Genetic variation in four maturity genes and photoperiod insensitivity effects on the yield components and on the growth duration periods of soybean
AbstractSoybean (Glycine max (L.) Merr.) is a typical short-day and thermophilic crop. Absence of or low sensitivity to photoperiod is necessary for short-day crops to adapt to high latitudes. Photoperiod insensitivity in soybeans is controlled by two genetic systems and involves three important maturity genes: E1, a repressor for two soybean orthologs of Arabidopsis FLOWERING LOCUS T, and E3 and E4, which are phytochrome A genes. The aim of this work was to investigate the role of four maturity genes (E1 through E4) on the yield components, seed quality and on phasic development of near isogenic by E genes lines of soybean: short-day (SD) lines with genotype e1E2E3E4e5E7, e1E2E3e4e5E7, E1e2e3E4e5E7 and photoperiodic insensitive (PPI) lines with genotype e1e2E3E4e5E7, e1e2e3E4e5E7 under a long photoperiod (the natural day length of 50 latitude) conditions and short day conditions. The results of the study showed that soybean development processes under conditions of different day lengths depend on the dominant/recessive state of the main maturity genes. In addition, the response to the photoperiod depends on certain combinations of genes. SD lines began flowering on average 16.9% later under the conditions of a natural long photoperiod. Dominant alleles of genes E1 and E3 extended the pre- and post-flowering phases under conditions of exposure to long and short photoperiods. The dominant allele of the E1 gene delayed the onset of flowering by an average of 26.9%, and the period of full maturity by 39.8% compared to the recessive e1. The dominant allele of the E3 gene, compared to the recessive e3, lengthened the transition to flowering by an average of 16.1%, and the period of full ripeness by 27.1%. The dominant allele of the E2 gene lengthened the duration of the vegetative phase by 20% under the conditions of a long photoperiod. No significant influence of the dominant E4 allele on the duration of the vegetative and generative phases of soybean development was found in our study. PPI lines begin flowering under the conditions of a long and short photoperiod at the same time, but the phases of flowering and full seed maturity in the line with genotype e1e2e3E4e5E7 occurred earlier, due to the loss of the photoperiod sensitivity of the E3 gene. PPI line with genotype e1e2e3E4e5E7 proved to be the most insensitive line to the effect of different photoperiod durations among the studied lines. It was shown that the dominant alleles of E1–E4 maturity genes reduced the parameters of seed weight per plant and the weight of 1000 seeds under the conditions of a natural long photoperiod in comparison with recessive alleles of these genes. The maximum weight of seeds per plant and the weight of 1000 seeds were recorded in the PPI line with genotype e1e2e3E4e5E7. It should be noted that the dominant alleles E1 and E3 increased yield under conditions of a short photoperiod. Maturity genes had different effects on the biochemical composition of seeds. It was shown that soybean lines with dominant E1, E2 and E4 genes showed a higher content of starch and a lower content of total nitrogen and oil in seeds under natural photoperiod conditions compared to lines with recessive alleles of these genes. The dominant E3 allele reduced the oil content and did not affect the starch and total nitrogen content of seeds under long day conditions compared to the recessive e3 allele. The analysis of the effect of photoperiod on the timing of phenophases, yield structure indicators and biochemical composition of seeds in soybean plants with different sensitivity to photoperiod showed that the PPI line with the genotype e1e2e3E4e5E7 was the most adapted to the natural conditions of 50 degrees latitude. The PPI line with the genotype e1e2e3E4e5E7 was characterized by the shortest phases of days from sowing to flowering and full maturity. As a result, this line had the shortest growing season without reducing the yield and seed quality. Clearly, photoperiod had strong effects on all stages of plant reproduction and often acted indirectly, as shown by delayed responses expressed in later phases of development. The obtained results can be useful for the selection of soybean cultivars adapted to the climatic conditions of cultivation of Kharkiv region.
Abugalieva, S., Didorenko, S., Anuarbek, S., Volkova, L., Gerasimova, Y., Sidorik, I., & Turuspekov, Y. (2016). Assessment of soybean flowering and seed maturation time in different latitude regions of Kazakhstan. PLoS One, 11(12), e0166894.
Ali, M. F., Brown, P., Thomas, J., Salmeron, M., & Kawashima, T. (2022). Effect of assimilate competition during early seed development on the pod and seed growth traits in soybean. Plant Reproduction, 35(3), 179–188.
Assefa, Y., Purcell, L. C., Salmeron, M., Naeve, S., Casteel, S. N., Kovács, P., Archontoulis, S., Licht, M., Below, F., Kandel, H., Lindsey, L. E., Gaska, J., Conley, S., Shapiro, C., Orlowski, J. M., Golden, B. R., Kaur, G., Singh, M., Thelen, K., Laurenz, R., Davidson, D., & Ciampitti, I. A. (2019). Assessing variation in US soybean seed composition (protein and oil). Frontiers in Plant Science, 10, 298.
Bueno, R. D., Borges, L. L., Good God, P. I. V., Piovesan, N. D., Teixeira, A. I., Cruz, C. D., & De Barros, E. G. (2018). Quantification of anti-nutritional factors and their correlations with protein and oil in soybeans. Anais da Academia Brasileira de Ciências, 90(1), 205–217.
Cao, D., Takeshima, R., Zhao, C., Liu, B., Jun, A., & Kong, F. (2017). Molecular mechanisms of flowering under long days and stem growth habit in soybean. Journal of Experimental Botany, 68(8), 1873–1884.
Chiluwal, A., Kawashima, T., & Salmeron, M. (2021). Soybean seed weight responds to increases in assimilate supply during late seed-fill phase. Journal of Crop Improvement, 36(2) 222–238.
Cober, E. R., Curtis, D. F., Stewart, D. W., & Morrison, M. J. (2014). Quantifying the effects of photoperiod, temperature and daily irradiance on flowering time of soybean isolines. Plants, 3(4), 476–497.
Dhungana, S. K., Kulkarni, K. P., Kim, M., Ha, B. K., Kang, S., Song, J. T., Shin, D. H., & Lee, J. D. (2017). Environmental stability and correlation of soybean seed starch with protein and oil contents. Plant Breeding and Biotechnology, 5(4), 293–303.
Dhungana, S. K., Kulkarni, K. P., Park, C. W., Jo, H., Song, J. T., Shin, D. H., & Lee, J. D. (2017). Mapping quantitative trait loci controlling soybean seed starch content in an interspecific cross of ‘Williams 82’ (Glycine max) and ‘PI 366121’ (Glycine soja). Plant Breeding, 136(3) 379–385.
Dong, L., Hou, Z., Li, H., Li, Z., Fang, C., Kong, L., Li, Y., Du, H., Li, T., Wang, L., He, M., Zhao, X., Cheng, Q., Kong, F., & Liu, B. (2022). Agronomical selection on loss‐of‐function of Gigantea simultaneously facilitates soybean salt tolerance and early maturity. Journal of Integrative Plant Biology, 61(10), 13332.
Hider, N. H. A.-H., & Zhmurko, V. (2020). Influence of different photoperiodic conditions on the protein and oil content in soybean seeds (Glycine max (L.) Merr.). ScienceRise: Biological Science, 22, 10–15.
Jiang, B., Nan, H., Gao, Y., Tang, L., Yue, Y., Lu, S., Ma, L., Cao, D., Sun, S., Wang, J., Wu, C., Yuan, X., Hou, W., & Liu, B. (2014). Allelic combinations of soybean maturity loci E1, E2, E3 and E4 result in diversity of maturity and adaptation to different latitudes. PLoS One, 9(8), e106042.
Kantolic, A. G., Peralta, G. E., & Slafer, G. A. (2013). Seed number responses to extended photoperiod and shading during reproductive stages in indeterminate soybean. European Journal of Agronomy, 51, 91–100.
Kawasakia, Y., Yamazakia, R., Katayamaa, K., Yamadac, T., & Funatsuk, H. (2018). Effects of maturity genes E2 and E3 on yield formation in soybean cultivar Enrei in warm region, Fukuyama in Japan. Plant Production Science, 21(4), 387–397.
Kumagai, E., Yamada, T., & Hasegawa, T. (2020). Is the yield change due to warming affected by photoperiod sensitivity? Effects of the soybean E4 locus. Food and Energy Security, 9(1), e186.
Kumawat, G., Yadav, A., Satpute, G. K., Gireesh, C., Patel, R., Shivakumar, M., Gupta, S., Chand, S., & Bhatia, V. S. (2019). Genetic relationship, population structure analysis and allelic characterization of flowering and maturity genes E1, E2, E3 and E4 among 90 Indian soybean landraces. Physiology and Molecular Biology of Plants, 25(2), 387–398.
Langewisch, T., Lenis, J., Jiang, G. L., Wang, D., Pantalone, V., & Bilyeu, K. (2017). The development and use of a molecular model for soybean maturity groups. BMC Plant Biology, 91, 1–13.
Liu, X., Wu, J.-A., Re, H., Qi, Y., Li, C., Cao, J., Zhang, X., Zhang, Z., Cai, Z., & Gai, J. (2017). Genetic variation of world soybean maturity date and geographic distribution of maturity groups. Breeding Science, 67(3), 221–232.
Lui, L. F., Gao, L., Zhang, L. X., Cai, Y. P., Song, W. W., Chen, L., Yuan, S., Jiang, B. J., Sun, S., Wu, C. X., Hou, W. S., & Han, T. F. (2022). Co-silencing E1 and its homologs in an extremely late-maturing soybean cultivar confers super-early maturity and adaptation to high-latitude short-season regions. Journal of Integrative Agriculture, 21(2), 326–335.
Nico, M., Miralles, D. J., & Kantolic, A. G. (2015). Post-flowering photoperiod and radiation interaction in soybean yield determination: Direct and indirect photoperiodic effects. Field Crops Research, 176, 45–55.
Ort, N. W. W., Morrison, M. J., Cober, E. R., Samanfar, B., & Lawley, Y. E. (2022). Photoperiod affects node appearance rate and flowering in early maturing soybean. Plants, 11(7), 871.
Piper, E. L., & Boote, K. I. (1999). Temperature and cultivar effects on soybean seed oil and protein concentrations. Journal of the American Oil Chemists’ Society, 76, 1233–1241.
Poeta, F. B., Rotundo, J. L., Borrás, L., & Westgate, M. E. (2014). Seed water concentration and accumulation of protein and oil in soybean seeds. Crop Science, 54(6), 2752–2759.
Saryoko, A., Homma, K., Lubis, I., & Shiraiw, T. (2017). Plant development and yield components under a tropical environment in soybean cultivars with temperate and tropical origins. Plant Production Science, 20(4), 375–383.
Song, W., Yang, R., Wu, T., Wu, C., Sun, S., Zhang, S. Jiang, B., Tian, S., Liu, X., & Han, T. (2016). Analyzing the effects of climate factors on soybean protein, oil contents, and composition by extensive and high-density sampling in China. Journal of Agricultural and Food Chemistry, 64(20), 4121–4130.
Tsubokura, Y., Matsumura, H., Xu, M. L., Liu, B. H., Nakashima, H., Anai, T., Kong, F. J., Yuan, X. H., Kanamori, H., Katayose, Y., Takahashi, R., Harada, K., & Abe, J. (2013). Genetic variation in soybean at the maturity locus E4 is involved in adaptation to long days at high latitudes. Agronomy, 3(1), 117–134.
Wang, C., Liu, X., Hao, X., Pan, Y., Zong, C., Zeng, W., Wang, W., Xing, G., He, J., & Gai, J. (2022). Evolutionary variation of accumulative day length and accumulative active temperature required for growth periods in global soybeans. Agronomy, 12(4), 962.
Wang, L., Li, H., He, M., Dong, L., Huang, Z., Chen, L., Nan, H., Kong, F., Liu, B., & Zhao X. (2022). Gigantea orthologs, E2 members, redundantly determine photoperiodic flowering and yield in soybean. Journal of Integrative Plant Biology, 65(1), 188–202.
Watanabe, S., Harada, K., & Abe, J. (2012). Genetic and molecular bases of photoperiod responses of flowering in soybean. Breed Science, 61(5), 531–543.
Xia, Z. J., Watanabe, S., Yamada, T., Tsubokura, Y., Nakashima, H., Zhai, H., Anai, T., Sato, S., Yamazaki, T., Lü, S., Wu, H. Y., Tabata, S., & Harada, K. (2012). Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proceedings of the National Academy of Sciences of the United States of America, 109(32), 2155–2164.
Xu, M., Xu, Z., Liu, B., Kong, F., Tsubokura, Y., Watanabe, S., Xia, Z., Harada, K., Kanazawa, A., Yamada, T., & Abe, J. (2013). Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean. BMC Plant Biology, 13, 91.
Yermakov, A. I., Arasimovich, V. V., & Yarosh, N. P. (1987). Metody biokhimicheskogo issledovaniya rastenii [Methods of biochemical research of plants]. Agropromizdat, Leningrad (in Russian).
Zhang, L. X., Liu, W., Mesfin, T., Xu, X., Qi, Y. P., Sapey, E., Liu, L. P., Wu, T. T., Sun, S., & Han, T. F. (2020). Principles and practices of the photo-thermal adaptability improvement in soybean. Journal of Integrative Agriculture, 19(2), 295–310.
Zharikova, D. O., Chebotar, G. O., Aksyonova, E. A., Temchenko, I. V., & Chebotar, S. V. (2019). Polymorphisms in SSR-loci associated with E genes in soybean mutant lines offer perspective for breeding. Agricultural Science and Practice, 6(3), 45–55.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.