Influence of Bradyrhizobium japonicum on the growth parameters and formation of the assimilation apparatus in E-gene isogenic lines of soybean
Keywords:
Glycine max; rhizobia; E-loci; photoperiod sensitivity; growth analysis; chlorophyll a and b; inoculation; leaf area
Abstract
The study investigated the impact of the interaction between soybean and rhizobia on the assimilation apparatus functioning and biomass accumulation in different soybean lines with varying photoperiod sensitivity. Nearly isogenic lines (NILs) of soybean were used, with genes E1, E2, and E3 in different allelic states: Clark (e1E2E3), L80-5879 (E1e2e3), L63-3117 (e1e2E3), and L71-920 (e1e2e3). The experimental group for each line was treated with Bradyrhizobium japonicum 634b. Plants were grown under natural long-day conditions (16 hours). Growth indicators of the studied lines, such as relative growth rate (RGR), net assimilation rate (NAR), leaf area ratio (LAR), and specific leaf area (SLA), were analyzed, as well as the content of chlorophylls A and B in the V3 and V5 developmental stages. The results demonstrate that the influence of rhizobia on the functioning of the assimilation apparatus and biomass accumulation depends on the soybean line genotype. In the study, RGR, which characterizes the biomass accumulation rate, has similar trends to those observed with NAR, characterizing the assimilation apparatus's functioning. However, each line showed its own tendencies. For instance, in the short-day variety Clark, under bacterial influence, the value of RGR and NAR decreased. Additionally, LAR and SLA values indicated a reduction in the total photosynthetic surface area and leaf dry matter. Bacterial inoculation did not significantly affect the content of photosynthetic pigments in Clark leaves. Another short-day line, L80-5879, showed no significant impact of bacterial inoculation on biomass accumulation. However, soybean interaction with Bradyrhizobium japonicum 634b led to a decrease in leaf surface area and dry matter content. Probably, bacterial inoculation supported assimilation processes by increasing auxiliary chlorophyll b in photosystem I. A general trend of significant RGR reduction in neutral-day soybean lines, L63-3117 and L71-920, was identified under bacterial influence. The interaction with rhizobia differently affected LAR and SLA values, indicating distinct adaptive mechanisms to the interactions. In conditions of almost zero plant biomass accumulation, Bradyrhizobium japonicum 634b caused a decrease in the total photosynthetic surface area and chlorophyll a and b content in the L63-3117 line. In L71-920, bacterial inoculation had no effect on the total photosynthetic surface area, while leaf dry matter and photosynthetic pigment content decreased. The obtained results demonstrate that interaction with rhizobia can influence the functioning of the assimilation apparatus in soybeans with varying photoperiod sensitivity that is determined by genotype. It is important in improving soybean productivity and its application in agricultural practices.References
Chen, Z., Tao, X., Khan, A., Tan, D. K. Y., & Luo, H. (2018). Biomass accumula-tion, photosynthetic traits and root development of cotton as affected by irriga-tion and nitrogen-fertilization. Frontiers in Plant Science, 9, 173.
Esteban, R., Barrutia, O., Artetxe, U., Fernández‐Marín, B., Hernández, A., & García-Plazaola, J. I. (2014). Internal and external factors affecting photosyn-thetic pigment composition in plants: A meta-analytical approach. New Phytol-ogist, 206(1), 268–280.
Fagorzi, C., Bacci, G., Huang, R., Cangioli, L., Checcucci, A., Fini, M., Perrin, E., Natali, C., diCenzo, G. C., & Mengoni, A. (2021). Nonadditive transcriptomic signatures of genotype-by-genotype interactions during the initiation of plant-Rhizobium symbiosis. MSystems, 6(1), e00974-20.
Hlushach, D., Zhmurko, V., & Avksentieva, O. (2023). Vplyv henotypu ta bakteryzatsiji na rist, rozvytok ta vmist rozchynnykh vuhlevodiv u izohennykh za E-henamy liniji soji kulturnoji [Influence of genotype and bacterization on growth, development, and soluble carbohydrate content in soybean E-genes isogenic lines]. The Journal of V. N. Karazin Kharkiv National University, Biology, 40, 59–70 (in Ukrainian).
Hu, Y., Chen, Y., Yang, X., Deng, L., & Lu, X. (2023). Enhancing soybean yield: The synergy of sulfur and rhizobia inoculation. Plants, 12(22), 3911.
Hunt, R. (2017). Growth analysis, individual plants. In: Thomas, B., Murray, B. G., & Murphy, D. J. (Eds.). Encyclopedia of applied plant sciences. 2nd ed. Aca-demic Press, Oxford. Pp. 421–429.
Keller, B., Zimmermann, L., Rascher, U., Matsubara, S., Steier, A., & Muller, O. (2021). Toward predicting photosynthetic efficiency and biomass gain in crop genotypes over a field season. Plant Physiology, 188(1), 301–317.
Kong, F., Nan, H., Cao, D., Li, Y., Wu, F., Wang, J., Lu, S., Yuan, X., Cober, E. R., Abe, J., & Liu, B. (2014). A new dominant gene E9 conditions early flowering and maturity in soybean. Crop Science, 54(6), 2529–2535.
Kozar, S. F., Skoryk, V. V., Usmanova, T. O., & Yevtushenko, T. A. (2012). Vplyv stabilizatoriv na rist, zhyttiezdatnist i funktsionalnu aktyvnist Bradyrhizobium japonicum [The influence of stabilizators on the growth, viability and functional activity of Bradyrhizobium japonicum]. Agricultural Microbiology, 15, 58–70 (in Ukrainian).
Lamont, B. B., Williams, M. R., & He, T. (2023). Relative growth rate (RGR) and other confounded variables: Mathematical problems and biological solutions. Annals of Botany, 131(4), 555–568.
Li, X., Schmid, B., Wang, F., & Paine, C. E. T. (2016). Net assimilation rate deter-mines the growth rates of 14 species of subtropical forest trees. PLoS One, 11(3), e0150644.
Li, Y., Hou, Z., Li, W., Li, H., Lu, S., Gan, Z., Du, H., Li, T., Zhang, Y., Kong, F., Cheng, Y., He, M., Ma, L., Liao, C., Li, Y., Dong, L., Liu, B., & Cheng, Q. (2021). The legume-specific transcription factor E1 controls leaf morphology in soybean. BMC Plant Biology, 21(1), 531.
Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical So-ciety Transactions, 11(5), 591–592.
Lie, T. A. (1971). Nodulation of rooted leaves in leguminous plants. Plant and Soil, 34(3), 663–673.
Liu, P.-C., Peacock, W. J., Wang, L., Furbank, R., Larkum, A., & Dennis, E. S. (2020). Leaf growth in early development is key to biomass heterosis in Arabidopsis. Journal of Experimental Botany, 71(8), 2439–2450.
Melnykova, N. M., & Kots, S. Y. (2019). Vplyv stabilizatoriv na rist, zhyttiezdatnist’ i funktsional’nu aktyvnist’ Bradyrhizobium japonicum 634b [Effect of goat’s rhizobia on the formation and functioning of the soybean – Bradyrhizobium japonicum 634b symbiosis]. Agricultural Microbiology, 29, 29–36 (in Ukrainian).
Mishra, P., & Panigrahi, K. C. (2015). GIGANTEA – an emerging story. Frontiers in Plant Science, 6, 8.
Osnato, M., Cota, I., Nebhnani, P., Cereijo, U., & Pelaz, S. (2022). Photoperiod control of plant growth: Flowering time genes beyond flowering. Frontiers in Plant Science, 12, 805635.
Pagano, M. C., & Miransari, M. (2016). The importance of soybean production worldwide. In: Miransari, M. (Ed.). Abiotic and biotic stresses in soybean pro-duction. Academic Press, Oxford. Pp. 1–26.
Rani, R., Raza, G., Ashfaq, H., Rizwan, M., Shimelis, H., Tung, M. H., & Arif, M. (2023). Analysis of genotype × environment interactions for agronomic traits of soybean (Glycine max [L.] Merr.) using association mapping. Frontiers in Genetics, 13, 1090994.
Roeber, V. M., Schmülling, T., & Cortleven, A. (2022). The photoperiod: Handling and causing stress in plants. Frontiers in Plant Science, 12, 781988.
Singh, A. (2022). GIGANTEA regulates lateral root formation by modulating auxin signaling in Arabidopsis thaliana. Plant Signaling and Behavior, 17(1), 2096780.
Sun, H., Jia, Z., Cao, D., Jiang, B., Wu, C., Hou, W., Liu, Y., Fei, Z., Zhao, D., & Han, T. (2011). GmFT2a, a soybean homolog of Flowering locus T, is involved in flowering transition and maintenance. PLoS One, 6(12), e29238.
Suzuki, A., Suriyagoda, L., Shigeyama, T., Tominaga, A., Sasaki, M., Hiratsuka, Y., Yoshinaga, A., Arima, S., Agarie, S., Sakai, T., Inada, S., Jikumaru, Y., Kamiya, Y., Uchiumi, T., Abe, M., Hashiguchi, M., Akashi, R., Sato, S., Kaneko, T., Tabata, S., & Hirsch, A. M. (2011). Lotus japonicus nodulation is photo-morphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proceedings of the National Academy of Sciences, 108(40), 16837–16842.
Taniguchi, T., Murayama, N., Ario, N., Nakagawa, A. C. S., Tanaka, S., Tomoita, Y., Hasegawa, M., Hamaoka, N., Iwaya-Inoue, M., & Ishibashi, Y. (2020). Photoperiod sensing of leaf regulates pod setting in soybean (Glycine max (L.) Merr.). Plant Production Science, 23(3), 360–365.
Tasma, I. M., & Shoemaker, R. C. (2003). Mapping flowering time gene homologs in soybean and their association with maturity (E) loci. Crop Science, 43(1), 319–328.
Tripathi, S., Hoang, Q. T. N., Han, Y. J., & Kim, J. I. (2019). Regulation of photo-morphogenic development by plant phytochromes. International Journal of Molecular Sciences, 20(24), 6165.
Tsubokura, Y., Watanabe, S., Xia, Z., Kanamori, H., Yamagata, H., Kaga, A., Ka-tayose, Y., Abe, J., Ishimoto, M., & Harada, K. (2013). Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Annals of Botany, 113(3), 429–441.
Waese, J., Fan, J., Pasha, A., Yu, H., Fucile, G., Shi, R., Cumming, M., Kelley, L. A., Sternberg, M. J., Krishnakumar, V., Ferlanti, E., Miller, J., Town, C., Stuer-zlinger, W., & Provart, N. J. (2017). ePlant: Visualizing and exploring multiple levels of data for hypothesis generation in plant biology. The Plant Cell, 29(8), 1806–1821.
Wang, T., Guo, J., Peng, Y., Lyu, X., Liu, B., Sun, S., & Wang, X. (2021). Light-induced mobile factors from shoots regulate rhizobium-triggered soybean root nodulation. Science, 374(6563), 65–71.
Wang, W., Cao, Y., Sheng, K., Chen, J., Zhu, S., & Zhao, T. (2023). GhFP positively regulates chlorophyll content and seedling biomass in upland cotton. Industrial Crops and Products, 204, 117388.
Wang, Y., Yang, W., Zuo, Y., Zhu, L., Hastwell, A. H., Chen, L., Tian, Y., Su, C., Ferguson, B. J., & Li, X. (2019). GmYUC2a mediates auxin biosynthesis dur-ing root development and nodulation in soybean. Journal of Experimental Bo-tany, 70(12), 3165–3176.
Wani, S. P., Gopalakrishnan, S. (2019). Plant growth-promoting microbes for sustainable agriculture. In: Sayyed, R., Reddy, M., & Antonius, S. (Eds.). Plant growth promoting rhizobacteria (PGPR): Prospects for sustainable agriculture. Springer, Singapore. Pp. 19–45.
Weraduwage, S. M., Chen, J., Anozie, F. C., Morales, A., Weise, S. E., & Sharkey, T. D. (2015). The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana. Frontiers in Plant Science, 6, 167.
Xia, Z., Watanabe, S., Yamada, T., Tsubokura, Y., Nakashima, H., Zhai, H., Anai, T., Sato, S., Yamazaki, T., Lü, S., Wu, H., Tabata, S., & Harada, K. (2012). Po-sitional cloning and characterization reveal the molecular basis for soybean ma-turity locus E1 that regulates photoperiodic flowering. Proceedings of the Na-tional Academy of Sciences, 109(32), e2155-e2164.
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(1), 91.
Yun, J., Wang, C., Zhang, F., Chen, L., Sun, Z., Cai, Y., Luo, Y., Liao, J., Wang, Y., Cha, Y., Zhang, X., Ren, Y., Wu, J., Hasegawa, P. M., Tian, C., Su, H., Fergu-son, B. J., Gresshoff, P. M., Hou, W., Han, T., & Li, X. (2023). A nitrogen fix-ing symbiosis-specific pathway required for legume flowering. Science Ad-vances, 9(2), eade1150.
Zhai, H., Wan, Z., Jiao, S., Zhou, J., Xu, K., Nan, H., Liu, Y., Xiong, S., Fan, R., Zhu, J., Jiang, W., Pang, T., Luo, X., Wu, H., Yang, G., Bai, X., Kong, F., & Xia, Z. (2022). GmMDE genes bridge the maturity gene E1 and florigens in photoperiodic regulation of flowering in soybean. Plant Physiology, 189(2), 1021–1036.
Zhang, X., Wu, T., Wen, H., Song, W., Xu, C., Han, T., Sun, S., & Wu, C. (2021). Allelic variation of soybean maturity genes E1–E4 in the Huang-Huai-Hai Riv-er Valley and the Northwest China. Agriculture, 11(6), 478.
Zhao, C., Takeshima, R., Zhu, J., Xu, M., Sato, M., Watanabe, S., Kanazawa, A., Liu, B., Kong, F., Yamada, T., & Abe, J. (2016). A recessive allele for delayed flowering at the soybean maturity locus E9 is a leaky allele of FT2a, a Flower-ing locus T ortholog. BMC Plant Biology, 16(1), 20.
Zhao, X., Cao, D., Huang, Z., Wang, J., Lu, S., Xu, Y., Liu, B., Kong, F., & Yuan, X. (2015). Dual functions of GmTOE4a in the regulation of photoperiod-mediated flowering and plant morphology in soybean. Plant Molecular Biology, 88(4–5), 343–355.
Zheng, N., Guo, Y., Wang, S., Zhang, H., Wang, L., Gao, Y., Xu, M., Wang, W., Liu, W., & Yang, W. (2023). Identification of E1-E4 allele combinations and ecological adaptability of soybean varieties from different geographical origins in China. Frontiers in Plant Science, 14, 1222755.
Zimmer, G., Miller, M. J., Steketee, C. J., Jackson, S. A., de Tunes, L. V. M., & Li, Z. (2021). Genetic control and allele variation among soybean maturity groups 000 through IX. The Plant Genome, 14(3), e20146.
Esteban, R., Barrutia, O., Artetxe, U., Fernández‐Marín, B., Hernández, A., & García-Plazaola, J. I. (2014). Internal and external factors affecting photosyn-thetic pigment composition in plants: A meta-analytical approach. New Phytol-ogist, 206(1), 268–280.
Fagorzi, C., Bacci, G., Huang, R., Cangioli, L., Checcucci, A., Fini, M., Perrin, E., Natali, C., diCenzo, G. C., & Mengoni, A. (2021). Nonadditive transcriptomic signatures of genotype-by-genotype interactions during the initiation of plant-Rhizobium symbiosis. MSystems, 6(1), e00974-20.
Hlushach, D., Zhmurko, V., & Avksentieva, O. (2023). Vplyv henotypu ta bakteryzatsiji na rist, rozvytok ta vmist rozchynnykh vuhlevodiv u izohennykh za E-henamy liniji soji kulturnoji [Influence of genotype and bacterization on growth, development, and soluble carbohydrate content in soybean E-genes isogenic lines]. The Journal of V. N. Karazin Kharkiv National University, Biology, 40, 59–70 (in Ukrainian).
Hu, Y., Chen, Y., Yang, X., Deng, L., & Lu, X. (2023). Enhancing soybean yield: The synergy of sulfur and rhizobia inoculation. Plants, 12(22), 3911.
Hunt, R. (2017). Growth analysis, individual plants. In: Thomas, B., Murray, B. G., & Murphy, D. J. (Eds.). Encyclopedia of applied plant sciences. 2nd ed. Aca-demic Press, Oxford. Pp. 421–429.
Keller, B., Zimmermann, L., Rascher, U., Matsubara, S., Steier, A., & Muller, O. (2021). Toward predicting photosynthetic efficiency and biomass gain in crop genotypes over a field season. Plant Physiology, 188(1), 301–317.
Kong, F., Nan, H., Cao, D., Li, Y., Wu, F., Wang, J., Lu, S., Yuan, X., Cober, E. R., Abe, J., & Liu, B. (2014). A new dominant gene E9 conditions early flowering and maturity in soybean. Crop Science, 54(6), 2529–2535.
Kozar, S. F., Skoryk, V. V., Usmanova, T. O., & Yevtushenko, T. A. (2012). Vplyv stabilizatoriv na rist, zhyttiezdatnist i funktsionalnu aktyvnist Bradyrhizobium japonicum [The influence of stabilizators on the growth, viability and functional activity of Bradyrhizobium japonicum]. Agricultural Microbiology, 15, 58–70 (in Ukrainian).
Lamont, B. B., Williams, M. R., & He, T. (2023). Relative growth rate (RGR) and other confounded variables: Mathematical problems and biological solutions. Annals of Botany, 131(4), 555–568.
Li, X., Schmid, B., Wang, F., & Paine, C. E. T. (2016). Net assimilation rate deter-mines the growth rates of 14 species of subtropical forest trees. PLoS One, 11(3), e0150644.
Li, Y., Hou, Z., Li, W., Li, H., Lu, S., Gan, Z., Du, H., Li, T., Zhang, Y., Kong, F., Cheng, Y., He, M., Ma, L., Liao, C., Li, Y., Dong, L., Liu, B., & Cheng, Q. (2021). The legume-specific transcription factor E1 controls leaf morphology in soybean. BMC Plant Biology, 21(1), 531.
Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical So-ciety Transactions, 11(5), 591–592.
Lie, T. A. (1971). Nodulation of rooted leaves in leguminous plants. Plant and Soil, 34(3), 663–673.
Liu, P.-C., Peacock, W. J., Wang, L., Furbank, R., Larkum, A., & Dennis, E. S. (2020). Leaf growth in early development is key to biomass heterosis in Arabidopsis. Journal of Experimental Botany, 71(8), 2439–2450.
Melnykova, N. M., & Kots, S. Y. (2019). Vplyv stabilizatoriv na rist, zhyttiezdatnist’ i funktsional’nu aktyvnist’ Bradyrhizobium japonicum 634b [Effect of goat’s rhizobia on the formation and functioning of the soybean – Bradyrhizobium japonicum 634b symbiosis]. Agricultural Microbiology, 29, 29–36 (in Ukrainian).
Mishra, P., & Panigrahi, K. C. (2015). GIGANTEA – an emerging story. Frontiers in Plant Science, 6, 8.
Osnato, M., Cota, I., Nebhnani, P., Cereijo, U., & Pelaz, S. (2022). Photoperiod control of plant growth: Flowering time genes beyond flowering. Frontiers in Plant Science, 12, 805635.
Pagano, M. C., & Miransari, M. (2016). The importance of soybean production worldwide. In: Miransari, M. (Ed.). Abiotic and biotic stresses in soybean pro-duction. Academic Press, Oxford. Pp. 1–26.
Rani, R., Raza, G., Ashfaq, H., Rizwan, M., Shimelis, H., Tung, M. H., & Arif, M. (2023). Analysis of genotype × environment interactions for agronomic traits of soybean (Glycine max [L.] Merr.) using association mapping. Frontiers in Genetics, 13, 1090994.
Roeber, V. M., Schmülling, T., & Cortleven, A. (2022). The photoperiod: Handling and causing stress in plants. Frontiers in Plant Science, 12, 781988.
Singh, A. (2022). GIGANTEA regulates lateral root formation by modulating auxin signaling in Arabidopsis thaliana. Plant Signaling and Behavior, 17(1), 2096780.
Sun, H., Jia, Z., Cao, D., Jiang, B., Wu, C., Hou, W., Liu, Y., Fei, Z., Zhao, D., & Han, T. (2011). GmFT2a, a soybean homolog of Flowering locus T, is involved in flowering transition and maintenance. PLoS One, 6(12), e29238.
Suzuki, A., Suriyagoda, L., Shigeyama, T., Tominaga, A., Sasaki, M., Hiratsuka, Y., Yoshinaga, A., Arima, S., Agarie, S., Sakai, T., Inada, S., Jikumaru, Y., Kamiya, Y., Uchiumi, T., Abe, M., Hashiguchi, M., Akashi, R., Sato, S., Kaneko, T., Tabata, S., & Hirsch, A. M. (2011). Lotus japonicus nodulation is photo-morphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proceedings of the National Academy of Sciences, 108(40), 16837–16842.
Taniguchi, T., Murayama, N., Ario, N., Nakagawa, A. C. S., Tanaka, S., Tomoita, Y., Hasegawa, M., Hamaoka, N., Iwaya-Inoue, M., & Ishibashi, Y. (2020). Photoperiod sensing of leaf regulates pod setting in soybean (Glycine max (L.) Merr.). Plant Production Science, 23(3), 360–365.
Tasma, I. M., & Shoemaker, R. C. (2003). Mapping flowering time gene homologs in soybean and their association with maturity (E) loci. Crop Science, 43(1), 319–328.
Tripathi, S., Hoang, Q. T. N., Han, Y. J., & Kim, J. I. (2019). Regulation of photo-morphogenic development by plant phytochromes. International Journal of Molecular Sciences, 20(24), 6165.
Tsubokura, Y., Watanabe, S., Xia, Z., Kanamori, H., Yamagata, H., Kaga, A., Ka-tayose, Y., Abe, J., Ishimoto, M., & Harada, K. (2013). Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Annals of Botany, 113(3), 429–441.
Waese, J., Fan, J., Pasha, A., Yu, H., Fucile, G., Shi, R., Cumming, M., Kelley, L. A., Sternberg, M. J., Krishnakumar, V., Ferlanti, E., Miller, J., Town, C., Stuer-zlinger, W., & Provart, N. J. (2017). ePlant: Visualizing and exploring multiple levels of data for hypothesis generation in plant biology. The Plant Cell, 29(8), 1806–1821.
Wang, T., Guo, J., Peng, Y., Lyu, X., Liu, B., Sun, S., & Wang, X. (2021). Light-induced mobile factors from shoots regulate rhizobium-triggered soybean root nodulation. Science, 374(6563), 65–71.
Wang, W., Cao, Y., Sheng, K., Chen, J., Zhu, S., & Zhao, T. (2023). GhFP positively regulates chlorophyll content and seedling biomass in upland cotton. Industrial Crops and Products, 204, 117388.
Wang, Y., Yang, W., Zuo, Y., Zhu, L., Hastwell, A. H., Chen, L., Tian, Y., Su, C., Ferguson, B. J., & Li, X. (2019). GmYUC2a mediates auxin biosynthesis dur-ing root development and nodulation in soybean. Journal of Experimental Bo-tany, 70(12), 3165–3176.
Wani, S. P., Gopalakrishnan, S. (2019). Plant growth-promoting microbes for sustainable agriculture. In: Sayyed, R., Reddy, M., & Antonius, S. (Eds.). Plant growth promoting rhizobacteria (PGPR): Prospects for sustainable agriculture. Springer, Singapore. Pp. 19–45.
Weraduwage, S. M., Chen, J., Anozie, F. C., Morales, A., Weise, S. E., & Sharkey, T. D. (2015). The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana. Frontiers in Plant Science, 6, 167.
Xia, Z., Watanabe, S., Yamada, T., Tsubokura, Y., Nakashima, H., Zhai, H., Anai, T., Sato, S., Yamazaki, T., Lü, S., Wu, H., Tabata, S., & Harada, K. (2012). Po-sitional cloning and characterization reveal the molecular basis for soybean ma-turity locus E1 that regulates photoperiodic flowering. Proceedings of the Na-tional Academy of Sciences, 109(32), e2155-e2164.
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(1), 91.
Yun, J., Wang, C., Zhang, F., Chen, L., Sun, Z., Cai, Y., Luo, Y., Liao, J., Wang, Y., Cha, Y., Zhang, X., Ren, Y., Wu, J., Hasegawa, P. M., Tian, C., Su, H., Fergu-son, B. J., Gresshoff, P. M., Hou, W., Han, T., & Li, X. (2023). A nitrogen fix-ing symbiosis-specific pathway required for legume flowering. Science Ad-vances, 9(2), eade1150.
Zhai, H., Wan, Z., Jiao, S., Zhou, J., Xu, K., Nan, H., Liu, Y., Xiong, S., Fan, R., Zhu, J., Jiang, W., Pang, T., Luo, X., Wu, H., Yang, G., Bai, X., Kong, F., & Xia, Z. (2022). GmMDE genes bridge the maturity gene E1 and florigens in photoperiodic regulation of flowering in soybean. Plant Physiology, 189(2), 1021–1036.
Zhang, X., Wu, T., Wen, H., Song, W., Xu, C., Han, T., Sun, S., & Wu, C. (2021). Allelic variation of soybean maturity genes E1–E4 in the Huang-Huai-Hai Riv-er Valley and the Northwest China. Agriculture, 11(6), 478.
Zhao, C., Takeshima, R., Zhu, J., Xu, M., Sato, M., Watanabe, S., Kanazawa, A., Liu, B., Kong, F., Yamada, T., & Abe, J. (2016). A recessive allele for delayed flowering at the soybean maturity locus E9 is a leaky allele of FT2a, a Flower-ing locus T ortholog. BMC Plant Biology, 16(1), 20.
Zhao, X., Cao, D., Huang, Z., Wang, J., Lu, S., Xu, Y., Liu, B., Kong, F., & Yuan, X. (2015). Dual functions of GmTOE4a in the regulation of photoperiod-mediated flowering and plant morphology in soybean. Plant Molecular Biology, 88(4–5), 343–355.
Zheng, N., Guo, Y., Wang, S., Zhang, H., Wang, L., Gao, Y., Xu, M., Wang, W., Liu, W., & Yang, W. (2023). Identification of E1-E4 allele combinations and ecological adaptability of soybean varieties from different geographical origins in China. Frontiers in Plant Science, 14, 1222755.
Zimmer, G., Miller, M. J., Steketee, C. J., Jackson, S. A., de Tunes, L. V. M., & Li, Z. (2021). Genetic control and allele variation among soybean maturity groups 000 through IX. The Plant Genome, 14(3), e20146.
Published
2024-02-20
How to Cite
Hlushach, D. V., & Avksentieva, O. O. (2024). Influence of Bradyrhizobium japonicum on the growth parameters and formation of the assimilation apparatus in E-gene isogenic lines of soybean . Regulatory Mechanisms in Biosystems, 15(1), 131-141. https://doi.org/10.15421/022420
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