Identification of two quantitative genes controlling soybean flowering using bulked-segregant analysis and genetic mapping

Photoperiod responsiveness is important to soybean production potential and adaptation to local environments. Varieties from temperate regions generally mature early and exhibit extremely low yield when grown under inductive short-day (SD) conditions. The long-juvenile (LJ) trait is essentially a reduction and has been introduced into soybean cultivars to improve yield in tropical environments. In this study, we used next-generation sequencing (NGS)-based bulked segregant analysis (BSA) to simultaneously map qualitative genes controlling the LJ trait in soybean. We identified two genomic regions on scaffold_32 and chromosome 18 harboring loci LJ32 and LJ18, respectively. Further, we identified LJ32 on the 228.7-kb scaffold_32 as the soybean pseudo-response-regulator gene Tof11 and LJ18 on a 301-kb region of chromosome 18 as a novel PROTEIN FLOWERING LOCUS T-RELATED gene, Glyma.18G298800. Natural variants of both genes contribute to LJ trait regulation in tropical regions. The molecular identification and functional characterization of Tof11 and LJ18 will enhance understanding of the molecular mechanisms underlying the LJ trait and provide useful genetic resources for soybean molecular breeding in tropical regions.

[1]  Fanjiang Kong,et al.  The control of compound inflorescences: insights from grasses and legumes. , 2021, Trends in plant science.

[2]  Yang Tang,et al.  Parallel selection of distinct Tof5 alleles drove the adaptation of cultivated and wild soybean to high latitude. , 2021, Molecular plant.

[3]  J. Weller,et al.  Genetic basis and adaptation trajectory of soybean from its temperate origin to tropics , 2021, Nature Communications.

[4]  Yang Tang,et al.  Overcoming the genetic compensation response of soybean florigens to improve adaptation and yield at low latitudes , 2021, Current Biology.

[5]  Baohui Liu,et al.  Natural variation and artificial selection of photoperiodic flowering genes and their applications in crop adaptation , 2021, aBIOTECH.

[6]  J. Weller,et al.  A critical role of the soybean evening complex in the control of photoperiod sensitivity and adaptation , 2021, Proceedings of the National Academy of Sciences.

[7]  Xingliang Hou,et al.  FT5a interferes with the Dt1-AP1 feedback loop to control flowering time and shoot determinacy in soybean. , 2021, Journal of integrative plant biology.

[8]  Baohui Liu,et al.  A recent retrotransposon insertion of J caused E6 locus facilitating soybean adaptation into low latitude. , 2020, Journal of integrative plant biology.

[9]  J. Weller,et al.  Molecular mechanisms for the photoperiodic regulation of flowering in soybean. , 2020, Journal of integrative plant biology.

[10]  Baohui Liu,et al.  Identification of major QTLs for flowering and maturity in soybean by genotyping-by-sequencing analysis , 2020, Molecular Breeding.

[11]  Baohui Liu,et al.  Soybean AP1 homologs control flowering time and plant height. , 2020, Journal of integrative plant biology.

[12]  Qun Cheng,et al.  Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication , 2020, Nature Genetics.

[13]  Tingting Wu,et al.  Mutagenesis of GmFT2a and GmFT5a mediated by CRISPR/Cas9 contributes for expanding the regional adaptability of soybean , 2019, Plant biotechnology journal.

[14]  Yang Tang,et al.  Rapid identification of consistent novel QTLs underlying long-juvenile trait in soybean by multiple genetic populations and genotyping-by-sequencing , 2019, Molecular Breeding.

[15]  Baohui Liu,et al.  A new dominant locus, E11, controls early flowering time and maturity in soybean , 2019, Molecular Breeding.

[16]  Tingting Wu,et al.  Natural variations of FT family genes in soybean varieties covering a wide range of maturity groups , 2019, BMC Genomics.

[17]  Baohui Liu,et al.  Quantitative Trait Locus Mapping of Soybean Maturity Gene E6 , 2017 .

[18]  Dong Cao,et al.  Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield , 2017, Nature Genetics.

[19]  Ashkan Golshani,et al.  Mapping and identification of a potential candidate gene for a novel maturity locus, E10, in soybean , 2017, Theoretical and Applied Genetics.

[20]  Baohui Liu,et al.  Molecular mechanisms of flowering under long days and stem growth habit in soybean. , 2016, Journal of experimental botany.

[21]  Hao Cheng,et al.  Development and application of a novel genome-wide SNP array reveals domestication history in soybean , 2016, Scientific Reports.

[22]  Baohui Liu,et al.  A recessive allele for delayed flowering at the soybean maturity locus E9 is a leaky allele of FT2a, a FLOWERING LOCUS T ortholog , 2016, BMC Plant Biology.

[23]  Dongyuan Liu,et al.  Domestication footprints anchor genomic regions of agronomic importance in soybeans. , 2015, The New phytologist.

[24]  Wei Liu,et al.  A Robust CRISPR/Cas9 System for Convenient, High-Efficiency Multiplex Genome Editing in Monocot and Dicot Plants. , 2015, Molecular plant.

[25]  Xinyi Shi,et al.  QTL mapping for flowering time in different latitude in soybean , 2015, Euphytica.

[26]  Baohui Liu,et al.  A New Dominant Gene E9 Conditions Early Flowering and Maturity in Soybean , 2014 .

[27]  Y. Li,et al.  GmFT2a and GmFT5a Redundantly and Differentially Regulate Flowering through Interaction with and Upregulation of the bZIP Transcription Factor GmFDL19 in Soybean , 2014, PloS one.

[28]  H. Matsumura,et al.  MutMap-Gap: whole-genome resequencing of mutant F2 progeny bulk combined with de novo assembly of gap regions identifies the rice blast resistance gene Pii. , 2013, The New phytologist.

[29]  H. Matsumura,et al.  MutMap+: Genetic Mapping and Mutant Identification without Crossing in Rice , 2013, PloS one.

[30]  R. Terauchi,et al.  QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. , 2013, The Plant journal : for cell and molecular biology.

[31]  T. Yamazaki,et al.  Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering , 2012, Proceedings of the National Academy of Sciences.

[32]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[33]  Satoshi Natsume,et al.  Genome sequencing reveals agronomically important loci in rice using MutMap , 2012, Nature Biotechnology.

[34]  Fang Yang,et al.  grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses , 2011, Proceedings of the National Academy of Sciences.

[35]  S. Tabata,et al.  A Map-Based Cloning Strategy Employing a Residual Heterozygous Line Reveals that the GIGANTEA Gene Is Involved in Soybean Maturity and Flowering , 2011, Genetics.

[36]  Detlef Weigel,et al.  Fast-forward genetics enabled by new sequencing technologies. , 2011, Trends in plant science.

[37]  S. Tabata,et al.  Two Coordinately Regulated Homologs of FLOWERING LOCUS T Are Involved in the Control of Photoperiodic Flowering in Soybean1[W][OA] , 2010, Plant Physiology.

[38]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[39]  E. Cober,et al.  A New Locus for Early Maturity in Soybean , 2010 .

[40]  M. Morrison,et al.  Regulation of seed yield and agronomic characters by photoperiod sensitivity and growth habit genes in soybean , 2010, Theoretical and Applied Genetics.

[41]  S. Tabata,et al.  Map-Based Cloning of the Gene Associated With the Soybean Maturity Locus E3 , 2009, Genetics.

[42]  Baohui Liu,et al.  Genetic Redundancy in Soybean Photoresponses Associated With Duplication of the Phytochrome A Gene , 2008, Genetics.

[43]  M. Chapman,et al.  Crop evolution: from genetics to genomics. , 2007, Current opinion in genetics & development.

[44]  K. Chase,et al.  A Soybean Transcript Map: Gene Distribution, Haplotype and Single-Nucleotide Polymorphism Analysis , 2007, Genetics.

[45]  C. Vance,et al.  Legumes: Importance and Constraints to Greater Use , 2003, Plant Physiology.

[46]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[47]  E. Cober,et al.  Low R:FR light quality delays flowering of E7E7 soybean lines , 2001 .

[48]  E. Cober,et al.  A New Soybean Maturity and Photoperiod-Sensitivity Locus Linked to E1 and T , 2001 .

[49]  V. Carpentieri-Pipolo,et al.  Photoperiodism and Genetic Control of the Long Juvenile Period in Soybean: A Review , 2001 .

[50]  N. Vello,et al.  E6, a dominant gene conditioning early flowering and maturity in soybeans , 1999 .

[51]  J. Ray,et al.  Genetic control of a long-juvenile trait in soybean , 1995 .

[52]  R. Doerge,et al.  Empirical threshold values for quantitative trait mapping. , 1994, Genetics.

[53]  K. Lark,et al.  Determining the linkage of quantitative trait loci to RFLP markers using extreme phenotypes of recombinant inbreds of soybean (Glycine max L. Merr.) , 1993, Theoretical and Applied Genetics.

[54]  T. Sinclair,et al.  Soybean flowering in response to the long-juvenile trait , 1992 .

[55]  S. Tanksley,et al.  Isolation of molecular markers from specific chromosomal intervals using DNA pools from existing mapping populations. , 1991, Nucleic acids research.

[56]  R. Michelmore,et al.  Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[57]  R. L. Bernard,et al.  A new gene affecting the time of flowering and maturity in soybeans , 1987 .

[58]  F. P. Gardner,et al.  Daylength and Sowing Date Responses of Soybean Lines with “Juvenile” Trait 1 , 1987 .

[59]  R. Buzzell.  INHERITANCE OF A SOYBEAN FLOWERING RESPONSE TO FLUORESCENT-DAYLENGTH CONDITIONS , 1971 .

[60]  R. L. Bernard.  Two Major Genes for Time of Flowering and Maturity in Soybeans 1 , 1971 .

[61]  Tingting Wu,et al.  Functional diversification of Flowering Locus T homologs in soybean: GmFT1a and GmFT2a/5a have opposite roles in controlling flowering and maturation , 2017, The New phytologist.

[62]  B. Yi,et al.  Fine mapping of the recessive genic male-sterile gene (Bnms1) in Brassica napus L. , 2006, Theoretical and Applied Genetics.

[63]  J. V. Ooijen,et al.  Software for the mapping of quantitative trait loci in experimental populations , 2004 .

[64]  R. Voorrips.  MapChart: software for the graphical presentation of linkage maps and QTLs. , 2002, The Journal of heredity.

[65]  V. Carpentieri-Pipolo,et al.  Inheritance of a long juvenile period under short-day conditions in soybean , 2002 .

[66]  Thomas D. Schmittgen,et al.  Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 2 DD C T Method , 2022 .