Association Mapping of Flowering Time QTLs and Insight into Their Contributions to Rapeseed Growth Habits

Plants have developed sophisticated systems to adapt to local conditions during evolution, domestication and natural or artificial selection. The selective pressures of these different growing conditions have caused significant genomic divergence within species. The flowering time trait is the most crucial factor because it helps plants to maintain sustainable development. Controlling flowering at appropriate times can also prevent plants from suffering from adverse growth conditions, such as drought, winter hardness, and disease. Hence, discovering the genome-wide genetic mechanisms that influence flowering time variations and understanding their contributions to adaptation should be a central goal of plant genetics and genomics. A global core collection panel with 448 inbred rapeseed lines was first planted in four independent environments, and their flowering time traits were evaluated. We then performed a genome-wide association mapping of flowering times with a 60 K SNP array for this core collection. With quality control and filtration, 20,342 SNP markers were ultimately used for further analyses. In total, 312 SNPs showed marker-trait associations in all four environments, and they were based on a threshold p-value of 4.06 × 10−4; the 40 QTLs showed significant association with flowering time variations. To explore flowering time QTLs and genes related to growth habits in rapeseed, selection signals related to divergent habits were screened at the genome-wide level and 117 genomic regions were found. Comparing locations of flowering time QTLs and genes with these selection regions revealed that 20 flowering time QTLs and 224 flowering time genes overlapped with 24 and 81 selected regions, respectively. Based on this study, a number of marker-trait associations and candidate genes for flowering time variations in rapeseed were revealed. Moreover, we also showed that both flowering time QTLs and genes play important roles in rapeseed growth habits. These results will be applied to rapeseed breeding programs, and they will aid in our understanding of the relation between flowering time variations and growth habits in plants.

[1]  C. Jung,et al.  Flowering time variation in oilseed rape (Brassica napus L.) is associated with allelic variation in the FRIGIDA homologue BnaA.FRI.a , 2011, Journal of experimental botany.

[2]  A. Dickson On Evolution , 1884, Science.

[3]  Kun Xu,et al.  Genome-Wide Association Study Dissects the Genetic Architecture of Seed Weight and Seed Quality in Rapeseed (Brassica napus L.) , 2014, DNA research : an international journal for rapid publication of reports on genes and genomes.

[4]  John M. Walker,et al.  Comparative Genomics , 2007, Methods In Molecular Biology™.

[5]  B Rannala,et al.  Finding Genes Influencing Susceptibility to Complex Diseases in the Post-Genome Era , 2001, American journal of pharmacogenomics : genomics-related research in drug development and clinical practice.

[6]  E. Sonnhammer,et al.  Genomic gene clustering analysis of pathways in eukaryotes. , 2003, Genome research.

[7]  B. S. Yandell,et al.  Mapping loci controlling vernalization requirement and flowering time in Brassica napus , 1995, Theoretical and Applied Genetics.

[8]  E. Richards,et al.  Preparation of Genomic DNA from Plant Tissue , 1994, Current protocols in molecular biology.

[9]  T. Mitchell-Olds,et al.  Evolutionary genetics of plant adaptation. , 2011, Trends in genetics : TIG.

[10]  Ruben C. Arslan Evolutionary Genetics , 2014 .

[11]  C. Jung,et al.  Comparative Analysis of FLC Homologues in Brassicaceae Provides Insight into Their Role in the Evolution of Oilseed Rape , 2012, PloS one.

[12]  D. Du,et al.  Quantitative trait analysis of flowering time in spring rapeseed (B. napus L.) , 2014, Euphytica.

[13]  Kede Liu,et al.  Association mapping of six yield-related traits in rapeseed (Brassica napus L.) , 2013, Theoretical and Applied Genetics.

[14]  R. Nielsen,et al.  Ascertainment biases in SNP chips affect measures of population divergence. , 2010, Molecular biology and evolution.

[15]  Kun Xu,et al.  Genome-wide investigation of genetic changes during modern breeding of Brassica napus , 2014, Theoretical and Applied Genetics.

[16]  R. Uptmoor,et al.  Prediction of flowering time in Brassica oleracea using a quantitative trait loci-based phenology model. , 2011, Plant biology.

[17]  T. Nishio,et al.  A Brassica rapa Linkage Map of EST-based SNP Markers for Identification of Candidate Genes Controlling Flowering Time and Leaf Morphological Traits , 2009, DNA Research.

[18]  C. R. McClung,et al.  Genetic architecture of the circadian clock and flowering time in Brassica rapa , 2011, Theoretical and Applied Genetics.

[19]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[20]  T. Fu,et al.  The genetic basis of flowering time and photoperiod sensitivity in rapeseed Brassica napus L. , 2008, Russian Journal of Genetics.

[21]  G. King,et al.  Bmc Evolutionary Biology the Evolution of Brassica Napus Flowering Locust Paralogues in the Context of Inverted Chromosomal Duplication Blocks , 2022 .

[22]  Patterns of Gene Duplication and Their Contribution to Expansion of Gene Families in Grapevine , 2013, Plant Molecular Biology Reporter.

[23]  Kaining Hu,et al.  Genome-wide association study reveals the genetic architecture of flowering time in rapeseed (Brassica napus L.) , 2015, DNA research : an international journal for rapid publication of reports on genes and genomes.

[24]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[25]  Corinne Da Silva,et al.  Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome , 2014, Science.

[26]  J. Higgins,et al.  Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses , 2010, PloS one.

[27]  Q. Wang,et al.  A naturally occurring InDel variation in BraA.FLC.b (BrFLC2) associated with flowering time variation in Brassica rapa , 2012, BMC Plant Biology.

[28]  R. Snowdon,et al.  Diverse regulatory factors associate with flowering time and yield responses in winter-type Brassica napus , 2015, BMC Genomics.

[29]  N. Wratten,et al.  Genetic and physical mapping of flowering time loci in canola (Brassica napus L.) , 2012, Theoretical and Applied Genetics.

[30]  B. Liu,et al.  A Tourist-like MITE insertion in the upstream region of the BnFLC.A10 gene is associated with vernalization requirement in rapeseed (Brassica napus L.) , 2012, BMC Plant Biology.

[31]  P. Visscher,et al.  GCTA: a tool for genome-wide complex trait analysis. , 2011, American journal of human genetics.

[32]  Jung Sun Kim,et al.  Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. , 2007, Journal of experimental botany.

[33]  Xinfa Wang,et al.  Linkage and regional association analysis reveal two new tightly-linked major-QTLs for pod number and seed number per pod in rapeseed (Brassica napus L.) , 2015, Scientific Reports.

[34]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[35]  A. Sweigart,et al.  Evolutionary genetics of plant adaptation: insights from new model systems. , 2014, Current opinion in plant biology.

[36]  Robert J. Elshire,et al.  TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline , 2014, PloS one.

[37]  I. Bancroft,et al.  Unraveling the Complex Trait of Crop Yield With Quantitative Trait Loci Mapping in Brassica napus , 2009, Genetics.

[38]  C. Helliwell,et al.  Control of flowering time by FLC orthologues in Brassica napus. , 2001, The Plant journal : for cell and molecular biology.

[39]  G. Coupland,et al.  Conserved structure and function of the Arabidopsis flowering time gene CONSTANS in Brassica napus , 1998, Plant Molecular Biology.

[40]  R. Amasino Vernalization, Competence, and the Epigenetic Memory of Winter , 2004, The Plant Cell Online.

[41]  A. Melchinger,et al.  Genome-wide association mapping of flowering time and northern corn leaf blight (Setosphaeria turcica) resistance in a vast commercial maize germplasm set , 2012, BMC Plant Biology.

[42]  Christian Jung,et al.  Flowering time control and applications in plant breeding. , 2009, Trends in plant science.

[43]  C. Zhang,et al.  Flowering Time Quantitative Trait Loci Analysis of Oilseed Brassica in Multiple Environments and Genomewide Alignment with Arabidopsis , 2007, Genetics.

[44]  R. Poethig,et al.  Phase Change and the Regulation of Developmental Timing in Plants , 2003, Science.

[45]  R. Snowdon,et al.  Sub-genomic selection patterns as a signature of breeding in the allopolyploid Brassica napus genome , 2014, BMC Genomics.

[46]  Peter Donnelly,et al.  Assessing population differentiation and isolation from single‐nucleotide polymorphism data , 2002 .

[47]  Nu Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. , 1935 .