Evolution of Centromeric Retrotransposons in Grasses

Sharma, Anupma; Presting, Gernot G.

doi:10.1093/gbe/evu096

Evolution of Centromeric Retrotransposons in Grasses

Journal Article · Fri May 09 00:00:00 EDT 2014 · Genome Biology and Evolution

DOI:https://doi.org/10.1093/gbe/evu096· OSTI ID:1625335

Sharma, Anupma ^[1]; Presting, Gernot G. ^[2]

Univ. of Hawaii at Manoa, Honolulu, HI (United States). Dept. of Molecular Biosciences and Bioengineering; DOE/OSTI
Univ. of Hawaii at Manoa, Honolulu, HI (United States). Dept. of Molecular Biosciences and Bioengineering

Centromeric retrotransposons (CRs) constitute a family of plant retroelements, some of which have the ability to target their insertion almost exclusively to the functional centromeres. Our exhaustive analysis of CR family members in four grass genomes revealed not only horizontal transfer (HT) of CR elements between the oryzoid and panicoid grass lineages but also their subsequent recombination with endogenous elements that in some cases created prolific recombinants in foxtail millet and sorghum. HT events are easily identifiable only in cases where host genome divergence significantly predates HT, thus documented HT events likely represent only a fraction of the total. If the more difficult to detect ancient HT events occurred at frequencies similar to those observable in present day grasses, the extant long terminal repeat retrotransposons represent the mosaic products of HT and recombination that are optimized for retrotransposition in their host genomes. This complicates not only phylogenetic analysis but also the establishment of a meaningful retrotransposon nomenclature, which we have nevertheless attempted to implement here. In contrast to the plant-centric naming convention used currently for CR elements, we classify elements primarily based on their phylogenetic relationships regardless of host plant, using the exhaustively studied maize elements assigned to six different subfamilies as a standard. The CR2 subfamily is the most widely distributed of the six CR subfamilies discovered in grass genomes to date and thus the most likely to play a functional role at grass centromeres.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625335

Journal Information:: Genome Biology and Evolution, Journal Name: Genome Biology and Evolution Journal Issue: 6 Vol. 6; ISSN 1759-6653

Publisher:: Society for Molecular Biology and EvolutionCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Cytological and molecular characterization of oat x maize partial hybrids Riera-Lizarazu, Oscar; Rines, Howard W.; Phillips, Ronald L. Theoretical and Applied Genetics, Vol. 93-93, Issue 1-2 https://doi.org/10.1007/bf00225737	journal	July 1996
Genetic variations in the hybrids of rice (Oryza sativa) and sorghum (Sorghum vulgare) Deming, Zu; Shanbao, Chen; Xiaolan, Duan Theoretical and Applied Genetics, Vol. 70, Issue 5 https://doi.org/10.1007/bf00305988	journal	August 1985
Retroelements and formation of chimeric retrogenes Buzdin, A. A. Cellular and Molecular Life Sciences, Vol. 61, Issue 16 https://doi.org/10.1007/s00018-004-4041-z	journal	August 2004
Nucleotide diversity and molecular evolution of the PSY1 gene in Zea mays compared to some other grass species Fu, Zhiyuan; Yan, Jianbing; Zheng, Yanping Theoretical and Applied Genetics, Vol. 120, Issue 4 https://doi.org/10.1007/s00122-009-1188-x	journal	November 2009
Variability, Recombination, and Mosaic Evolution of the Barley BARE-1 Retrotransposon Vicient, Carlos M.; Kalendar, Ruslan; Schulman, Alan H. Journal of Molecular Evolution, Vol. 61, Issue 3 https://doi.org/10.1007/s00239-004-0168-7	journal	July 2005
Centromeric retrotransposon lineages predate the maize/rice divergence and differ in abundance and activity Sharma, Anupma; Presting, Gernot G. Molecular Genetics and Genomics, Vol. 279, Issue 2 https://doi.org/10.1007/s00438-007-0302-5	journal	November 2007
Localization and transcription of a retrotransposon-derived element on the maize B chromosome Lamb, Jonathan C.; Riddle, Nicole C.; Cheng, Ya-Ming Chromosome Research https://doi.org/10.1007/s10577-007-1135-0	journal	April 2007
Nested Ty3-gypsy retrotransposons of a single Beta procumbens centromere contain a putative chromodomain Weber, Beatrice; Schmidt, Thomas Chromosome Research, Vol. 17, Issue 3 https://doi.org/10.1007/s10577-009-9029-y	journal	March 2009
Gene trees and species trees are not the same Nichols, Richard Trends in Ecology & Evolution, Vol. 16, Issue 7 https://doi.org/10.1016/s0169-5347(01)02203-0	journal	July 2001
The paleontology of intergene retrotransposons of maize SanMiguel, Phillip; Gaut, Brandon S.; Tikhonov, Alexander Nature Genetics, Vol. 20, Issue 1 https://doi.org/10.1038/1695	journal	September 1998
High outcrossing rates in fields with mixed sorghum landraces: how are landraces maintained? Barnaud, A.; Trigueros, G.; McKey, D. Heredity, Vol. 101, Issue 5 https://doi.org/10.1038/hdy.2008.77	journal	August 2008
Genome sequencing and analysis of the model grass Brachypodium distachyon No authors listed Nature, Vol. 463, Issue 7282, p. 763-768 https://doi.org/10.1038/nature08747	journal	February 2010
Reference genome sequence of the model plant Setaria Bennetzen, Jeffrey L.; Schmutz, Jeremy; Wang, Hao Nature Biotechnology, Vol. 30, Issue 6 https://doi.org/10.1038/nbt.2196	journal	May 2012
Evolutionary dynamics of grass genomes: Tansley review no. 132 Gaut, Brandon S. New Phytologist, Vol. 154, Issue 1 https://doi.org/10.1046/j.1469-8137.2002.00352.x	journal	April 2002
Transfer of photosynthesis genes to and from Prochlorococcus viruses Lindell, D.; Sullivan, M. B.; Johnson, Z. I. Proceedings of the National Academy of Sciences, Vol. 101, Issue 30 https://doi.org/10.1073/pnas.0401526101	journal	July 2004
Rapid recent growth and divergence of rice nuclear genomes Ma, J.; Bennetzen, J. L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 34 https://doi.org/10.1073/pnas.0403715101	journal	July 2004
Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations Sharma, Anupma; Schneider, Kevin L.; Presting, Gernot G. Proceedings of the National Academy of Sciences, Vol. 105, Issue 40 https://doi.org/10.1073/pnas.0805694105	journal	October 2008
Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Wolfe, K. H.; Gouy, M.; Yang, Y. W. Proceedings of the National Academy of Sciences, Vol. 86, Issue 16 https://doi.org/10.1073/pnas.86.16.6201	journal	August 1989
DNA sequence evidence for the segmental allotetraploid origin of maize Gaut, B. S.; Doebley, J. F. Proceedings of the National Academy of Sciences, Vol. 94, Issue 13 https://doi.org/10.1073/pnas.94.13.6809	journal	June 1997
Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions Ananiev, E. V.; Phillips, R. L.; Rines, H. W. Proceedings of the National Academy of Sciences, Vol. 95, Issue 22 https://doi.org/10.1073/pnas.95.22.13073	journal	October 1998
Long terminal repeat retrotransposons jump between species Flavell, Andrew J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 22 https://doi.org/10.1073/pnas.96.22.12211	journal	October 1999
Evidence for the recent horizontal transfer of long terminal repeat retrotransposon Jordan, I. K.; Matyunina, L. V.; McDonald, J. F. Proceedings of the National Academy of Sciences, Vol. 96, Issue 22 https://doi.org/10.1073/pnas.96.22.12621	journal	October 1999
Evolution and taxonomic split of the model grass Brachypodium distachyon Catalán, Pilar; Müller, Jochen; Hasterok, Robert Annals of Botany, Vol. 109, Issue 2 https://doi.org/10.1093/aob/mcr294	journal	January 2012
Retrotransposon-Related DNA Sequences in the Centromeres of Grass Chromosomes Miller, Joseph T.; Dong, Fenggao; Jackson, Scott A. Genetics, Vol. 150, Issue 4 https://doi.org/10.1093/genetics/150.4.1615	journal	December 1998
Different Types and Rates of Genome Evolution Detected by Comparative Sequence Analysis of Orthologous Segments From Four Cereal Genomes Ramakrishna, Wusirika; Dubcovsky, Jorge; Park, Yong-Jin Genetics, Vol. 162, Issue 3 https://doi.org/10.1093/genetics/162.3.1389	journal	November 2002
Evolutionary Genomics of Chromoviruses in Eukaryotes Gorinšek, Benjamin; Gubenšek, Franc; Kordiš, Dušan Molecular Biology and Evolution, Vol. 21, Issue 5 https://doi.org/10.1093/molbev/msh057	journal	May 2004
A Large Variation in the Rates of Synonymous Substitution for RNA Viruses and Its Relationship to a Diversity of Viral Infection and Transmission Modes Hanada, Kousuke; Suzuki, Yoshiyuki; Gojobori, Takashi Molecular Biology and Evolution, Vol. 21, Issue 6 https://doi.org/10.1093/molbev/msh109	journal	June 2004
Estimating a Nucleotide Substitution Rate for Maize from Polymorphism at a Major Domestication Locus Clark, Richard M.; Tavaré, Simon; Doebley, John Molecular Biology and Evolution, Vol. 22, Issue 11 https://doi.org/10.1093/molbev/msi228	journal	August 2005
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Close Split of Sorghum and Maize Genome Progenitors Swigonova, Z. Genome Research, Vol. 14, Issue 10a https://doi.org/10.1101/gr.2332504	journal	September 2004
Dynamic Evolution of Oryza Genomes Is Revealed by Comparative Genomic Analysis of a Genus-Wide Vertical Data Set Ammiraju, Jetty S. S.; Lu, Fei; Sanyal, Abhijit The Plant Cell, Vol. 20, Issue 12 https://doi.org/10.1105/tpc.108.063727	journal	December 2008
The B73 Maize Genome: Complexity, Diversity, and Dynamics Schnable, P. S.; Ware, D.; Fulton, R. S. Science, Vol. 326, Issue 5956, p. 1112-1115 https://doi.org/10.1126/science.1178534	journal	November 2009
Widespread Horizontal Gene Transfer from Double-Stranded RNA Viruses to Eukaryotic Nuclear Genomes Liu, H.; Fu, Y.; Jiang, D. Journal of Virology, Vol. 84, Issue 22 https://doi.org/10.1128/jvi.00955-10	journal	September 2010
Full-Length Human Immunodeficiency Virus Type 1 Genomes from Subtype C-Infected Seroconverters in India, with Evidence of Intersubtype Recombination Lole, Kavita S.; Bollinger, Robert C.; Paranjape, Ramesh S. Journal of Virology, Vol. 73, Issue 1 https://doi.org/10.1128/jvi.73.1.152-160.1999	journal	January 1999
Phylogenomic analysis of chromoviruses Gorinšek, B.; Gubenšek, F.; Kordiš, D. Cytogenetic and Genome Research, Vol. 110, Issue 1-4 https://doi.org/10.1159/000084987	journal	January 2005
Widespread Horizontal Gene Transfer from Circular Single-stranded DNA Viruses to Eukaryotic Genomes Liu, Huiquan; Fu, Yanping; Li, Bo BMC Evolutionary Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2148-11-276	journal	September 2011
Whole genome surveys of rice, maize and sorghum reveal multiple horizontal transfers of the LTR-retrotransposon Route66 in Poaceae Roulin, Anne; Piegu, Benoit; Fortune, Philippe M. BMC Evolutionary Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2148-9-58	journal	January 2009
Tandem repeats derived from centromeric retrotransposons Sharma, Anupma; Wolfgruber, Thomas K.; Presting, Gernot G. BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-142	journal	January 2013
How Athila retrotransposons survive in the Arabidopsis genome Marco, Antonio; Marín, Ignacio BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-219	journal	January 2008
Plant centromeric retrotransposons: a structural and cytogenetic perspective Neumann, Pavel; Navrátilová, Alice; Koblížková, Andrea Mobile DNA, Vol. 2, Issue 1 https://doi.org/10.1186/1759-8753-2-4	journal	January 2011
Analysis of 142 genes resolves the rapid diversification of the rice genus Zou, Xin-Hui; Zhang, Fu-Min; Zhang, Jian-Guo Genome Biology, Vol. 9, Issue 3 https://doi.org/10.1186/gb-2008-9-3-r49	journal	January 2008
Estimation of the outcrossing rate for annual Asian wild rice under field conditions Phan, Phuong Dang Thai; Kageyama, Hiroki; Ishikawa, Ryo Breeding Science, Vol. 62, Issue 3 https://doi.org/10.1270/jsbbs.62.256	journal	January 2012
Horizontal Transfer of a Plant Transposon Diao, Xianmin; Freeling, Michael; Lisch, Damon PLoS Biology, Vol. 4, Issue 1 https://doi.org/10.1371/journal.pbio.0040005	journal	December 2005
Exceptional Diversity, Non-Random Distribution, and Rapid Evolution of Retroelements in the B73 Maize Genome Baucom, Regina S.; Estill, James C.; Chaparro, Cristian PLoS Genetics, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pgen.1000732	journal	November 2009
Some physiological and photosynthetic characters of rice × sorghum and rice × wheat hybrids Srivastava, N. K.; Yoshida, S. Euphytica, Vol. 49, Issue 3 https://doi.org/10.1007/BF00036289	journal	September 1990
Cytological and molecular characterization of oat x maize partial hybrids Riera-Lizarazu, Oscar; Rines, Howard W.; Phillips, Ronald L. Theoretical and Applied Genetics, Vol. 93-93, Issue 1-2 https://doi.org/10.1007/BF00225737	journal	July 1996
Genetic variations in the hybrids of rice (Oryza sativa) and sorghum (Sorghum vulgare) Deming, Zu; Shanbao, Chen; Xiaolan, Duan Theoretical and Applied Genetics, Vol. 70, Issue 5 https://doi.org/10.1007/BF00305988	journal	August 1985
Compact genomes and complex evolution in the genus Brachypodium Wolny, Elzbieta; Lesniewska, Karolina; Hasterok, Robert Chromosoma, Vol. 120, Issue 2 https://doi.org/10.1007/s00412-010-0303-8	journal	December 2010
Gene trees and species trees are not the same Nichols, Richard Trends in Ecology & Evolution, Vol. 16, Issue 7 https://doi.org/10.1016/S0169-5347(01)02203-0	journal	July 2001
Evolution of Viruses by Acquisition of Cellular RNA or DNA Nucleotide Sequences and Genes: An Introduction Becker, Yechiel Virus Genes, Vol. 21, Issue 1/2, p. 7-12 https://doi.org/10.1023/A:1008100923033	journal	January 2000
The Sorghum bicolor genome and the diversification of grasses Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy Nature, Vol. 457, Issue 7229 https://doi.org/10.1038/nature07723	journal	January 2009
ATY3/GYPSYretrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes: Centromeric retrotransposon of barley Received 23 July 1998; revised 22 October 1998; accepted 28 October 1998. Presting, Gernot G.; Malysheva, Ludmilla; Fuchs, Jörg The Plant Journal, Vol. 16, Issue 6 https://doi.org/10.1046/j.1365-313x.1998.00341.x	journal	December 1998
Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics Paterson, A. H.; Bowers, J. E.; Chapman, B. A. Proceedings of the National Academy of Sciences, Vol. 101, Issue 26 https://doi.org/10.1073/pnas.0307901101	journal	May 2004
Acc homoeoloci and the evolution of wheat genomes Chalupska, D.; Lee, H. Y.; Faris, J. D. Proceedings of the National Academy of Sciences, Vol. 105, Issue 28 https://doi.org/10.1073/pnas.0803981105	journal	July 2008
Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Gaut, B. S.; Morton, B. R.; McCaig, B. C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 19 https://doi.org/10.1073/pnas.93.19.10274	journal	September 1996
People, Plants and Genes Murphy, Denis J. Oxford Academic https://doi.org/10.1093/acprof:oso/9780199207145.001.0001	book	July 2007
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Analyses of LTR-Retrotransposon Structures Reveal Recent and Rapid Genomic DNA Loss in Rice Ma, J. Genome Research, Vol. 14, Issue 5 https://doi.org/10.1101/gr.1466204	journal	May 2004
A Complete Set of Maize Individual Chromosome Additions to the Oat Genome Kynast, Ralf G.; Riera-Lizarazu, Oscar; Vales, M. Isabel Plant Physiology, Vol. 125, Issue 3 https://doi.org/10.1104/pp.125.3.1216	journal	March 2001
Dynamic Evolution of Oryza Genomes Bertoni, Gregory The Plant Cell, Vol. 20, Issue 12 https://doi.org/10.1105/tpc.108.201213	journal	December 2008
Evidence of multiple horizontal transfers of the long terminal repeat retrotransposon RIRE1 within the genus Oryza: Multiple horizontal transfers of the LTR retrotransposon RIRE1 in Oryza Roulin, Anne; Piegu, Benoît; Wing, Rod A. The Plant Journal, Vol. 53, Issue 6 https://doi.org/10.1111/j.1365-313X.2007.03388.x	journal	December 2007
Widespread Horizontal Gene Transfer from Double-Stranded RNA Viruses to Eukaryotic Nuclear Genomes Liu, H.; Fu, Y.; Jiang, D. Journal of Virology, Vol. 84, Issue 22 https://doi.org/10.1128/JVI.00955-10	journal	September 2010
Full-Length Human Immunodeficiency Virus Type 1 Genomes from Subtype C-Infected Seroconverters in India, with Evidence of Intersubtype Recombination Lole, Kavita S.; Bollinger, Robert C.; Paranjape, Ramesh S. Journal of Virology, Vol. 73, Issue 1 https://doi.org/10.1128/JVI.73.1.152-160.1999	journal	January 1999
Estimate of outcrossing rates in a rice plant (Oryza sativa L.) under field conditions using a purple grain rice cultivar, Okunomurasaki Endo, Takashi; Sato, Hideki; Yamaguchi, Masayuki Breeding Science, Vol. 59, Issue 2 https://doi.org/10.1270/jsbbs.59.195	journal	January 2009
A New Family of Ty1- copia -Like Retrotransposons Originated in the Tomato Genome by a Recent Horizontal Transfer Event Cheng, Xudong; Zhang, Dongfeng; Cheng, Zhukuan Genetics, Vol. 181, Issue 4 https://doi.org/10.1534/genetics.108.099150	journal	April 2009

Cited By (12)

Sequencing a Juglans regia × J. microcarpa hybrid yields high-quality genome assemblies of parental species Zhu, Tingting; Wang, Le; You, Frank M. Horticulture Research, Vol. 6, Issue 1 https://doi.org/10.1038/s41438-019-0139-1	journal	March 2019
Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives Gent, Jonathan I.; Wang, Na; Dawe, R. Kelly Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1249-4	journal	June 2017
Stable Patterns of CENH3 Occupancy Through Maize Lineages Containing Genetically Similar Centromeres Gent, Jonathan I.; Wang, Kai; Jiang, Jiming Genetics, Vol. 200, Issue 4 https://doi.org/10.1534/genetics.115.177360	journal	June 2015
High Quality Maize Centromere 10 Sequence Reveals Evidence of Frequent Recombination Events Wolfgruber, Thomas K.; Nakashima, Megan M.; Schneider, Kevin L. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00308	journal	March 2016
Retrotransposons in Plant Genomes: Structure, Identification, and Classification through Bioinformatics and Machine Learning Orozco-Arias, Simon; Isaza, Gustavo; Guyot, Romain International Journal of Molecular Sciences, Vol. 20, Issue 15 https://doi.org/10.3390/ijms20153837	journal	August 2019
Inbreeding drives maize centromere evolution Schneider, Kevin L.; Xie, Zidian; Wolfgruber, Thomas K. Proceedings of the National Academy of Sciences, Vol. 113, Issue 8 https://doi.org/10.1073/pnas.1522008113	journal	February 2016
Becoming a Selfish Clan: Recombination Associated to Reverse-Transcription in LTR Retrotransposons Drost, Hajk-Georg; Sanchez, Diego H. Genome Biology and Evolution, Vol. 11, Issue 12 https://doi.org/10.1093/gbe/evz255	journal	November 2019
Transposon Insertions, Structural Variations, and SNPs Contribute to the Evolution of the Melon Genome Sanseverino, Walter; Hénaff, Elizabeth; Vives, Cristina Molecular Biology and Evolution, Vol. 32, Issue 10 https://doi.org/10.1093/molbev/msv152	journal	July 2015
The impact of the Tekay chromoviral elements on genome organisation and evolution of Anemone s.l. (Ranunculaceae) Mlinarec, J.; Franjević, D.; Harapin, J. Plant Biology, Vol. 18, Issue 2 https://doi.org/10.1111/plb.12393	journal	October 2015
Becoming a Selfish Clan: Recombination Associated to Reverse-Transcription in LTR Retrotransposons. Drost, Hajk-Georg; Sanchez, Diego H. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.47415	text	January 2019
Physical Map of Repetitive DNA Sites in Brachiaria spp.: Intravarietal and Interspecific Polymorphisms Nani, Thaís Furtado; Pereira, Daniele Laís; Souza Sobrinho, Fausto Crop Science, Vol. 56, Issue 4 https://doi.org/10.2135/cropsci2015.12.0760	journal	July 2016
Structure and Distribution of Centromeric Retrotransposons at Diploid and Allotetraploid Coffea Centromeric and Pericentromeric Regions de Castro Nunes, Renata; Orozco-Arias, Simon; Crouzillat, Dominique Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00175	journal	February 2018

Similar Records

Genome sequence analysis of the model grass Brachypodium distachyon: insights into grass genome evolution

Journal Article · Sun Aug 09 00:00:00 EDT 2009 · Nature · OSTI ID:1165583

Structure, Function, and Evolution of Rice Centromeres

Technical Report · Wed Feb 03 23:00:00 EST 2010 · OSTI ID:971493

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
CRM
Evolutionary Biology
Genetics & Heredity
centromeric retrotransposon
horizontal transfer
interelement recombination
phylogeny

Evolution of Centromeric Retrotransposons in Grasses

Citation Formats

References (65)

Cited By (12)

Similar Records

Related Subjects