

[26]   Laemmli, U.K. (1970) Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage. Nature, 227, 680-685.

[27]   Sallam, A. and Scott, H.D. (1987a) Effects of Prolonged Flooding on Soybean at the R2 Growth Stage: I. Dry Matter and N and P Accumulation. Journal of Plant Nutrition, 10, 567-592.

[28]   Tjepkema, J.D. and Yocum, C.Y. (1973) Respiration and Oxygen Transport in Soybean Nodules. Planta, 115, 59-72.

[29]   Letey, J. and Stolzy, L.H. (1967) Limiting Distances between Root and Gas Phase for Adequate Oxygen Supply. Soil Science, 103, 404-409.

[30]   Boru, G., Vantoai, T., Alves, J., Hua, D. and Knee, M. (2003) Response of Soybean to Oxygen Deficiency and Elevated Root-Zone Carbon Dioxide Concentration. Annals of Botany, 91, 447-453.

[31]   Greenway, H., Armstrong, W. and Colmer, T.D. (2006) Condition Leading to High CO2 (> 5 kPa) in Waterlogged-Flooded Soils and Possible Effects on Root Growth and Metabolism. Annals of Botany, 98, 9-32.

[32]   Irving, L.J., Sheng, Y.B., Woolley, D. and Matthew, C. (2007) Physiological Effects of Waterlogging on Two Lucerne Varieties Grown under Glasshouse Conditions. Journal of Agronomy and Crop Science, 193, 345-356.

[33]   Wiengweera, A., Greenway, H. and Thomson, C.J. (1997) The Use of Agar Nutrient Solution to Simulate Lack of Convection in Waterlogged Soils. Annals of Botany, 80, 115-123.

[34]   Bouma, T.J., Nielsen, K.L., Eissenstat, D.M. and Lynch, J.P. (1997) Soil CO2 Concentration Does Not Affect Growth or Root Respiration in Bean and Citrus. Plant, Cell and Environment, 20, 1495-1505.

[35]   Moldovan, D., Spriggs, A., Yang, J., Pogson, B.J., Dennis, E.S. and Wilson, I.W. (2010) Hypoxia-Responsive microRNAs and trans-Acting Small Interfering RNAs in Arabidopsis. Journal of Experimental Botany, 61, 165-177.

[36]   Sairam, R.K., Kumutha, D., Ezhilmathi, K., Deshmukh, P.S. and Srivastava, G.C. (2008) Physiology and Biochemistry of Waterlogging Tolerance in Plants. Biologia Plantarum, 52, 401-412.

[37]   Sallam, A. and Scott, H.D. (1987b) Effects of Prolonged Flooding on Soybeans during Early Vegetative Growth. Soil Science, 144, 61-66.

[38]   Kramer, P.J. and Boyer, J.S. (1995) Historical Review, Some General Concepts, Soil-Plant-Atmosphere Continuum and Ohm’s Law Analogy. In: Kramer, P.J. and Boyer, J.S., Eds., Water Relations of Plants and Soils, Academic Press, London, 9.

[39]   Suga, S., Murai, M., Kuwagata, T. and Maeshima, M. (2003) Differences in Aquaporin Levels among Cell Type of Radish and Measurement of Osmotic Water Permeability of Individual Protoplasts. Plant and Cell Physiology, 44, 277-286.

[40]   Matsuo, N., Nanjo, Y., Tougou, M., Nakamura, T., Nishizawa, K., Komatsu, S. and Shimamura, S. (2012) Identification of Putative Aquaporin Genes and Their Expression Analysis under Hypoxic Conditions in Soybean (Glycine max (L.) Merr.). Plant Production Science, 15, 278-283.

[41]   Lopez, F., Bousser, A., Sissoeff, I., Hoarau, J. and Mahé, A. (2004) Characterization in Maize of ZmTIP2-3, a Root-Specific Tonoplast Intrinsic Protein Exhibiting Aquaporin Activity. Journal of Experimental Botany, 55, 539-541.

[42]   Suga, S. and Maeshima, M. (2004) Water Channel Activity of Radish Plasma Membrane Aquaporins Heterologously Expressed in Yeast and Their Modification by Site-Directed Mutagenesis. Plant and Cell Physiology, 45, 823-830.

[43]   Liu, C., Fukumoto, T., Matsumoto, T., Gena, P., Frascaria, D., Kaneko, T., Katsuhara, M., Zhong, S., Sun, X., Zhu, Y., Iwasaki, I., Ding, X., Calamita, G. and Kitagawa, Y. (2013) Aquaporin OsPIP1. 1 Promotes Rice Salt Resistance and Seed Germination. Plant Physiology and Biochemistry, 63, 151-158.

[44]   Yaneff, A., Vitali, V. and Amodeo, G. (2015) PIP1 Aquaporins: Intrinsic Water Channels or PIP2 Aquaporin Modulators? FEBS Letters, 589, 3508-3515.

[45]   Siefritz, F., Tyree, M.T., Lovisolo, C., Schubert, A. and Kaldenhoff, R. (2002) PIP1 Plasma Membrane Aquaporins in Tobacco: From Cellular Effects to Function in Plants. The Plant Cell, 14, 869-876.

[46]   Tournaire-Roux, C., Sutka, M., Javot, H., Gout, E., Gerbeau, P., Luu, D.T., Bligny, R. and Maurel, C. (2003) Cytosolic pH Regulates Root Water Transport during Anoxic Stress through Gating of Aquaporins. Nature, 425, 393-397.

[47]   Sadok, W. and Sinclair, T.R. (2010) Genetic Variability of Transpiration Response of Soybean (Glycine max (L.) Merr.) Shoots to Leaf Hydraulic Conductance Inhibitor AgNO3. Crop Science, 50, 1423-1430.

[48]   Valliyodan, B., Van Toai, T.T., Alves, J.D., Goulart, P.D.P., Lee, J.D., Fritschi, F.B., Rahman, M.A., Islam, R., Shannon, J.G. and Nguyen, H.T. (2014) Expression of Root-Related Transcription Factors Associated with Flooding Tolerance of Soybean (Glycine max). International Journal of Molecular Sciences, 15, 17622-17643.

[49]   Mutava, R.N., Prince, S.J.K., Syed, N.H., Song, L., Valliyodan, B., Chen, W. and Nguyen, H.T. (2015) Understanding Abiotic Stress Tolerance Mechanisms in Soybean: A Comparative Evaluation of Soybean Response to Drought and Flooding Stress. Plant Physiology and Biochemistry, 86, 109-120.

[50]   Komatsu, S., Hiraga, S. and Nouri, M.Z. (2014) Analysis of Flooding-Responsive Proteins Localized in the Nucleus of Soybean Root Tips. Molecular Biology Reports, 41, 1127-1139.

[51]   Borella, J., do Amarante, L., de Olibeira, D.D.C., de Olibeira, A.C.B. and Braga, E.J.B. (2014) Waterlogging-Induced Changes in Fermentative Metabolism in Roots and Nodules of Soybean Genotypes. Scientia Agricola, 71, 499-508.

[52]   Jung, G., Matsunami, T., Oki, Y. and Kokubun, M. (2008) Effects of Waterlogging on Nitrogen Fixation and Photosynthesis in Supernodulating Soybean Cultivar Kanto 100. Plant Production Science, 11, 291-297.