Abstract
Interspecific hybridization has been considered the major mode of evolution in Pyrus (pear), and thus, the genetic relationships within this genus have not been well documented. Retrotransposons are ubiquitous components of plant genomes and 42.4 % of the pear genome was reported to be long terminal repeat (LTR) retrotransposons, implying that retrotransposons might be significant in the evolution of Pyrus. In this study, 1,836 putative full-length LTR retrotransposons were isolated and 196 retrotransposon-based insertion polymorphism (RBIP) primers were developed, of which 24 pairs to the Ppcr1 subfamily of copia retrotransposons were used to analyze genetic diversity among 110 Pyrus accessions from Eurasia. Our results showed that Ppcr1 replicated many times in the development of cultivated Asian pears. The genetic structure analysis and the unweighted pair group method with arithmetic mean (UPGMA) dendrogram indicated that all accessions could be divided into Oriental and Occidental groups. In Oriental pears, wild pea pears clustered separately into independent groups in accordance with their morphological classifications. Cultivars of P. ussuriensis Maxim, P. pyrifolia Nakai, and P. pyrifolia Chinese white pear were mingled together, which inferred that hybridization events occurred during the development of the cultivated Asian pears. In Occidental pears, two clades were obtained in the UPGMA dendrogram in accordance with their geographical distribution; one contained the European species and the other included species from North Africa and West Asia. New findings in this study will be important to further understand the phylogeny of Pyrus and origins of cultivated pears.
Similar content being viewed by others
References
Aldasoro JJ, Aedo C, Garmendia FM (1996) The genus Pyrus L. (Rosaceae) in south-west Europe and North Africa. Bot J Linn Soc 121(2):143–158
Bailey LH (1917) Pyrus. Standard cyclopedia of horticulture, vol V. Macmillan, New York, pp 2865–2878
Bao L, Chen K, Zhang D, Cao Y, Yamamoto T, Teng Y (2007) Genetic diversity and similarity of pear (Pyrus L.) cultivars native to East Asia revealed by SSR (simple sequence repeat) markers. Genet Resour Crop Evol 54(5):959–971
Bao L, Chen K, Zhang D, Li X, Teng Y (2008) An assessment of genetic variability and relationships within Asian pears based on AFLP (amplified fragment length polymorphism) markers. Sci Hortic 116(4):374–380
Bassil N, Postman JD (2010) Identification of European and Asian pears using EST-SSRs from Pyrus. Genet Resour Crop Evol 57(3):357–370
Baucom RS, Estill JC, Leebens-Mack J, Bennetzen JL (2009) Natural selection on gene function drives the evolution of LTR retrotransposon families in the rice genome. Genome Res 19(2):243–254
Bergman CM, Quesneville H (2007) Discovering and detecting transposable elements in genome sequences. Brief Bioinform 8(6):382–392
Cavallini A, Natali L, Zuccolo A, Giordani T, Jurman I, Ferrillo V, Vitacolonna N, Sarri V, Cattonaro F, Ceccarelli M, Cionini PG, Morgante M (2010) Analysis of transposons and repeat composition of the sunflower (Helianthus annuus L.) genome. Theor Appl Genet 120(3):491–508
Challice JS, Westwood MN (1973) Numerical taxonomic studies of the genus Pyrus using both chemical and botanical characters. Bot J Linn Soc 67(2):121–148
Cossu RM, Buti M, Giordani T, Natali L, Cavallini A (2012) A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome. Tree Genet Genomes 8(1):61–75
Diwan N, Cregan PB (1997) Automated sizing of fluorescent-labeled simple sequence repeat (SSR) markers to assay genetic variation in soybean. Theor Appl Genet 95(5–6):723–733
Dondoshansky I, Wolf Y (2002) Blastclust (NCBI Software Development Toolkit). NCBI, Bethesda
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361
Ellinghaus D, Kurtz S, Willhoeft U (2008) LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinform 9(1):18
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
Fan L, Zhang M, Liu Q, Li L, Song Y, Wang L, Zhang S, Wu J (2013) Transferability of newly developed pear SSR markers to other Rosaceae Species. Plant Mol Biol Rep 31(6):1271–1282
Flavell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R, Kumar A (1992) Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res 20(14):3639–3644
Havecker ER, Gao X, Voytas DF (2004) The diversity of LTR retrotransposons. Genome Biol 5(6):225
Iketani H, Katayama H, Uematsu C, Mase N, Sato Y, Yamamoto T (2012) Genetic structure of East Asian cultivated pears (Pyrus spp.) and their reclassification in accordance with the nomenclature of cultivated plants. Plant Syst Evol 298(9):1689–1700
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(4):1801–1806
Jing R, Knox MR, Lee JM, Vershinin AV, Ambrose M, Ellis TN, Flavell AJ (2005) Insertional polymorphism and antiquity of PDR1 retrotransposon insertions in Pisum species. Genetics 171(2):741–752
Kalendar R, Schulman AH (2006) IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nat Protoc 1(5):2478–2484
Kalendar R, Flavell AJ, Ellis TH, Sjakste T, Moisy C, Schulman AH (2011) Analysis of plant diversity with retrotransposon-based molecular markers. Heredity (Edinb) 106(4):520–530
Kim H, Yamamoto M, Hosaka F, Terakami S, Nishitani C, Sawamura Y, Yamane H, Wu JZ, Matsumoto T, Matsuyama T, Yamamoto T (2011) Molecular characterization of novel Ty1-copia-like retrotransposons in pear (Pyrus pyrifolia). Tree Genet Genomes 7(4):845–856
Kim H, Terakami S, Nishitani C, Kurita K, Kanamori H, Katayose Y, Sawamura Y, Saito T, Yamamoto T (2012) Development of cultivar-specific DNA markers based on retrotransposon-based insertional polymorphism in Japanese pear. Breed Sci 62(1):53–62
Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinform 7:474
Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23(10):1289–1291
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948
McNeill J (2012) International Code of Nomenclature for algae, fungi and plants (Melbourne Code). Koeltz Scientific Books, Germany
Monte-Corvo L, Cabrita L, Oliveira C, Leitao J (2000) Assessment of genetic relationships among Pyrus species and cultivars using AFLP and RAPD markers. Genet Resour Crop Evol 47(3):257–265
Nei M, Li W (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76(10):5269–5273
Oliveira CM, Mota M, Monte-Corvo L, Goulao L, Silva DM (1999) Molecular typing of Pyrus based on RAPD markers. Sci Hortic 79(3):163–174
Peterson DG, Schulze SR, Sciara EB, Lee SA, Bowers JE, Nagel A, Jiang N, Tibbitts DC, Wessler SR, Paterson AH (2002) Integration of Cot analysis, DNA cloning, and high-throughput sequencing facilitates genome characterization and gene discovery. Genome Res 12(5):795–807
Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266(1–2):5–43
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Rohlf FJ (1998) Numerical taxonomy and multivariate analysis system version 2.0. Exeter Publishing, Setauket
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4(1):137–138
Sabot F, Schulman AH (2006) Parasitism and the retrotransposon life cycle in plants: a hitchhiker’s guide to the genome. Heredity (Edinb) 97(6):381–388
SanMiguel P, Tikhonov A, Jin YK et al (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274(5288):765–768
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20(1):43–45
Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115
Smit AFA, Hubley R, Green P (1996–2004). RepeatMasker: Open-3.0. Published on the web. http://www.repeatmasker.org. Accessed 31 January 2014
Teng Y, Tanabe K (2004) Reconsideration on the origin of cultivated pears native to East Asia. Fourth Int Symp Taxon Cultiv Plants 634:175–182
Teng Y, Tanabe K, Tamura F, Itai A (2001) Genetic relationships of pear cultivars in Xinjiang, China, as measured by RAPD markers. J Hortic Sci Biotechnol 76(6):771–779
Teng Y, Tanabe K, Tamura F, Itai A (2002) Genetic relationships of Pyrus species and cultivars native to East Asia revealed by randomly amplified polymorphic DNA markers. J Am Soc Hortic Sci 127(2):262–270
Velasco R, Zharkikh A, Affourtit J et al (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42(10):833–839
Vicient CM, Kalendar R, Anamthawat-Jonsson K, Schulman AH (1999) Structure, functionality, and evolution of the BARE-1 retrotransposon of barley. Genetica 107(1–3):53–63
Waugh R, McLean K, Flavell AJ, Pearce SR, Kumar A, Thomas BB, Powell W (1997) Genetic distribution of Bare-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol Gen Genet 253(6):687–694
Wicker T, Sabot F, Hua-Van A et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982
Wierdl M, Dominska M, Petes TD (1997) Microsatellite instability in yeast: dependence on the length of the microsatellite. Genetics 146(3):769–779
Wu J, Wang Z, Shi Z et al (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23(2):396–408
Yamada NA, Smith GA, Castro A, Roques CN, Boyer JC, Farber RA (2002) Relative rates of insertion and deletion mutations in dinucleotide repeats of various lengths in mismatch repair proficient mouse and mismatch repair deficient human cells. Mutat Res Fund Mol M 499(2):213–225
Yamamoto T, Kimura T, Sawamura Y, Manabe T, Kotobuki K, Hayashi T, Ban Y, Matsuta N (2002) Simple sequence repeats for genetic analysis in pear. Euphytica 124(1):129–137
Yao L, Zheng X, Cai D, Gao Y, Wang K, Cao Y, Teng Y (2010) Exploitation of Malus EST-SSRs and the utility in evaluation of genetic diversity in Malus and Pyrus. Genet Resour Crop Evol 57(6):841–851
Yu T (1979) Taxonomy of the fruit tree in China. Agriculture Press, Beijing (in Chinese)
Zheng X, Cai D, Yao L, Teng Y (2008) Non-concerted ITS evolution, early origin and phylogenetic utility of ITS pseudogenes in Pyrus. Mol Phylogenet Evol 48(3):892–903
Zheng X, Hu C, Spooner D, Liu J, Cao J, Teng Y (2011) Molecular evolution of Adh and LEAFY and the phylogenetic utility of their introns in Pyrus (Rosaceae). BMC Evol Biol 11(1):255
Zheng X, Cai D, Potter D, Postman J, Liu J, Teng Y (2014) Phylogeny and evolutionary histories of Pyrus L. revealed by phylogenetic trees and networks based on data from multiple DNA sequences. Mol Phylogenet Evol. doi:10.1016/j.ympev.2014.07.009
Acknowledgments
This work was financed by a Grant from the National Natural Science Foundation of China (No. 31201592), a Specialized Research Fund for the Doctoral Program of Higher Education (20110101110091), and a Grant for Innovative Research Team of Zhejiang Province of China (2013TD05).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Hohmann.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jiang, S., Zong, Y., Yue, X. et al. Prediction of retrotransposons and assessment of genetic variability based on developed retrotransposon-based insertion polymorphism (RBIP) markers in Pyrus L. Mol Genet Genomics 290, 225–237 (2015). https://doi.org/10.1007/s00438-014-0914-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-014-0914-5