Mechanisms underlying key agronomic traits and implications for molecular breeding in soybean

Chao Fang; Haiping Du; Lingshuang Wang; Baohui Liu; Fanjiang Kong

doi:10.1016/j.jgg.2023.09.004

Volume 51 Issue 4

Apr. 2024

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2024 > 51(4): 379-393

PDF( 1763 KB)

Mechanisms underlying key agronomic traits and implications for molecular breeding in soybean

doi: 10.1016/j.jgg.2023.09.004

Guangdong Key Laboratory of Plant Adaptation and Molecular Design, Guangzhou Key Laboratory of Crop Gene Editing, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou, Guangdong 510006, China

Funds:

This work was supported by the National Natural Science Foundation of China (32090064 and 32001503) and the National Key Research and Development Program of China (2022YFD1201400).

Received Date: 2023-05-01
Accepted Date: 2023-09-05
Rev Recd Date: 2023-09-05
Publish Date: 2023-09-17

Abstract

Abstract

Soybean (Glycine max [L.] Merr.) is an important crop that provides protein and vegetable oil for human consumption. As soybean is a photoperiod-sensitive crop, its cultivation and yield are limited by the photoperiodic conditions in the field. In contrast to other major crops, soybean has a special plant architecture and a special symbiotic nitrogen fixation system, representing two unique breeding directions. Thus, flowering time, plant architecture, and symbiotic nitrogen fixation are three critical or unique yield-determining factors. This review summarizes the progress made in our understanding of these three critical yield-determining factors in soybean. Meanwhile, we propose potential research directions to increase soybean production, discuss the application of genomics and genomic-assisted breeding, and explore research directions to address future challenges, particularly those posed by global climate changes.
- Soybean,
- Grain yield,
- Flowering time,
- Plant architecture,
- Nodulation,
- Symbiotic nitrogen fixation,
- Genome study

FullText(HTML)

References(200)

References

Achom, M., Roy, P., Lagunas, B., Picot, E., Richards, L., Bonyadi-Pour, R., Pardal, A.J., Baxter, L., Richmond, B.L., Aschauer, N., et al., 2022. Plant circadian clock control of medicago truncatula nodulation via regulation of nodule cysteine-rich peptides. J Exp Bot 73, 2142-2156.

Ahmad, M.Z., Zhang, Y., Zeng, X., Li, P., Wang, X., Benedito, V.A.,Zhao, J., 2021. Isoflavone malonyl-coa acyltransferase gmmat2 is involved in nodulation of soybean by modifying synthesis and secretion of isoflavones. J Exp Bot 72, 1349-1369.

Bai, M., Yuan, C., Kuang, H., Sun, Q., Hu, X., Cui, L., Lin, W., Peng, C., Yue, P., Song, S., et al., 2022. Combination of two multiplex genome-edited soybean varieties enables customization of protein functional properties. Molecular Plant 15, 1081-1083.

Balboa, G.R., Sadras, V.O.,Ciampitti, I.A., 2018. Shifts in soybean yield, nutrient uptake, and nutrient stoichiometry: A historical synthesis-analysis. Crop Science 58, 43-54.

Bao, A., Chen, H., Chen, L., Chen, S., Hao, Q., Guo, W., Qiu, D., Shan, Z., Yang, Z., Yuan, S., et al., 2019. Crispr/cas9-mediated targeted mutagenesis of gmspl9 genes alters plant architecture in soybean. BMC Plant Biol 19, 131.

Bernard, R.L., 1971. Two major genes for time of flowering and maturity in soybean. Crop Science 11, 242-244.

Bernard, R.L., 1972. Two genes affecting stem termination in soybeans.Pdf. Crop Science 12, 235-239.

Bernard, R.L., Weiss, M.G., 1973. Qualitative genetics. In: Caldwell, b.E. (Ed.), Soybeans: Improvement, Production and Uses. American Society of Agronomy, USA.

Bicudo Da Silva, R.F., Batistella, M., Moran, E., Celidonio, O.L.D.M.,Millington, J.D.A., 2020. The soybean trap: Challenges and risks for brazilian producers. Frontiers in Sustainable Food Systems 4.

Bonato, E.R.,Vello, N.A., 1999. E6, a dominant gene conditioning early flowering and maturity in soybeans.Pdf. Genetics and Molecular Biology 22, 229-232.

Bonnier, C.,Sironval, C., 1956. Influence of day-length on nodule formation in soja hispida by a specific rhizobium strain. Nature 177, 93-94.

Bu, T., Lu, S., Wang, K., Dong, L., Li, S., Xie, Q., Xu, X., Cheng, Q., Chen, L., Fang, C., et al., 2021. A critical role of the soybean evening complex in the control of photoperiod sensitivity and adaptation. Proc Natl Acad Sci U S A 118.

Buzzell, R.I., 1971. Inheritance of a soybean fowering response to fluorescent-daylength conditions. J Genet Cytol 13, 703-707.

Cai, Z., Wang, Y., Zhu, L., Tian, Y., Chen, L., Sun, Z., Ullah, I.,Li, X., 2017. Gmtir1/gmafb3-based auxin perception regulated by mir393 modulates soybean nodulation. New Phytol 215, 672-686.

Cai, Z., Xian, P., Cheng, Y., Ma, Q., Lian, T., Nian, H.,Ge, L., 2021. Crispr/cas9-mediated gene editing of gmjagged1 increased yield in the low-latitude soybean variety huachun 6. Plant Biotechnol J 19, 1898-1900.

Canfield, D.E., Glazer, A.N.,Falkowski, P.G., 2010. The evolution and future of earth's nitrogen cycle. Science 330, 192-196.

Chan, C., Qi, X., Li, M.-W., Wong, F.-L.,Lam, H.-M., 2012. Recent developments of genomic research in soybean. J. Genet. Genomics 39, 317-324.

Chen, L., Nan, H., Kong, L., Yue, L., Yang, H., Zhao, Q., Fang, C., Li, H., Cheng, Q., Lu, S., et al., 2020. Soybean ap1 homologs control flowering time and plant height. J Integr Plant Biol 62, 1868-1879.

Chen, L., Qin, L., Zhou, L., Li, X., Chen, Z., Sun, L., Wang, W., Lin, Z., Zhao, J., Yamaji, N., et al., 2019. A nodule-localized phosphate transporter gmpt7 plays an important role in enhancing symbiotic n(2) fixation and yield in soybean. New Phytol 221, 2013-2025.

Chen, L., Yang, H., Fang, Y., Guo, W., Chen, H., Zhang, X., Dai, W., Chen, S., Hao, Q., Yuan, S., et al., 2021. Overexpression of gmmyb14 improves high-density yield and drought tolerance of soybean through regulating plant architecture mediated by the brassinosteroid pathway. Plant Biotechnol J 19, 702-716.

Chen, Y.,Nelson, R.L., 2004. Evaluation and classification of leaflet shape and size in wild soybean. Crop Science 44, 671-677.

Cheng, Q., Dong, L., Su, T., Li, T., Gan, Z., Nan, H., Lu, S., Fang, C., Kong, L., Li, H., et al., 2019. Crispr/cas9-mediated targeted mutagenesis of gmlhy genes alters plant height and internode length in soybean. BMC Plant Biol 19, 562.

Choudhury, S.R.,Pandey, S., 2013. Specific subunits of heterotrimeric g proteins play important roles during nodulation in soybean. Plant Physiol 162, 522-533.

Choudhury, S.R.,Pandey, S., 2015. Phosphorylation-dependent regulation of g-protein cycle during nodule formation in soybean. Plant Cell 27, 3260-3276.

Chung, W.H., Jeong, N., Kim, J., Lee, W.K., Lee, Y.G., Lee, S.H., Yoon, W., et al., 2014. Population structure and domestication revealed by high-depth resequencing of Korean cultivated and wild soybean genomes. DNA Res 21, 153–167.

Cober, E.R., Molnar, S.J., Charette, M.,Voldeng, H.D., 2010. A new locus for early maturity in soybean. Crop Science 50, 524-527.

Cober, E.R., Tanner, J.W.,Voldeng, H.D., 1996. Soybean photoperiod-sensitivity loci respond differentially to light quality. Crop Science 36, 606-610.

Cober, E.R.,Voldeng, H.D., 2001. A new soybean maturity and photoperiod-sensitivity locus linked to e1 and t. Crop Science 41.

Delves, A.C., Mathews, A., Day, D.A., Carter, A.S., Carroll, B.J.,Gresshoff, P.M., 1986. Regulation of the soybean-rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82, 588-590.

Do, T.D., Vuong, T.D., Dunn, D., Clubb, M., Valliyodan, B., Patil, G., Chen, P., Xu, D., Nguyen, H.T.,Shannon, J.G., 2019. Identification of new loci for salt tolerance in soybean by high-resolution genome-wide association mapping. BMC Genomics 20, 318.

Dong, L., Cheng, Q., Fang, C., Kong, L., Yang, H., Hou, Z., Li, Y., Nan, H., Zhang, Y., Chen, Q., et al., 2022a. Parallel selection of distinct tof5 alleles drove the adaptation of cultivated and wild soybean to high latitudes. Mol Plant 15, 308-321.

Dong, L., Fang, C., Cheng, Q., Su, T., Kou, K., Kong, L., Zhang, C., Li, H., Hou, Z., Zhang, Y., et al., 2021. Genetic basis and adaptation trajectory of soybean from its temperate origin to tropics. Nat Commun 12, 5445.

Dong, L., Hou, Z., Li, H., Li, Z., Fang, C., Kong, L., Li, Y., Du, H., Li, T., Wang, L., et al., 2022b. Agronomical selection on loss-of-function of gigantea simultaneously facilitates soybean salt tolerance and early maturity. J Integr Plant Biol 64, 1866-1882.

Dong, L., Li, S., Wang, L., Su, T., Zhang, C., Bi, Y., Lai, Y., Kong, L., Wang, F., Pei, X., et al., 2023. The genetic basis of high-latitude adaptation in wild soybean. Curr Biol 33, 252-262 e254.

dos Santos, J.V.M., Valliyodan, B., Joshi, T., Khan, S.M., Liu, Y., Wang, J.X., Vuong, T.D., et al., 2016. Evaluation of genetic variation among Brazilian soybean cultivars through genome resequencing. BMC Genom 17, 110.

Eaton, V., S., 1931. Effects of variation in day-length and clipping of plants on nodule development and growth of soy bean. Botanical Gazette, 113-143.

Fang, C., Chen, L., Nan, H., Kong, L., Li, Y., Zhang, H., Li, H., Li, T., Tang, Y., Hou, Z., et al., 2019. Rapid identification of consistent novel qtls underlying long-juvenile trait in soybean by multiple genetic populations and genotyping-by-sequencing. Molecular Breeding 39.

Fang, C., Li, W., Li, G., Wang, Z., Zhou, Z., Ma, Y., Shen, Y., Li, C., Wu, Y., Zhu, B., et al., 2013. Cloning of ln gene through combined approach of map-based cloning and association study in soybean. J Genet Genomics 40, 93-96.

Fang, C., Liu, J., Zhang, T., Su, T., Li, S., Cheng, Q., Kong, L., Li, X., Bu, T., Li, H., et al., 2021. A recent retrotransposon insertion of j caused e6 locus facilitating soybean adaptation into low latitude. J Integr Plant Biol 63, 995-1003.

Fang, C., Ma, Y., Wu, S., Liu, Z., Wang, Z., Yang, R., Hu, G., Zhou, Z., Yu, H., Zhang, M., et al., 2017. Genome-wide association studies dissect the genetic networks underlying agronomical traits in soybean. Genome Biol 18, 161.

Fehr, W.R., 1972. Genetic control of leaflet number in soybeans. Crop Science, 221-224.

Fu, M., Sun, J., Li, X., Guan, Y.,Xie, F., 2022. Asymmetric redundancy of soybean nodule inception (nin) genes in root nodule symbiosis. Plant Physiol 188, 477-489.

Gao, J., Yang, S., Cheng, W., Fu, Y., Leng, J., Yuan, X., Jiang, N., Ma, J.,Feng, X., 2017. Gmilpa1, encoding an apc8-like protein, controls leaf petiole angle in soybean. Plant Physiol 174, 1167-1176.

Gao, J.P., Xu, P., Wang, M., Zhang, X., Yang, J., Zhou, Y., Murray, J.D., Song, C.P.,Wang, E., 2021. Nod factor receptor complex phosphorylates gmgef2 to stimulate rop signaling during nodulation. Curr Biol 31, 3538-3550 e3535.

Godfray, H.C., Beddington, J.R., Crute, I.R., Haddad, L., Lawrence, D., Muir, J.F., Pretty, J., Robinson, S., Thomas, S.M.,Toulmin, C., 2010. Food security: The challenge of feeding 9 billion people. Science 327, 812-818.

Guo, T., Yu, X., Li, X., Zhang, H., Zhu, C., Flint-Garcia, S., McMullen, M.D., Holland, J.B., Szalma, S.J., Wisser, R.J., et al., 2019. Optimal designs for genomic selection in hybrid crops. Mol. Plant 12, 390-401.

Han, C., Wang, L., Lyu, J., Shi, W., Yao, L., Fan, M.,Bai, M.-Y., 2023. Brassinosteroid signaling and molecular crosstalk with nutrients in plants. J. Genet. Genomics 50, 541-553.

Han, Y., Zhao, X., Liu, D., Li, Y., Lightfoot, D.A., Yang, Z., Zhao, L., et al., 2016. Domestication footprints anchor genomic regions of agronomic importance in soybeans. New Phytol 209, 871–884.

Hartwig, E.E.,Kiihl, R.A.S., 1979. Identification and utilization of a delayed flowering character in soybeans for short-day conditions. Field Crops Research 2, 145-151.

Hassan, S.,Mathesius, U., 2012. The role of flavonoids in root-rhizosphere signalling: Opportunities and challenges for improving plant-microbe interactions. J Exp Bot 63, 3429-3444.

Hayashi, M., Shiro, S., Kanamori, H., Mori-Hosokawa, S., Sasaki-Yamagata, H., Sayama, T., Nishioka, M., Takahashi, M., Ishimoto, M., Katayose, Y., et al., 2014. A thaumatin-like protein, rj4, controls nodule symbiotic specificity in soybean. Plant Cell Physiol 55, 1679-1689.

He, C., Gao, H., Wang, H., Guo, Y., He, M., Peng, Y.,Wang, X., 2021. Gsk3-mediated stress signaling inhibits legume-rhizobium symbiosis by phosphorylating gmnsp1 in soybean. Mol Plant 14, 488-502.

Heydarian, Z., Sasidharan, R., Cox, M.C., Pierik, R., Voesenek, L.A.,Peeters, A.J., 2010. A kinetic analysis of hyponastic growth and petiole elongation upon ethylene exposure in rumex palustris. Ann Bot 106, 429-435.

Hirsch, S., Kim, J., Munoz, A., Heckmann, A.B., Downie, J.A.,Oldroyd, G.E., 2009. Gras proteins form a DNA binding complex to induce gene expression during nodulation signaling in medicago truncatula. Plant Cell 21, 545-557.

Indrasumunar, A.,Gresshoff, P.M., 2010. Duplicated nod-factor receptor 5 (nfr5) genes are mutated in soybean. Plant Signal Behav 5, 535-536.

Indrasumunar, A., Kereszt, A., Searle, I., Miyagi, M., Li, D., Nguyen, C.D., Men, A., Carroll, B.J.,Gresshoff, P.M., 2010. Inactivation of duplicated nod factor receptor 5 (nfr5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (glycine max l. Merr.). Plant Cell Physiol 51, 201-214.

Indrasumunar, A., Searle, I., Lin, M.H., Kereszt, A., Men, A., Carroll, B.J.,Gresshoff, P.M., 2011. Nodulation factor receptor kinase 1alpha controls nodule organ number in soybean (glycine max l. Merr). Plant J 65, 39-50.

Jeong, N., Moon, J.K., Kim, H.S., Kim, C.G.,Jeong, S.C., 2011. Fine genetic mapping of the genomic region controlling leaflet shape and number of seeds per pod in the soybean. Theor Appl Genet 122, 865-874.

Jeong, N., Suh, S.J., Kim, M.H., Lee, S., Moon, J.K., Kim, H.S.,Jeong, S.C., 2012. Ln is a key regulator of leaflet shape and number of seeds per pod in soybean. Plant Cell 24, 4807-4818.

Jeong, S.C., Kim, J.H.,Bae, D.N., 2017. Genetic analysis of the lf1 gene that controls leaflet number in soybean. Theor Appl Genet 130, 1685-1692.

Ji, H., Xiao, R., Lyu, X., Chen, J., Zhang, X., Wang, Z., Deng, Z., Wang, Y., Wang, H., Li, R., et al., 2022. Differential light-dependent regulation of soybean nodulation by papilionoid-specific hy5 homologs. Curr Biol 32, 783-795 e785.

Jiang, B., Nan, H., Gao, Y., Tang, L., Yue, Y., Lu, S., Ma, L., Cao, D., Sun, S., Wang, J., et al., 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, e106042.

Jin, D., Meng, X., Wang, Y., Wang, J., Zhao, Y.,Chen, M., 2018. Computational investigation of small rnas in the establishment of root nodules and arbuscular mycorrhiza in leguminous plants. Sci China Life Sci 61, 706-717.

Kajiya-Kanegae, H., Nagasaki, H., Kaga, A., Hirano, K., Ogiso-Tanaka, E., Matsuoka, M., Ishimori, M., et al., 2021. Whole-genome sequence diversity and association analysis of 198 soybean accessions in mini-core collections. DNA Res 28, dsaa032.

Kim, Y.K., Kim, S., Um, J.H., Kim, K., Choi, S.K., Um, B.H., Kang, S.W., Kim, J.W., Takaichi, S., Song, S.B., et al., 2013. Functional implication of beta-carotene hydroxylases in soybean nodulation. Plant Physiol 162, 1420-1433.

Kong, F., Liu, B., Xia, Z., Sato, S., Kim, B.M., Watanabe, S., Yamada, T., Tabata, S., Kanazawa, A., Harada, K., et al., 2010. Two coordinately regulated homologs of flowering locus t are involved in the control of photoperiodic flowering in soybean. Plant Physiol 154, 1220-1231.

Kong, F., Nan, H., Cao, D., Li, Y., Wu, F., Wang, J., Lu, S., Yuan, X., Cober, E.R., Abe, J., et al., 2014. A new dominant gene e9 conditions early flowering and maturity in soybean. Crop Science 54, 2529-2535.

Kim, M.Y., Lee, S., Van, K., Kim, T.H., Jeong, S.C., Choi, I.Y., Kim, D.S., et al., 2010. Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc. Natl Acad. Sci. USA 107, 22032–22037.

Kong, Y., Han, L., Liu, X., Wang, H., Wen, L., Yu, X., Xu, X., Kong, F., Fu, C., Mysore, K.S., et al., 2020. The nodulation and nyctinastic leaf movement is orchestrated by clock gene lhy in medicago truncatula. J Integr Plant Biol 62, 1880-1895.

Koornneef, M.,Veen, J.H.v.d., 1980. Induction and analysis of gibbereuin sensitive mutants in arabidopsis thaliana (l.) heynh. Theoretical and applied genetics 58, 257-263.

Kou, K., Yang, H., Li, H., Fang, C., Chen, L., Yue, L., Nan, H., Kong, L., Li, X., Wang, F., et al., 2022. A functionally divergent soc1 homolog improves soybean yield and latitudinal adaptation. Curr Biol 32, 1728-1742 e1726.

Kouchi, H., Shimomura, K., Hata, S., Hirota, A., Wu, G.J., Kumagai, H., Tajima, S., Suganuma, N., Suzuki, A., Aoki, T., et al., 2004. Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, lotus japonicus. DNA Res 11, 263-274.

Lam, H.M., Xu, X., Liu, X., Chen, W., Yang, G., Wong, F.L., Li, M.W., et al., 2010. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42, 1053–1059.

Lamlom, S.F., Zhang, Y., Su, B., Wu, H., Zhang, X., Fu, J., Zhang, B.,Qiu, L.-J., 2020. Map-based cloning of a novel qtl qbn-1 influencing branch number in soybean [glycine max (l.) merr.]. The Crop Journal 8, 793-801.

Laporte, P., Lepage, A., Fournier, J., Catrice, O., Moreau, S., Jardinaud, M.F., Mun, J.H., Larrainzar, E., Cook, D.R., Gamas, P., et al., 2014. The ccaat box-binding transcription factor nf-ya1 controls rhizobial infection. J Exp Bot 65, 481-494.

Li, Fang C., Yang, Y., Lv, T., Su, T., Chen, L., Nan, H., Li, S., Zhao, X., Lu, S., et al., 2021a. Overcoming the genetic compensation response of soybean florigens to improve adaptation and yield at low latitudes. Curr Biol 31, 3755-3767 e3754.

Li, C., Li, Y.H., Li, Y., Lu, H., Hong, H., Tian, Y., Li, H., Zhao, T., Zhou, X., Liu, J., et al., 2020a. A domestication-associated gene gmprr3b regulates the circadian clock and flowering time in soybean. Mol Plant 13, 745-759.

Li, H., Du, H., He, M., Wang, J., Wang, F., Yuan, W., Huang, Z., Cheng, Q., Gou, C., Chen, Z., et al., 2023. Natural variation of fkf1 controls flowering and adaptation during soybean domestication and improvement. New Phytol 238, 1671-1684.

Li, X., Wu, P., Lu, Y., Guo, S., Zhong, Z., Shen, R.,Xie, Q., 2020b. Synergistic interaction of phytohormones in determining leaf angle in crops. Int J Mol Sci 21.

Li, X., Zhou, H., Cheng, L., Ma, N., Cui, B., Wang, W., Zhong, Y.,Liao, H., 2022. Shoot-to-root translocated gmnn1/ft2a triggers nodulation and regulates soybean nitrogen nutrition. PLoS Biol 20, e3001739.

Li, Y., Hou, Z., Li, W., Li, H., Lu, S., Gan, Z., Du, H., Li, T., Zhang, Y., Kong, F., et al., 2021b. The legume-specific transcription factor e1 controls leaf morphology in soybean. BMC Plant Biol 21, 531.

Li, Y.H., Li, W., Zhang, C., Yang, L., Chang, R.Z., Gaut, B.S.,Qiu, L.J., 2010. Genetic diversity in domesticated soybean (glycine max) and its wild progenitor (glycine soja) for simple sequence repeat and single-nucleotide polymorphism loci. New Phytol 188, 242-253.

Li, Z., Cheng, Q., Gan, Z., Hou, Z., Zhang, Y., Li, Y., Li, H., Nan, H., Yang, C., Chen, L., et al., 2021c. Multiplex crispr/cas9-mediated knockout of soybean lnk2 advances flowering time. The Crop Journal 9, 767-776.

Li, Z.F., Guo, Y., Ou, L., Hong, H., Wang, J., Liu, Z.X., Guo, B., Zhang, L.,Qiu, L., 2018. Identification of the dwarf gene gmdw1 in soybean (glycine max l.) by combining mapping-by-sequencing and linkage analysis. Theor Appl Genet 131, 1001-1016.

Li, Y.H., Zhou, G., Ma, J., Jiang, W., Jin, L.G., Zhang, Z., Guo, Y., et al., 2014b. De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat. Biotechnol. 32, 1045–1052.

Liang, Q., Chen, L., Yang, X., Yang, H., Liu, S., Kou, K., Fan, L., Zhang, Z., Duan, Z., Yuan, Y., et al., 2022. Natural variation of dt2 determines branching in soybean. Nat Commun 13, 6429.

Lillo, C., Lea, U.S.,Ruoff, P., 2008. Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ 31, 587-601.

Lim, C.W., Lee, Y.W.,Hwang, C.H., 2011. Soybean nodule-enhanced cle peptides in roots act as signals in gmnark-mediated nodulation suppression. Plant Cell Physiol 52, 1613-1627.

Lim, C.W., Lee, Y.W., Lee, S.C.,Hwang, C.H., 2014. Nitrate inhibits soybean nodulation by regulating expression of cle genes. Plant Sci 229, 1-9.

Lin, J.S., Li, X., Luo, Z., Mysore, K.S., Wen, J.,Xie, F., 2018. Nin interacts with nlps to mediate nitrate inhibition of nodulation in medicago truncatula. Nat Plants 4, 942-952.

Lin, X., Dong, L., Tang, Y., Li, H., Cheng, Q., Li, H., Zhang, T., Ma, L., Xiang, H., Chen, L., et al., 2022. Novel and multifaceted regulations of photoperiodic flowering by phytochrome a in soybean. Proc Natl Acad Sci U S A 119, e2208708119.

Lin, X., Liu, B., Weller, J.L., Abe, J.,Kong, F., 2021. Molecular mechanisms for the photoperiodic regulation of flowering in soybean. J Integr Plant Biol 63, 981-994.

Liu, Li H., Gou, Z., Zhang, Y., Wang, X., Ren, H., Wen, Z., Kang, B.K., Li, Y., Yu, L., et al., 2020a. Genome-wide association study of soybean seed germination under drought stress. Mol Genet Genomics 295, 661-673.

Liu, Zhang, M., Feng, F.,Tian, Z., 2020b. Toward a "green revolution" for soybean. Mol Plant 13, 688-697.

Liu, B., Kanazawa, A., Matsumura, H., Takahashi, R., Harada, K.,Abe, J., 2008. Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome a gene. Genetics 180, 995-1007.

Liu, B., Watanabe, S., Uchiyama, T., Kong, F., Kanazawa, A., Xia, Z., Nagamatsu, A., Arai, M., Yamada, T., Kitamura, K., et al., 2010. The soybean stem growth habit gene dt1 is an ortholog of arabidopsis terminal flower1. Plant Physiol 153, 198-210.

Liu, C.W., Murray, J.D., 2016. The role of flavonoids in nodulation host-range specificity: An update. Plants (Basel) 5.

Liu, L., Song, W., Wang, L., Sun, X., Qi, Y., Wu, T., Sun, S., Jiang, B., Wu, C., Hou, W., et al., 2020c. Allele combinations of maturity genes e1-e4 affect adaptation of soybean to diverse geographic regions and farming systems in china. PLoS One 15, e0235397.

Liu, X., Hu, B.,Chu, C., 2022. Nitrogen assimilation in plants: Current status and future prospects. J Genet Genomics 49, 394-404.

Liu, Y., Du, H., Li, P., Shen, Y., Peng, H., Liu, S., Zhou, G.A., Zhang, H., Liu, Z., Shi, M., et al., 2020d. Pan-genome of wild and cultivated soybeans. Cell 182, 162-176 e113.

Liu, Y., Zhang, D., Ping, J., Li, S., Chen, Z.,Ma, J., 2016. Innovation of a regulatory mechanism modulating semi-determinate stem growth through artificial selection in soybean. PLoS Genet 12, e1005818.

Liu, Z., Kong, X., Long, Y., Liu, S., Zhang, H., Jia, J., Cui, W., Zhang, Z., Song, X., Qiu, L., et al., 2023. Integrated single-nucleus and spatial transcriptomics captures transitional states in soybean nodule maturation. Nat Plants 9, 515-524.

Lu, M., Cheng, Z., Zhang, X.M., Huang, P., Fan, C., Yu, G., Chen, F., Xu, K., Chen, Q., Miao, Y., et al., 2020a. Spatial divergence of phr-pht1 modules maintains phosphorus homeostasis in soybean nodules. Plant Physiol 184, 236-250.

Lu, S., Dong, L., Fang, C., Liu, S., Kong, L., Cheng, Q., Chen, L., Su, T., Nan, H., Zhang, D., et al., 2020b. Stepwise selection on homeologous prr genes controlling flowering and maturity during soybean domestication. Nat Genet 52, 428-436.

Lu, S., Zhao, X., Hu, Y., Liu, S., Nan, H., Li, X., Fang, C., Cao, D., Shi, X., Kong, L., et al., 2017. Natural variation at the soybean j locus improves adaptation to the tropics and enhances yield. Nat Genet 49, 773-779.

Luo, L., Zhang, Y., Xu, G.,Takahashi, H., 2020. How does nitrogen shape plant architecture? Journal of Experimental Botany 71, 4415-4427.

Luo, Y., Liu, W., Sun, J., Zhang, Z.-R.,Yang, W.-C., 2023. Quantitative proteomics reveals key pathways in the symbiotic interface and the likely extracellular property of soybean symbiosome. J. Genet. Genomics 50, 7-19.

Magori, S.,Kawaguchi, M., 2009. Long-distance control of nodulation: Molecules and models. Mol Cells 27, 129-134.

Maj, D., Wielbo, J., Marek-Kozaczuk, M.,Skorupska, A., 2010. Response to flavonoids as a factor influencing competitiveness and symbiotic activity of rhizobium leguminosarum. Microbiological Research 165, 50-60.

McBlain, B.A.,Bernard, R.L., 1987. A new gene affecting the time of__flowering and maturity in soybeans. J Hered 78, 60-162.

Mueller, N.D., Gerber, J.S., Johnston, M., Ray, D.K., Ramankutty, N.,Foley, J.A., 2012. Closing yield gaps through nutrient and water management. Nature 490, 254-257.

Murakami, E., Cheng, J., Gysel, K., Bozsoki, Z., Kawaharada, Y., Hjuler, C.T., Sorensen, K.K., Tao, K., Kelly, S., Venice, F., et al., 2018. Epidermal lysm receptor ensures robust symbiotic signalling in lotus japonicus. Elife 7.

Nahar, K., Hasanuzzaman, M.,Fujita, M. 2016. Heat stress responses and thermotolerance in soybean, Abiotic and biotic stresses in soybean production, pp. 261-284.

Nizampatnam, N.R., Schreier, S.J., Damodaran, S., Adhikari, S.,Subramanian, S., 2015. Microrna160 dictates stage-specific auxin and cytokinin sensitivities and directs soybean nodule development. Plant J 84, 140-153.

Peng, J., Richards, D.E., Hartley, N.M., Murphy, G.P., Devos, K.M., Flintham, J.E., Beales, J., Fish, L.J., Worland, A.J., Pelica, F., et al., 1999. ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400, 256-261.

Peng, S., Huang, J., Sheehy, J.E., Laza, R.C., Visperas, R.M., Zhong, X., Centeno, G.S., Khush, G.S.,Cassman, K.G., 2004. Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci U S A 101, 9971-9975.

Penmetsa, R.V.,Cook, D.R., 1997. A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527-530.

Ping, J., Liu, Y., Sun, L., Zhao, M., Li, Y., She, M., Sui, Y., Lin, F., Liu, X., Tang, Z., et al., 2014. Dt2 is a gain-of-function mads-domain factor gene that specifies semideterminacy in soybean. Plant Cell 26, 2831-2842.

Ping, J., Liu, Y., Sun, L., Zhao, M., Li, Y., She, M., Sui, Y., Lin, F., Liu, X., Tang, Z., et al., 2014. Dt2 is a.

Qi, X., Li, M.W., Xie, M., Liu, X., Ni, M., Shao, G., Song, C., Kay-Yuen Yim, A., Tao, Y., Wong, F.L., et al., 2014. Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Commun 5, 4340.

Qin, C., Li, H., Zhang, S., Lin, X., Jia, Z., Zhao, F., Wei, X., Jiao, Y., Li, Z., Niu, Z., et al., 2023. Gmeid1 modulates light signaling through the evening complex to control flowering time and yield in soybean. Proc Natl Acad Sci U S A 120, e2212468120.

Qiu, J., Wang, Y., Wu, S., Wang, Y.Y., Ye, C.Y., Bai, X., Li, Z., et al., 2014. Genome re-sequencing of semi-wild soybean reveals a complex Soja population structure and deep introgression. PLoS One 9, e108479.

Ray, J.D., Hinson, K., Mankono, J.E.B., Malo, M.F., 1995. Genetic control of a long-juvenile trait in soybean. Crop Science 35, 1001-1006.

Reid, D.E., Ferguson, B.J., Hayashi, S., Lin, Y.H.,Gresshoff, P.M., 2011. Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108, 789-795.

Riedelsheimer, C., Czedik-Eysenberg, A., Grieder, C., Lisec, J., Technow, F., Sulpice, R., Altmann, T., Stitt, M., Willmitzer, L.,Melchinger, A.E., 2012. Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat Genet 44, 217-220.

Roy, S., Liu, W., Nandety, R.S., Crook, A., Mysore, K.S., Pislariu, C.I., Frugoli, J., Dickstein, R.,Udvardi, M.K., 2020. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell 32, 15-41.

Sa, T.M.,Israel, D.W., 1991. Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97, 928-935.

Samanfar, B., Molnar, S.J., Charette, M., Schoenrock, A., Dehne, F., Golshani, A., Belzile, F.,Cober, E.R., 2017. Mapping and identification of a potential candidate gene for a novel maturity locus, e10, in soybean. Theor Appl Genet 130, 377-390.

Sayama, T., Hwang, T.-Y., Yamazaki, H., Yamaguchi, N., Komatsu, K., Takahashi, M., Suzuki, C., Miyoshi, T., Tanaka, Y., Xia, Z., et al., 2010. Mapping and comparison of quantitative trait loci for soybean branching phenotype in two locations. Breeding Science 60, 380-389.

Sayama, T., Tanabata, T., Saruta, M., Yamada, T., Anai, T., Kaga, A.,Ishimoto, M., 2017. Confirmation of the pleiotropic control of leaflet shape and number of seeds per pod by the ln gene in induced soybean mutants. Breed Sci 67, 363-369.

Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., et al., 2010. Genome sequence of the palaeopolyploid soybean. Nature 463, 178-183.

Schulze, J., Temple, G., Temple, S.J., Beschow, H.,Vance, C.P., 2006. Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98, 731-740.

Searle, I.R., Men, A.E., Laniya, T.S., Buzas, D.M., Iturbe-Ormaetxe, I., Carroll, B.J.,Gresshoff, P.M., 2003. Long-distance signaling in nodulation directed by a clavata1-like receptor kinase. Science 299, 109-112.

Sedivy, E.J., Wu, F.,Hanzawa, Y., 2017. Soybean domestication: The origin, genetic architecture and molecular bases. New Phytol 214, 539-553.

Shen, Y., Du, H., Liu, Y., Ni, L., Wang, Z., Liang, C., Tian, Z., 2019. Update soybean Zhonghuang 13 genome to a golden reference. Sci. China Life. Sci. 62, 1257–1260.

Shen, Y., Liu, J., Geng, H., Zhang, J., Liu, Y., Zhang, H., Xing, S., Du, J., Ma, S.,Tian, Z., 2018. De novo assembly of a chinese soybean genome. Sci China Life Sci 61, 871-884.

Shim, S., Ha, J., Kim, M.Y., Choi, M.S., Kang, S.T., Jeong, S.C., Moon, J.K.,Lee, S.H., 2019. Gmbrc1 is a candidate gene for branching in soybean (glycine max (l.) merrill). Int J Mol Sci 20.

Shoemaker, R.C.,Specht, J.E., 1995. Integration of the soybean molecular and classical genetic linkage groups. Crop Science 35, 436-446.

Su, C., Wang, L.,Kong, F., 2023. Mir172: A messenger between nodulation and flowering. Trends Plant Sci.

Su, Q., Chen, L., Cai, Y., Chen, Y., Yuan, S., Li, M., Zhang, J., Sun, S., Han, T.,Hou, W., 2022. Functional redundancy of flowering locus t 3b in soybean flowering time regulation. Int J Mol Sci 23.

Subramanian, S., Stacey, G.,Yu, O., 2006. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and bradyrhizobium japonicum. Plant J 48, 261-273.

Sugawara, M., Takahashi, S., Umehara, Y., Iwano, H., Tsurumaru, H., Odake, H., Suzuki, Y., Kondo, H., Konno, Y., Yamakawa, T., et al., 2018. Variation in bradyrhizobial nopp effector determines symbiotic incompatibility with rj2-soybeans via effector-triggered immunity. Nat Commun 9, 3139.

Sun, S., Chen, D., Li, X., Qiao, S., Shi, C., Li, C., Shen, H.,Wang, X., 2015. Brassinosteroid signaling regulates leaf erectness in oryza sativa via the control of a specific u-type cyclin and cell proliferation. Dev Cell 34, 220-228.

Suzuki, A., Suriyagoda, L., Shigeyama, T., Tominaga, A., Sasaki, M., Hiratsuka, Y., Yoshinaga, A., Arima, S., Agarie, S., Sakai, T., et al., 2011. Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (r/fr) ratio through jasmonic acid (ja) signaling. Proc Natl Acad Sci U S A 108, 16837-16842.

Swarnalakshmi, K., Yadav, V., Tyagi, D., Dhar, D.W., Kannepalli, A.,Kumar, S., 2020. Significance of plant growth promoting rhizobacteria in grain legumes: Growth promotion and crop production. Plants (Basel) 9.

Takahashi, N., 1934. Linkage relation between the genes for the form of leaves and the number of seeds per pod of soybeans. Jpn J Genet 9, 208-225.

Tamagno, S., Sadras, V.O., Haegele, J.W., Armstrong, P.R.,Ciampitti, I.A., 2018. Interplay between nitrogen fertilizer and biological nitrogen fixation in soybean: Implications on seed yield and biomass allocation. Sci Rep 8, 17502.

Tang, F., Yang, S., Liu, J.,Zhu, H., 2016. Rj4, a gene controlling nodulation specificity in soybeans, encodes a thaumatin-like protein but not the one previously reported. Plant Physiol 170, 26-32.

Tang, Y., Lu, S., Fang, C., Liu, H., Dong, L., Li, H., Su, T., Li, S., Wang, L., Cheng, Q., et al., 2023. Diverse flowering responses subjecting to ambient high temperature in soybean under short-day conditions. Plant Biotechnol J 21, 782-791.

Tian, Z., Wang, X., Lee, R., Li, Y., Specht, J.E., Nelson, R.L., McClean, P.E., Qiu, L.,Ma, J., 2010. Artificial selection for determinate growth habit in soybean. Proc Natl Acad Sci U S A 107, 8563-8568.

Torkamaneh, D., Laroche, J., Tardivel, A., O’Donoughue, L., Cober, E., Rajcan, I., Belzile, F., 2018. Comprehensive description of genomewide nucleotide and structural variation in short-season soya bean. Plant Biotechnol. J. 16, 749–759.

Tsyganova, A.V., Brewin, N.J.,Tsyganov, V.E., 2021. Structure and development of the legume-rhizobial symbiotic interface in infection threads. Cells 10.

Turner, M., Nizampatnam, N.R., Baron, M., Coppin, S., Damodaran, S., Adhikari, S., Arunachalam, S.P., Yu, O.,Subramanian, S., 2013. Ectopic expression of mir160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol 162, 2042-20

Valliyodan, B, Cannon, SB, Bayer, PE, et al., 2019. Construction and comparison of three reference-quality genome assemblies for soybean. The Plant Journal : for Cell and Molecular Biology 100, 1066–1082.

Valliyodan, B., Dan, Q., Patil, G., Zeng, P., Huang, J., Dai, L., Chen, C., et al., 2016. Landscape of genomic diversity and trait discovery in soybean. Sci. Rep. 6, 23598.

Velandia, K., Reid, J.B.,Foo, E., 2022. Right time, right place: The dynamic role of hormones in rhizobial infection and nodulation of legumes. Plant Commun 3, 100327.

Vu, L.D., Xu, X., Gevaert, K.,De Smet, I., 2019. Developmental plasticity at high temperature. Plant Physiol 181, 399-411.

Wang, C., Li, M., Zhao, Y., Liang, N., Li, H., Li, P., Yang, L., Xu, M., Bian, X., Wang, M., et al., 2022. Short-root paralogs mediate feedforward regulation of d-type cyclin to promote nodule formation in soybean. Proc Natl Acad Sci U S A 119.

Wang, F., Nan, H., Chen, L., Fang, C., Zhang, H., Su, T., Li, S., Cheng, Q., Dong, L., Liu, B., et al., 2019a. A new dominant locus, e11, controls early flowering time and maturity in soybean. Molecular Breeding 39.

Wang, K., Abid, M.A., Rasheed, A., Crossa, J., Hearne, S.,Li, H., 2023a. Dnngp, a deep neural network-based method for genomic prediction using multi-omics data in plants. Molecular Plant 16, 279-293.

Wang, L., Li, H., He, M., Dong, L., Huang, Z., Chen, L., Nan, H., Kong, F., Liu, B.,Zhao, X., 2023b. Gigantea orthologs, e2 members, redundantly determine photoperiodic flowering and yield in soybean. J Integr Plant Biol 65, 188-202.

Wang, L., Sun, S., Wu, T., Liu, L., Sun, X., Cai, Y., Li, J., Jia, H., Yuan, S., Chen, L., et al., 2020a. Natural variation and crispr/cas9-mediated mutation in gmprr37 affect photoperiodic flowering and contribute to regional adaptation of soybean. Plant Biotechnol J 18, 1869-1881.

Wang, T., Guo, J., Peng, Y., Lyu, X., Liu, B., Sun, S.,Wang, X., 2021a. Light-induced mobile factors from shoots regulate rhizobium-triggered soybean root nodulation. Science 374, 65-71.

Wang, X., Li, M.W., Wong, F.L., Luk, C.Y., Chung, C.Y., Yung, W.S., Wang, Z., Xie, M., Song, S., Chung, G., et al., 2021b. Increased copy number of gibberellin 2-oxidase 8 genes reduced trailing growth and shoot length during soybean domestication. Plant J 107, 1739-1755.

Wang, Y., Li, K., Chen, L., Zou, Y., Liu, H., Tian, Y., Li, D., Wang, R., Zhao, F., Ferguson, B.J., et al., 2015. Microrna167-directed regulation of the auxin response factors gmarf8a and gmarf8b is required for soybean nodulation and lateral root development. Plant Physiol 168, 984-999.

Wang, Y., Wang, L., Zou, Y., Chen, L., Cai, Z., Zhang, S., Zhao, F., Tian, Y., Jiang, Q., Ferguson, B.J., et al., 2014. Soybean mir172c targets the repressive ap2 transcription factor nnc1 to activate enod40 expression and regulate nodule initiation. Plant Cell 26, 4782-4801.

Wang, Y., Xu, C., Sun, J., Dong, L., Li, M., Liu, Y., Wang, J., Zhang, X., Li, D., Sun, J., et al., 2021c. Gmrav confers ecological adaptation through photoperiod control of flowering time and maturity in soybean. Plant Physiol 187, 361-377.

Wang, Y., Yang, W., Zuo, Y., Zhu, L., Hastwell, A.H., Chen, L., Tian, Y., Su, C., Ferguson, B.J.,Li, X., 2019b. Gmyuc2a mediates auxin biosynthesis during root development and nodulation in soybean. J Exp Bot 70, 3165-3176.

Wang, Y., Yang, Z., Kong, Y., Li, X., Li, W., Du, H.,Zhang, C., 2020b. Gmpap12 is required for nodule development and nitrogen fixation under phosphorus starvation in soybean. Front Plant Sci 11, 450.

Watanabe, S., Hideshima, R., Xia, Z., Tsubokura, Y., Sato, S., Nakamoto, Y., Yamanaka, N., Takahashi, R., Ishimoto, M., Anai, T., et al., 2009. Map-based cloning of the gene associated with the soybean maturity locus e3. Genetics 182, 1251-1262.

Watanabe, S., Xia, Z., Hideshima, R., Tsubokura, Y., Sato, S., Yamanaka, N., Takahashi, R., Anai, T., Tabata, S., Kitamura, K., et al., 2011. A map-based cloning strategy employing a residual heterozygous line reveals that the gigantea gene is involved in soybean maturity and flowering. Genetics 188, 395-407.

Xia, Z., Watanabe, S., Yamada, T., Tsubokura, Y., Nakashima, H., Zhai, H., Anai, T., Sato, S., Yamazaki, T., Lu, S., et al., 2012. Positional cloning and characterization reveal the molecular basis for soybean maturity locus e1 that regulates photoperiodic flowering. Proc Natl Acad Sci U S A 109, E2155-2164.

Xie, M., Chung, C.Y., Li, M.W., Wong, F.L., Wang, X., Liu, A., Wang, Z., et al., 2019. A reference-grade wild soybean genome. Nat. Commun. 10, 1216.

Xing, X., Du, H., Yang, Z., Li, X., Kong, Y., Li, W.,Zhang, C., 2022. Gmspx8, a nodule-localized regulator confers nodule development and nitrogen fixation under phosphorus starvation in soybean. BMC Plant Biol 22, 161.

Xu, M., Yamagishi, N., Zhao, C., Takeshima, R., Kasai, M., Watanabe, S., Kanazawa, A., Yoshikawa, N., Liu, B., Yamada, T., et al., 2015. The soybean-specific maturity gene e1 family of floral repressors controls night-break responses through down-regulation of flowering locus t orthologs. Plant Physiol 168, 1735-1746.

Xu, Z., Wang, R., Kong, K., Begum, N., Almakas, A., Liu, J., Li, H., Liu, B., Zhao, T.,Zhao, T., 2022. An apetala2/ethylene responsive factor transcription factor gmcrf4a regulates plant height and auxin biosynthesis in soybean. Front Plant Sci 13, 983650.

Xue, R.,Zhang, B., 2007. Increased endogenous methyl jasmonate altered leaf and root development in transgenic soybean plants. J. Genet. Genomics 34, 339-346.

Yan, Q., Wang, L.,Li, X., 2018. Gmbehl1, a bes1/bzr1 family protein, negatively regulates soybean nodulation. Sci Rep 8, 7614.

Yang, Zheng, J., Zhou, H., Chen, S., Gao, Z., Yang, Y., Li, X.,Liao, H., 2021a. The soybean beta-expansin gene gmins1 contributes to nodule development in response to phosphate starvation. Physiol Plant 172, 2034-2047.

Yang, H., Xue, Q., Zhang, Z., Du, J., Yu, D.,Huang, F., 2018. Gmmyb181, a soybean r2r3-myb protein, increases branch number in transgenic arabidopsis. Front Plant Sci 9, 1027.

Yang, S., Tang, F., Gao, M., Krishnan, H.B.,Zhu, H., 2010. R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc Natl Acad Sci U S A 107, 18735-18740.

Yang, Y., Lei, Y., Bai, Z., Wei, B., Zhang, H.,Zhang, R., 2021b. Physical mapping and candidate gene prediction of branch number on the main stem in soybean [glycine max (l.) merr.]. Genetic Resources and Crop Evolution 68, 2907-2921.

Yao, Z., Tian, J.,Liao, H., 2014. Comparative characterization of gmspx members reveals that gmspx3 is involved in phosphate homeostasis in soybean. Ann Bot 114, 477-488.

Yuan, S., Wang, Y., Wang, J., Zhang, C., Zhang, L., Jiang, B., Wu, T., Chen, L., Xu, X., Cai, Y., et al., 2022. Gmft3a fine-tunes flowering time and improves adaptation of soybean to higher latitudes. Front Plant Sci 13, 929747.

Yue, L., Li, X., Fang, C., Chen, L., Yang, H., Yang, J., Chen, Z., Nan, H., Chen, L., Zhang, Y., et al., 2021. Ft5a interferes with the dt1-ap1 feedback loop to control flowering time and shoot determinacy in soybean. J Integr Plant Biol 63, 1004-1020.

Yun, J., Wang, C., Zhang, F., Chen, L., Sun, Z., Cai, Y., Luo, Y., Liao, J., Wang, Y., Cha, Y., et al., 2023. A nitrogen fixing symbiosis-specific pathway required for legume flowering. Sci Adv 9, eade1150.

Zhai, H., Wan, Z., Jiao, S., Zhou, J., Xu, K., Nan, H., Liu, Y., Xiong, S., Fan, R., Zhu, J., et al., 2022. Gmmde genes bridge the maturity gene e1 and florigens in photoperiodic regulation of flowering in soybean. Plant Physiol 189, 1021-1036.

Zhang, B., Wang, M., Sun, Y., Zhao, P., Liu, C., Qing, K., Hu, X., Zhong, Z., Cheng, J., Wang, H., et al., 2021. Glycine max nnl1 restricts symbiotic compatibility with widely distributed bradyrhizobia via root hair infection. Nat Plants 7, 73-86.

Zhang, J., Zhou, X., Xu, Y., Yao, M., Xie, F., Gai, J., Li, Y.,Yang, S., 2016. Soybean spx1 is an important component of the response to phosphate deficiency for phosphorus homeostasis. Plant Sci 248, 82-91.

Zhang, M., Liu, S., Wang, Z., Yuan, Y., Zhang, Z., Liang, Q., Yang, X., Duan, Z., Liu, Y., Kong, F., et al., 2022a. Progress in soybean functional genomics over the past decade. Plant Biotechnol J 20, 256-282.

Zhang, Y., Cheng, Q., Liao, C., Li, L., Gou, C., Chen, Z., Wang, Y., Liu, B., Kong, F.,Chen, L., 2022b. Gmtoc1b inhibits nodulation by repressing gmnin2a and gmenod40-1 in soybean. Front Plant Sci 13, 1052017.

Zhang, Z., Gao, L., Ke, M., Gao, Z., Tu, T., Huang, L., Chen, J., Guan, Y., Huang, X.,Chen, X., 2022c. Gmpin1-mediated auxin asymmetry regulates leaf petiole angle and plant architecture in soybean. J Integr Plant Biol 64, 1325-1338.

Zhao, C., Liu, B., Piao, S., Wang, X., Lobell, D.B., Huang, Y., Huang, M., Yao, Y., Bassu, S., Ciais, P., et al., 2017. Temperature increase reduces global yields of major crops in four independent estimates. Proc Natl Acad Sci U S A 114, 9326-9331.

Zhou, Z., Jiang, Y., Wang, Z., Gou, Z., Lyu, J., Li, W., Yu, Y., Shu, L., Zhao, Y., Ma, Y., et al., 2015. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 33, 408-414.

Zhou, Z., Jiang, Y., Wang, Z., Gou, Z., Lyu, J., Li, W., Yu, Y., Shu, L., Zhao, Y., Ma, Y., et al., 2016. Erratum: Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 34, 441.

Zhu, J., Takeshima, R., Harigai, K., Xu, M., Kong, F., Liu, B., Kanazawa, A., Yamada, T.,Abe, J., 2018. Loss of function of the e1-like-b gene associates with early flowering under long-day conditions in soybean. Front Plant Sci 9, 1867.

Zhuang, Q., Xue, Y., Yao, Z., Zhu, S., Liang, C., Liao, H.,Tian, J., 2021. Phosphate starvation responsive gmspx5 mediates nodule growth through interaction with gmnf-yc4 in soybean (glycine max). Plant J 108, 1422-1438.

Zipfel, C.,Oldroyd, G.E., 2017. Plant signalling in symbiosis and immunity. Nature 543, 328-336.

Zuanazzi, J.A.S., Clergeot, P.H., Quirion, J.-C., Husson, H.-P., Kondorosi, A.,Ratet, P., 1998. Production of sinorhizobium meliloti nod gene activator and repressor flavonoids from medicago sativa roots. Molecular Plant-Microbe Interactions^® 11, 784-794.55.

Relative Articles

Supplements(0)

Cited By

Proportional views