Discovery and annotation of a novel transposable element family in Gossypium

[en] Background: Fluorescence in situ hybridization (FISH) is an efficient cytogenetic technology to study chromosome structure. Transposable element (TE) is an important component in eukaryotic genomes and can provide insights in the structure and evolution of eukaryotic genomes. Results: A FISH probe derived from bacterial artificial chromosome (BAC) clone 299N22 generated striking signals on all 26 chromosomes of the cotton diploid A genome (AA, 2x=26) but very few on the diploid D genome (DD, 2x=26). All 26 chromosomes of the A sub genome (At) of tetraploid cotton (AADD, 2n=4x=52) also gave positive signals with this FISH probe, whereas very few signals were observed on the D sub genome (Dt). Sequencing and annotation of BAC clone 299N22, revealed a novel Ty3/gypsy transposon family, which was named as ‘CICR’. This family is a significant contributor to size expansion in the A (sub) genome but not in the D (sub) genome. Further FISH analysis with the LTR of CICR as a probe revealed that CICR is lineage-specific, since massive repeats were found in A and B genomic groups, but not in C–G genomic groups within the Gossypium genus. Molecular evolutionary analysis of CICR suggested that tetraploid cottons evolved after silence of the transposon family 1–1.5 million years ago (Mya). Furthermore, A genomes are more homologous with B genomes, and the C, E, F, and G genomes likely diverged from a common ancestor prior to 3.5–4 Mya, the time when CICR appeared. The genomic variation caused by the insertion of CICR in the A (sub) genome may have played an important role in the speciation of organisms with A genomes. Conclusions: The CICR family is highly repetitive in A and B genomes of Gossypium, but not amplified in the C–G genomes. The differential amount of CICR family in At and Dt will aid in partitioning sub genome sequences for chromosome assemblies during tetraploid genome sequencing and will act as a method for assessing the accuracy of tetraploid genomes by looking at the proportion of CICR elements in resulting pseudochromosome sequences. The timeline of the expansion of CICR family provides a new reference for cotton evolutionary analysis, while the impact on gene function caused by the insertion of CICR elements will be a target for further analysis of investigating phenotypic differences between A genome and D genome species.

Disciplines :

Agriculture & agronomy

Author, co-author :

Lu, Hejun ; Université de Liège - ULiège > Terra

Cui, Xinglei

Liu, Zhen

Liu, Yuling

Wang, Xingxing

Zhou, Zhongli

Cai, Xiaoyan

Zhenmai, Zhang

Language :

English

Title :

Discovery and annotation of a novel transposable element family in Gossypium

Publication date :

28 November 2018

Journal title :

BMC Plant Biology

eISSN :

1471-2229

Publisher :

BioMed Central, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 12 December 2019

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Bibliography

Thomas CA Jr. The genetic organization of chromosomes. Annu Rev Genet. 1971;5(1):237-56.
Ibarra-Laclette E, Lyons E, Hernandez-Guzman G, Anahi Perez-Torres C, Carretero-Paulet L, Chang T-H, Lan T, Welch AJ, Abraham Juarez MJ, Simpson J, et al. Architecture and evolution of a minute plant genome. Nature. 2013;498(7452):94-+.
Kellogg EA, Bennetzen JL. The evolution of nuclear genome structure in seed plants. Am J Bot. 2004;91(10):1709-25.
Deutsch M, Long M. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 1999;27(15):3219-28.
Ku HM, Vision T, Liu JP, Tanksley SD. Comparing sequenced segments of the tomato and Arabidopsis genomes: Large-scale duplication followed by selective gene loss creates a network of synteny. Proc Natl Acad Sci USA. 2000;97(16):9121-6.
Vision TJ, Brown DG, Tanksley SD. The origins of genomic duplications in Arabidopsis. Science. 2000;290(5499):2114-7.
Adams KL, Palmer JD. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol. 2003;29(3):380-95.
Petrov D, Wendel J. Evolution of eukaryotic genome structure. In: Evolutionary genetics: Concepts and case studies; 2006.
Bennetzen JL, Wang H. The Contributions of Transposable Elements to the Structure, Function, and Evolution of Plant Genomes. Annu Rev Plant Biol. 2014;65:505-30.
Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF. Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res. 2006;16(10):1252-61.
Kidwell MG. Transposable elements and the evolution of genome size in eukaryotes. Genetica. 2002;115(1):49-63.
Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, et al. Doubling genome size without polyploidization: Dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 2006;16(10):1262-9.
Sanmiguel P, Bennetzen JL. Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot. 1998;82:37-44.
Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, et al. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol. 2015;33(5):531-U252.
Yuan D, Tang Z, Wang M, Gao W, Tu L, Jin X, Chen L, He Y, Zhang L, Zhu L, et al. The genome sequence of Sea-Island cotton (Gossypium barbadense) provides insights into the allopolyploidization and development of superior spinnable fibres. Sci Rep. 2015;5(1):17662.
Liu X, Zhao B, Zheng H-J, Hu Y, Lu G, Yang C-Q, Chen J-D, Chen J-J, Chen D-Y, Zhang L, et al. Gossypium barbadense genome sequence provides insight into the evolution of extra-long staple fiber and specialized metabolites. Sci Rep. 2015;5(1):14139.
Li F, Fan G, Lu C, Xiao G, Zou C, Kohel RJ, Ma Z, Shang H, Ma X, Wu J, et al. Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol. 2015;33(5):524-U242.
Li F, Fan G, Wang K, Sun F, Yuan Y, Song G, Li Q, Ma Z, Lu C, Zou C, et al. Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet. 2014;46(6):567-72.
Wang K, Wang Z, Li F, Ye W, Wang J, Song G, Yue Z, Cong L, Shang H, Zhu S, et al. The draft genome of a diploid cotton Gossypium raimondii. Nat Genet. 2012;44(10):1098-+.
Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker KC, Shu S, Udall J, et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature. 2012;492(7429):423-+.
Grover CE, Grupp KK, Wanzek RJ, Wendel JF. Assessing the monophyly of polyploid Gossypium species. Plant Syst Evol. 2012;298(6):1177-83.
Hendrix B, Stewart JM. Estimation of the nuclear DNA content of Gossypium species. Ann Bot. 2005;95(5):789-97.
Wendel JF, Cronn RC. Polyploidy and the evolutionary history of cotton. Adv Agron. 2003, 78:139-86.
Grover CE, Zhu X, Grupp KK, Jareczek JJ, Gallagher JP, Szadkowski E, Seijo JG, Wendel JF. Molecular confirmation of species status for the allopolyploid cotton species, Gossypium ekmanianum Wittmack. Genet Resour Crop Evol. 2015;62(1):103-14.
Wang K, Guan B, Guo W, Zhou B, Hu Y, Zhu Y, Zhang T. Completely distinguishing individual a-genome chromosomes and their Karyotyping analysis by multiple bacterial artificial chromosome-fluorescence in situ hybridization. Genetics. 2008;178(2):1117-22.
Choi H-I, Waminal NE, Park HM, Kim N-H, Choi BS, Park M, Choi D, Lim YP, Kwon S-J, Park B-S, et al. Major repeat components covering one-third of the ginseng (Panax ginseng C.A. Meyer) genome and evidence for allotetraploidy. Plant J. 2014;77(6):906-16.
Liu Y, Peng R, Liu F, Wang X, Cui X, Zhou Z, Wang C, Cai X, Wang Y, Lin Z, et al. A Gossypium BAC clone contains key repeat components distinguishing subgenome of allotetraploidy cottons. Mol Cytogenet. 2016;9:27.
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45(D1):D200-3.
Kohany O, Gentles AJ, Hankus L, Jurka J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinf. 2006;7(1):474.
Bao W, Kojima KK, Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob DNA. 2015;6(1):11.
Wang K, Wang W, Wang C, Song G, Cui R, Li S, Zhang X. Studies of FISH and karyotype of Gossypium barbadense. Yi chuan xue bao. 2000;28(1):69-75.
Peng R, Zhang T, Liu F, Ling J, Wang C, Li S, Zhang X, Wang Y, Wang K. Preparations of meiotic pachytene chromosomes and extended DNA fibers from cotton suitable for fluorescence in situ hybridization. PloS One. 2012;7(3):e33847.
Cui X, Liu F, Liu Y, Zhou Z, Zhao Y, Wang C, Wang X, Cai X, Wang Y, Meng F, et al. Construction of cytogenetic map of Gossypium herbaceum chromosome 1 and its integration with genetic maps. Molecular Cytogenet. 2015;8(1):2.
Xu Z, Wang H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007;35(Web Server issue):W265-8.
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8(12):973-82.
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792-7.
Olson SA. Emboss opens up sequence analysis. Brief Bioinform. 2002;3(1):87-91.
Ma JX, Bennetzen JL. Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad of Sci USA. 2004;101(34):12404-10.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10(1):421.
Wyatt AW, Mo F, Wang Y, Collins CC. The diverse heterogeneity of molecular alterations in prostate cancer identified through next-generation sequencing. Asian J Androl. 2013;15(3):301.
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 2006;34(suppl 2):W293-7.
Cui X, Liu F, Liu Y, Zhou Z, Wang C, Zhao Y, Meng F, Wang X, Cai X, Wang Y, et al. Screening and chromosome localization of two cotton BAC clones. Comparative Cytogenetics. 2016;10(1):1-15.
Senchina DS, Alvarez I, Cronn RC, Liu B, Rong JK, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF. Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol Biol Evol. 2003;20(4):633-43.
Grover CE, Kim HR, Wing RA, Paterson AH, Wendel JF. Incongruent patterns of local and global genome size evolution in cotton. Genome Research. 2004;14(8):1474-82.
Kokosar J, Kordis D. Genesis and regulatory wiring of retroelement-derived domesticated genes: a phylogenomic perspective. Mol Biol Evol. 2013;30(5):1015-31.
Wendel JF, Albert VA. Phylogenetics of the cotton genus (Gossypium): character-state weighted parsimony analysis of chloroplast-DNA restriction site data and its systematic and biogeographic implications. Syst Bot. 1992;17(1):115-43.
Wendel JF. New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci. 1989;86(11):4132-6.
Chen ZJ, Scheffler BE, Dennis E, Triplett BA, Zhang T, Guo W, Chen X, Stelly DM, Rabinowicz PD, Town CD. Toward sequencing cotton (Gossypium) genomes. Plant Physiol. 2007;145(4):1303-10.
Lisch D, Bennetzen JL. Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol. 2011;14(2):156-61.
Wei L, Gu L, Song X, Cui X, Lu Z, Zhou M, Wang L, Hu F, Zhai J, Meyers BC. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci. 2014;111(10):3877-82.
Mao H, Wang H, Liu S, Li Z, Yang X, Yan J, Li J, Tran L-SP, Qin F. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Comm. 2015;6.
Shen J, Liu J, Xie K, Xing F, Xiong F, Xiao J, Li X, Xiong L. Translational repression by a miniature inverted-repeat transposable element in the 3' untranslated region. Nat Commun. 2017;8.
Rong J: A Ty1 LTR-Retrotransposon Insertion in GbHD1 Gene Is the Prevailing Cause of Trichomeless Phenotypes in Sea Island Cotton (G. barbadense). In: Plant and Animal Genome XXII Conference: 2014. Plant and Animal Genome.
Samadder P, Sivamani E, Lu J, Li X, Qu R. Transcriptional and post-transcriptional enhancement of gene expression by the 5' UTR intron of rice rubi3 gene in transgenic rice cells. Mol Gen Genomics. 2008;279(4):429-39.
Laxa M. Intron-Mediated Enhancement: A Tool for Heterologous Gene Expression in Plants? Front Plant Sci. 2017;7:1977.