Genome‐wide association study of multiple yield traits in a diversity panel of polyploid sugarcane (Saccharum spp.)

Sugarcane (Saccharum spp.) is an important economic crop, contributing up to 80% of sugar and approximately 60% of biofuel globally. To meet the increased demand for sugar and biofuel supplies, it is critical to breed sugarcane cultivars with robust performance in yield traits. Therefore, dissection of causal DNA sequence variants is of great importance, as it provides genetic resources and fundamental information for crop improvement. In this study, we analyzed nine yield traits in a sugarcane diversity panel consisting of 308 accessions primarily selected from the World Collection of Sugarcane and Related Grasses. By genotyping the diversity panel via target enrichment sequencing, we identified a large number of sequence variants. Genome‐wide association studies between the markers and traits were conducted, taking dosages and gene actions into consideration. In total, 217 nonredundant markers and 225 candidate genes were identified to be significantly associated with the yield traits, which can serve as a comprehensive genetic resource database for future gene identification, characterization, and selection for sugarcane improvement. We further investigated runs of homozygosity (ROH) in the sugarcane diversity panel. We characterized 282 ROHs and found that the occurrence of ROHs in the genome were nonrandom and probably under selection. The ROHs were associated with total weight and dry weight, and high ROHs resulted in a decrease in the two traits. This study suggests that genomic inbreeding has led to negative impacts on sugarcane yield.

[1]  W. H. Longley Taxonomy and Evolution , 1933, Nature.

[2]  D. R. Dewey,et al.  A CORRELATION AND PATH COEFFICIENT ANALYSIS OF COMPONENTS OF CRESTED WHEAT GRASS AND SEED PRODUCTION , 1959 .

[3]  J. Daniels,et al.  Taxonomy and Evolution , 1987 .

[4]  C. Deren Genetic base of U.S. Mainland sugarcane , 1995 .

[5]  Todd Ogden,et al.  Statistical Analysis with Webstat, a Java applet for the World Wide Web , 1997 .

[6]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[7]  A. P. de Souza,et al.  Analysis of genetic similarity detected by AFLP and coefficient of parentage among genotypes of sugar cane (Saccharum spp.) , 2002, Theoretical and Applied Genetics.

[8]  J. Glaszmann,et al.  Oligoclonal interspecific origin of ‘North Indian’ and ‘Chinese’ sugarcanes , 2004, Chromosome Research.

[9]  A. D'Hont,et al.  Unraveling the genome structure of polyploids using FISH and GISH; examples of sugarcane and banana , 2005, Cytogenetic and Genome Research.

[10]  J. Glaszmann,et al.  Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics , 1996, Molecular and General Genetics MGG.

[11]  J. Gilbert,et al.  Complement Factor H Variant Increases the Risk of Age-Related Macular Degeneration , 2005, Science.

[12]  Xianming Wei,et al.  Associations between DNA markers and resistance to diseases in sugarcane and effects of population substructure , 2006, Theoretical and Applied Genetics.

[13]  J. Glaszmann,et al.  Analysis of genome-wide linkage disequilibrium in the highly polyploid sugarcane , 2008, Theoretical and Applied Genetics.

[14]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[15]  M. Gore,et al.  Status and Prospects of Association Mapping in Plants , 2008 .

[16]  Thibaut Jombart,et al.  adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[17]  David H. Alexander,et al.  Fast model-based estimation of ancestry in unrelated individuals. , 2009, Genome research.

[18]  Mihaela M. Martis,et al.  The Sorghum bicolor genome and the diversification of grasses , 2009, Nature.

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

[20]  A. Kilian,et al.  Simultaneously accounting for population structure, genotype by environment interaction, and spatial variation in marker-trait associations in sugarcane. , 2010, Genome.

[21]  F. Balloux,et al.  Discriminant analysis of principal components: a new method for the analysis of genetically structured populations , 2010, BMC Genetics.

[22]  Yves Rosseel,et al.  lavaan: An R Package for Structural Equation Modeling , 2012 .

[23]  Zhou Du,et al.  PlantGSEA: a gene set enrichment analysis toolkit for plant community , 2013, Nucleic Acids Res..

[24]  Erik Dahlquist,et al.  Biomass as Energy Source : Resources, Systems and Applications , 2013 .

[25]  Jianping Wang,et al.  Promoting Utilization of Saccharum spp. Genetic Resources through Genetic Diversity Analysis and Core Collection Construction , 2014, PloS one.

[26]  A. D'Hont,et al.  Prospecting sugarcane resistance to Sugarcane yellow leaf virus by genome-wide association , 2014, Theoretical and Applied Genetics.

[27]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[28]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[29]  Jianping Wang,et al.  Phenotypic characterization of the Miami World Collection of sugarcane (Saccharum spp.) and related grasses for selecting a representative core , 2014, Genetic Resources and Crop Evolution.

[30]  M. Gouy,et al.  Genome wide association mapping of agro-morphological and disease resistance traits in sugarcane , 2014, Euphytica.

[31]  Mingyao Li,et al.  Runs of Homozygosity: Association with Coronary Artery Disease and Gene Expression in Monocytes and Macrophages. , 2015, American journal of human genetics.

[32]  Sergio Contrino,et al.  Cross‐organism analysis using InterMine , 2015, Genesis.

[33]  Sacha Epskamp,et al.  semPlot: Unified Visualizations of Structural Equation Models , 2015 .

[34]  R. Houlston,et al.  Genome-wide homozygosity signature and risk of Hodgkin lymphoma , 2015, Scientific Reports.

[35]  Ji-Gang Zhang,et al.  Genome‐Wide Survey of Runs of Homozygosity Identifies Recessive Loci for Bone Mineral Density in Caucasian and Chinese Populations , 2015, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[36]  M. I. Cuenya,et al.  Genome-wide association mapping of quantitative traits in a breeding population of sugarcane , 2016, BMC Plant Biology.

[37]  Jeffrey B. Endelman,et al.  Software for Genome‐Wide Association Studies in Autopolyploids and Its Application to Potato , 2016, The plant genome.

[38]  U. Krasuska,et al.  Canavanine Alters ROS/RNS Level and Leads to Post-translational Modification of Proteins in Roots of Tomato Seedlings , 2016, Front. Plant Sci..

[39]  Jianping Wang,et al.  Natural Allelic Variations in Highly Polyploidy Saccharum Complex , 2016, Front. Plant Sci..

[40]  Xinxin Zhao,et al.  Association of candidate genes with heading date in a diverse Dactylis glomerata population. , 2017, Plant science : an international journal of experimental plant biology.

[41]  Jianping Wang,et al.  Mining sequence variations in representative polyploid sugarcane germplasm accessions , 2017, BMC Genomics.

[42]  R. I. Valbuena,et al.  Genetic diversity and association mapping in the Colombian Central Collection of Solanum tuberosum L. Andigenum group using SNPs markers , 2017, PloS one.

[43]  R. Ventura,et al.  Assessment of runs of homozygosity islands and estimates of genomic inbreeding in Gyr (Bos indicus) dairy cattle , 2018, BMC Genomics.

[44]  L. Erazzú,et al.  Pedigree comparison highlights genetic similarities and potential industrial values of sugarcane cultivars , 2017, Euphytica.

[45]  Thomas Julou,et al.  Monitoring single-cell gene regulation under dynamically controllable conditions with integrated microfluidics and software , 2018, Nature Communications.

[46]  M. Hufford,et al.  The interplay of demography and selection during maize domestication and expansion , 2017, Genome Biology.

[47]  Dan G. Bock,et al.  Evolution of invasiveness by genetic accommodation , 2018, Nature Ecology & Evolution.

[48]  M. Kirst,et al.  Understanding the Complexity of Cold Tolerance in White Clover using Temperature Gradient Locations and a GWAS Approach , 2018, The plant genome.

[49]  Molecular dissection of sugar related traits and it’s attributes in Saccharum spp. hybrids , 2018, Euphytica.

[50]  Jianping Wang,et al.  Phenotypic evaluation of a diversity panel selected from the world collection of sugarcane (Saccharum spp) and related grasses , 2018 .

[51]  B. Simmons,et al.  A mosaic monoploid reference sequence for the highly complex genome of sugarcane , 2018, Nature Communications.

[52]  K. Rybak,et al.  Novel sources of resistance to Septoria nodorum blotch in the Vavilov wheat collection identified by genome-wide association studies , 2018, Theoretical and Applied Genetics.

[53]  David Sankoff,et al.  Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. , 2018, Nature Genetics.

[54]  Peter K. Joshi,et al.  Runs of homozygosity: windows into population history and trait architecture , 2018, Nature Reviews Genetics.

[55]  R. Ming,et al.  Target enrichment sequencing of 307 germplasm accessions identified ancestry of ancient and modern hybrids and signatures of adaptation and selection in sugarcane (Saccharum spp.), a ‘sweet’ crop with ‘bitter’ genomes , 2018, Plant biotechnology journal.