Genome assembly and resequencing shed light on evolution, population selection, and sex identification in Vernicia montana

Wenying Li , Xiang Dong , Xingtan Zhang , Jie Cao , Meilan Liu , Xu Zhou , Hongxu Long , Heping Cao , Hai Lin , Lin Zhang

Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) : 141

PDF (12137KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) :141 DOI: 10.1093/hr/uhae141
Article
research-article
Genome assembly and resequencing shed light on evolution, population selection, and sex identification in Vernicia montana
Author information +
History +
PDF (12137KB)

Abstract

Vernicia montana is a dioecious plant widely cultivated for high-quality tung oil production and ornamental purposes in the Euphorbiaceae family. The lack of genomic information has severely hindered molecular breeding for genetic improvement and early sex identification in V. montana. Here, we present a chromosome-level reference genome of a male V. montana with a total size of 1.29 Gb and a contig N50 of 3.69 Mb. Genome analysis revealed that different repeat lineages drove the expansion of genome size. The model of chromosome evolution in the Euphorbiaceae family suggests that polyploidization-induced genomic structural variation reshaped the chromosome structure, giving rise to the diverse modern chromosomes. Based on whole-genome resequencing data and analyses of selective sweep and genetic diversity, several genes associated with stress resistance and flavonoid synthesis such as CYP450 genes and members of the LRR-RLK family, were identified and presumed to have been selected during the evolutionary process. Genome-wide association studies were conducted and a putative sex-linked insertion and deletion (InDel) (Chr 2: 102 799 917-102 799 933 bp) was identified and developed as a polymorphic molecular marker capable of effectively detecting the gender of V. montana. This InDel is located in the second intron of VmBASS4, suggesting a possible role of VmBASS4 in sex determination in V. montana. This study sheds light on the genome evolution and sex identification of V. montana, which will facilitate research on the development of agronomically important traits and genomics-assisted breeding.

Cite this article

Download citation ▾
Wenying Li, Xiang Dong, Xingtan Zhang, Jie Cao, Meilan Liu, Xu Zhou, Hongxu Long, Heping Cao, Hai Lin, Lin Zhang. Genome assembly and resequencing shed light on evolution, population selection, and sex identification in Vernicia montana. Horticulture Research, 2024, 11 (7) : 141 DOI:10.1093/hr/uhae141

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This study was supported by the National Natural Science Foundation of China (grants. 32171843, 32230073), and the Science and Technology Innovation Program of Hunan Province (2022RC3055). We thank Tao Ma, Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China, for providing suggestions on the research design of the study. We thank PubBio-Tech, Wuhan, for providing suggestions on the phylogenetic and genome-wide association analysis.

Author contributions

L.Z. and W.L. contributed to the conception and design of the study. Field and lab experiments, plant materials collection, and data analysis were performed by W.L., X.D., J.C., M.L., X.Z., H.L., and L.Z. The first draft of the manuscript was written by L.Z. and W.L.. X.Z., H.C., and H.L. gave some useful comments and revised the manuscript. All authors read and commented on the manuscript.

Data Availability Statement

The PacBio sequencing data, Hi-C data, ISO-seq data, and resequencing short reads have been deposited in the Genome Sequence Archive (Genomics, Proteomics & Bioinformatics 2021) in the National Genomics Data Center (Nucleic Acids Res 2022), China National Center for Bioinformation / Beijing Institute of Genomics, Chinese Academy of Sciences (GSA: CRA007017 and CRA009450) that are publicly accessible at https://ngdc.cncb.ac.cn/gsa.

Conflict of Interests

The authors declare that they have no conflicts of interest associated with this work.

Supplementary Information

Supplementary data is available at Horticulture Research online.

References

[1]

Cao HP, Zhang L, Tan XF. et al. Identification, classification and differential expression of Oleosin genes in Tung tree (Vernicia fordii). PLoS One. 2014; 9:e88409-e88409

[2]

Chen YH, Chen JH, Chang CY. et al. Biodiesel production from tung (Vernicia montana) oil and its blending properties in different fatty acid compositions. Bioresour Technol. 2010; 101:9521-6

[3]

Wang Y, Luo A, Lyu T. et al. Global distribution and evolutionary transitions of angiosperm sexual systems. Ecol Lett. 2021; 24:1835-47

[4]

Li WY, Chen JZ, Dong X. et al. Flower development and sexual dimorphism in Vernicia montana. Horticultural Plant Journal. 2024; 10:586-600

[5]

Akagi T, Henry I, Ohtani H. et al. A Y-encoded suppressor of feminization arose via lineage-specific duplication of a cytokinin response regulator in kiwifruit. Plant Cell. 2018; 30:780-95

[6]

Akagi T, Pilkington SM, Varkonyi-Gasic E. et al. Two Y-chromosome-encoded genes determine sex in kiwifruit. Nature Plants. 2019; 5:801-9

[7]

Zhang L, Liu M, Long H. et al. Tung tree (Vernicia fordii) genome provides a resource for understanding genome evolution and improved oil production. Genomics Proteomics & Bioinformatics. 2019; 17:558-75

[8]

Charlesworth D. Plant sex determination and sex chromosomes. Heredity. 2002; 88:94-101

[9]

Henry IM, Akagi T, Tao R. et al. One hundred ways to invent the sexes: theoretical and observed paths to dioecy. Annu Rev Plant Biol. 2018; 69:553-75

[10]

Jiao Y, Paterson AH. Polyploidy-associated genome modifications during land plant evolution. Philosophical Transactions of the Royal Society B-Biological Sciences. 2014; 369:20130355

[11]

Yu J, Wang L, Guo H. et al. Genome evolutionary dynamics followed by diversifying selection explains the complexity of the Sesamum indicum genome. BMC Genomics. 2017; 18:257

[12]

Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980; 16:111-20

[13]

Mimida N, Kotoda N, Ueda T. et al. Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus x domestica Borkh.). Plant Cell Physiol. 2009; 50:394-412

[14]

Varkonyi-Gasic E, Wang T, Voogd C. et al. Mutagenesis of kiwifruit CENTRORADIALIS-like genes transforms a climbing woody perennial with long juvenility and axillary flowering into a compact plant with rapid terminal flowering. Plant Biotechnol J. 2019; 17:869-80

[15]

Zhang F, Wang Y, Irish VF. CENTRORADIALIS maintains shoot meristem indeterminacy by antagonizing THORN IDENTITY1 in citrus. Curr Biol. 2021; 31:2261

[16]

Webster GL. Classification of the Euphorbiaceae. Ann Mo Bot Gard. 1994; 81:3

[17]

Soto JC, Ortiz JF, Perlaza-Jiménez L. et al. A genetic map of cassava (Manihot esculenta Crantz) with integrated physical mapping of immunity-related genes. BMC Genomics. 2015; 16:190

[18]

Lau NS, Makita Y, Kawashima M. et al. The rubber tree genome shows expansion of gene family associated with rubber biosynthesis. Sci Rep. 2016; 6:28594

[19]

Ha J, Shim S, Lee T. et al. Genome sequence of Jatropha curcas L., a non-edible biodiesel plant, provides a resource to improve seed-related traits. Plant Biotechnol J. 2019; 17:517-30

[20]

Lu J, Pan C, Fan W. et al. A chromosome-level genome assembly of wild castor provides new insights into its adaptive evolution in tropical desert. Genomics Proteomics & Bioinformatics. 2022; 20:42-59

[21]

Angiosperm Phylogeny Group, Chase MW, Christenhusz MJM. et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc. 2016; 181:1-20

[22]

Li H-T, Yi TS, Gao LM. et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nature Plants. 2019; 5:461-70

[23]

Zhang L, Chen F, Zhang X. et al. The water lily genome and the early evolution of flowering plants. Nature. 2020; 577:79-84

[24]

Zhao L, Li X, Zhang N. et al. Phylogenomic analyses of large-scale nuclear genes provide new insights into the evolutionary relationships within the rosids. Mol Phylogenet Evol. 2016; 105:166-76

[25]

Rice DW, Alverson AJ, Richardson AO. et al. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science. 2013; 342:1468-73

[26]

Stegemann S, Greiner S. et al. Keuthe M, Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA. 2012; 109:2434-8

[27]

Smith DR. Mutation rates in plastid genomes: they are lower than you might think. Genome Biology and Evolution. 2015; 7:1227-34

[28]

Li W, Fu W, Hou J. et al. Evolution of plant sex and molecular mechanisms underlying plants sex separation. Forestry Research. 2023; 3:0

[29]

Liang S, Li Y, Chen Y. et al. Application and prospects of single-cell and spatial omics technologies in woody plants. Forestry Research. 2023; 3:0

[30]

Liao Z, Zhang TW, Lei WL. et al. A telomere-to-telomere reference genome of ficus (Ficus hispida) provides new insights into sex determination. Horticulture Research. 2024; 11:uhad257

[31]

Zhang X, Wang G, Zhang SC. et al. Genomes of the banyan tree and pollinator wasp provide insights into fig-wasp coevolution. Cell. 2020; 183:875-889.e17

[32]

Harkess A, Zhou J, Xu C. et al. The asparagus genome sheds light on the origin and evolution of a young Y chromosome. Nat Commun. 2017; 8:1279

[33]

Harkess A, Huang K, van der Hulst R. et al. Sex determination by two Y-linked genes in garden asparagus. Plant Cell. 2020; 32:1790-6

[34]

Renner SS, Müller NA. Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration. Nature Plants. 2021; 7:392-402

[35]

Durand NC, Robinson JT, Shamim MS. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Systems. 2016; 3:99-101

[36]

Marçais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011; 27:764-70

[37]

Xiao CL, Chen Y, Xie SQ. et al. MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads. Nat Methods. 2017; 14:1072-4

[38]

Burton JN, Adey A, Patwardhan RP. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol. 2013; 31:1119-25

[39]

Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. 2013; 0:1-3

[40]

Ou S, Su W, Liao Y. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 2019; 20:275

[41]

Campbell MS, Holt C, Moore B. et al. Genome annotation and curation using MAKER and MAKER-P. Curr Protoc Bioinformatics. 2014; 48:4-11

[42]

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30:2114-20

[43]

Kim D, Paggi JM, Park C. et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37:907-15

[44]

Stanke M, Steinkamp R, Waack S. et al. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 2004; 32:W309-12

[45]

Birney E, Clamp M, Durbin R. GeneWise and Genomewise. Genome Res. 2004; 14:988-95

[46]

Manni M, Berkeley MR, Seppey M. et al. BUSCO: assessing genomic data quality and beyond. Current Protocols. 2021; 1:e323-e323

[47]

Schneider M, Tognolli M, Bairoch A. The Swiss-Prot protein knowledgebase and ExPASy: providing the plant community with high quality proteomic data and tools. Plant Physiol Biochem. 2004; 42:1013-21

[48]

Finn RD, Bateman A, Clements J. et al. Pfam: the protein families database. Nucleic Acids Res. 2014; 42:D222-30

[49]

Ashburner M, Ball CA, Blake JA. et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25:25-9

[50]

Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000; 28:27-30

[51]

Chan PP, Lin BY, Mak AJ. et al. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res. 2021; 49:9077-96

[52]

Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003; 13:2178-89

[53]

Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006; 34:W609-12

[54]

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009; 25:1972-3

[55]

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30:1312-3

[56]

Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24:1586-91

[57]

Kumar S, Stecher G, Suleski M. et al. TimeTree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol. 2017; 34:1812-9

[58]

Wang Y, Tang H, DeBarry JD. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40:e49-e49

[59]

Murat F, Armero A, Pont C. et al. Reconstructing the genome of the most recent common ancestor of flowering plants. Nat Genet. 2017; 49:490-6

[60]

Weber JA, Aldana R, Gallagher BD. et al. Sentieon DNA pipeline for variant detection-software-only solution, over 20 × faster than GATK 3.3 with identical results. Peer J PrePrints. 2016; 4:e1672v2

[61]

McKenna A, Hanna M, Banks E. et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation dna sequencing data. Genome Res. 2010; 20:1297-303

[62]

Danecek P, Auton A, Abecasis G. et al. The variant call format and VCFtools. Bioinformatics. 2011; 27:2156-8

[63]

Alexander DH, Lange K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics. 2011; 12:246

[64]

Zhang C, Dong SS, Xu JY. et al. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics. 2019; 35:1786-8

[65]

Zhou X, Stephens M. Efficient multivariate linear mixed model algorithms for genome-wide association studies. Nat Methods. 2014; 11:407-9

[66]

Li MX, Yeung JM, Cherny SS. et al. Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet. 2012; 131:747-56

[67]

Dong S, He W, Ji J. et al. LDBlockShow: a fast and convenient tool for visualizing linkage disequilibrium and haplotype blocks based on variant call format files. Brief Bioinform. 2021; 22:bbaa227

PDF (12137KB)

106

Accesses

0

Citation

Detail

Sections
Recommended

/