The transcriptomic signature of developing soybean seeds reveals the genetic basis of seed trait adaptation during domestication.

Cultivated soybean has undergone many transformations during domestication. In this paper we report a comprehensive assessment of the evolution of gene co-expression networks based on the analysis of 40 transcriptomes from developing soybean seeds in cultivated and wild soybean accessions. We identified 2680 genes that are differentially expressed during seed maturation and established two cultivar-specific gene co-expression networks. Through analysis of the two networks and integration with quantitative trait locus data we identified two potential key drivers for seed trait formation, GA20OX and NFYA. GA20OX encodes an enzyme in a rate-limiting step of gibberellin biosynthesis, and NFYA encodes a transcription factor. Overexpression of GA20OX and NFYA enhanced seed size/weight and oil content, respectively, in seeds of transgenic plants. The two genes showed significantly higher expression in cultivated than in wild soybean, and the increases in expression were associated with genetic variations in the promoter region of each gene. Moreover, the expression of GA20OX and NFYA in seeds of soybean accessions correlated with seed weight and oil content, respectively. Our study reveals transcriptional adaptation during soybean domestication and may identify a mechanism of selection by expression for seed trait formation, providing strategies for future breeding practice.

[1]  Hui Xiang,et al.  Erratum: Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean , 2015, Nature Biotechnology.

[2]  Y. Liu,et al.  Salinity tolerance in soybean is modulated by natural variation in GmSALT3. , 2014, The Plant journal : for cell and molecular biology.

[3]  W. Phippen,et al.  New approaches to facilitate rapid domestication of a wild plant to an oilseed crop: example pennycress (Thlaspi arvense L.). , 2014, Plant science : an international journal of experimental plant biology.

[4]  Ruiqiang Li,et al.  De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits , 2014, Nature Biotechnology.

[5]  J. Specht,et al.  Dt2 Is a Gain-of-Function MADS-Domain Factor Gene That Specifies Semideterminacy in Soybean[C][W] , 2014, Plant Cell.

[6]  S. Chen,et al.  Soybean GmMYB73 promotes lipid accumulation in transgenic plants , 2014, BMC Plant Biology.

[7]  Xia Yang,et al.  Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean , 2014, Nature Communications.

[8]  Hong-Kyu Choi,et al.  Population Structure and Domestication Revealed by High-Depth Resequencing of Korean Cultivated and Wild Soybean Genomes , 2013, DNA research : an international journal for rapid publication of reports on genes and genomes.

[9]  Yu Zhang,et al.  P-MITE: a database for plant miniature inverted-repeat transposable elements , 2013, Nucleic Acids Res..

[10]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[11]  S. Chen,et al.  Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants , 2013, Journal of experimental botany.

[12]  Anthony M. Bolger,et al.  Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato , 2013, Proceedings of the National Academy of Sciences.

[13]  Yang Liu,et al.  VisANT 4.0: Integrative network platform to connect genes, drugs, diseases and therapies , 2013, Nucleic Acids Res..

[14]  L. Vodkin,et al.  Using RNA-Seq to Profile Soybean Seed Development from Fertilization to Maturity , 2013, PloS one.

[15]  Runzhi Li,et al.  Soybean oil biosynthesis: role of diacylglycerol acyltransferases , 2013, Functional & Integrative Genomics.

[16]  J. Mu,et al.  Arabidopsis transcription factor genes NF-YA1, 5, 6, and 9 play redundant roles in male gametogenesis, embryogenesis, and seed development. , 2013, Molecular plant.

[17]  Jun Wang,et al.  Molecular footprints of domestication and improvement in soybean revealed by whole genome re-sequencing , 2013, BMC Genomics.

[18]  Bifeng Yuan,et al.  Highly sensitive and quantitative profiling of acidic phytohormones using derivatization approach coupled with nano-LC-ESI-Q-TOF-MS analysis. , 2012, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[19]  V. Calvenzani,et al.  Interactions and CCAAT-Binding of Arabidopsis thaliana NF-Y Subunits , 2012, PloS one.

[20]  H. Lam,et al.  Recent developments of genomic research in soybean. , 2012, Journal of genetics and genomics = Yi chuan xue bao.

[21]  Xun Xu,et al.  Comparative population genomics of maize domestication and improvement , 2012, Nature Genetics.

[22]  Chengming Fan,et al.  Validation of reference genes for real-time quantitative PCR normalization in soybean developmental and germinating seeds , 2012, Plant Cell Reports.

[23]  O. Nilsson,et al.  Analysis of the Developmental Roles of the Arabidopsis Gibberellin 20-Oxidases Demonstrates That GA20ox1, -2, and -3 Are the Dominant Paralogs[C][W] , 2012, Plant Cell.

[24]  David R. Kelley,et al.  Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks , 2012, Nature Protocols.

[25]  M. Kim,et al.  Tracing soybean domestication history: From nucleotide to genome , 2012, Breeding science.

[26]  P. Wittkopp,et al.  Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence , 2011, Nature Reviews Genetics.

[27]  G. Crawford,et al.  Archaeological Soybean (Glycine max) in East Asia: Does Size Matter? , 2011, PloS one.

[28]  Z. Qi,et al.  Soybean oil content QTL mapping and integrating with meta-analysis method for mining genes , 2011, Euphytica.

[29]  Cole Trapnell,et al.  Improving RNA-Seq expression estimates by correcting for fragment bias , 2011, Genome Biology.

[30]  R. Stupar.  Into the wild: The soybean genome meets its undomesticated relative , 2010, Proceedings of the National Academy of Sciences.

[31]  J. Schmutz,et al.  Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome , 2010, Proceedings of the National Academy of Sciences.

[32]  Bo Wang,et al.  Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection , 2010, Nature Genetics.

[33]  K. Olsen,et al.  Genetic perspectives on crop domestication. , 2010, Trends in plant science.

[34]  Zhou Du,et al.  agriGO: a GO analysis toolkit for the agricultural community , 2010, Nucleic Acids Res..

[35]  J. Specht,et al.  Artificial selection for determinate growth habit in soybean , 2010, Proceedings of the National Academy of Sciences.

[36]  Steven B. Cannon,et al.  SoyBase, the USDA-ARS soybean genetics and genomics database , 2009, Nucleic Acids Res..

[37]  Jianxin Ma,et al.  SoyTEdb: a comprehensive database of transposable elements in the soybean genome , 2010, BMC Genomics.

[38]  M. Hudson,et al.  Endogenous, Tissue-Specific Short Interfering RNAs Silence the Chalcone Synthase Gene Family in Glycine max Seed Coats[W][OA] , 2009, The Plant Cell Online.

[39]  Ruibo Hu,et al.  Evaluation of putative reference genes for gene expression normalization in soybean by quantitative real-time RT-PCR , 2009, BMC Molecular Biology.

[40]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[41]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[42]  O. Nilsson,et al.  The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. , 2007, The Plant journal : for cell and molecular biology.

[43]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[44]  E. Balázs,et al.  From Crop Domestication to Super-domestication , 2007, Annals of botany.

[45]  S. Chen,et al.  The soybean Dof-type transcription factor genes, GmDof4 and GmDof11, enhance lipid content in the seeds of transgenic Arabidopsis plants. , 2007, The Plant journal : for cell and molecular biology.

[46]  G. Wray.  The evolutionary significance of cis-regulatory mutations , 2007, Nature Reviews Genetics.

[47]  Qinglu Zeng,et al.  Isolating high-quality RNA from mangroves without liquid nitrogen , 2004, Plant Molecular Biology Reporter.

[48]  Bruce D. Smith,et al.  The Molecular Genetics of Crop Domestication , 2006, Cell.

[49]  S. Horvath,et al.  Conservation and evolution of gene coexpression networks in human and chimpanzee brains , 2006, Proceedings of the National Academy of Sciences.

[50]  A. Saxton,et al.  Quantitative Trait Loci for Seed Protein and Oil Concentration, and Seed Size in Soybean , 2005 .

[51]  S. Horvath,et al.  Statistical Applications in Genetics and Molecular Biology , 2011 .

[52]  D. Geschwind,et al.  Human brain evolution: insights from microarrays , 2004, Nature Reviews Genetics.

[53]  S. Clough,et al.  Tissue-Specific Gene Silencing Mediated by a Naturally Occurring Chalcone Synthase Gene Cluster in Glycine max , 2004, The Plant Cell Online.

[54]  S. Pääbo,et al.  Intra- and Interspecific Variation in Primate Gene Expression Patterns , 2002, Science.

[55]  James E. Specht,et al.  Soybean response to water : A QTL analysis of drought tolerance , 2001 .

[56]  Feng-Chi Chen,et al.  Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. , 2001, American journal of human genetics.

[57]  David S. Wishart,et al.  PepTool™ and GeneTool™: , 2000 .

[58]  G. Pelletier,et al.  In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. , 1998, Methods in molecular biology.

[59]  L. Vodkin,et al.  Duplications That Suppress and Deletions That Restore Expression from a Chalcone Synthase Multigene Family. , 1996, The Plant cell.

[60]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[61]  D. Wolfe,et al.  Nonparametric Statistical Methods. , 1974 .