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PMID: 27072125 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Molecular and geographic evolutionary support for the essential role of GIGANTEAa in soybean domestication of flowering time.

BMC evolutionary biology ·Vol. 16 ·2016-04-12 ·Pages 79

Wang Y, Gu Y, Gao H, Qiu L, Chang R, Chen S, He C

Abstract

Flowering time is a domestication trait of Glycine max and varies in soybeans, yet, a gene for flowering time variation has not been associated with soybean domestication. GIGANTEA (GI) is a major gene involved in the control of flowering time in Arabidopsis, although three GI homologs complicate this model in the soybean genome. In the present work, we revealed that the geographic evolution of the GIGANTEAa (GIa) haplotypes in G. max (GmGIa) and Glycine soja (GsGIa). Three GIa haplotypes (H1, H2, and H3) were found among cultivated soybeans and their wild relatives, yet an additional 44 diverse haplotypes were observed in wild soybeans. H1 had a premature stop codon in the 10(th) exon, whereas the other haplotypes encoded full-length GIa protein isoforms. In both wild-type and cultivated soybeans, H2 was present in the Southern region of China, and H3 was restricted to areas near the Northeast region of China. H1 was genetically derived from H2, and it was dominant and widely distributed among cultivated soybeans, whereas in wild populations, the ortholog of this domesticated haplotype H1 was only found in Yellow River basin with a low frequency. Moreover, this mutated GIa haplotype significantly correlated with early flowering. We further determined that the differences in gene expression of the three GmGIa haplotypes were not correlated to flowering time variations in cultivated soybeans. However, only the truncated GmGIa H1 could partially rescue gi-2 Arabidopsis from delayed flowering in transgenic plants, whereas both GmGIa H2 and H3 haplotypes could significantly repress flowering in transgenic Arabidopsis with a wild-type background. Thus, GmGIa haplotype diversification may have contributed to flowering time adaptation that facilitated the radiation of domesticated soybeans. In light of the evolution of the GIa gene, soybean domestication history for an early flowering phenotype is discussed.

Keywords
Domestication Evolution Flowering time GIGANTEA Haplotype Soybean
MeSH Terms
Arabidopsis/genetics,physiology Biological Evolution China Evolution, Molecular Flowers/physiology Genetic Variation Haplotypes Plant Breeding Plant Proteins/genetics Plants, Genetically Modified Soybeans/classification,genetics,physiology
Chemicals
Plant Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Wang Yan
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, 100093, Beijing, China.
Gu Yongzhe
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, 100093, Beijing, China. | Graduate University, Chinese Academy of Sciences, Yuquan Road 19, 100049, Beijing, China.
Gao Huihui
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, 100093, Beijing, China. | Graduate University, Chinese Academy of Sciences, Yuquan Road 19, 100049, Beijing, China.
Qiu Lijuan
The National Key Facility for Crop Gene Resources and Genetic Improvement (NFCRI)/Key Lab of Germplasm Utilization (MOA), Institute of Crop Science, Chinese Academy of Agricultural Sciences, 100081, Beijing, China.
Chang Ruzhen
The National Key Facility for Crop Gene Resources and Genetic Improvement (NFCRI)/Key Lab of Germplasm Utilization (MOA), Institute of Crop Science, Chinese Academy of Agricultural Sciences, 100081, Beijing, China.
Chen Shouyi
National Key Laboratory of Plant Genomic, Institute of Genetics and Developmental Biology, Chinese Academy of sciences, 100101, Beijing, China.
He Chaoying
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, 100093, Beijing, China. chaoying@ibcas.ac.cn.
References (55)
55 references, click to expand
  1. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.
    Nature. 2001 Apr 26;410(6832):1116-20 PMID: 11323677
  2. Archaeological soybean (Glycine max) in East Asia: does size matter?
    PLoS One. 2011;6(11):e26720 PMID: 22073186
  3. QTL mapping of domestication-related traits in soybean (Glycine max).
    Ann Bot. 2007 Nov;100(5):1027-38 PMID: 17684023
  4. A bountiful harvest: genomic insights into crop domestication phenotypes.
    Annu Rev Plant Biol. 2013;64:47-70 PMID: 23451788
  5. Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean.
    BMC Plant Biol. 2013;13:91 PMID: 23799885
  6. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice.
    Nat Genet. 2010 Jul;42(7):635-8 PMID: 20543848
  7. A transposon in tb1 drove maize domestication.
    Nat Genet. 2011 Nov;43(11):1048-50 PMID: 22030605
  8. The molecular genetics of crop domestication.
    Cell. 2006 Dec 29;127(7):1309-21 PMID: 17190597
  9. Genetic diversity and peculiarity of annual wild soybean (G. soja Sieb. et Zucc.) from various eco-regions in China.
    Theor Appl Genet. 2009 Jul;119(2):371-81 PMID: 19449177
  10. The wheat TaGI1, involved in photoperiodic flowering, encodes an Arabidopsis GI ortholog.
    Plant Mol Biol. 2005 May;58(1):53-64 PMID: 16028116
  11. A single domestication for maize shown by multilocus microsatellite genotyping.
    Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6080-4 PMID: 11983901
  12. Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field.
    Plant Cell. 2011 May;23(5):1741-55 PMID: 21571948
  13. Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity.
    J Exp Bot. 2007;58(6):1231-44 PMID: 17420173
  14. Regulation of flowering time: all roads lead to Rome.
    Cell Mol Life Sci. 2011 Jun;68(12):2013-37 PMID: 21611891
  15. Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa.
    Proc Natl Acad Sci U S A. 2015 Mar 24;112(12):3829-34 PMID: 25775524
  16. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize.
    Proc Natl Acad Sci U S A. 2013 Oct 15;110(42):16969-74 PMID: 24089449
  17. GmHs1-1, encoding a calcineurin-like protein, controls hard-seededness in soybean.
    Nat Genet. 2015 Aug;47(8):939-43 PMID: 26098868
  18. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  19. Contributions of flowering time genes to sunflower domestication and improvement.
    Genetics. 2011 Jan;187(1):271-87 PMID: 20944017
  20. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
    Mol Biol Evol. 2011 Oct;28(10):2731-9 PMID: 21546353
  21. A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering.
    Genetics. 2011 Jun;188(2):395-407 PMID: 21406680
  22. Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome.
    Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22032-7 PMID: 21131573
  23. Population-based resequencing reveals that the flowering time adaptation of cultivated barley originated east of the Fertile Crescent.
    Mol Biol Evol. 2008 Oct;25(10):2211-9 PMID: 18669581
  24. Pea LATE BLOOMER1 is a GIGANTEA ortholog with roles in photoperiodic flowering, deetiolation, and transcriptional regulation of circadian clock gene homologs.
    Plant Physiol. 2007 Jun;144(2):648-61 PMID: 17468223
  25. Seasonal and developmental timing of flowering.
    Plant J. 2010 Mar;61(6):1001-13 PMID: 20409274
  26. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection.
    Nat Genet. 2010 Dec;42(12):1053-9 PMID: 21076406
  27. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  28. Adaptation of photoperiodic control pathways produces short-day flowering in rice.
    Nature. 2003 Apr 17;422(6933):719-22 PMID: 12700762
  29. Heading date 1 (Hd1), an ortholog of Arabidopsis CONSTANS, is a possible target of human selection during domestication to diversify flowering times of cultivated rice.
    Genes Genet Syst. 2011;86(3):175-82 PMID: 21952207
  30. Impacts of genetic bottlenecks on soybean genome diversity.
    Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):16666-71 PMID: 17068128
  31. Divergence of flowering genes in soybean.
    J Biosci. 2012 Nov;37(5):857-70 PMID: 23107921
  32. GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11698-703 PMID: 21709243
  33. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis.
    Plant Cell. 2005 Aug;17(8):2255-70 PMID: 16006578
  34. Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA.
    Theor Appl Genet. 2005 Mar;110(5):925-31 PMID: 15682288
  35. A pair of related genes with antagonistic roles in mediating flowering signals.
    Science. 1999 Dec 3;286(5446):1960-2 PMID: 10583960
  36. Identification and molecular characterization of FKF1 and GI homologous genes in soybean.
    PLoS One. 2013;8(11):e79036 PMID: 24236086
  37. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.
    Bioinformatics. 2009 Jun 1;25(11):1451-2 PMID: 19346325
  38. Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs.
    Mol Biol Evol. 2003 Jan;20(1):67-75 PMID: 12519908
  39. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis.
    Science. 2007 Oct 12;318(5848):261-5 PMID: 17872410
  40. A single origin and moderate bottleneck during domestication of soybean (Glycine max): implications from microsatellites and nucleotide sequences.
    Ann Bot. 2010 Sep;106(3):505-14 PMID: 20566681
  41. Activation tagging of the floral inducer FT.
    Science. 1999 Dec 3;286(5446):1962-5 PMID: 10583961
  42. Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean.
    Ann Bot. 2014 Feb;113(3):429-41 PMID: 24284817
  43. Constitutive expression of the GIGANTEA ortholog affects circadian rhythms and suppresses one-shot induction of flowering in Pharbitis nil, a typical short-day plant.
    Plant Cell Physiol. 2011 Apr;52(4):638-50 PMID: 21382978
  44. De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits.
    Nat Biotechnol. 2014 Oct;32(10):1045-52 PMID: 25218520
  45. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains.
    EMBO J. 1999 Sep 1;18(17):4679-88 PMID: 10469647
  46. Diversity of chloroplast DNA SSRs in wild and cultivated soybeans: evidence for multiple origins of cultivated soybean.
    Theor Appl Genet. 2002 Oct;105(5):645-653 PMID: 12582476
  47. Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent.
    Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3289-94 PMID: 17360640
  48. Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean.
    Nat Commun. 2014;5:3352 PMID: 24549030
  49. Artificial selection for determinate growth habit in soybean.
    Proc Natl Acad Sci U S A. 2010 May 11;107(19):8563-8 PMID: 20421496
  50. The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis.
    Plant Cell. 2007 Sep;19(9):2736-48 PMID: 17890372
  51. Genetic diversity in domesticated soybean (Glycine max) and its wild progenitor (Glycine soja) for simple sequence repeat and single-nucleotide polymorphism loci.
    New Phytol. 2010 Oct;188(1):242-53 PMID: 20618914
  52. Genetic and molecular bases of photoperiod responses of flowering in soybean.
    Breed Sci. 2012 Jan;61(5):531-43 PMID: 23136492
  53. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean.
    Nat Biotechnol. 2015 Apr;33(4):408-14 PMID: 25643055
  54. Allelic combinations of soybean maturity Loci E1, E2, E3 and E4 result in diversity of maturity and adaptation to different latitudes.
    PLoS One. 2014;9(8):e106042 PMID: 25162675
  55. A single amino acid converts a repressor to an activator of flowering.
    Proc Natl Acad Sci U S A. 2005 May 24;102(21):7748-53 PMID: 15894619
Article Info
Journal
BMC evolutionary biology
Abbr.
BMC Evol Biol
ISSN
1471-2148
DOI
10.1186/s12862-016-0653-9
Email
chaoying@ibcas.ac.cn
Published
2016-04-12
Epub
2016-00-12
Pages
79
Language
English
Region
England
NLM ID
100966975
PMCID
PMC4830004
Subset
IM
External Links
PubMed source DOI: 10.1186/s12862-016-0653-9 PMC Full Text View journal details
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