Effects of elevated air temperature coupling with soil drought on carbohydrate metabolism and oil synthesis during cottonseed development.
Journal
Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
revised:
18
10
2021
received:
05
09
2021
accepted:
31
01
2022
pubmed:
2
2
2022
medline:
26
2
2022
entrez:
1
2
2022
Statut:
ppublish
Résumé
Cotton, as the fifth-largest oilseed crop, often faces the coupling stress of heat and drought. Still, the effects of combined stress on cottonseed oil synthesis and its closely related carbon metabolism are poorly investigated. To this end, experiments were conducted with two cultivars (Sumian 15 and PHY370WR) under two temperature regimes: ambient temperature (AT) and elevated temperature (ET, which was 2.5°C-2.7°C higher than AT) and three water regimes: optimum soil moisture (soil relative water content [SRWC] at 75% ± 5%), and drought (SD) including SRWC 60% ± 5% and SRWC 45% ± 5%, during 2016-2018. Results showed that ET plus SD decreased cottonseed kernel yield, seed index, kernel weight, and kernel percentage more than either single stress. The content of hexoses, the carbon skeleton source for oil synthesis, was decreased by ET while increased by SD. The combined stress increased the hexose content by increasing the activities of sucrose synthase (SuSy, EC 2.4.1.13) and invertase (Inv, EC 3.2.1.26) and upregulating GhSuSy expression; however, hexose content under combined stress was lower than that under SD alone. Increased oil content under SD was attributed to the high phosphoenolpyruvate carboxylase (PEPCase, EC 4.1.1.31), acetyl-CoA carboxylase (ACCase, EC 6.4.1.2), and diacylglycerol acyltransferase (DGAT, EC 2.3.1.20) activities, whereas the opposite effects were seen under ET. Under combined stress, although ACCase activity decreased, PEPCase and DGAT activities, and GhPEPC-1 and GhDGAT-1 expression upregulated, enhancing carbon flow into oil metabolism and triacylglycerol synthesis, ultimately generating higher oil content.
Substances chimiques
Cottonseed Oil
0
Soil
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13643Subventions
Organisme : China Agriculture Research System of MOF and MARA
ID : CARS-15-14
Organisme : China Postdoctoral Science Foundation
ID : 2020M681633
Organisme : High-level Talent Introduction Program of Nanjing Agricultural University
Organisme : Jiangsu Collaborative Innovation Center for Modern Crop Production
ID : JCIC-MCP
Organisme : National Natural Science Foundation of China
ID : 31630051
Organisme : National Natural Science Foundation of China
ID : 31901463
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20190524
Informations de copyright
© 2022 Scandinavian Plant Physiology Society.
Références
Behal, R.H., Nikolau, B.J., Wurtele, E.S. & Oliver, D.J. (2000) The role of pyruvate dehydrogenase and acetyl-coenzyme synthetase in fatty acid synthesis in developing arabidopsis seeds. Plant Physiology and Biochemistry, 123, 497-508.
Braun, D.M., Wang, L. & Ruan, Y.L. (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. Journal of Experimental Botany, 65, 1713-1735.
Brown, P.T. & Caldeira, K. (2017) Greater future global warming inferred from Earth's recent energy budget. Nature, 552, 45-50.
Chen, J.Q., Lang, C.X., Hu, Z.H., Liu, Z.H. & Huang, R.Z. (1999) Antisense PEP gene regulates to ratio of protein and lipid content in Brassica napus seeds. Journal of Agricultural Science, 7, 316-320.
Dai, Y.J., Chen, B.L., Meng, Y.L., Zhao, W.Q., Zhou, Z.G., Oosterhuis, D.M. et al. (2015) Effects of elevated temperature on sucrose metabolism and cellulose synthesis in cotton fibre during secondary cell wall development. Functional Plant Biology, 42, 909-919.
Dowd, M., Wakelyn, P. & Chaudhry, R. (2010) Cottonseed current and future utilization. In: Wakelyn, P.J. & Chaudhry, M.R. (Eds.) Cotton: technology for the 21st century. Washington, DC: ICAC Press, pp. 437-460.
Du, Y.L., Zhao, Q., Chen, L.R., Yao, X.D., Zhang, H.J., Wu, J.J. et al. (2020) Effect of drought stress during soybean R2-R6 growth stages on sucrose metabolism in leaf and seed. International Journal of Molecular Sciences, 21, 618-636.
Egli, M.A., Gengenbach, B.G., Gronwald, J.W., Somers, D.A. & Wyse, D.L. (1993) Character ization of maize acety l coenzyme a car boxy lase. Plant Physiology, 101, 499-506.
FAO. (2020). Food and Agriculture Organization of the United Nations. Food and Agricultural Commodities Production. Available at: http://www.fao.org/statistics/en/. [Accessed 22, Dec 2020].
Farooq, M., Wahid, A., Kobayashi, N., Fujita, D. & Basra, S.M. (2009) Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development, 29, 185-212.
Gao, M., Snider, J.L., Bai, H., Hu, W., Wang, R., Meng, Y.L. et al. (2020) Drought effects on cotton (Gossypium hirsutum L.) fibre quality and fibre sucrose metabolism during the flowering and boll-formation period. Journal of Agronomy and Crop Science, 206, 309-321.
Gao, M., Xu, B.J., Wang, Y.H., Zhou, Z.G. & Hu, W. (2021) Quantifying individual and interactive effects of elevated temperature and drought stress on cotton yield and fibre quality. Journal of Agronomy and Crop Science, 207, 422-436.
Hendrix, D.L. (1990) Carbohydrates and carbohydrate enzymes in developing cotton ovules. Physiologia Plantarum, 78, 85-92.
Hendrix, D.L. (1993) Rapid extraction and analysis of nonstructural carbohydrates in plant tissues. Crop Science, 33, 1306-1311.
Hu, W., Cao, Y., Loka, D.A., Harris-Shultz, K.R., Reiter, R.J., Ali, S. et al. (2020a) Exogenous melatonin improves cotton (Gossypium hirsutum L.) pollen fertility under drought by regulating carbohydrate metabolism in male tissues. Plant Physiology and Biochemistry, 151, 579-588.
Hu, W., Dai, Y., Zhao, W., Meng, Y., Chen, B., Wang, Y. et al. (2017) Effects of long-term elevation of air temperature on sucrose metabolism in cotton leaves at different positions. Journal of Agronomy and Crop Science, 203, 539-552.
Hu, W., Dai, Z., Yang, J., Snider, J.L., Wang, S., Chen, B. et al. (2018) The variability of cottonseed yield under different potassium levels is associated with the changed oil metabolism in embryo. Field Crops Research, 224, 80-90.
Hu, W., Huang, Y., Bai, H., Liu, Y., Wang, S. & Zhou, Z. (2020b) Influence of drought stress on pistil physiology and reproductive success of two Gossypium hirsutum cultivars differing in drought tolerance. Physiologia Plantarum, 168, 909-920.
Hu, W., Ma, Y., Lv, F., Liu, J., Zhao, W., Chen, B. et al. (2016) Effects of late planting and shading on sucrose metabolism in cotton fiber. Environmental and Experimental Botany, 131, 164-172.
Ichihara, K., Murota, N. & Fujii, S. (1990) Intracellular translocation of phosphatidate phosphatase in maturing safflower seeds: a possible mechanism of feedforward control of triacylglycerol synthesis by fatty acids. Biochimica et Biophysica Acta, 1043, 227-234.
IPCC. (2014) Climate change 2014: synthesis report. In: Core Writing Team, Pachauri, R.K. & Meyer, L.A. (Eds.) Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. Geneva, Switzerland: IPCC.
Jako, C., Kumar, A., Wei, Y., Zou, J., Barton, D.L., Giblin, E.M. et al. (2001) Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiology, 126, 861-874.
Janette, O., Doug, B., Ron, C., Maureen, D., Hawkins, D.J., Hui, X. et al. (2011) Expression of fungal diacylglycerol acyltransferase2 genes to increase kernel oil in maize. Plant Physiology, 155, 1146-1157.
Juroszek, P., Racca, P., Link, S., Farhumand, J. & Kleinhenz, B. (2020) Overview on the review articles published during the past 30 years relating to the potential climate change effects on plant pathogens and crop disease risks. Plant Pathology, 69, 179-193.
Leclere, S., Schmelz, E.A. & Chourey, P.S. (2010) Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiology and Biochemistry, 153, 306-318.
Li, Z.L., Hua, S.J., Zhang, D.Q., Yu, H.S., Zhang, Y.F., Lin, B.G. et al. (2016) Comparison on the carbohydrate metabolic enzyme activities and their gene expression patterns in canola differing seed oil content. Plant Growth Regulation, 78, 357-369.
Liu, Q., Llewellyn, D., Singh, S. & Green, A. (2012) Cotton seed development: opportunities to add value to a byproduct of fibre production. In: Oosterhuis, D. & Cothren, T. (Eds.) Cotton flowering and fruiting. Cordova, TN: The Cotton Foundation, pp. 353-382.
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 − δδ ct method. Methods in Cell Science, 25, 402-408.
Loka, D.A., Oosterhuis, D.M., Baxevanos, D., Noulas, C. & Hu, W. (2020) Single and combined effects of heat and water stress and recovery on cotton (Gossypium hirsutum L.) leaf physiology and sucrose metabolism. Plant Physiology and Biochemistry, 148, 166-179.
Lung, S.C. & Weselake, R.J. (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids, 41, 1073-1088.
Naik, S.N., Goud, V.V., Rout, P.K. & Dalai, A.K. (2010) Production of first and second generation biofuels: a comprehensive review. Renewable and Sustainable Energy Reviews, 14, 578-597.
OECD/FAO. (2020) OECD-FAO Agricultural Outlook 2020-2029. Paris/FAO, Rome: OECD Publishing.
Ohlrogge, J.B. & Browse, J.G. (1995) Lipid biosynthesis. Plant Cell, 7, 957-970.
Pourmeidani, A., Jafari, A.A. & Mirza, M. (2017) Studying drought tolerance in Thymus kotschyanus accessions for cultivation in dry land farming and low efficient grassland. Journal of Rangeland Science, 7(4), 331-340.
Razal, R.A., Daracan, V.C., Calapis, R.M., Angon, C.M.M. & Demafelis, R.B. (2012) Solvent extraction of oil from bani (Pongamia pinnata [L.] Pierre) seeds. Philippine Journal of Crop Science, 37, 1-7.
Roesler, K., Shen, B., Bermudez, E., Li, C.J., Hunt, J., Damude, H.G. et al. (2016) An improved variant of soybean type 1 diacylglycerol acyltransferase increases the oil content and decreases the soluble carbohydrate content of soybeans. Plant Physiology, 171, 878-893.
Ruan, Y.L., Jin, Y., Yang, Y.J., Li, G.J. & Boyer, J.S. (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Molecular Plant, 3, 942-955.
Salerno, G.L. & Curatti, L. (2003) Origin of sucrose metabolism in higher plants: when, how and why? Trends in Plant Science, 8, 63-69.
Sanchez, J. & Harwood, J.L. (2002) Biosynthesis of triacylglycerols and volatiles in olive. European Journal of Lipid Science and Technology, 104, 564-573.
Shu, H., Zhou, Z., Xu, N., Wang, Y. & Zheng, M. (2009) Sucrose metabolism in cotton (Gossypium hirsutum L.) fibre under low temperature during fibre development. European Journal of Agronomy, 31, 61-68.
Slabas, A.R. & Fawcett, T. (1992) The biochemistry and molecular biology of plant lipid biosynthesis. Plant Molecular Biology, 19, 169-191.
Snider, J.L. & Oosterhuis, D.M. (2015) Physiology. In: Fang, D. & Percy, R. (Eds.) Agronomy monograph 57, cotton, 2nd edition. Madison, WI: ASA-CSSA-SSSA, pp. 339-400.
Stitt, M. (2013) Progress in understanding and engineering primary plant metabolism. Curr. Opin. Biotechnol., 24, 229-238.
Tang, F.Y. & Xiao, W.J. (2013) Dry matter accumulation and partitioning in various fractions of cotton bolls. Experimental Agriculture, 49, 543-555.
Turchettozolet, A.C., Maraschin, F.D., De Morais, G.L., Cagliari, A., Andrade, C.M., Margispinheiro, M. et al. (2011) Evolutionary view of acyl-CoA diacylglycerol acyltransferase (DGAT), a key enzyme in neutral lipid biosynthesis. BMC Evolutionary Biology, 11, 263-263.
Turner, N.C. & Meyer, R. (2011) Synthesis of regional impacts and global agricultural adjustments. In: Yadav, S.S., Redden, R.J., Hatfield, J.L., Lotze-Campen, H. & Hall, A.E. (Eds.) Crop adaptation to climate change. Chichester, UK: Wiley-Blackwell, pp. 156-165.
Urban, O., Hlavacova, M., Klem, K., Novotna, K., Rapantova, B., Smutna, P. et al. (2018) Combined effects of drought and high temperature on photosynthetic characteristics in four winter wheat genotypes. Field Crops Research, 223, 137-149.
USDA-FAS. (2022) Oilseeds: world markets and trade. Available at: https://apps.fas.usda.gov/psdonline/circulars/oilseeds.pdf. [Accessed 22, Jan 2022].
Wang, H.M., Chen, Y.L., Hu, W., Wang, S.S., Snider, J.L. & Zhou, Z.G. (2017) Carbohydrate metabolism in the subtending leaf cross-acclimates to waterlogging and elevated temperature stress and influences boll biomass in cotton (Gossypium hirsutum). Physiologia Plantarum, 161, 339-354.
Wang, H.S., Vicente-Serrano, S.M., Tao, F.L., Zhang, X.D., Wang, P.X., Zhang, C. et al. (2016a) Monitoring winter wheat drought threat in northern China using multiple climate-based drought indices and soil moisture during 2000-2013. Agricultural and Forest Meteorology, 228-229, 1-12.
Wang, R., Ji, S., Zhang, P., Meng, Y.L., Wang, Y.H., Chen, B.L. et al. (2016b) Drought effects on cotton yield and fiber quality on different fruiting branches. Crop Science, 56, 1265-1276.
Weber, H., Borisjuk, L. & Wobus, U. (2005) Molecular physiology of legume seed development. Annual Review of Plant Biology, 56, 253-279.
Weselake, R.J., Shah, S., Tang, M., Quant, P.A., Snyder, C.L., Furukawastoffer, T.L. et al. (2008) Metabolic control analysis is helpful for informed genetic manipulation of oilseed rape (Brassica napus) to increase seed oil content. Journal of Experimental Botany, 59, 3543-3549.
White, J.A., Todd, J.F., Newman, T.C., Focks, N., Girke, T., de Ilarduya, O.M. et al. (2000) A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil. Plant Physiology, 124, 1582-1594.
Xu, B.J., Chen, Y.L., Wang, H.M., Zhao, W.Q. & Zhou, Z.G. (2021) Elevated temperature and waterlogging decrease cotton seed quality by altering the accumulation and distribution of carbohydrates, oil and protein. Physiologia Plantarum, 171, 108-124.
Xu, B.J., Gao, M., Hu, W., Zhao, W.Q., Wang, S.S. & Zhou, Z.G. (2022) Individual and interactive influences of elevated air temperature and soil drought at the flowering and boll-forming stage on cottonseed yield and nutritional quality. Crop Journal, 10, 128-139.
Xu, Z., Li, J., Guo, X., Jin, S. & Zhang, X. (2016) Metabolic engineering of cottonseed oil biosynthesis pathway via RNA interference. Science Report, 6, 33342-33355.
Yang, H.K., Zhang, X.Y., Chen, B.L., Meng, Y.L., Wang, Y.H., Zhao, W.Q. et al. (2017) Integrated management strategies increase cottonseed, oil and protein production: the key role of carbohydrate metabolism. Frontiers in Plant Science, 8, 48-66.
Yang, H.K., Zhang, X.Y., Chen, B.L., Meng, Y.L., Zhao, W.Q., Wang, Y.H. et al. (2018) Integrated soil-cotton system management enhances triacylglycerol yield and favourable fatty acid profile. Industrial Crops and Products, 117, 393-403.
Zhao, Y.P., Wang, Y.M., Huang, Y., Cui, Y.P. & Hua, J.P. (2018) Gene network of oil accumulation reveals expression profiles in developing embryos and fatty acid composition in upland cotton. Journal of Plant Physiology, 228, 101-112.
Zheng, P., Allen, W.B., Roesler, K., Williams, M.E., Zhang, S., Li, J. et al. (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nature Genetics, 40, 367-372.