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Evolutionary origin of Rosaceae-specific active non-autonomous hAT elements and their contribution to gene regulation and genomic structural variation

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Abstract

Transposable elements account for approximately 30 % of the Prunus genome; however, their evolutionary origin and functionality remain largely unclear. In this study, we identified a hAT transposon family, termed Moshan, in Prunus. The Moshan elements consist of three types, aMoshan, tMoshan, and mMoshan. The aMoshan and tMoshan types contain intact or truncated transposase genes, respectively, while the mMoshan type is miniature inverted-repeat transposable element (MITE). The Moshan transposons are unique to Rosaceae, and the copy numbers of different Moshan types are significantly correlated. Sequence homology analysis reveals that the mMoshan MITEs are direct deletion derivatives of the tMoshan progenitors, and one kind of mMoshan containing a MuDR-derived fragment were amplified predominately in the peach genome. The mMoshan sequences contain cis-regulatory elements that can enhance gene expression up to 100-fold. The mMoshan MITEs can serve as potential sources of micro and long noncoding RNAs. Whole-genome re-sequencing analysis indicates that mMoshan elements are highly active, and an insertion into S-haplotype-specific F-box gene was reported to cause the breakdown of self-incompatibility in sour cherry. Taken together, all these results suggest that the mMoshan elements play important roles in regulating gene expression and driving genomic structural variation in Prunus.

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References

  • Arensburger P, Hice RH, Zhou L, Smith RC, Tom AC, Wright JA, Knapp J, O’Brochta DA, Craig NL, Atkinson PW (2011) Phylogenetic and functional characterization of the hAT transposon superfamily. Genetics 188:45–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benjak A, Boué S, Forneck A, Casacuberta JM (2009) Recent amplification and impact of MITEs on the genome of grapevine (Vitis vinifera L.). Genome Biol Evol 20:75–84

    Google Scholar 

  • Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 65:505–530

    Article  CAS  PubMed  Google Scholar 

  • Bureau TE, Wessler SR (1992) Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4:1283–1294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao K, Zheng Z, Wang L et al (2014) Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol 15:415

    PubMed  PubMed Central  Google Scholar 

  • Chen J, Hu Q, Zhang Y, Lu C, Kuang H (2014) P-MITE: a database for plant miniature inverted-repeat transposable elements. Nucleic Acids Res 42:D1176–D1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dufresne M, Hua-Van A, El Wahab HA, Ben M’Barek S, Vasnier C, Teysset L, Kema GH, Daboussi MJ (2007) Transposition of a fungal miniature inverted-repeat transposable element through the action of a Tc1-like transposase. Genetics 175:441–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falchi R, Vendramin E, Zanon L, Scalabrin S, Cipriani G, Verde I, Vizzotto G, Morgante M (2013) Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach. Plant J 76:175–187

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fedoroff N, Wessler S, Shure M (1983) Isolation of the transposable maize controlling elements Ac and Ds. Cell 35:235–242

    Article  CAS  PubMed  Google Scholar 

  • Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341

    Article  CAS  PubMed  Google Scholar 

  • Feschotte C, Swamy L, Wessler SR (2003) Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs). Genetics 163:747–758

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fresnedo-Ramírez J, Martínez-García PJ, Parfitt DE, Crisosto CH, Gradziel TM (2013) Heterogeneity in the entire genome for three genotypes of peach [Prunus persica (L.) Batsch] as distinguished from sequence analysis of genomic variants. BMC Genomic 14:750

    Article  Google Scholar 

  • Halász J, Kodad O, Hegedűs A (2014) Identification of a recently active Prunus-specific non-autonomous Mutator element with considerable genome shaping force. Plant J 79:220–231

    Article  PubMed  Google Scholar 

  • Hancock CN, Zhang F, Wessler SR (2010) Transposition of the Tourist-MITE mPing in yeast: an assay that retains key features of catalysis by the class 2 PIF/Harbinger superfamily. Mob DNA 1:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Hauck NR, Ikeda K, Tao R, Iezzoni AF (2006) The mutated S1-haplotype in sour cherry has an altered S-haplotype-specific F-box protein gene. J Hered 97:514–520

    Article  CAS  PubMed  Google Scholar 

  • Hehl R, Nacken WKF, Krause A, Saedler H, Sommer S (1991) Structural analysis of Tam3, a transposable element from Antirrhinum majus, reveals homologies to the Ac element from maize. Plant Mol Biol 16:369–371

    Article  CAS  PubMed  Google Scholar 

  • Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Hickman AB, Ewis HE, Li X, Knapp JA, Laver T, Doss AL, Tolun G, Steven AC, Grishaev A, Bax A, Atkinson PW, Craig NL, Dyda F (2014) Structural basis of hAT transposon end recognition by Hermes, an octameric DNA transposase from Musca domestica. Cell 17:353–367

    Article  Google Scholar 

  • International Peach Genome Initiative (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Article  Google Scholar 

  • Jiang N, Wessler SR (2001) Insertion preference of maize and rice miniature inverted repeat transposable elements as revealed by the analysis of nested elements. Plant Cell 13:2553–2564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, McCouch SR, Wessler SR (2003) An active DNA transposon family in rice. Nature 421:163–167

    Article  CAS  PubMed  Google Scholar 

  • Jiang N, Feschotte C, Zhang X, Wessler SR (2004) Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol 7:115–119

    Article  CAS  PubMed  Google Scholar 

  • Kapitonov VV, Jurka J (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 9:411–412

    Article  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49–63

    Article  CAS  PubMed  Google Scholar 

  • Knip M, de Pater S, Hooykaas PJ (2012) The SLEEPER genes: a transposase-derived angiosperm-specific gene family. BMC Plant Biol 12:192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornienko AE, Guenzl PM, Barlow DP, Pauler FM (2013) Gene regulation by the act of long non-coding RNA transcription. BMC Biol 11:59

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuang H, Padmanabhan C, Li F, Kamei A, Bhaskar PB, Ouyang S, Jiang J, Buell CR, Baker B (2009) Identification of miniature inverted-repeat transposable elements (MITEs) and biogenesis of their siRNAs in the Solanaceae: new functional implications for MITEs. Genome Res 19:42–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XW, Meng XQ, Jia HJ, Yu ML, Ma RJ, Wang LR, Cao K, Shen ZJ, Niu L, Tian JB, Chen MJ, Xie M, Arus P, Gao ZS, Aranzana MJ (2013) Peach genetic resources: diversity, population structure and linkage disequilibrium. BMC Genet 14:84

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu C, Chen J, Zhang Y, Hu Q, Su W, Kuang H (2012) Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol Biol Evol 29:1005–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA 36:344–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menzel G, Krebs C, Diez M, Holtgräwe D, Weisshaar B, Minoche AE, Dohm JC, Himmelbauer H, Schmidt T (2012) Survey of sugar beet (Beta vulgaris L.) hAT transposons and MITE-like hATpin derivatives. Plant Mol Biol 78:393–405

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Vázquez S, Ning J, Meyers BC (2005) hATpin, a family of MITE-like hAT mobile elements conserved in diverse plant species that forms highly stable secondary structures. Plant Mol Biol 58:869–886

    Article  PubMed  Google Scholar 

  • Naito K, Cho E, Yang G, Campbell MA, Yano K, Okumoto Y, Tanisaka T, Wessler SR (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA 103:17620–17625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    Article  CAS  PubMed  Google Scholar 

  • Rebollo R, Romanish MT, Mager DL (2012) Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46:21–42

    Article  CAS  PubMed  Google Scholar 

  • Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scorza R, Mehlenbacher SA, Lightner GW (1985) Inbreeding and coancestry of freestone peach cultivars of the Eastern United States and implications for peach germoplasm improvement. J Am Soc Hortic Sci 110:547–552

    Google Scholar 

  • Seberg O, Petersen G (2009) A unified classification system for eukaryotic transposable elements should reflect their phylogeny. Nat Rev Genet 10:276

    Article  CAS  PubMed  Google Scholar 

  • Streck RD, MacGaffey JE, Beckendorf SK (1986) The structure of hobo transposable elements and their insertion sites. EMBO J 5:3615–3623

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tian Y, Xing C, Cao Y, Wang C, Guan F, Li R, Meng F (2015) Evaluation of genetic diversity on Prunus mira Koehne by using ISSR and RAPD markers. Biotechnol Biotech Equip 29:1053–1061

    Article  Google Scholar 

  • Vendramin E, Pea G, Dondini L, Pacheco I, Dettori MT, Gazza L, Scalabrin S, Strozzi F, Tartarini S, Bassi D, Verde I, Rossini L (2014) A unique mutation in a MYB gene cosegregates with the nectarine phenotype in peach. PLoS One 9:e90574

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang L, Zhao S, Gu C, Zhou Y, Zhou H, Ma J, Cheng J, Han Y (2013) Deep RNA-Seq uncovers the peach transcriptome landscape. Plant Mol Biol 83:365–377

    Article  CAS  PubMed  Google Scholar 

  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Hall TC (2003) MDM-1 and MDM-2: two mutator-derived MITE families in rice. J Mol Evol 56:255–264

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Lee YH, Jiang Y, Shi X, Kertbundit S, Hall TC (2005) A two-edged role for the transposable element Kiddo in the rice ubiquitin2 promoter. Plant Cell 17:1559–1568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang G, Nagel DH, Feschotte C, Hancock CN, Wessler SR (2009) Tuned for transposition: molecular determinants underlying the hyperactivity of a Stowaway MITE. Science 325:1391–1394

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Arbuckle J, Wessler SR (2000) Recent, extensive, and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker into genic regions of maize. Proc Natl Acad Sci USA 97:1160–1165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Feschotte C, Zhang Q, Jiang N, Eggleston WB, Wessler SR (2001) P instability factor: an active maize transposon system associated with the amplification of Tourist-like MITEs and a new superfamily of transposases. Proc Natl Acad Sci USA 98:12572–12577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Jiang N, Feschotte C, Wessler SR (2004) PIF- and Pong-like transposable elements: distribution, evolution and relationship with Tourist-like miniature inverted-repeat transposable elements. Genetics 166:971–986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Chen W, Sun L et al (2012) The genome of Prunus mume. Nat Commun 3:1318

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Lin-Wang K, Wang H, Gu C, Dare AP, Espley RV, He H, Allan AC, Han Y (2015) Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. Plant J 82:105–121

    Article  CAS  PubMed  Google Scholar 

  • Zhuang J, Wang J, Theurkauf W, Weng Z (2014) TEMP: a computational method for analyzing transposable element polymorphism in populations. Nucleic Acids Res 42:6826–6838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 31420103914), the Overseas Construction Plan for Science and Education Base, China-Africa Center for Research and Education, Chinese Academy of Sciences (Grant No. SAJC201327), and the National 863 program of China (Grant No. 2011AA100206).

Author contributions

Y.H. and L.W. conceived and designed the experiments. Q.P., J.Z., F.R., H.Z., W.W., and L.L. performed the experiments. Y.H. and L.W. wrote the paper. A.O. and Q.J. revised the manuscript.

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Authors and Affiliations

  1. Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden of the Chinese Academy of Sciences, Wuhan, 430074, People’s Republic of China

    Lu Wang, Qian Peng, Hui Zhou, Wei Wang, Liao Liao, Albert Owiti & Yuepeng Han

  2. Institute of Forestry and Pomology, Beijing Academy of Agriculture and Forestry Sciences, A12, Ruiwangfen, Beijing, 100093, People’s Republic of China

    Jianbo Zhao, Fei Ren & Quan Jiang

  3. Graduate University of Chinese Academy of Sciences, 19A Yuquanlu, Beijing, 100049, People’s Republic of China

    Qian Peng, Hui Zhou & Albert Owiti

  4. Sino-African Joint Research Center, Chinese Academy of Sciences, Wuhan, 430074, People’s Republic of China

    Liao Liao & Yuepeng Han

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  1. Lu Wang
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Correspondence to Quan Jiang or Yuepeng Han.

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Wang, L., Peng, Q., Zhao, J. et al. Evolutionary origin of Rosaceae-specific active non-autonomous hAT elements and their contribution to gene regulation and genomic structural variation. Plant Mol Biol 91, 179–191 (2016). https://doi.org/10.1007/s11103-016-0454-y

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