Genome assembly and resequencing analyses provide new insights into the evolution, domestication and ornamental traits of crape myrtle

Yang Zhou , Tangchun Zheng , Ming Cai , Lu Feng , Xiufeng Chi , Ping Shen , Xin Wang , Zhiting Wan , Cunquan Yuan , Man Zhang , Yu Han , Jia Wang , Huitang Pan , Tangren Cheng , Qixiang Zhang

Horticulture Research ›› 2023, Vol. 10 ›› Issue (9) : 146

PDF (7689KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (9) :146 DOI: 10.1093/hr/uhad146
Article
research-article
Genome assembly and resequencing analyses provide new insights into the evolution, domestication and ornamental traits of crape myrtle
Author information +
History +
PDF (7689KB)

Abstract

Crape myrtle (Lagerstroemia indica) is a globally used ornamental woody plant and is the representative species of Lagerstroemia. However, studies on the evolution and genomic breeding of L. indica have been hindered by the lack of a reference genome. Here we assembled the first high-quality genome of L. indica using PacBio combined with Hi-C scaffolding to anchor the 329.14-Mb genome assembly into 24 pseudochromosomes. We detected a previously undescribed independent whole-genome triplication event occurring 35.5 million years ago in L. indica following its divergence from Punica granatum. After resequencing 73 accessions of Lagerstroemia, the main parents of modern crape myrtle cultivars were found to be L. indica and L. fauriei. During the process of domestication, genetic diversity tended to decrease in many plants, but this was not observed in L. indica. We constructed a high-density genetic linkage map with an average map distance of 0.33 cM. Furthermore, we integrated the results of quantitative trait locus (QTL) using genetic mapping and bulk segregant analysis (BSA), revealing that the major-effect interval controlling internode length (IL) is located on chr1, which contains CDL15, CRG98, and GID1b1 associated with the phytohormone pathways. Analysis of gene expression of the red, purple, and white flower-colour flavonoid pathways revealed that differential expression of multiple genes determined the flower colour of L. indica, with white flowers having the lowest gene expression. In addition, BSA of purple- and green-leaved individuals of populations of L. indica was performed, and the leaf colour loci were mapped to chr12 and chr17. Within these intervals, we identified MYB35, NCED, and KAS1. Our genome assembly provided a foundation for investigating the evolution, population structure, and differentiation of Myrtaceae species and accelerating the molecular breeding of L. indica.

Cite this article

Download citation ▾
Yang Zhou, Tangchun Zheng, Ming Cai, Lu Feng, Xiufeng Chi, Ping Shen, Xin Wang, Zhiting Wan, Cunquan Yuan, Man Zhang, Yu Han, Jia Wang, Huitang Pan, Tangren Cheng, Qixiang Zhang. Genome assembly and resequencing analyses provide new insights into the evolution, domestication and ornamental traits of crape myrtle. Horticulture Research, 2023, 10 (9) : 146 DOI:10.1093/hr/uhad146

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by National Key R&D Program of China (2019YFD1001004, 2019YFD1000402), the program for Science and Technology of Beijing (Z181100002418006) and the Special Fund for Beijing Common Construction Project.

Author contributions

Q.X.Z., H.T.P., and T.R.C. conceived and designed experiments. Y.Z., T.C.Z., M.C., L.F., X.W., C.Q.Y., M.Z., Y.H., and J.W. collected all materials and phenotypic data. Y.Z., T.C.Z., and M.C. contributed to genome sequencing and assembly. Y.Z., T.C.Z., X.F.C., P.S., and Z.T.W. contributed to SNP calling, population analysis, genetic map construction, transcriptome sequencing, and BSA analysis. Y.Z., T.C.Z., and H.T.P. wrote the manuscript. Q.X.Z. and T.R.C. revised and finalized the manuscript. All authors approved the manuscript before submission.

Data availability

The final assembly and annotation of the L. indica genome, the whole-genome sequences, raw resequencing data of populations, and raw transcriptome RNA-seq data are available at the National Genomics Data Centre (NGDC) under BioProject ID PRJCA013427.

Conflict of interest

The authors declare that they have no conflict of interest.

References

[1]

Foce Committee, C. Flora of China. Beijing: Science Press; 2007.

[2]

Chen J, Cheng X . The Classic of Flower in China. Shanghai: Shanghai Culture Publishing House; 1993.

[3]

Pooler M . Crapemyrtle - Lagerstroemia indica. In Anderson NO (ed.), Flower Breeding and Genetics: Issues, Challenges and Opportunities for the 21st Century. New York: Springer, 2006, 439-57.

[4]

Zhang Q . Studies on cultivars of crape-myrtles (Lagerstroemia indica) and their uses in urban greening. J Beijing For Univ. 1991; 4: 57-66.

[5]

Egolf DR . The Lagerstroemia Handbook/Checklist: A Guide to Crape-myrtle Cultivars. Wilmington: American Association of Botanical Gardens and Arboreta; 1978.

[6]

Wang J, Liu X, Chen Z . Research progress in breeding of Lagerstroemia plant. Acta Hortic Sin. 2013; 9: 1795-804.

[7]

Ju Y, Feng L, Wu J et al. Transcriptome analysis of the genes regulating phytohormone and cellular patterning in Lagerstroemia plant architecture. Sci Rep. 2018; 8: 15162.

[8]

Zhou Y, Ju Y, Chi X et al. Three CYCDs positively regulate plant height of crape myrtle by increasing cell division. Sci Hortic. 2023; 315: 111954.

[9]

Zhou Y, Ye Y, Feng L. et al. A genetic linkage map of BC2 population reveals QTL associated with plant architecture traits in Lagerstroemia . Forests. 2021; 12: 322.

[10]

Lin QF, Liu T, Liu J et al. Flavonoids composition and content in petals of Lagerstroemia and Heimia species and cultivars. Acta Hortic Sin. 2021; 48: 12.

[11]

Li Y, Zhang Z, Wang P et al. Comprehensive transcriptome analysis discovers novel candidate genes related to leaf color in a Lagerstroemia indica yellow leaf mutant. Genes Genomics. 2015; 37: 851-63.

[12]

Qiao Z, Liu S, Zeng H et al. Exploring the molecular mechanism underlying the stable purple-red leaf phenotype in Lagerstroemia indica cv. Ebony Embers. Int J Mol Sci. 2019; 20: 5636.

[13]

Zheng T, Li P, Li L et al. Research advances in and prospects of ornamental plant genomics. Hortic Res. 2021; 8: 65.

[14]

Zhao G, Lian Q, Zhang Z et al. A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat Genet. 2019; 51: 1607-15.

[15]

Cai X, Sun X, Xu C et al. Genomic analyses provide insights into spinach domestication and the genetic basis of agronomic traits. Nat Commun. 2021; 12: 7246.

[16]

Myburg AA, Grattapaglia D, Tuskan GA et al. The genome of Eucalyptus grandis. Nature. 2014; 510: 356-62.

[17]

Luo X, Li H, Wu Z et al. The pomegranate (Punica granatum L.) draft genome dissects genetic divergence between soft- and hard-seeded cultivars. Plant Biotechnol J. 2020; 18: 955-68.

[18]

Lu RS, Chen Y, Zhang XY et al. Genome sequencing and transcriptome analyses provide insights into the origin and domestication of water caltrop (Trapa spp., Lythraceae). Plant Biotechnol J. 2022; 20: 761-76.

[19]

Ouadi S, Sierro N, Goepfert S et al. The clove (Syzygium aromaticum) genome provides insights into the eugenol biosynthesis pathway. Commun Biol. 2022; 5: 684.

[20]

Majoros WH, Pertea M, Salzberg SL . TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics. 2004; 20: 2878-9.

[21]

Wang J, Yang B, Pan L et al. Karyotype analysis of Lagerstroemia species with 45S rDNA-FISH. Acta Botan Boreali-Occiden Sin. 2016; 1: 30-6.

[22]

Liu T, Liang X, Zhang Y et al. Determination of 13 taxa of Lagerstroemia L. and two closely related genera. J Plant Genet Resour. 2020; 4: 1020-9.

[23]

Badouin H, Gouzy J, Grassa CJ et al. The sunflower genome provides insights into oil metabolism, flowering and asterid evolution. Nature. 2017; 546: 148-52.

[24]

Laureano-Marin AM, Aroca Á, Pérez-Pérez ME et al. Abscisic acid-triggered persulfidation of the cys protease ATG4 mediates regulation of autophagy by sulfide. Plant Cell. 2020; 32: 3902-20.

[25]

Wang J, He W, Liao X et al. Phylogeny, molecular evolution, and dating of divergences in Lagerstroemia using plastome sequences. Hortic Plant J. 2023; 9: 345-55.

[26]

Zhang L, Wu S, Chang X et al. The ancient wave of polyploidization events in flowering plants and their facilitated adaptation to environmental stress. Plant Cell Environ. 2020; 43: 2847-56.

[27]

Hao Y, Zhou YZ, Chen B et al. The Melastoma dodecandrum genome and the evolution of Myrtales. J Genet Genomics. 2022; 49: 120-31.

[28]

Liang Y, Li F, Gao Q et al. The genome of Eustoma grandiflorum reveals the whole-genome triplication event contributing to ornamental traits in cultivated Lisianthus. Plant Biotechnol J. 2022; 20: 1856-8.

[29]

Yang FS, Nie S, Liu H et al. Chromosome-level genome assembly of a parent species of widely cultivated azaleas. Nat Commun. 2020; 11: 5269.

[30]

O’Brien CL, Huber M, Thomas E et al. The enigma of Oligocene climate and global surface temperature evolution. Proc Natl Acad Sci USA. 2020; 117: 25302-9.

[31]

Akagi T, Shirasawa K, Nagasaki H et al. The persimmon genome reveals clues to the evolution of a lineage-specific sex determination system in plants. PLoS Genet. 2020; 16: e1008566.

[32]

Duan N, Bai Y, Sun H et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat Commun. 2017; 8: 249.

[33]

De Wilde WJJO, Duyfjes BEE . Survey of Lagerstroemia L. (Lythraceae) in Indochina (excl. Thailand) with the description of Lagerstroemia densiflora, sp. nov., a new species from Vietnam. Adansonia. 2016; 38: 241-55.

[34]

Egolf DR . ‘Choctaw’ Lugerstroemia. HortScience. 1990; 25: 992-3.

[35]

Chen W, Chen L, Zhang X. et al. Convergent selection of a WD40 protein that enhances grain yield in maize and rice. Science. 2022; 375: eabg7985.

[36]

Krost C, Petersen R, Lokan S et al. Evaluation of the hormonal state of columnar apple trees (Malus x domestica) based on high throughput gene expression studies. Plant Mol Biol. 2013; 81: 211-20.

[37]

Wang L, Ming L, Liao K et al. Bract suppression regulated by the miR156/529-SPLs-NL1-PLA1 module is required for the transition from vegetative to reproductive branching in rice. Mol Plant. 2021; 14: 1168-84.

[38]

Duan E, Wang Y, Li X et al. OsSHI1 regulates plant architecture through modulating the transcriptional activity of IPA1 in rice. Plant Cell. 2019; 31: 1026-42.

[39]

Zhang X, Lin Z, Wang J et al. The tin1 gene retains the function of promoting tillering in maize. Nat Commun. 2019; 10: 5608.

[40]

Maurya JP, Miskolczi PC, Mishra S et al. A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen. Proc Natl Acad Sci USA. 2020; 117: 11523-30.

[41]

Hill JL Jr, Hollender CA . Branching out: new insights into the genetic regulation of shoot architecture in trees. Curr Opin Plant Biol. 2019; 47: 73-80.

[42]

Wang B, Smith SM, Li J . Genetic regulation of shoot architecture. Annu Rev Plant Biol. 2018; 69: 437-68.

[43]

Ye Y, Wu JY, Feng L et al. Heritability and gene effects for plant architecture traits of crape myrtle using major gene plus polygene inheritance analysis. Sci Hortic. 2017; 225: 335-42.

[44]

Qu L, Wei Z, Chen HH et al. Plant casein kinases phosphorylate and destabilize a cyclin-dependent kinase inhibitor to promote cell division. Plant Physiol. 2021; 187: 917-30.

[45]

Su S, Hong J, Chen X et al. Gibberellins orchestrate panicle architecture mediated by DELLA-KNOX signalling in rice. Plant Biotechnol J. 2021; 19: 2304-18.

[46]

Van De Velde K, Thomas SG, Heyse F et al. N-terminal truncated RHT-1 proteins generated by translational reinitiation cause semi-dwarfing of wheat green revolution alleles. Mol Plant. 2021; 14: 679-87.

[47]

Cheng J, Zhang M, Tan B et al. A single nucleotide mutation in GID1c disrupts its interaction with DELLA1 and causes a GA-insensitive dwarf phenotype in peach. Plant Biotechnol J. 2019; 17: 1723-35.

[48]

Yang FX, Gao J, Wei YL et al. The genome of Cymbidium sinense revealed the evolution of orchid traits. Plant Biotechnol J. 2021; 19: 2501-16.

[49]

Zhang J, Wang LS, Gao JM et al. Determination of anthocyanins and exploration of relationship between their composition and petal coloration in crape myrtle (Lagerstroemia hybrid). J Integr Plant Biol. 2008; 50: 581-8.

[50]

Ma B, Wu J, Shi TL et al. Lilac (Syringa oblata) genome provides insights into its evolution and molecular mechanism of petal color change. Commun Biol. 2022; 5: 686.

[51]

Zhou LJ, Geng Z, Wang Y et al. A novel transcription factor CmMYB012 inhibits flavone and anthocyanin biosynthesis in response to high temperatures in chrysanthemum. Hortic Res. 2021; 8: 248.

[52]

Su W, Tao R, Liu W et al. Characterization of four polymorphic genes controlling red leaf colour in lettuce that have undergone disruptive selection since domestication. Plant Biotechnol J. 2020; 18: 479-90.

[53]

Li X, Cai K, Han Z et al. Chromosome-level genome assembly for Acer pseudosieboldianum and highlights to mechanisms for leaf color and shape change. Front Plant Sci. 2022; 13: 850054.

[54]

Gould KS . Nature’s Swiss Army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol. 2004; 2004: 314-20.

[55]

Wei K, Wang L, Zhang Y et al. A coupled role for CsMYB75 and CsGSTF1 in anthocyanin hyperaccumulation in purple tea. Plant J. 2019; 97: 825-40.

[56]

Zhang Q, Wang L, Liu Z et al. Transcriptome and metabolome profiling unveil the mechanisms of Ziziphus jujuba Mill. Peel coloration. Food Chem. 2020; 312: 125903.

[57]

Zhang Z, Tian C, Zhang Y et al. Transcriptomic and metabolomic analysis provides insights into anthocyanin and procyanidin accumulation in pear. BMC Plant Biol. 2020; 20: 129.

[58]

Jiang F, Zhang J, Wang S et al. The apricot (Prunus armeniaca L.) genome elucidates Rosaceae evolution and beta-carotenoid synthesis. Hortic Res. 2019; 6: 128.

[59]

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25: 1754-60.

[60]

Li H, Handsaker B, Wysoker A et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25: 2078-9.

[61]

Wang K, Li M, Hakonarson H . ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010; 38: e164.

[62]

Servant N, Varoquaux N, Lajoie BR et al. HiC-pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol. 2015; 16: 259.

[63]

Durand NC, Shamim MS, Machol I et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 2016; 3: 95-8.

[64]

Dudchenko O, Batra SS, Omer AD et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017; 356: 92-5.

[65]

Xu Z, Wang H . LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007; 35: W265-8.

[66]

Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999; 27: 573-80.

[67]

Stanke M, Keller O, Gunduz I et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006; 34: W435-9.

[68]

Burge C, Karlin S . Prediction of complete gene structures in human genomic DNA. J Mol Biol. 1997; 268: 78-94.

[69]

Kent WJ . BLAT-the BLAST-like alignment tool. Genome Res. 2002; 12: 656-64.

[70]

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

[71]

Kim D, Langmead B, Salzberg SL . HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015; 12: 357-60.

[72]

Pertea M, Pertea GM, Antonescu CM et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015; 33: 290-5.

[73]

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.

[74]

Lowe TM, Eddy SR . tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25: 955-64.

[75]

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

[76]

Edgar RC . MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32: 1792-7.

[77]

Huelsenbeck JP, Ronquist F . MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17: 754-5.

[78]

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

[79]

De Bie T, Cristianini N, Demuth JP et al. CAFE: a computational tool for the study of gene family evolution. Bioinformatics. 2006; 22: 1269-71.

[80]

Yang Z, Nielsen R . Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 2002; 19: 908-17.

[81]

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.

[82]

Chen C, Chen H, Zhang Y et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13: 1194-202.

[83]

Yang J, Lee SH, Goddard ME et al. GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet. 2011; 88: 76-82.

[84]

Schiffels S, Durbin R . Inferring human population size and separation history from multiple genome sequences. Nat Genet. 2014; 46: 919-25.

[85]

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.

[86]

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

[87]

Rastas P . Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data. Bioinformatics. 2017; 33: 3726-32.

[88]

Weigel D, Glazebrook J . Transformation of Agrobacterium using the freeze-thaw method. CSH Protoc. 2006; 7: pdb.prot4666.

[89]

Clough SJ, Bent AF . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998; 16: 735-43.

[90]

Chen Y, Chen Y, Shi C et al. SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. Gigascience. 2018; 7: 1-6.

[91]

Trapnell C, Roberts A, Goff L et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012; 7: 562-78.

[92]

Kong L, Zhang Y, Ye ZQ et al. CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 2007; 35: W345-9.

[93]

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.

[94]

Langmead B, Salzberg SL . Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9: 357-9.

[95]

Li B, Dewey CN . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12: 323.

PDF (7689KB)

81

Accesses

0

Citation

Detail

Sections
Recommended

/