Skip to main content
Log in

The interactive effect of high temperature and water deficit stress on nitrogen fixation, photosynthesis, chlorophyll fluorescence, seed yield and quality in soybean (Glycine max)

  • Original Article
  • Published:
Plant Physiology Reports Aims and scope Submit manuscript

Abstract

Drought and heat stress are important abiotic stresses restricting plant growth, while the two stresses often occur at the same time in nature, little is known about when these stresses occur in combination. Therefore, attempts were made to understand the impact of water stress imposed under different temperature conditions on various physiological parameters such as nitrogen fixation, photosynthesis, chlorophyll fluorescence, seed yield and quality. Cultivar JS 97–52 was grown in pots under polyhouses maintained at day/night temperatures of 30/22, 34/24, 38/26 and 42/28 °C. At each temperature, pots were divided into two sets, one set was unstressed while second was subjected to water stress at reproductive stage (beginning of seed fill). An increase in temperature and water stress caused the reduction in CO2 exchange, which ultimately affected the nitrogen fixation. Nitrogenase activity was significantly declined in the nodules with an increase in temperature. There was a concomitant decline in leghemoglobin, heme-chrome and ureids content in the nodules which ultimately resulted in the reduction of nitrate reductase activity, chlorophyll content and total free amino acid under high temperatures. A decline in nitrogen and carbon fixation ultimately caused a reduction in seed yield and quality. Water stress when imposed at different temperature further aggravated the effects of temperature, and the combination of water stress and high temperature had more detrimental effect. Thus, understanding the mechanisms by which plants acclimate to water deficit combined with high temperature is crucial for identifying stress tolerant soybean cultivars and to pave the way for obtaining cultivars with higher productivity under combined stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahmed, I. M., Dai, H., Zheng, W., Cao, F., Zhang, G., Sun, D., & Wu, F. (2013). Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley. Plant Physiolgy and Biochemistry., 63, 49–60.

    Article  CAS  Google Scholar 

  • Alamillo, M. J., Díaz-Leal, J. L., Sánchez-Moran, M. V., & Pineda, M. (2010). Molecular analysis of ureide accumulation under drought stress in Phaseolus vulgaris L. Plant Cell and Environment., 33, 1828–1837.

    Article  CAS  Google Scholar 

  • Alsajri, F. A., Wijewardana, C., Irby, J., Bellaloui, N., Krutz, L. J., Golden, B., Gao, W., & Reddy, K. R. (2020). Developing functional relationships between temperature and soybean yield and seed quality. Agronomy Journal., 112, 194–204.

    Article  CAS  Google Scholar 

  • Appleby, C. A., & Bergersen, F. J. (1980). Preparation and experimental use of leghemoglobin. In F. J. Bergersen (Ed.), Methods of Evaluating Biological Nitrogen Fixation (pp. 315–335). Chichester: Wiley.

    Google Scholar 

  • Aranjuelo, I., Arrese-Igor, C., & Molero, G. (2014). Nodule performance within a changing environmental context. Journal of Plant Physiology., 171, 1076–1090.

    Article  CAS  PubMed  Google Scholar 

  • Aranjuelo, I., Irigoyen, J. J., & Sanchez-Diaz, M. (2007). Effect of elevated temperature and water availability on CO2 exchange and nitrogen fixation of nodulated alfalfa plants. Environmental and Experimental Botany, 59, 99–108.

    Article  CAS  Google Scholar 

  • Aranjuelo, I., Irigoyen, J. J., Sánchez-Díaz, M., & Nogués, S. (2008). Carbon partitioning in N2 fixing Medicago sativa plants exposed to different CO2 and temperature conditions. Functional Plant Biology, 35, 306–317.

    Article  CAS  PubMed  Google Scholar 

  • Aranjuelo, I., Irigoyen, J. J., Sánchez-Díaz, M., & Nogués, S. (2009). Elevated CO2 and water-availability effect on gas exchange and nodule development in N2-fixing alfalfa plants. Environmental and Experimental Botany, 65, 18–26.

    Article  CAS  Google Scholar 

  • Ashraf, M. (2004). Some important physiological selection criteria for salt tolerance in plants. Flora, 199, 361–376.

    Article  Google Scholar 

  • Ashraf, M., & Harris, P. J. C. (2013). Photosynthesis under stressful environments: An overview. Photosynthetica, 51, 163–190.

    Article  CAS  Google Scholar 

  • Awasthi, R., Kaushal, N., Vadez, V., Turner, N. C., Berger, J., Siddique, K. H. M., & Nayyar, H. (2014). Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Functional Plant Biology., 41, 1148–1167.

    Article  CAS  PubMed  Google Scholar 

  • Balfagon, D., Zandalinas, S. I., Mittler, R., & Gomez-Cadenas, A. (2020). High temperatures modify plant responses to abiotic stress conditions. Physiologia Plantarum., 170, 335–344.

    Article  CAS  PubMed  Google Scholar 

  • Bhandari, K., Sharma, K., Siddique, B. H. K., Gaur, P., Kumar, S., Nair, R., & Nayyar, H. (2017). Temperature sensitivity of food legumes: A physiological insight. Acta Physiologia Plantarum., 68, 39–68.

    Google Scholar 

  • Bhatia, V. S., & Jumrani, K. (2016). A maximin–minimax approach for classifying soybean genotypes for drought tolerance based on yield potential and loss. Plant Breeding, 136, 691–700.

    Article  Google Scholar 

  • Bhatia, V. S., Jumrani, K., & Pandey, G. P. (2014a). Developing drought tolerance in soybean using physiological approaches. Soybean Research, 12, 1–19.

    Google Scholar 

  • Bhatia, V. S., Jumrani, K., & Pandey, G. P. (2014b). Evaluation of the usefulness of senescing agent potassium iodide as a screening tool for tolerance to terminal drought in soybean. Plant Knowledge Journal, 3, 23–30.

    Google Scholar 

  • Boote, K. J. (2011). Improving soybean cultivars for adaptation to climate change and climate variability. In S. S. Yadav, R. J. Redden, J. L. Hatfield, H. Lotze-Campen, & E. A. Hall (Eds.), Crop Adaptation to Climate Change (pp. 370–395). West Sussex: John Wiley and Sons, Ltd.

    Chapter  Google Scholar 

  • Borrell, A. K., Hammer, G., & van Oosterom, E. (2001). Stay-green: A consequence of the balance between supply and demand for nitrogen during grain filling. Annual Applied Biology, 138, 91–95.

    Article  Google Scholar 

  • Camejo, D., Rodriguez, P., Morales, M. A., Dell’Amico, J. M., Torrecillas, A., & Alarcon, J. J. (2005). High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of Plant Physiology, 162, 281–289.

    Article  CAS  PubMed  Google Scholar 

  • Centritto, M., Loreto, F., & Chartzoulakis, K. (2003). The use of low (CO2) to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. Plant Cell and Environment, 26, 585–594.

    Article  Google Scholar 

  • Chebrolu, K., Fritschi, F. B., Ye, S., Krishnan, H. B., Smith, J. R., & Gillman, J. D. (2016). Impact of heat stress during seed development on soybean seed metabolome. Metabolomics, 12, 28.

    Article  Google Scholar 

  • Chilakala, A. R., Mali, K. V., Irulappan, V., Patil, B. S., Pandey, P., Rangappa, K., Ramegowda, V., Kumar, M. N., Puli, C. O. R., Mohan-Raju, B., et al. (2022). Combined drought and heat stress influences the root water relation and determine the dry root rot disease development under field conditions: A study using contrasting chickpea genotypes. Frontier in Plant Science., 13, 890551.

    Article  Google Scholar 

  • Christophe, S., Jean-Christophe, A., Annabelle, L., Alain, O., Marion, P., & Anne-Sophie, V. (2011). Plant N fluxes and modulation by nitrogen, heat and water stresses: A review based on comparison of legumes and non-legume plants. In A. Shanker & B. Venkateswarlu (Eds.), Abiotic Stress in Plants—Mechanisms and Adaptations (pp. 79–118). Intech Open Access Publisher.

    Google Scholar 

  • Cohen, I., Zandalinas, S. I., Fritschi, F. B., Sengupta, S., Fichman, Y., Azad, R. K., & Mittler, R. (2021b). The impact of water deficit and heat stress combination on the molecular response, physiology, and seed production of soybean. Physiologia Plantarum., 172, 41–52.

    Article  CAS  PubMed  Google Scholar 

  • Cohen, I., Zandalinas, S. I., Huck, C., Fritschi, F. B., & Mittler, R. (2021a). Meta- analysis of drought and heat stress combination impact on crop yield and yield components. Physiologia Plantarum, 171, 66–76.

    Article  CAS  PubMed  Google Scholar 

  • Cotrim, M. F., Gava, R., Campos, C. N. S., De David, C. H. O., Reis, I. D. A., Teodoro, L. P. R., et al. (2021). Physiological performance of soybean genotypes grown under irrigated and rainfed conditions. Journal of Agronomy and Crop Science., 207, 34–43.

    Article  CAS  Google Scholar 

  • Craine, J. M., & Jackson, R. D. (2010). Plant nitrogen and phosphorus limitation in 98 North American grassland soils. Plant and Soil, 334, 73–84.

    Article  CAS  Google Scholar 

  • David, W., & Lawlor, H. (2002). Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. Journal of Experimental Botany, 53(I15), 773–787.

    Google Scholar 

  • Dayoub, E., Lamichhane, J. R., Schoving, C., Debaeke, P., & Maury, P. (2021). Early-stage phenotyping of root traits provides insights into the drought tolerance level of soybean cultivars. Agronomy, 11, 188.

    Article  CAS  Google Scholar 

  • De Moraes, M. T., & Gusmao, A. G. (2021). How do water, compaction and heat stresses affect soybean root elongation? A Review. Rhizosphere, 19, 100403.

    Article  Google Scholar 

  • Djanaguiraman, M., & Prasad, P. V. V. (2010). Ethylene production under high temperature stress causes premature leaf senescence in soybean. Functional Plant Biology, 37, 1071–1084.

    Article  CAS  Google Scholar 

  • Djanaguiraman, M., Schapaugh, W., Fritschi, F., Nguyen, H., & Prasad, P. V. V. (2019). Reproductive success of soybean (Glycine max L. Merril) cultivars and exotic lines under high daytime temperature. Plant Cell and Environment., 42, 321–336.

    Article  CAS  Google Scholar 

  • Du, Y., Zhao, Q., Chen, L., Yao, X., Zhang, W., Zhang, B., & Xie, F. (2020). Effect of drought stress on sugar metabolism in leaves and roots of soybean seedlings. Plant Physiology and Biochemistry., 146, 1–12.

    Article  CAS  PubMed  Google Scholar 

  • Dutta, S., Mohanty, S., & Tripathy, B. C. (2009). Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiology., 150, 1050–1061.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egli, D. B. (2010). Soybean reproductive sink size and short-term reductions in photosynthesis during flowering and pod set. Crop Science, 50, 1971–1977.

    Article  Google Scholar 

  • Egli, D. B., TeKrony, D. M., Heitholt, J. J., & Rupe, J. (2005). Air temperature during seed filling and soybean seed germination and vigor. Crop Science., 45, 1329–1335.

    Article  Google Scholar 

  • Erice, G. E., Sanz-Saez, A., Aroca, R., Ruiz-Lozano, J. M., Avice, J. C., Irigoyen, J. J., Sanchez-Diaz, M., & Aranjuelo, I. (2014). Photosynthetic down-regulation in N2 -fixing alfalfa under elevated CO2 alters rubisco content and decreases nodule metabolism via nitrogenase and tricarboxylic acid cycle. Acta Physiologia Plantarum, 36, 2607–2617.

    Article  CAS  Google Scholar 

  • Fageria, N., & Baligar, V. (2005). Enhancing nitrogen use efficiency in crop plants. Advances in Agronomy, 88, 97–185.

    Article  CAS  Google Scholar 

  • Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., & Basra, S. M. A. (2009). Plant drought stress: Effects, mechanisms and management. Agronomy and Sustainable Devlopment, 29, 185–212.

    Article  Google Scholar 

  • Foyer, C. H., Lam, H.-M., Nguyen, H. T., Siddique, K. H., Varshney, R. K., Colmer, T. D., et al. (2016). Neglecting legumes has compromised human health and sustainable food production. Nature Plants., 2, 1–10.

    Article  Google Scholar 

  • Gálvez, L., González, E. M., & Arrese-Igor, C. (2005). Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. Journal of Experimental. Botany., 56, 2551–2561.

    Article  PubMed  Google Scholar 

  • Gargallo-Garriga, A., Sardans, J., Pérez-Trujillo, M., Oravec, M., Urban, O., Jentsch, A., Kreyling, J., Beierkuhnlein, C., Parella, T., & Peñuelas, J. (2015). Warming differentially influences the effects of drought on stoichiometry and metabolomics in shoots and roots. New Phytologist, 207, 591–603.

    Article  CAS  PubMed  Google Scholar 

  • Garstka, M., Venema, J. H., Rumak, I., Gieczewska, K., Rosiak, M., & Kierdaszuk, K. L. (2007). Contrasting effect of dark chilling on chloroplast structure and arrangement of chlorophyll protein complexes in pea and tomato plants with a different susceptibility to non freezing temperature. Planta, 226, 1165–1181.

    Article  CAS  PubMed  Google Scholar 

  • Georgieva, K., Tsonev, T., Velikova, V., & Yordanov, I. (2000). Photosynthetic activity during high temperature of pea plants. Journal of Plant Physiology., 157, 169–176.

    Article  CAS  Google Scholar 

  • Guenni, O., Baruch, Z., & Marın, D. (2004). Responses to drought of five Brachiaria species. II. Water relations and leaf gas exchange. Plant and Soil, 258, 249–260.

    Article  CAS  Google Scholar 

  • Gunawardena, M., & De Silva, C. (2014). Identifying the impact of temperature and water stress on growth and yield parameters of chilli (Capsicum annuum L.). OUSL Journal, 7, 25–42.

    Article  Google Scholar 

  • Gupta, A., & Senthil-Kumar, M. (2017). Concurrent stresses are perceived as new state of stress by the plants: Overview of impact of abiotic and biotic stress combinations. In M. Senthil-Kumar (Ed.), Plant Tolerance to Individual and Concurrent Stresses (pp. 1–31). New delhi: Springer Pvt Ltd.

    Google Scholar 

  • Hamayun, M., Hussain, A., Iqbal, A., Khan, S. A., Gul, S., Khan, H., Ur Rehman, K., Bibi, H., & Lee, I. J. (2021). Penicillium glabrum acted as a heat stress relieving endophyte in soybean and sunflower. Polish Journal of Environmental Studies, 30, 9955.

    Google Scholar 

  • Hamerlynck, E. P., Huxman, T. E., Loik, M. E., & Smith, S. D. (2000). Effects of extreme high temperature, drought and elevated CO2 on photosynthesis of Mojave Desert evergreen shrub, Larrea dridentata. Plant Ecology, 148, 183–193.

    Article  Google Scholar 

  • Hardy, R. W. F., Burns, R. C., & Holsten, R. D. (1973). Applications of the acetylene-ethylene assay for measurement of nitrogen fixation. Soil Biology and Biochemistry, 5, 47–81.

    Article  CAS  Google Scholar 

  • Herridge, D. F., Peoples, M. B., & Boddey, R. M. (2008). Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil, 311, 1–18.

    Article  CAS  Google Scholar 

  • Herritt, M. T., & Fritschi, F. B. (2020). Characterization of photosynthetic phenotypes and chloroplast ultrastructural changes of soybean (Glycine max) in responses to elevated air temperature. Frontier in Plant Science, 11, 153.

    Article  Google Scholar 

  • Hiscox, J. D., & Israelstam, G. F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian Journal of Botany, 57, 1332–1334.

    Article  CAS  Google Scholar 

  • Hisokava, K. (2004). Interspecific difference in the photosynthesis-nitrogen relationship: Patterns, physiological causes, and ecological importance. Journal of Plant Research., 117, 481–494.

    Article  Google Scholar 

  • Houlton, B. Z., Wang, Y. P., Vitousek, P. M., & Field, C. B. (2008). A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature, 454, 327–330.

    Article  CAS  PubMed  Google Scholar 

  • Hungria, M., & Vargas, M. A. T. (2000). Environmental factors affecting N2 fixation in grain legumes in tropics with an emphasis on Brazil. Field Crops Research, 65, 151–154.

    Article  Google Scholar 

  • IPCC, Climate Change (2014). Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.

  • Jagadish, S. V. K., Way, D. A., & Sharkey, T. D. (2021). Plant heat stress: Concepts directing future research. Plant Cell and Environment., 44, 1992–2005.

    Article  CAS  Google Scholar 

  • Jaworski, E. K. (1971). Nitrate reductase assay in intact plant tissues. Biochemistry Biophysical Reserach Commmunication., 43, 1274–1279.

    Article  CAS  Google Scholar 

  • Jianing, G., Yuhong, G., Yijun, G., Rasheed, A., Qian, Z., Zhiming, X., Mahmood, A., Shuheng, Z., Zhuo, Z., Zhuo, Z., & Xiaoxue, W. (2022). Improvement of heat stress tolerance in soybean (Glycine max L), by using conventional and molecular tools. Frontiers in Plant Science, 13, 993189.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin, Z., Zhuang, Q., Wang, J., Archontoulis, S. V., Zobel, Z., & Kotamarthi, V. R. (2017). The combined and separate impacts of climate extremes on the current and future US rainfed maize and soybean production under elevated CO2. Global Change Biology, 23, 2687–2704.

    Article  PubMed  Google Scholar 

  • Jumrani, K., & Bhatia, V. S. (2018a). Impact of combined stress of high temperature and water deficit on growth and seed yield of soybean. Physiology and Molecular Biology of Plants, 24, 37–50.

    Article  PubMed  Google Scholar 

  • Jumrani, K., & Bhatia, V. S. (2018b). Combined effect of temperature and water stress imposed at vegetative and reproductive stage on seed quality in soybean. Plant Physiology Reports., 23, 227–244.

    CAS  Google Scholar 

  • Jumrani, K., & Bhatia, V. S. (2019a). Identification of drought tolerant genotypes using physiological traits in soybean. Physiology and Molecular Biology of Plants, 25(667–681), 7.

    Google Scholar 

  • Jumrani, K., & Bhatia, V. S. (2019b). Combined effect of temperature and water stress on physiological and biochemical processes in soybean (Glycine max). Physiology and Molecular Biology of Plants, 25, 697–711.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jumrani, K., Bhatia, V. S., Kataria, S., Alamri, S., Siddiqui, M. H., & Rastogi, A. (2022a). Inoculation with arbuscular mycorrhizal fungi alleviates the adverse effects of high temperature in soybean. Plants, 11, 2210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jumrani, K., Bhatia, V. S., Kataria, S., & Landi, M. (2022b). Screening soybean genotypes for high-temperature tolerance by maximin-minimax method based on yield potential and loss. Agronomy, 12, 2854.

    Article  CAS  Google Scholar 

  • Jumrani, K., Bhatia, V. S., & Pandey, G. P. (2017). Impact of elevated temperatures on specific leaf weight, stomatal density, photosynthesis and chlorophyll fluorescence in soybean. Photosynthesis Reserach., 131, 333–350.

    Article  CAS  Google Scholar 

  • Jun, H. K., Sarath, G., & Wagner, F. W. (1994). Detection and purification of modified leghemoglobins from soybean root nodules. Plant Science, 100, 31–40.

    Article  CAS  Google Scholar 

  • Kant, S., Seneweera, S., Rodin, J., Materne, M., Burch, D., Rothstein, S., & Spangenberg, G. (2012). Improving yield potential in crops under elevated CO2: Integrating the photosynthetic and nitrogen utilization efficiencies. Frontier in Plant Science, 3, 162.

    CAS  Google Scholar 

  • Keerio, M. I. (2001). Nitrogenase activity of soybean root nodules inhibited after heat stress. Online Journal of Biological Science, 1, 297–300.

    Google Scholar 

  • Klimenko, S., Peshkova, A., & Dorofeev, N. (2006). Nitrate reductase activity during heat shock in winter wheat. Journal of Stress Physiology and Biochemistry, 2, 50–55.

    Google Scholar 

  • Kobraee, S., Shamsi, K., & Rasekhi, B. (2011). Soybean production under water defcit conditions. Annals of Biological Research, 2, 423–434.

    Google Scholar 

  • Kosová, K., Vítámvás, P., Prášil, I. T., & Renaut, J. (2011). Plant proteome changes under abiotic stress contribution of proteomics studies to understanding plant stress response. Journal of Proteomics, 74, 1301–1322.

    Article  PubMed  Google Scholar 

  • Kumangai, E., & Sameshima, R. (2014). Genotypic differences in soybean yield responses to increasing temperature in a cool climate are related to maturity group. Agriculture and Forest Meteorology., 198–199, 265–272.

    Article  Google Scholar 

  • Larrainzar, E., Wienkoop, S., Scherling, C., Kempa, S., Ladrera, R., Arrese-Igor, C., Weckwerth, W., & Gonzalez, E. M. (2009). Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery. Molecular Plant-Microbe Interactions, 22, 1565–1576.

    Article  CAS  PubMed  Google Scholar 

  • Lira, M. A., Lima, A. S. T., Arruda, J. R. F., & Smith, D. L. (2005). Effect of root temperature on nodule development of bean, lentil, and pea. Soil Biology and Biochemistry., 37, 235–239.

    Article  Google Scholar 

  • Liu, G. T., Ma, L., Duan, W., Wang, B. C., Li, J. H., Xu, H. G., Yan, X. Q., Yan, B. F., Li, S. H., & Wang, L. J. (2014). Differential proteomic analysis of grapevine leaves by iTRAQ reveals responses to heat stress and subsequent recovery. BMC Plant Biology, 14, 1–17.

    Article  Google Scholar 

  • Liu, X. B., Jin, J., Wang, G. H., & Herbert, S. J. (2008). Soybean yield physiology and development of high yielding practices in Northeast China. Field Crops Research., 105, 157–171.

    Article  Google Scholar 

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biology and Chemistry, 193, 265–275.

    Article  CAS  Google Scholar 

  • Luan, X., Bommarco, R., Scaini, A., & Vico, G. (2021). Combined heat and drought suppress rainfed maize and soybean yields and modify irrigation benefits in the USA. Environmental Research Letters., 16, 064023.

    Article  Google Scholar 

  • Lugan, R., Niogret, M. F., Leport, L., Guegan, J. P., Larher, F. R., Savoure, A., Kopka, J., & Bouchereau, A. (2010). Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. Plant Journal., 64, 215–229.

    Article  CAS  Google Scholar 

  • Maleki, A., Naderi, A., Naseri, R., Fathi, A., Bahamin, S., & Maleki, R. (2013). Physiological performance of soybean cultivars under drought stress. Bulletin of Environmental, Pharmacology and Life Sciences., 2, 38–44.

    Google Scholar 

  • Martinelli, T., Whittaker, A., Bochicchio, A., Vazzana, C., Suzuki, A., & Masclaux-Daubresse, C. (2007). Amino acid pattern and glutamate metabolism during dehydration stress in the ‘“resurrection”’ plant Sporobolus stapfianus: A comparison between desiccation-sensitive and desiccation-tolerant leaves. Journal of Experimental Botany., 58, 3037–3046.

    Article  CAS  PubMed  Google Scholar 

  • Matiu, M., Ankerst, D. P., & Menzel, A. (2017). Interactions between temperature and drought in global and regional crop yield variability during 1961–2014. PLoS ONE, 12, e0178339.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends in Plant Science., 11, 15–19.

    Article  CAS  PubMed  Google Scholar 

  • Mmbaga, G. W., Mtei, K. M., & Ndakidemi, P. A. (2014). Extrapolation on the use of rhizobium inoculants supplemented with phosphorus (P) and potassium (K) on growth and nutrition of legumes. Agriculture. Science., 5, 1207–1226.

    Google Scholar 

  • Mohammadi, K., Sohrabi, Y., Heidari, G., Khalesro, S., & Majidi, M. (2012). Effective factors on biological nitrogen fixation. African Journal of Agricultural Research, 7, 1782–1788.

    Google Scholar 

  • Monneveux, P., Pastenes, C., & Reynolds, M. P. (2003). Limitations to photosynthesis under light and heat stress in three high-yielding wheat genotypes. Journal of Plant Physiology, 160, 657–666.

    Article  CAS  PubMed  Google Scholar 

  • Nahar, M., Hasanuzzaman, H., & M., Fujita,. (2016). Heat stress responses and thermotolerance in soybean. In M. Miransari (Ed.), Abiotic Biotic Stress (pp. 261–284). Soybean Production: Academic Press, San Diego.

    Chapter  Google Scholar 

  • Nakagawa, A. C. S., Ario, N., Tomita, Y., Tanka, S., Murayama, N., Mizuta, C., IwayaInoue, M., & Ishibashi, Y. (2020). High temperature during soybean seed development differentially alters lipid and protein metabolism. Plant Production Science, 23, 504–516.

    Article  CAS  Google Scholar 

  • Naya, L., Ladrera, R., Ramos, J., Gonzalez, E. M., Arrese-Igor, C., Minchin, F. R., et al. (2007). The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiology, 144, 1104–1114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noorudeen, A. M., & Kulandaivelu, G. (1982). On the possible site of inhibition of photosynthetic electron transport by UV-B radiation. Physiologia Plantarum, 55, 161–166.

    Article  CAS  Google Scholar 

  • Obata, T., Witt, S., Lisec, J., Palacios-Rojas, N., Florez-Sarasa, I., Yousfi, S., Araus, J. L., Cairns, J. E., & Fernie, A. R. (2015). Metabolite profiles of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiology, 169, 2665–2683.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohyama, T., Matsumoto, K., Goto, H., Saito, A., & Higuchi, K. (2023). Nitrogen metabolism in non-nodulated and nodulated soybean plants related to ureide synthesis. Nitrogen, 4, 209–222.

    Article  CAS  Google Scholar 

  • Oldroyd, G. E. D., & Downie, J. A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology, 59, 519–546.

    Article  CAS  PubMed  Google Scholar 

  • Ortiz, A. C., De Smet, I., Sozzani, R., & Locke, A. M. (2021). Field-grown soybean shows genotypic variation in physiological and seed composition responses to heat stress during seed development. Environmental and Experimental Botany., 195, 104768.

    Article  Google Scholar 

  • Oukarroum, A., Madidi, S. E., Schansker, G., & Strasser, R. J. (2007). Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and rewatering. Environmental and Experimental Botany, 60, 438–446.

    Article  CAS  Google Scholar 

  • Pandey, P., Ramegowda, V., & Senthil-Kumar, M. (2015). Shared and unique responses of plants to multiple individual stresses and stress combinations: Physiological and molecular mechanisms. Frontier in Plant Science, 6, 723.

    Google Scholar 

  • Piao, S., Ciais, P., Friedlingstein, P., Peylin, P., Reichstein, M., Luyssaert, S., Margolis, H., Fang, J., Barr, A., Chen, A., et al. (2008). Net carbon di oxide losses of northern ecosystems in response to autumn warming. Nature, 451, 49–52.

    Article  CAS  PubMed  Google Scholar 

  • Pipolo, E. A., Sinclair, T. S., & Camara, G. M. S. (2004). Effects of temperature on oil and protein concentration in soybean seeds cultured in vitro. Annual Applied Biology., 144, 71–76.

    Article  CAS  Google Scholar 

  • Priya, R., Patil, M., Pandey, P., Singh, A., Sudha Babu, V., & Senthil-Kumar, M. (2022). Stress combinations and their interactions in plants database (SCIPDb): A onestop resource for understanding combined stress responses in plants. The Plant Journal. https://doi.org/10.1111/tpj.16497

    Article  Google Scholar 

  • Pshybytko, N. L., Kruk, J., Kabashnikova, L. F., & Strzalka, K. (2008). Function of plastoquinone in heat stress reactions of plants. Biochimistry Biophyics Acta, 1777, 1393–1399.

    Article  CAS  Google Scholar 

  • Pushpavalli, R., Zaman-Allah, M., Turner, N. C., Baddam, R., Rao, M. V., & Vadez, V. (2015). Higher flower and seed number leads to higher yield under water stress conditions imposed during reproduction in chickpea. Functional Plant Biology., 42, 162–174.

    Article  CAS  PubMed  Google Scholar 

  • Puteh, A., Thuzar, M., Mondal, M., Abdullah, N. P. B., & Halim, M. (2013). Soybean (Glycine max (L.) Merrill) seed yield response to high temperature stress during reproductive growth stages. Australian Journal of Crop Science., 7, 1472–1479.

    Google Scholar 

  • Rahnama, A., Poustini, K., & Tavakkol-Afshari, R. (2010). Growth and stomatal responses of bread wheat genotypes in tolerance to salt stress. International Journal of Biology and Life Sciences., 6, 216–221.

    Google Scholar 

  • Rai, V. K. (2002). Role of amino acids in plant responses to stresses. Biologia Plantarum, 45, 481–487.

    Article  CAS  Google Scholar 

  • Rastogi, A., Kovar, M., He, X., Zivcak, M., Kataria, S., Kalaji, H. M., Skalicky, M., Ibrahimova, U. F., Hussain, S., Mbarki, S., et al. (2020). JIP-test as a tool to identify salinity tolerance in sweet sorghum genotypes. Phostosynthetica, 58, 518–520.

    Article  CAS  Google Scholar 

  • Rivero, R. M., Mittler, R., Blumwald, E., & Zandalinas, S. I. (2022). Developing climate- resilient crops: Improving plant tolerance to stress combination. The Plant Journal, 109, 373–389.

    Article  CAS  PubMed  Google Scholar 

  • Rizhsky, L., Liang, H. J., Shuman, J., Shulaev, V., Davletova, S., & Mittler, R. (2004). When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology., 134, 1683–1696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers, A., Gibon, Y., Stitt, M., Morgan, P. B., Bernacchi, C. J., Ort, D. R., & Long, S. P. (2006). Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant Cell and Environment., 29, 1651–1658.

    Article  CAS  Google Scholar 

  • Rustad, L. E., Campbell, J. L., Marion, G. M., Norby, R. J., Mitchell, M. J., Hartle, A. E., Cornelissen, J. H. C., Gurevitch, J., GCTE-NEWS. (2001). A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia, 126, 543–562.

    Article  CAS  PubMed  Google Scholar 

  • Saibo, N. J. M., Lourenço, T., & Oliveira, M. M. (2009). Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Annals of Botany, 103, 609–623.

    Article  CAS  PubMed  Google Scholar 

  • Salvagiotti, F., Cassman, K. G., Specht, J. E., Walter, D. T., Weiss, A., & Dobermann, A. (2008). Nitrogen uptake, fixation and response to fertilizer N in soybeans: A review. Field Crops Research., 108, 1–13.

    Article  Google Scholar 

  • Salvucci, M. E., DeRidder, B. P., & Portis, A. R. (2006). Effect of activase level and isoform on the thermotolerance of photosynthesis in Arabidopsis. Journal of Experimental Botany., 57, 3793–3799.

    Article  CAS  PubMed  Google Scholar 

  • Schar, C., Vidale, P. L., Lüthi, D., Frei, C., Haberli, C., Liniger, M. A., & Appenzeller, C. (2004). The role of increasing temperature variability in European summer heatwaves. Nature, 427, 332–336.

    Article  PubMed  Google Scholar 

  • Schauberger, B., Rolinski, S., Schaphof, S., & Müller, C. (2019). Global historical soybean and wheat yield loss estimates from ozone pollution considering water and temperature as modifying efects. Agriculture and Forest Meteorology., 265, 1–15.

    Article  Google Scholar 

  • Sehgal, A., Sita, K., Kumar, J., Kumar, S., Singh, S., Siddique, K. H. M., & Nayyar, H. (2017). Effects of drought, heat and their interaction on the growth, yield and photosynthetic function of lentil (Lens culinaris Medikus) genotypes varying in heat and drought sensitivity. Frontier in Plant Science., 8, 1776.

    Article  Google Scholar 

  • Senthil-Kumar, M., Kumar, G., Srikanthbabu, V., & Udayakumar, M. (2007). Assessment of variability in acquired thermotolerance: Potential option to study genotypic response and the relevance of stress genes. Journal of Plant Physiology., 164, 111–125.

    Article  CAS  PubMed  Google Scholar 

  • Shah, N. H., & Paulsen, G. M. (2003). Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant and Soil, 257, 219–226.

    Article  CAS  Google Scholar 

  • Sinha, R., Zandalinas, S. I., Fichman, Y., Sen, S., Zeng, S., Gómez- Cadenas, A., Joshi, T., Fritschi, F. B., & Mittler, R. (2022). Differential regulation of flower transpiration during abiotic stress in annual plants. New Phytologist, 235, 611–629.

    Article  CAS  PubMed  Google Scholar 

  • Soba, D., Zhou, B., Arrese-Igor, C., Munn’e-Bosch, S., & Aranjuelo, I. (2019). Physiological, hormonal and metabolic responses of two alfalfa cultivars with contrasting responses to drought. International Journal of Molecular Science., 20, 5099.

    Article  CAS  Google Scholar 

  • Strasser, R. J., Tsimilli-Michael, M., & Srivastava, A. (2004). Analysis of the chlorophyll fluorescence transient. In G. C. Papageorgiou & R. Govindjee (Eds.), Chlorophyll Fluorescence: A Signature of Photosynthesis, Advances in Photosynthesis and Respiration (Vol. 19, pp. 321–362). Springer.

    Chapter  Google Scholar 

  • Tacarindua, C. R. P., Shiraiwa, T., Homma, K., Kumagai, E., & Sameshima, R. (2012). The response of soybean seed growth characteristics to increased temperature under near-field conditions in a temperature gradient chamber. Field Crop Research., 131, 26–31.

    Article  Google Scholar 

  • Tacarindua, C. R. P., Shiraiwa, T., Homma, K., Kumagai, E., & Sameshima, R. (2013). The effects of increased temperature on crop growth and yield of soybean grown in a temperature gradient chamber. Field Crop Research., 131, 74–81.

    Article  Google Scholar 

  • Taub, D. R., Seemann, J. R., & Coleman, J. S. (2000). Growth in elevated CO2 protects photosynthesis against high-temperature damage. Plant Cell and Environment, 23, 649–656.

    Article  CAS  Google Scholar 

  • Todd, C. D., Tipton, P. A., Blevins, D. G., Piedras, P., Pineda, M., & Polacco, J. C. (2006). Update on ureide degradation in legumes. Journal of Experimental Botany., 57, 5–12.

    Article  CAS  PubMed  Google Scholar 

  • Troll, W., & Cannan, R. K. (1953). A modified photometric ninhydrin method for the analysis of amino and imino acids. Journal of Biology Chemistry., 200, 803–811.

    Article  CAS  Google Scholar 

  • Tsikou, D., Kalloniati, C., Fotelli, M. N., Nikolopoulos, D., Katinakis, P., Udvardi, M. K., Rennenberg, H., & Flemetakis, E. (2013). Cessation of photosynthesis in Lotus japonicus leaves leads to reprogramming of nodule metabolism. Journal of Experimental Botany., 64, 1317–1332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udvardi, M., & Poole, P. S. (2013). Transport and metabolism in legume-rhizobia symbioses. Annual Review of Plant Biology, 64, 781–805.

    Article  CAS  PubMed  Google Scholar 

  • Vance, C. P. (2008). Carbon and nitrogen metabolism in legume nodules. Nitrogen-Fixing Legum Symbiosis, 23, 293–320.

    Article  Google Scholar 

  • Vautard, R., Yiou, P., Andrea, F. D., de Noblet, N., Viovy, N., Cassou, C., Polcher, J., Ciais, P., Kageyama, M., & Fan, Y. (2007). Summertime European heat and drought waves induced by wintertime Mediterranean rainfall deficit. Geophysical Research Letter., 34, 549965.

    Article  Google Scholar 

  • Vital, R. G., Müller, C., Freire, F. B. S., Silva, F. B., Batista, P. F., Fuentes, D., Rodrigues, A. A., Moura, L. M. F., Daloso, D. M., Silva, A. A., Merchant, A., & Costa, A. C. (2022). Metabolic, physiological and anatomical responses of soybean plants under water deficit and high temperature condition. Scientific Report., 12, 16467.

    Article  CAS  Google Scholar 

  • Wahid, A., Gelani, S., Ashraf, M., & Foolad, M. R. (2007). Heat tolerance in plants: An overview. Environmental and Experimental Botany., 61, 199–223.

    Article  Google Scholar 

  • Wei, W., Liang, D. W., Bian, X. H., Shen, M., Xiao, J. H., Zhang, W. K., et al. (2019). GmWRKY54 improves drought tolerance through activating genes in abscisic acid and Ca2+ signaling pathways in transgenic soybean. Plant Journal, 100, 384–398.

    Article  CAS  Google Scholar 

  • Wellburn, A. R., & Lichtenthaler, H. (1984). Advances in photosynthesis Research. Sybesma Martinus Nijhoff Co, the Hague, 2, 9–12.

    CAS  Google Scholar 

  • Whittington, H. R., Deede, L., & Powers, J. S. (2012). Growth responses, biomass partitioning, and nitrogen isotopes of prairie legumes in response to elevated temperature and varying nitrogen source in a growth chamber experiment. American Journal of Botany., 99, 838–846.

    Article  PubMed  Google Scholar 

  • Yamori, W., Hikosaka, K., & Way, D. A. (2014). Temperature response of photosynthesis in C3, C4, and CAM plants: Temperature acclimation and temperature adaptation. Photosynthesis Research, 119, 101–117.

    Article  CAS  PubMed  Google Scholar 

  • Yamori, W., Noguchi, K., Hikosaka, K., & Terashima, I. (2009). Cold tolerant crop species have greater temperature homeostasis of leaf respiration and photosynthesis than cold sensitive species. Plant Cell and Physiology, 50, 203–215.

    Article  CAS  Google Scholar 

  • Yordanov, I., Velikova, V., & Tsonev, T. (2000). Plant responses to drought, acclimation and stress tolerance. Photosynthetica, 38, 171–186.

    Article  CAS  Google Scholar 

  • Young, E. G., & Conway, C. F. (1942). On the estimation of allantoin by the Rimini– Schryver reaction. Journal of Biology and Chemistry., 142, 839–853.

    Article  CAS  Google Scholar 

  • Zandalinas, S. I., Rivero, R. M., Martínez, V., Gómez-Cadenas, A., & Arbona, V. (2016). Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biology, 16, 1–6.

    Article  Google Scholar 

  • Zhang, R., & Sharkey, T. D. (2009). Photosynthetic electron transport and proton flux under moderate heat stress. Photosynthesis Research, 100, 29–43.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge funding for this work from Indian Council of Agricultural Research. Kanchan Jumrani would like to acknowledge the Council of Scientific and Industrial Research (CSIR)/University Grants commission (UGC), Government of India (20–06/2010 (i) EU-IV) for providing the financial support in the form of Research Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kanchan Jumrani.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jumrani, K., Bhatia, V.S., Kataria, S. et al. The interactive effect of high temperature and water deficit stress on nitrogen fixation, photosynthesis, chlorophyll fluorescence, seed yield and quality in soybean (Glycine max). Plant Physiol. Rep. 29, 125–140 (2024). https://doi.org/10.1007/s40502-023-00763-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40502-023-00763-3

Keywords

Navigation