Comprehensive genomic analyses of Vigna unguiculata provide insights into population differentiation and the genetic basis of key agricultural traits

Summary Vigna unguiculata is an important legume crop worldwide. The subsp. sesquipedalis and unguiculata are the two major types grown; the former is mainly grown in Asia to produce fresh pods, while the latter is mainly grown in Africa to produce seeds. Here, a chromosome‐scale genome for subsp. sesquipedalis was generated by combining high‐fidelity (HiFi) long‐read sequencing with high‐throughput chromosome conformation capture (Hi‐C) technology. The genome size for all contigs and N50 were 594 and 18.5 Mb, respectively. The Hi‐C interaction map helped cluster 91% of the contigs into 11 chromosomes. Genome comparisons between subsp. sesquipedalis and unguiculata revealed extensive genomic variations, and some variations resulted in gene loss. A germplasm panel with 315 accessions of V. unguiculata was resequenced, and a genomic variation map was constructed. Population structure and phylogenetic analyses suggested that subsp. sesquipedalis originated from subsp. unguiculata. Highly differentiated genomic regions were also identified, and a number of genes functionally enriched in adaptations were located in these regions. Two traits, pod length (PL) and pod width (PW), were observed for this germplasm, and genome‐wide association analysis of these traits was performed. The quantitative trait loci (QTLs) for these two traits were identified, and their candidate genes were uncovered. Interestingly, genomic regions of PL QTLs also showed strong signals of artificial selection. Taken together, the results of this study provide novel insights into the population differentiation and genetic basis of key agricultural traits in V. unguiculata.

[1]  Honglin Chen,et al.  Genomic analyses of rice bean landraces reveal adaptation and yield related loci to accelerate breeding , 2022, Nature Communications.

[2]  Liyu Huang,et al.  The chromosome-scale genome sequence of Triadica sebifera provides insight into fatty acids and anthocyanin biosynthesis , 2022, Communications Biology.

[3]  M. Agarwal,et al.  Long‐read‐based draft genome sequence of Indian black gram IPU‐94‐1 ‘Uttara’: Insights into disease resistance and seed storage protein genes , 2022, The plant genome.

[4]  Jing Zhao,et al.  Genomic selection and genetic architecture of agronomic traits during modern rapeseed breeding , 2022, Nature Genetics.

[5]  M. Smale,et al.  IITA’s genebank, cowpea diversity on farms, and farmers’ welfare in Nigeria , 2022, CABI Agriculture and Bioscience.

[6]  R. Varshney,et al.  QTL-seq for the identification of candidate genes for days to flowering and leaf shape in pigeonpea , 2022, Heredity.

[7]  R. VanBuren,et al.  Representation and participation across 20 years of plant genome sequencing , 2021, Nature Plants.

[8]  D. Scott,et al.  An Open-Source Toolkit That Powers the Genome-Wide Analysis of Mature B-Cell Lymphomas (GAMBL) Project , 2021, Blood.

[9]  O. Boukar,et al.  Genetic Diversity and Population Structure of Cowpea [Vigna unguiculata (L.) Walp.] Germplasm Collected from Togo Based on DArT Markers , 2021, Genes.

[10]  F. Zhao,et al.  Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation , 2021, BMC biology.

[11]  Heng Li,et al.  Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm , 2021, Nature Methods.

[12]  P. Kaushik,et al.  Developments and Prospects in Imperative Underexploited Vegetable Legumes Breeding: A Review , 2020, International journal of molecular sciences.

[13]  C. Bermúdez-Santana,et al.  Comprehensive genomic resources related to domestication and crop improvement traits in Lima bean , 2020, Nature Communications.

[14]  S. Koren,et al.  Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies , 2020, Genome Biology.

[15]  A. N’Diaye,et al.  Evaluation of variant calling tools for large plant genome re-sequencing , 2020, BMC Bioinformatics.

[16]  Ira A. Herniter,et al.  Genetic, textual, and archaeological evidence of the historical global spread of cowpea (Vigna unguiculata [L.] Walp) , 2020, bioRxiv.

[17]  Margaret H. Frank,et al.  TBtools - an integrative toolkit developed for interactive analyses of big biological data. , 2020, Molecular plant.

[18]  Mark N. Puttick,et al.  MCMCtreeR: functions to prepare MCMCtree analyses and visualize posterior ages on trees , 2019, Bioinform..

[19]  Steven L Salzberg,et al.  Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype , 2019, Nature Biotechnology.

[20]  P. Schnable,et al.  Identification of loci controlling adaptation in Chinese soya bean landraces via a combination of conventional and bioclimatic GWAS , 2019, Plant biotechnology journal.

[21]  Huanming Yang,et al.  The genome assembly of asparagus bean, Vigna unguiculata ssp. sesquipedialis , 2019, Scientific Data.

[22]  S. Shu,et al.  The genome of cowpea (Vigna unguiculata [L.] Walp.) , 2019, bioRxiv.

[23]  S. Kelly,et al.  OrthoFinder: phylogenetic orthology inference for comparative genomics , 2019, Genome Biology.

[24]  M. Gedil,et al.  Genetic diversity and population structure of a mini-core subset from the world cowpea (Vigna unguiculata (L.) Walp.) germplasm collection , 2018, Scientific Reports.

[25]  Chi Zhang,et al.  PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files , 2018, Bioinform..

[26]  S. Jackson,et al.  High‐density genetic map using whole‐genome resequencing for fine mapping and candidate gene discovery for disease resistance in peanut , 2018, Plant biotechnology journal.

[27]  Ira A. Herniter,et al.  Identification of QTL controlling domestication-related traits in cowpea (Vigna unguiculata L. Walp) , 2018, Scientific Reports.

[28]  Ira A. Herniter,et al.  Identification of QTL controlling domestication-related traits in cowpea (Vigna unguiculata L. Walp) , 2018, Scientific Reports.

[29]  M. Wang,et al.  Genetic diversity and a population structure analysis of accessions in the Chinese cowpea [Vigna unguiculata (L.) Walp.] germplasm collection , 2017 .

[30]  Jihun Kim,et al.  Whole-genome resequencing of 292 pigeonpea accessions identifies genomic regions associated with domestication and agronomic traits , 2017, Nature Genetics.

[31]  S. Koren,et al.  Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation , 2016, bioRxiv.

[32]  T. Close,et al.  Genomic regions, cellular components and gene regulatory basis underlying pod length variations in cowpea (V. unguiculata L. Walp) , 2016, Plant biotechnology journal.

[33]  B. Mou,et al.  Genetic Diversity and Population Structure of Cowpea (Vigna unguiculata L. Walp) , 2016, PloS one.

[34]  Neva C. Durand,et al.  Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments. , 2016, Cell systems.

[35]  Tim Sutton,et al.  Prioritization of candidate genes in “QTL-hotspot” region for drought tolerance in chickpea (Cicer arietinum L.) , 2015, Scientific Reports.

[36]  Evgeny M. Zdobnov,et al.  BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs , 2015, Bioinform..

[37]  Rajeev K. Varshney,et al.  Genome sequencing of adzuki bean (Vigna angularis) provides insight into high starch and low fat accumulation and domestication , 2015, Proceedings of the National Academy of Sciences.

[38]  Rajeev K. Varshney,et al.  Genome sequence of mungbean and insights into evolution within Vigna species , 2014, Nature Communications.

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

[40]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[41]  M. Stephens,et al.  Efficient Algorithms for Multivariate Linear Mixed Models in Genome-wide Association Studies , 2013, Nature Methods.

[42]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[43]  D. Gianola,et al.  A Genome-Wide Scan for Evidence of Selection in a Maize Population Under Long-Term Artificial Selection for Ear Number , 2013, Genetics.

[44]  Pablo Cingolani,et al.  © 2012 Landes Bioscience. Do not distribute. , 2022 .

[45]  Gonçalo R. Abecasis,et al.  The variant call format and VCFtools , 2011, Bioinform..

[46]  David Reich,et al.  Population differentiation as a test for selective sweeps. , 2010, Genome research.

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

[48]  Jun Yu,et al.  γ-MYN: a new algorithm for estimating Ka and Ks with consideration of variable substitution rates , 2009, Biology Direct.

[49]  Jonathan E. Allen,et al.  Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments , 2007, Genome Biology.

[50]  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.

[51]  Burkhard Morgenstern,et al.  AUGUSTUS: ab initio prediction of alternative transcripts , 2006, Nucleic Acids Res..

[52]  Ewan Birney,et al.  Automated generation of heuristics for biological sequence comparison , 2005, BMC Bioinformatics.

[53]  Steven Salzberg,et al.  TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders , 2004, Bioinform..

[54]  Stephen M. Mount,et al.  Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. , 2003, Nucleic acids research.

[55]  R. Pasquet.  Allozyme diversity of cultivated cowpea Vigna unguiculata (L.) Walp. , 2000, Theoretical and Applied Genetics.

[56]  Bernard R. Baum,et al.  Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components , 1997, Plant Molecular Biology Reporter.

[57]  Ratikanta Behura,et al.  Cowpea [Vigna unguiculata (L.) Walp]. , 2015, Methods in molecular biology.

[58]  J. Verbelen,et al.  Over-expression of AtEXLA2 alters etiolated arabidopsis hypocotyl growth. , 2015, Annals of botany.

[59]  M. Timko,et al.  Cowpea, a multifunctional legume. , 2008 .

[60]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[61]  R. Pasquet.  Morphological study of cultivated cowpea Vigna unguiculata (L.) Walp. Importance of ovule number and definition of cv gr Melanophthalmus , 1998 .

[62]  O. Chambliss,et al.  Recent advances in cowpea breeding , 1997 .