Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-25T00:39:03.272Z Has data issue: false hasContentIssue false

Phytohormone dynamics impact fatty acid and oil accumulation during soybean seed maturation

Published online by Cambridge University Press:  09 November 2021

Thien Q. Nguyen*
Affiliation:
Department of Biology, Trent University, 1600 West Bank Drive, Peterborough, Ontario, Canada K9L 0G2 Department of Chemistry, Trent University, 1600 West Bank Drive, Peterborough, Ontario, Canada K9L 0G2
Anna B. Kisiala
Affiliation:
Department of Biology, Trent University, 1600 West Bank Drive, Peterborough, Ontario, Canada K9L 0G2
Nguyen Ngoc Hai
Affiliation:
Environmental & Life Sciences Graduate Program, Trent University, Peterborough, Ontario, Canada K9L 0G2
Suresh Narine
Affiliation:
Department of Chemistry, Trent University, 1600 West Bank Drive, Peterborough, Ontario, Canada K9L 0G2
R. J. Neil Emery
Affiliation:
Department of Biology, Trent University, 1600 West Bank Drive, Peterborough, Ontario, Canada K9L 0G2
*
Author for Correspondence: Thien Q. Nguyen, E-mail: thiennguyenquoc@trentu.ca

Abstract

Fatty acid (FA) levels and profiles are vital for soybean oil quality, while cytokinins (CKs) and abscisic acid (ABA) are potent regulators of plant growth and development. Previous research suggested associations between FA biosynthesis and hormonal signalling networks; however, hormonal regulation of FA accumulation during soybean (Glycine max) seed maturation has never been measured. We analysed hormone and FA profiles obtained from HPLC-(ESI)-MS/MS and GC-FID screening during soybean seed maturation. A multilayered data processing approach, involving heat-maps, principal component analysis (PCA), correlation and multiregression models, suggested a strong relationship between hormone metabolism and FA/oil accumulation during seed maturation. Most strikingly, positive correlations were found between the levels of CK ribosides [transZeatin riboside (tZR), N6-isopentenyladenosine (iPR)] at the early stages of SM (R5-R6) and C18:0, C18:2 and oil content at the R8 stage. Moreover, multiple regression models revealed functional linkages between several CK derivatives and FA and oil content in mature seeds. To further test the significance of hormone regulation in FA metabolism, plants of two soybean accessions with contrasting hormone and FA profiles were sprayed with exogenous ABA and transZeatin (tZ) during the seed-filling period (R5-R6). Depending on the hormone type and concentration, these treatments distinctly modified biosynthesis of all tested FAs, except for C18:0. Most remarkably, tZ (50 nM) promoted production of C16:0, C18:1, C18:2, C18:3, and oil accumulation in maturing seeds. Overall, the results indicate impactful roles for ABA and CKs in FA accumulation during SM and represent a further step towards understanding FA biosynthesis, and potential improvements of soybean oil profiles.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ashikari, M, Sakakibara, H, Lin, S, Yamamoto, T, Takashi, T, Nishimura, A, Angeles, ER, Qian, Q, Kitano, H and Matsuoka, M (2005) Cytokinin oxidase regulates rice grain production. Science 309, 741745.CrossRefGoogle ScholarPubMed
Attree, SM, Pomeroy, MK and Fowke, LC (1992) Manipulation of conditions for the culture of somatic embryos of white spruce for improved triacylglycerol biosynthesis and desiccation tolerance. Planta 187, 395404.CrossRefGoogle ScholarPubMed
Audran, C, Borel, C, Frey, A, Sotta, B, Meyer, C, Simonneau, T and Marion-Poll, A (1998) Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiology 118, 10211028.CrossRefGoogle ScholarPubMed
Bartrina, I, Otto, E, Strnad, M, Werner, T and Schmülling, T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. The Plant Cell Online 23, 6980. https://doi.org/10.1105/tpc.110.079079.CrossRefGoogle ScholarPubMed
Brocard-Gifford, IM, Lynch, TJ and Finkelstein, RR (2003) Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiology 131, 7892. https://doi.org/10.1104/pp.011916.CrossRefGoogle ScholarPubMed
Dang, DH, Tessier, E, Lenoble, V, Durrieu, G, Omanović, D, Mullot, J-U, Pfeifer, H-R, Mounier, S and Garnier, C (2014) Key parameters controlling arsenic dynamics in coastal sediments: an analytical and modeling approach. Marine Chemistry 161, 3446.CrossRefGoogle Scholar
Davies, HV and Chapman, JM (1984) The influence of benzyladenine on phospholipid metabolism in seeds of Cucumis sativus L. Annals of Botany 53, 6572.Google Scholar
Décima Oneto, C, Otegui, ME, Baroli, I, Beznec, A, Faccio, P, Bossio, E, Blumwald, E and Lewi, D (2016) Water deficit stress tolerance in maize conferred by expression of an isopentenyltransferase (IPT) gene driven by a stress- and maturation-induced promoter. Journal of Biotechnology 220, 6677. https://doi.org/10.1016/J.JBIOTEC.2016.01.014.CrossRefGoogle ScholarPubMed
Dornbos, DL and McDonald, MB (1986) Mass and composition of developing soybean seeds at five reproductive growth stages. Crop Science 26, 624630.Google Scholar
Dornbos, DL and Mullen, RE (1992) Soybean seed protein and oil contents and fatty acid composition adjustments by drought and temperature. Journal of the American Oil Chemists Society 69, 228231.CrossRefGoogle Scholar
Dunne, A and Maple-Grødem, J (2014) Modifying fatty acid profiles through a new cytokinin-based plastid transformation system. The Plant Journal 80, 11311138.CrossRefGoogle ScholarPubMed
Emery, RJN, Ma, Q and Atkins, CA (2000) The forms and sources of cytokinins in developing white lupine seeds and fruits. Plant Physiology 123, 15931604. https://doi.org/10.1104/pp.123.4.1593.CrossRefGoogle ScholarPubMed
Emery, RJN, Atkins, C and Basra, AS (2006) Cytokinins and seed development, pp. 6393 in Basra, AS (Ed) Handbook of seed science and technology. Binghamton, NY: Haworth Press.Google Scholar
Farrow, SC and Emery, RJN (2012) Concurrent profiling of indole-3-acetic acid, abscisic acid, and cytokinins and structurally related purines by high-performance-liquid-chromatography tandem electrospray mass spectrometry. Plant Methods 8, 118.CrossRefGoogle ScholarPubMed
Fehr, W and Caviness, C (1977) Stages of soybean development, pp. 3–11. Special Report 80. Agriculture and Home Economics Experiment Station, Iowa State University.Google Scholar
Fehr, W, Caviness, C, Burmood, D and Pennington, J (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Science 11, 929931.Google Scholar
Finkelstein, RR (2010) The role of hormones during seed development and germination, pp. 549573 in Davies, PJ (Ed) Plant hormones. Dordrecht: Springer.Google Scholar
Finkelstein, R and Somerville, C (1989) Abscisic acid or high osmoticum promote accumulation of long-chain fatty acids in developing embryos of Brassica napus. Plant Science 61, 213217.CrossRefGoogle Scholar
Frébort, I, Kowalska, M, Hluska, TT, Frébortová, J and Galuszka, P (2011) Evolution of cytokinin biosynthesis and degradation. Journal of Experimental Botany 62, 24312452.CrossRefGoogle ScholarPubMed
Frey, A, Godin, B, Bonnet, M, Sotta, B and Marion-Poll, A (2004) Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia. Planta 218, 958964. https://doi.org/10.1007/s00425-003-1180-7.CrossRefGoogle ScholarPubMed
Gibson, SI (2004) Sugar and phytohormone response pathways: navigating a signalling network. Journal of Experimental Botany 55, 253264. https://doi.org/10.1093/jxb/erh048.CrossRefGoogle ScholarPubMed
Goodstein, DM, Shu, S, Howson, R, Neupane, R, Hayes, RD, Fazo, J, Mitros, T, Dirks, W, Hellsten, U, Putnam, N and Rokhsar, DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178D1186. https://doi.org/10.1093/nar/gkr944.Google ScholarPubMed
Graef, G, LaVallee, BJ, Tenopir, P, Tat, M, Schweiger, B, Kinney, AJ, Van Gerpen, JH and Clemente, TE (2009) A high-oleic-acid and low-palmitic-acid soybean: agronomic performance and evaluation as a feedstock for biodiesel. Plant Biotechnology Journal 7, 411421.Google ScholarPubMed
Hirose, N and Takei, K (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. Journal of Experimental Botany 59, 7583.CrossRefGoogle ScholarPubMed
Holbrook, LA, Magus, JR and Taylor, DC (1992) Abscisic acid induction of elongase activity, biosynthesis and accumulation of very long chain monounsaturated fatty acids and oil body proteins in microspore-derived embryos of Brassica napus L. cv Reston. Plant Science 84, 99115.CrossRefGoogle Scholar
Ivosev, G, Burton, L and Bonner, R (2008) Dimensionality reduction and visualization in principal component analysis. Analytical Chemistry 80, 49334944.CrossRefGoogle ScholarPubMed
Jameson, PE and Song, J (2016) Cytokinin: a key driver of seed yield. Journal of Experimental Botany 67, 593606. https://doi.org/10.1093/jxb/erv461.CrossRefGoogle ScholarPubMed
Janeczko, A, Hura, K, Skoczowski, A, Idzik, I, Biesaga-Kościelniak, J and Niemczyk, E (2008) Temperature-dependent impact of 24-epibrassinolide on the fatty acid composition and sugar content in winter oilseed rape callus. Acta Physiologiae Plantarum 31, 7179. https://doi.org/10.1007/s11738-008-0202-2.Google Scholar
Ji, X, Dong, B, Shiran, B, Talbot, MJ, Edlington, JE, Hughes, T, White, RG, Gubler, F and Dolferus, R (2011) Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiology 156, 647662. https://doi.org/10.1104/pp.111.176164.CrossRefGoogle ScholarPubMed
Jo, L, Pelletier, JM, Hsu, S-W, Baden, R, Goldberg, RB and Harada, JJ (2020) Combinatorial interactions of the LEC1 transcription factor specify diverse developmental programs during soybean seed development. Proceedings of the National Academy of Sciences of the United States of America 117, 12231232. https://doi.org/10.1073/PNAS.1918441117.CrossRefGoogle ScholarPubMed
Jokić, S, Sudar, R, Svilović, S, Vidović, S, Bilić, M, Velić, D and Jurković, V (2013) Fatty acid composition of oil obtained from soybeans by extraction with supercritical carbon dioxide. Czech Journal of Food Sciences 31, 116125.CrossRefGoogle Scholar
Jones, RJ and Brenner, ML (1987) Distribution of abscisic acid in maize kernel during grain filling. Plant Physiology 83, 905909.CrossRefGoogle ScholarPubMed
Kambhampati, S, Kurepin, L, Kisiala, A, Bruce, K, Cober, E, Morrison, M and Emery, RJN (2017) Yield associated traits correlate with cytokinin profiles in developing pods and seeds of field-grown soybean cultivars. Field Crops Research 214, 175184. https://doi.org/10.1016/j.fcr.2017.09.009.Google Scholar
Kant, S, Burch, D, Badenhorst, P, Palanisamy, R, Mason, J and Spangenberg, G (2015) Regulated expression of a cytokinin biosynthesis gene IPT delays leaf senescence and improves yield under rainfed and irrigated conditions in canola (Brassica napus L.). PLoS One 10, e0116349. https://doi.org/10.1371/journal.pone.0116349.Google ScholarPubMed
Kull, U and Büxenstein, R (1974) Effect of cytokinins on the lipid fatty acids of leaves. Phytochemistry 13, 3944.CrossRefGoogle Scholar
Kull, U, Kühn, B, Schweizer, J and Weiser, H (1978) Short-term effects of cytokinins on the lipid fatty acids of green leaves. Plant and Cell Physiology 19, 801810.Google Scholar
Kuppu, S, Mishra, N, Hu, R, Sun, L, Zhu, X, Shen, G, Blumwald, E, Payton, P and Zhang, H (2013) Water-deficit inducible expression of a cytokinin biosynthetic gene IPT improves drought tolerance in cotton. PLoS One 8, e64190. https://doi.org/10.1371/journal.pone.0064190.CrossRefGoogle ScholarPubMed
Kushiro, T, Okamoto, M, Nakabayashi, K, Yamagishi, K, Kitamura, S, Asami, T, Hirai, N, Koshiba, T, Kamiya, Y and Nambara, E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. The EMBO Journal 23, 16471656.CrossRefGoogle ScholarPubMed
Le, DT, Nishiyama, R, Watanabe, Y, Vankova, R, Tanaka, M, Seki, M, Yamaguchi-Shinozaki, K, Shinozaki, K and Tran, L-SP (2012) Identification and expression analysis of cytokinin metabolic genes in soybean under normal and drought conditions in relation to cytokinin levels. PLoS One 7, e42411.CrossRefGoogle ScholarPubMed
Li-Beisson, Y, Shorrosh, B, Beisson, F, Andersson, MX, Arondel, V, Bates, PD, Baud, S, Bird, D, Debono, A, Durrett, TP, Franke, RB, Graham, IA, Katayama, K, Kelly, AA, Larson, T, Markham, JE, Miquel, M, Molina, I, Nishida, I, Rowland, O, Samuels, L, Schmid, KM, Wada, H, Welti, R, Xu, C, Zallot, R and Ohlrogge, J (2013) Acyl-lipid metabolism. The Arabidopsis book / American Society of Plant Biologists 11, e0161.Google ScholarPubMed
Liu, B, Liu, X, Wang, C, Jin, J and Herbert, SJ (2010) Endogenous hormones in seed, leaf, and pod wall and their relationship to seed filling in soybeans. Crop and Pasture Science 61, 103.CrossRefGoogle Scholar
Liu, B, Liu, X, Li, Y-S and Herbert, SJ (2013) Effects of enhanced UV-B radiation on seed growth characteristics and yield components in soybean. Field Crops Research 154, 158163.CrossRefGoogle Scholar
Liu, H, Li, H, Gu, J, Deng, L, Ren, L, Hong, Y, Lu, Q, Chen, X, Liang, X, Liu, H, Li, H, Gu, J, Deng, L, Ren, L, Hong, Y, Lu, Q, Chen, X and Liang, X (2018) Identification of the candidate proteins related to oleic acid accumulation during peanut (Arachis hypogaea L.) seed development through comparative proteome analysis. International Journal of Molecular Sciences 19, 1235. https://doi.org/10.3390/ijms19041235.CrossRefGoogle ScholarPubMed
Morris, D. (1996) Hormonal regulation of source-sink relationships: an overview of potential control mechanisms, pp. 441465 in Zamski, E. and Schaffer Arthur, A. (Eds.) Photoassimilate distribution plants and crops source-sink relationships. New York, CRC Press.Google Scholar
Moustakime, Y, Hazzoumi, Z and Amrani Joutei, K (2017) Effect of the exogenous application of abscisic acid (ABA) at fruit set and at veraison on cell ripeness of olives Olea europaea L. and the extractability of phenolic compounds in virgin olive oil. Chemical and Biological Technologies in Agriculture 4, 23. https://doi.org/10.1186/s40538-017-0104-x.CrossRefGoogle Scholar
Nambara, E and Marion-Poll, A (2003) ABA action and interactions in seeds. Trends in Plant Science 8, 213217.CrossRefGoogle ScholarPubMed
Nambara, E and Marion-Poll, A (2005) Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165185.CrossRefGoogle ScholarPubMed
Narine, SS, Yue, J and Kong, X (2007) Production of polyols from canola oil and their chemical identification and physical properties. Journal of the American Oil Chemists’ Society 84, 173179.Google Scholar
Nguyen, Q, Kisiala, A, Andreas, P, Emery, RJN and Narine, S (2016) Soybean seed development: fatty acid and phytohormone metabolism and their interactions. Current Genomics 17, 241260.CrossRefGoogle ScholarPubMed
Ohlrogge, JB and Kuo, T-M (1984) Control of lipid synthesis during soybean seed development: enzymic and immunochemical assay of acyl carrier protein. Plant Physiology 74, 622625.CrossRefGoogle ScholarPubMed
Ohlrogge, J, Thrower, N, Mhaske, V, Stymne, S, Baxter, M, Yang, W, Liu, J, Shaw, K, Shorrosh, B, Zhang, M, Wilkerson, C and Matthäus, B (2018) PlantFAdb: a resource for exploring hundreds of plant fatty acid structures synthesized by thousands of plants and their phylogenetic relationships. The Plant Journal 96, 12991308. https://doi.org/10.1111/tpj.14102.Google ScholarPubMed
Park, W-K, Yoo, G, Moon, M, Kim, CW, Choi, Y-E and Yang, J-W (2013) Phytohormone supplementation significantly increases growth of Chlamydomonas reinhardtii cultivated for biodiesel production. Applied Biochemistry and Biotechnology 171, 11281142.CrossRefGoogle ScholarPubMed
Pham, A-T, Lee, J-D, Shannon, JG and Bilyeu, KD (2010) Mutant alleles of FAD2-1A and FAD2-1B combine to produce soybeans with the high oleic acid seed oil trait. BMC Plant Biology 10, 195.CrossRefGoogle ScholarPubMed
Pham, A-T, Lee, J-D, Shannon, JG and Bilyeu, KD (2011) A novel FAD2-1 a allele in a soybean plant introduction offers an alternate means to produce soybean seed oil with 85% oleic acid content. TAG. Theoretical and Applied Genetics. Theoretische und Angewandte Genetik 123, 793802. https://doi.org/10.1007/s00122-011-1627-3.CrossRefGoogle Scholar
Qin, H, Gu, Q, Zhang, J, Sun, LL, Kuppu, S, Zhang, Y, Burow, M, Payton, P, Blumwald, E and Zhang, H (2011) Regulated expression of an isopentenyltransferase gene (IPT) in peanut significantly improves drought tolerance and increases yield under field conditions. Plant & Cell Physiology 52, 19041914. https://doi.org/10.1093/pcp/pcr125.CrossRefGoogle ScholarPubMed
Refaat, AA (2009) Correlation between the chemical structure of biodiesel and its physical properties. International Journal of Environmental Science & Technology 6, 677694.Google Scholar
Reske, J, Siebrecht, J and Hazebroek, J (1997) Triacylglycerol composition and structure in genetically modified sunflower and soybean oils. Journal of the American Oil Chemists’ Society 74, 989998.CrossRefGoogle Scholar
Ross, JHE and Murphy, DJ (1993) Differential accumulation of oleosins, starch, storage proteins and triacylglycerols in embryos and cell cultures of Daucus carota L. Plant Science 88, 111.CrossRefGoogle Scholar
Rubel, A, Rinne, RW and Canvin, DT (1972) Protein, oil, and fatty acid in developing soybean seeds. Crop Science 12, 739741.Google Scholar
Sakakibara, H (2006) Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57, 431449. https://doi.org/10.1146/annurev.arplant.57.032905.105231.CrossRefGoogle ScholarPubMed
Schaller, GE, Bishopp, A and Kieber, JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. The Plant Cell 27, 4463. https://doi.org/10.1105/tpc.114.133595.CrossRefGoogle ScholarPubMed
Spíchal, L (2012) Cytokinins - recent news and views of evolutionally old molecules. Functional Plant Biology 39, 267.CrossRefGoogle Scholar
Stearns, EM and Morton, WT (1975) Effects of growth regulators on fatty acids of soybean suspension cultures. Phytochemistry 14, 619622.Google Scholar
Vishwakarma, K, Upadhyay, N, Kumar, N, Yadav, G, Singh, J, Mishra, RK, Kumar, V, Verma, R, Upadhyay, RG, Pandey, M and Sharma, S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Frontiers in Plant Science 8. https://doi.org/10.3389/fpls.2017.00161.CrossRefGoogle ScholarPubMed
Wang, ML, Chen, CY, Tonnis, B, Pinnow, D, Davis, J, An, Y-QC and Dang, P (2018) Changes of seed weight, fatty acid composition, and oil and protein contents from different peanut FAD2 genotypes at different seed developmental and maturation stages. Journal of Agricultural and Food Chemistry 66, 36583665. https://doi.org/10.1021/acs.jafc.8b01238.CrossRefGoogle ScholarPubMed
Wani, SH, Kumar, V, Shriram, V and Sah, SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. The Crop Journal 4, 162176. https://doi.org/10.1016/J.CJ.2016.01.010.CrossRefGoogle Scholar
Weber, H, Borisjuk, L and Wobus, U (2005) Molecular physiology of legume seed development. Annual Review of Plant Biology 56, 253279.CrossRefGoogle ScholarPubMed
Wilkinson, S and Davies, WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell & Environment 33, 510525.CrossRefGoogle ScholarPubMed
Yan, A and Chen, Z (2017) The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Reports 36, 689703. https://doi.org/10.1007/s00299-016-2082-z.CrossRefGoogle ScholarPubMed
Zhang, D, Zhao, M, Li, S, Sun, L, Wang, W, Cai, C, Dierking, EC and Ma, J (2017) Plasticity and innovation of regulatory mechanisms underlying seed oil content mediated by duplicated genes in the palaeopolyploid soybean. The Plant Journal 90, 11201133. https://doi.org/10.1111/tpj.13533.Google ScholarPubMed
Supplementary material: File

Nguyen et al. supplementary material

Nguyen et al. supplementary material

Download Nguyen et al. supplementary material(File)
File 118.6 KB