Agar-based polyethylene glycol (PEG) infusion model for pea (Pisum sativum L.) — perspectives of translation to legume crop plants

Authors

  • Tatiana Leonova Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle, 06120, Germany; Department of Biochemistry, Faculty of Biology, Saint Petersburg State University, Srednij pr., 41–43, Saint Petersburg, 199004, Russian Federation https://orcid.org/0000-0002-7153-5059
  • Julia Shumilina Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle, 06120, Germany; Department of Biochemistry, Faculty of Biology, Saint Petersburg State University, Srednij pr., 41–43, Saint Petersburg, 199004, Russian Federation; Sirius University of Science and Technology, Olimpijskij pr., 1, Sochi, 354340, Russian Federation https://orcid.org/0000-0002-9747-5779
  • Ahyoung Kim Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle, 06120, Germany https://orcid.org/0000-0002-5199-993X
  • Nadezhda Frolova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-1895-1133
  • Ludger Wessjohann Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle, 06120, Germany
  • Tatiana Bilova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-6024-3667
  • Andrej Frolov Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle, 06120, Germany; Department of Biochemistry, Faculty of Biology, Saint Petersburg State University, Srednij pr., 41–43, Saint Petersburg, 199004, Russian Federation; Sirius University of Science and Technology, Olimpijskij pr., 1, Sochi, 354340, Russian Federation https://orcid.org/0000-0003-3250-5858

DOI:

https://doi.org/10.21638/spbu03.2022.309

Abstract

Due to the oncoming climate changes water deficit represents one of the most important abiotic stressors which dramatically affects crop productivity worldwide. Because of their importance as the principal source of food protein, legumes attract a special interest of plant scientists. Moreover, legumes are involved in symbiotic association with rhizobial bacteria, which is morphologically localized to root nodules. These structures are critical for fixation of atmospheric nitrogen and highly sensitive to drought. Therefore, new drought-tolerant legume cultivars need to be developed to meet the growing food demand. However, this requires a comprehensive knowledge of the molecular mechanisms behind the plant stress response. To access these mechanisms, adequate and reliable drought stress models need to be established. The agar-based polyethylene glycol (PEG) infusion model allows a physiologically relevant reduction of soil water potential (Ψw), although it is restricted to seedlings and does not give access to proteomics and metabolomics studies. Earlier, we successfully overcame this limitation and optimized this model for mature Arabidopsis plants. Here we make the next step forward and address its application to one of the major crop legumes — pea. Using a broad panel of physiological and biochemical markers, we comprehensively prove the applicability of this setup to legumes. The patterns of drought-related physiological changes are well-interpretable and generally resemble the stress response of plants grown in soil-based stop-watering models. Thus, the proposed model can be efficiently used in the study of stress-related metabolic adjustment in green parts, roots and root nodules of juvenile and flowering plants.

Keywords:

agar-based PEG infusion model, biochemical stress markers, drought, osmotic stress, oxidative stress, physiological stress markers, polyethylene glycol (PEG)

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References

Balcke, G. U., Handrick, V., Bergau, N., Fichtner, M., Henning, A., Stellmach, H., Tissier, A., Hause, B., and Frolov, A. 2012. An UPLC-MS/MS method for highly sensitive high-throughput analysis of phytohormones in plant tissues. Plant Methods 8:47. https://doi.org/10.1186/1746-4811-8-47

Bodner, G., Nakhforoosh, A., and Kaul, H.-P. 2015. Management of crop water under drought: a review. Agronomy for Sustainable Development 35:401–442. https://doi.org/10.1007/s13593-015-0283-4

Ceylan, H. A., Türkan, I., and Sekmen, A. H. 2013. Effect of coronatine on antioxidant enzyme response of chickpea roots to combination of PEG-induced osmotic stress and heat stress. Journal of Plant Growth Regulation 32:72–82. https://doi.org/10.1007/s00344-012-9277-5

Chen, T. and Fluhr, R. 2018. Singlet oxygen plays an essential role in the root’s response to osmotic stress. Plant Physiology 177:1717–1727. https://doi.org/10.1104/pp.18.00634

De Domenico, S., Bonsegna, S., Horres, R., Pastor, V., Taurino, M., Poltronieri, P., Imtiaz, M., Kahl, G., Flors, V., Winter, P., and Santino, A. 2012. Transcriptomic analysis of oxylipin biosynthesis genes and chemical profiling reveal an early induction of jasmonates in chickpea roots under drought stress. Plant Physiology and Biochemistry 61:115–122. https://doi.org/10.1016/j.plaphy.2012.09.009

Deikman, J., Petracek, M., and Heard, J. E. 2012. Drought tolerance through biotechnology: improving translation from the laboratory to farmers’ fields. Current Opinion in Biotechnology, Food biotechnology — Plant Biotechnology 23:243–250. https://doi.org/10.1016/j.copbio.2011.11.003

Dellagi, A., Quillere, I., and Hirel, B. 2020. Beneficial soil-borne bacteria and fungi: a promising way to improve plant nitrogen acquisition. Journal of Experimental Botany 71:4469–4479. https://doi.org/10.1093/jxb/eraa112

Fahad, S., Bajwa, A. A., Nazir, U., Anjum, S. A., Farooq, A., Zohaib, A., Sadia, S., Nasim, W., Adkins, S., Saud, S., Ihsan, M. Z., Alharby, H., Wu, C., Wang, D., and Huang, J. 2017. Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science 8:1147. https://doi.org/10.3389/fpls.2017.01147

Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., and Basra, S. M. A. 2009. Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development 29:185–212. https://doi.org/10.1051/agro:2008021

Frolov, A., Bilova, T., Paudel, G., Berger, R., Balcke, G. U., Birkemeyer, C., and Wessjohann, L. A. 2017. Early responses of mature Arabidopsis thaliana plants to reduced water potential in the agar-based polyethylene glycol infusion drought model. Journal of Plant Physiology 208:70–83. https://doi.org/10.1016/j.jplph.2016.09.013

Hohl, M. and Schopfer, P. 1991. Water relations of growing maize coleoptiles : comparison between mannitol and polyethylene glycol 6000 as external osmotica for adjusting turgor pressure. Plant Physiology 95:716–722. https://doi.org/10.1104/pp.95.3.716

Ji, H., Liu, L., Li, K., Xie, Q., Wang, Z., Zhao, X., and Li, X. 2014. PEG-mediated osmotic stress induces premature differentiation of the root apical meristem and outgrowth of lateral roots in wheat. Journal of Experimental Botany 65:4863–4872. https://doi.org/10.1093/jxb/eru255

Jiang, J., Su, M., Chen, Y., Gao, N., Jiao, C., Sun, Z., Li, F., and Wang, C. 2013. Correlation of drought resistance in grass pea (Lathyrus sativus) with reactive oxygen species scavenging and osmotic adjustment. Biologia 68:231–240. https://doi.org/10.2478/s11756-013-0003-y

Juzoń, K., Czyczyło-Mysza, I., Ostrowska, A., Marcińska, I., and Skrzypek, E. 2019. Chlorophyll fluorescence for prediction of yellow lupin (Lupinus luteus L.) and pea (Pisum sativum L.) susceptibility to drought. Photosynthetica 57:950–959. https://doi.org/10.32615/ps.2019.102

Khaleghi, A., Naderi, R., Brunetti, C., Maserti, B. E., Salami, S. A., and Babalar, M. 2019. Morphological, physiochemical and antioxidant responses of Maclura pomifera to drought stress. Scientific Reports 9:19250. https://doi.org/10.1038/s41598-019-55889-y

Khatun, M., Sarkar, S., Era, F.M., Islam, A. K. M. M., Anwar, Md. P., Fahad, S., Datta, R., and Islam, A. K. M. A. 2021. Drought stress in grain legumes: effects, tolerance mechanisms and management. Agronomy 11:2374. https://doi.org/10.3390/agronomy11122374

Kibido, T., Kunert, K., Makgopa, M., Greve, M., and Vorster, J. 2020. Improvement of rhizobium-soybean symbiosis and nitrogen fixation under drought. Food and Energy Security 9:e177. https://doi.org/10.1002/fes3.177

Lamaoui, M., Jemo, M., Datla, R., and Bekkaoui, F. 2018. Heat and drought stresses in crops and approaches for their mitigation. Frontiers in Chemistry 6:26. https://doi.org/10.3389/fchem.2018.00026

Larrainzar, E., Wienkoop, S., Scherling, C., Kempa, S., Ladrera, R., Arrese-Igor, C., Weckwerth, W., and González, 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. https://doi.org/10.1094/MPMI-22-12-1565

Leonova, T., Popova, V., Tsarev, A., Henning, C., Antonova, K., Rogovskaya, N., Vikhnina, M., Baldensperger, T., Soboleva, A., Dinastia, E., Dorn, M., Shiroglasova, O., Grishina, T., Balcke, G.U., Ihling, C., Smolikova, G., Medvedev, S., Zhukov, V. A., Babakov, V., Tikhonovich, I. A., Glomb, M. A., Bilova, T., and Frolov, A. 2020. Does protein glycation impact on the drought-related changes in metabolism and nutritional properties of mature pea (Pisum sativum L.) seeds? International Journal of Molecular Sciences 21:567. https://doi.org/10.3390/ijms21020567

Lesk, C., Rowhani, P., and Ramankutty, N. 2016. Influence of extreme weather disasters on global crop production. Nature 529:84–87. https://doi.org/10.1038/nature16467

Maphosa, Y. and Jideani, V. A. 2017. The role of legumes in human nutrition, in: Hueda, M. C. (Ed.), Functional Food — Improve Health through Adequate Food. InTech. https://doi.org/10.5772/intechopen.69127

Min, C. W., Gupta, R., Kim, S. W., Lee, S. E., Kim, Y. C., Bae, D. W., Han, W. Y., Lee, B. W., Ko, J. M., Agrawal, G. K., Rakwal, R., and Kim, S. T. 2015. Comparative biochemical and proteomic analyses of soybean seed cultivars differing in protein and oil content. Journal of Agricultural and Food Chemistry 63:7134–7142. https://doi.org/10.1021/acs.jafc.5b03196

Osmolovskaya, N., Shumilina, J., Kim, A., Didio, A., Grishina, T., Bilova, T., Keltsieva, O. A., Zhukov, V., Tikhonovich, I., Tarakhovskaya, E., Frolov, A., and Wessjohann, L. A. 2018. Methodology of drought stress research: experimental setup and physiological characterization. International Journal of Molecular Sciences 19:4089. https://doi.org/10.3390/ijms19124089

Paudel, G., Bilova, T., Schmidt, R., Greifenhagen, U., Berger, R., Tarakhovskaya, E., Stöckhardt, S., Balcke, G. U., Humbeck, K., Brandt, W., Sinz, A., Vogt, T., Birkemeyer, C., Wessjohann, L., and Frolov, A. 2016. Osmotic stress is accompanied by protein glycation in Arabidopsis thaliana. Journal of Experimental Botany 67:6283–6295. https://doi.org/10.1093/jxb/erw395

Riemann, M., Dhakarey, R., Hazman, M., Miro, B., Kohli, A., and Nick, P. 2015. Exploring jasmonates in the hormonal network of drought and salinity responses. Frontiers in Plant Science 6:1077. https://doi.org/10.3389/fpls.2015.01077

Shumilina, J., Gorbach, D., Popova, V., Tsarev, A., Kusnetsova, A., Grashina, M., Dorn, M., Lukasheva, E., Osmolovskaya, N., Romanovskaya, E., Zhukov, V. A., Ihling, C., Grishina, T., Bilova, T., Frolov, A. 2021. Protein glycation and drought response of pea (Pisum sativum L.) root nodule proteome: a proteomics approach. Biological Communications 66(3):210–224. https://doi.org/10.21638/spbu03.2021.303

Smolikova, G. 2014. Application of the method of accelerated aging to evaluate the stress tolerance of seeds. Vestnik of Saint Petersburg University. Series 3. Biology 2:82–93. (In Russian)

Sunaina, N. A. and Singh, N. B. 2016. PEG imposed water deficit and physiological alterations in hydroponic cabbage. Iranian Journal of Plant Physiology 6(2):1651–1658.

van der Weele, C. M., Spollen, W. G., Sharp, R. E., and Baskin, T. I. 2000. Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. Journal of Experimental Botany 51:1555–1562. https://doi.org/10.1093/jexbot/51.350.1555

Velikova, V., Yordanov, I., and Edreva, A. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Science 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1

Verslues, P. E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J., and Zhu, J.-K. 2006. Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal 45:523–539. https://doi.org/10.1111/j.1365-313X.2005.02593.x

Wan, J., Griffiths, R., Ying, J., McCourt, P., and Huang, Y. 2009. Development of drought-tolerant canola (Brassica napus L.) through genetic modulation of ABA-mediated stomatal responses. Crop Science 49:1539–1554. https://doi.org/10.2135/cropsci2008.09.0568

Wang, W.-B., Kim, Y.-H., Lee, H.-S., Kim, K.-Y., Deng, X.-P., and Kwak, S.-S. 2009. Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiology and Biochemistry 47:570–577. https://doi.org/10.1016/j.plaphy.2009.02.009

Wang, X., Cai, X., Xu, C., Wang, Q., and Dai, S. 2016. Drought-responsive mechanisms in plant leaves revealed by proteomics. International Journal of Molecular Sciences 17:E1706. https://doi.org/10.3390/ijms17101706

Yang, J., Isabel Ordiz, M., Jaworski, J. G., and Beachy, R. N. 2011. Induced accumulation of cuticular waxes enhances drought tolerance in Arabidopsis by changes in development of stomata. Plant Physiology and Biochemistry 49:1448–1455. https://doi.org/10.1016/j.plaphy.2011.09.006

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Published

2022-10-10

How to Cite

Leonova, T., Shumilina, J., Kim, A., Frolova, N., Wessjohann, L., Bilova, T., & Frolov, A. (2022). Agar-based polyethylene glycol (PEG) infusion model for pea (<em>Pisum sativum</em> L.) — perspectives of translation to legume crop plants. Biological Communications, 67(3), 236–244. https://doi.org/10.21638/spbu03.2022.309

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Vol. 67 No. 3 (2022)

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Brief communications

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Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.

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