Abstract
Soybean (Glycine max (L.) Merrill) is an important legume crop worldwide. Plant height (PH) is a quantitative trait that is closely related to node number (NN) and internode length (IL) on the main stem, which together affect soybean yield. To identify candidate genes controlling these three traits in soybean, we examined a recombinant inbred line (RIL) population derived from a cross between two soybean varieties with semi-determinate stems (Dt1Dt1Dt2Dt2), JKK378 and HXW. A quantitative trait locus (QTL) named qPH18 was identified that simultaneously controls PH, NN, and IL; this region harbors the semi-determinant gene Dt2. Sequencing of the Dt2 promoter from JKK378 identified three polymorphisms relative to HXW, including two single nucleotide polymorphism (SNPs) and an 18-bp insertion/deletion polymorphism (Indel). Dt2 expression was lower in the qPH18JKK378 group than in the qPH18HXW group, whereas the expression level of the downstream gene Dt1 showed the opposite tendency. A transient transfection assay confirmed that Dt2 promoter activity is lower in JKK378 compared to HXW. We propose that the polymorphisms in the dominant Dt2 promoter underlie the differences in Dt2 expression and its downstream gene Dt1 in the two parents, thereby affecting PH, NN, IL, and grain weight per plant without altering stem growth habit. Compared to the PH18HXW allele, the qPH18JKK378 allele suppresses Dt2 expression, which releases the inhibition of Dt1 expression, thus enhancing NN and grain yield. Our findings shed light on the mechanism underlying NN and PH in soybean and provide a molecular marker to facilitate breeding.
Similar content being viewed by others
Data availability
Not applicable.
References
Allen LH, Zhang L, Boote KJ, Hauser BA (2018) Elevated temperature intensity, timing, and duration of exposure affect soybean internode elongation, mainstem node number, and pod number per plant. Crop J 6:148–161. https://doi.org/10.1016/j.cj.2017.10.005
Ashikari M, Sasaki A, Ueguchi-Tanaka M et al (2002) Loss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), Led to the Rice “Green Revolution.” Breed Sci 52:143–150
Assefa T, Otyama PI, Brown AV et al (2019) Genome-wide associations and epistatic interactions for internode number, plant height, seed weight and seed yield in soybean. BMC Genomics 20:527
Bernard RL (1971) Two major genes for time of flowering and maturity in soybeans1. Crop Sci 11:242–244. https://doi.org/10.2135/cropsci1971.0011183X001100020022x
Bernard RL (1972) Two genes affecting stem termination in soybeans1. Crop Sci 12:235–239
Chang F, Guo C, Sun F et al (2018) Genome-wide association studies for dynamic plant height and number of nodes on the main stem in summer sowing soybeans. Front Plant Sci 9:1184. https://doi.org/10.3389/fpls.2018.01184
Chen L, Nan H, Kong L et al (2020) Soybean AP1 homologs control flowering time and plant height. J Integr Plant Biol 62(12):1868–1879
Cheng W, Liu F, Li M et al (2015) Variation detection based on next-generation sequencing of type Chinese 1 strains of Toxoplasma gondii with different virulence from China. BMC Genomics 16:888. https://doi.org/10.1186/s12864-015-2106-z
Fang C, Chin L, Nan H (2019) Rapid identification of consistent novel QTLs underlying long-juvenile trait in soybean by multiple genetic populations and genotyping-by-sequencing. Mol Breed 39:80
Guzman PS, Diers BW, Neece DJ et al (2007) QTL associated with yield in three backcross-derived populations of soybean. Crop Sci 47:111. https://doi.org/10.2135/cropsci2006.01.0003
Heatherly L, Smith J (2004) Effect of soybean stem growth habit on height and node number after beginning bloom in the midsouthern USA. Crop Sci 44:1855–1858. https://doi.org/10.2135/cropsci2004.1855
Hedden P (2003) The genes of the green revolution. Trends Genet 19:5–9
Ivanova A, Law SR, Narsai R et al (2014) A functional antagonistic relationship between auxin and mitochondrial retrograde signaling regulates alternative oxidase1a expression in arabidopsis. Plant Physiol 165:1233
Kabelka EA, Diers BW, Fehr WR et al (2004) Putative alleles for increased yield from soybean plant introductions. Crop Sci 44:784–791. https://doi.org/10.2135/cropsci2004.0784
Kasajima I, Ohkama-Ohtsu N et al (2006) The BIG gene is involved in regulation of sulfur deficiency-responsive genes in Arabidopsis thaliana. Physiol Plant 129(2):351–363
Kim KS, Diers BW, Hyten DL et al (2012) Identification of positive yield QTL alleles from exotic soybean germplasm in two backcross populations. Theor Appl Genet 125:1353–1369. https://doi.org/10.1007/s00122-012-1944-1
Kong L, Lu S, Wang Y et al (2018a) Quantitative trait locus mapping of flowering time and maturity in soybean using next-generation sequencing-based analysis. Front Plant Sci 9:1–20. https://doi.org/10.3389/fpls.2018.00995
Kong L, Sijia L, Yanping W et al (2018) Quantitative trait locus mapping of flowering time and maturity in soybean using next-generation sequencing-based analysis. Frontiers in Plant Science 9:995
Li H (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics (Oxford, England) 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Liu B, Watanabe S, Uchiyama T et al (2010) The soybean stem growth habit gene Dt1 is an ortholog of arabidopsis TERMINAL FLOWER1. Plant Physiol 153:198–210. https://doi.org/10.1104/pp.109.150607
Liu W, Kim MY, Van K et al (2011) QTL identification of yield-related traits and their association with flowering and maturity in soybean. J Crop Sci Biotechnol 14:65–70
Liu Y, Zhang D, Ping J et al (2016) Innovation of a regulatory mechanism modulating semi-determinate stem growth through artificial selection in soybean. PLoS Genet 12(1):e1005818. https://doi.org/10.1371/journal.pgen.1005818
Lu S, Dong L, Fang C et al (2020) Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication. Nat Genet 52:1–9. https://doi.org/10.1038/s41588-020-0604-7
Meng L, Huihui Li et al (2015) QTL IciMapping:Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. The Crop Journal (3):3269–283. https://doi.org/10.1016/j.cj.2015.01.001
Monna L, Noriyuki K, Rika Y et al (2002) Positional cloning of rice semidwarfing gene, sd-1: rice “green revolution gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9(1):11–17
Nobutoshi Y, Mitsuhiro S, Hidehiro F et al (2007) CRM1/BIG-mediated auxin action regulates arabidopsis inflorescence development. Plant Cell Physiol 48:1275–1290
Peng J, Richards DE, Hartley NM et al (1999) “Green revolution” genes encode mutant gibberellin response modulators. Nature 400:256–261
Ping J, Liu Y, Sun L et al (2014) Dt2 Is a gain-of-function MADS-domain factor gene that specifies Semideterminacy in Soybean. Plant Cell 26:2831–2842
Qi ZM, Wu Q, Han X et al (2011) Soybean oil content QTL mapping and integrating with meta-analysis method for mining genes. Euphytica 179:499–514. https://doi.org/10.1007/s10681-011-0386-1
Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. https://doi.org/10.1038/nature08670
Setiyono T, Weiss A, Specht J et al (2007) Understanding and modeling the effect of temperature and daylength on soybean phenology under high-yield conditions. Field Crop Res 100:257–271. https://doi.org/10.1016/j.fcr.2006.07.011
Song QX, Li QT et al (2013) Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants. J Exp Bot 64(14):4329–4341
Sun D, Li W, Zhang Z et al (2006) Quantitative trait loci analysis for the developmental behavior of Soybean (Glycine max L. Merr.). Theor Appl Genet 112:665–673. https://doi.org/10.1007/s00122-005-0169-y
Takeshima R, Nan H, Harigai K, Dong L (2019) Functional divergence between soybean flowering Locus T orthologues, FT2a and FT5a, in post-flowering stem growth. J Exp Bot 67:5247–5258
Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:164–164. https://doi.org/10.1093/nar/gkq603
Xu M, Xu Z, Liu B et al (2013) Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean. BMC Plant Biol 13:91
Zhou Z, Zhang C, Zhou Y et al (2016) Genetic dissection of maize plant architecture with an ultra-high density bin map based on recombinant inbred lines. BMC Genomics 17:1–15. https://doi.org/10.1186/s12864-016-2555-z
Zhuang X, Jiang J, Li J et al (2010) Over-expression of OsAGAP, an ARF-GAP, interferes with auxin influx, vesicle trafficking and root development. Plant J 48:581–591
Acknowledgements
We would like to acknowledge Mrs. Yafeng Liu for phenotyping and managing the field.
Funding
This work was supported by National Natural Science Foundation of China (31930083) and EUCLEG Horizon 2020 of European Union (No.727312). This work was also funded by the National Key Research and Development Program (Nos. 2017YFE0111000), National Natural Science Foundation of China (31701445, 31930083, 31725021, 31801384), the Major Program of Guangdong Basic and Applied Research (2019B030302006), and Open Project Foundation of National Key Laboratory for Crop Genetics and Germplasm Enhancement (ZKW201901).
Author information
Authors and Affiliations
Contributions
CF, FK, and BL designed the experiments. KK, TS, YW, HY, HD, MH, TL, LM, CL, CY, WS, LC, YL, and BY carried out the experiments. KK, LK, SL, LW, XZ, SL, BL, FK, and CF analyzed the data. KK, FK, BL, and CF wrote the paper.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kou, K., Su, T., Wang, Y. et al. Natural variation of the Dt2 promoter controls plant height and node number in semi-determinant soybean. Mol Breeding 41, 40 (2021). https://doi.org/10.1007/s11032-021-01235-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-021-01235-y