LTR retrotransposon

Last updated
A. Genetic structure of LTR-retrotransposons (gypsy-type). B. Mechanism of retrotransposition, occurring inside viral-like particles in the cytoplasm. Reverse transcription initiates at a host tRNA primer binding site (PBS) located immediately downstream of the 5'LTR. The newly synthesized minus-strand cDNA copy of the 5'LTR is then transferred to the 3'LTR and used as a primer for reverse-transcription of the entire minus-strand sequence. An RNase H-resistant polypurine tract then serves as a primer for plus-strand synthesis of the 3'LTR and complementary PBS. The newly synthesized plus-strand PBS then associates with the already-synthesized minus-strand PBS, and double-stranded cDNA is finally produced. Double-stranded cDNA is then transferred to the nucleus by integrase proteins, and a new copy is integrated into the genome. LTR retrotransposon.png
A. Genetic structure of LTR-retrotransposons (gypsy-type). B. Mechanism of retrotransposition, occurring inside viral-like particles in the cytoplasm. Reverse transcription initiates at a host tRNA primer binding site (PBS) located immediately downstream of the 5'LTR. The newly synthesized minus-strand cDNA copy of the 5'LTR is then transferred to the 3'LTR and used as a primer for reverse-transcription of the entire minus-strand sequence. An RNase H-resistant polypurine tract then serves as a primer for plus-strand synthesis of the 3'LTR and complementary PBS. The newly synthesized plus-strand PBS then associates with the already-synthesized minus-strand PBS, and double-stranded cDNA is finally produced. Double-stranded cDNA is then transferred to the nucleus by integrase proteins, and a new copy is integrated into the genome.

LTR retrotransposons are class I transposable elements (TEs) characterized by the presence of long terminal repeats (LTRs) directly flanking an internal coding region. As retrotransposons, they mobilize through reverse transcription of their mRNA and integration of the newly created cDNA into another genomic location. Their mechanism of retrotransposition is shared with retroviruses, with the difference that the rate of horizontal transfer in LTR-retrotransposons is much lower than the vertical transfer by passing active TE insertions to the progeny. LTR retrotransposons that form virus-like particles are classified under Ortervirales .

Contents

Their size ranges from a few hundred base pairs to 30 kb, the largest species reported to date are members of the Burro retrotransposon family in Schmidtea mediterranea . [1]

In plant genomes, LTR retrotransposons are the major repetitive sequence class constituting more than 75% of the maize genome. [2] LTR retrotransposons make up about 8% of the human genome and approximately 10% of the mouse genome. [3]

Structure and propagation

LTR retrotransposons have direct long terminal repeats that range from ~100 bp to over 5 kb in size. LTR retrotransposons are further sub-classified into the Ty1-copia-like (Pseudoviridae), Ty3-like (Metaviridae, formally referred to as Gypsy-like, a name that is being considered for retirement [4] ), and BEL-Pao-like (Belpaoviridae) groups based on both their degree of sequence similarity and the order of encoded gene products. Ty1-copia and Ty3-Metaviridae groups of retrotransposons are commonly found in high copy number (up to a few million copies per haploid nucleus) in animals, fungi, protista, and plants genomes. BEL-Pao like elements have so far only been found in animals. [5] [6]

All functional LTR-retrotransposons encode a minimum of two genes, gag and pol, that are sufficient for their replication. Gag encodes a polyprotein with a capsid and a nucleocapsid domain. [7] Gag proteins form virus-like particles in the cytoplasm inside which reverse-transcription occurs. The Pol gene produces three proteins: a protease (PR), a reverse transcriptase endowed with an RT (reverse-transcriptase) and an RNAse H domains, and an integrase (IN). [8]

Typically, LTR-retrotransposon mRNAs are produced by the host RNA pol II acting on a promoter located in their 5' LTR. The Gag and Pol genes are encoded in the same mRNA. Depending on the host species, two different strategies can be used to express the two polyproteins: a fusion into a single open reading frame (ORF) that is then cleaved or the introduction of a frameshift between the two ORFs. [9] Occasional ribosomal frameshifting allows the production of both proteins, while ensuring that much more Gag protein is produced to form virus-like particles.[ citation needed ]

Reverse transcription usually initiates at a short sequence located immediately downstream of the 5'-LTR and termed the primer binding site (PBS). Specific host tRNAs bind to the PBS and act as primers for reverse-transcription, which occurs in a complex and multi-step process, ultimately producing a double- stranded cDNA molecule. The cDNA is finally integrated into a new location, creating short TSDs (Target Site Duplications) [10] and adding a new copy in the host genome

Types

Ty1-copia retrotransposons

Ty1-copia retrotransposons are abundant in species ranging from single-cell algae to bryophytes, gymnosperms, and angiosperms. They encode four protein domains in the following order: protease, integrase, reverse transcriptase, and ribonuclease H.

At least two classification systems exist for the subdivision of Ty1-copia retrotransposons into five lineages: [11] [12] Sireviruses/Maximus, Oryco/Ivana, Retrofit/Ale, TORK (subdivided in Angela/Sto, TAR/Fourf, GMR/Tork), and Bianca.[ citation needed ]

Sireviruses/Maximus retrotransposons contain an additional putative envelope gene. This lineage is named for the founder element SIRE1 in the Glycine max genome, [13] and was later described in many species such as Zea mays , [14] Arabidopsis thaliana , [15] Beta vulgaris , [16] and Pinus pinaster . [17] Plant Sireviruses of many sequenced plant genomes are summarized at the MASIVEdb Sirevirus database. [18]

Ty3-retrotransposons (formally gypsy)

Ty3-retrotransposons are widely distributed in the plant kingdom, including both gymnosperms and angiosperms. They encode at least four protein domains in the order: protease, reverse transcriptase, ribonuclease H, and integrase. Based on structure, presence/absence of specific protein domains, and conserved protein sequence motifs, they can be subdivided into several lineages:

Errantiviruses contain an additional defective envelope ORF with similarities to the retroviral envelope gene. First described as Athila-elements in Arabidopsis thaliana , [19] [20] they have been later identified in many species, such as Glycine max [21] and Beta vulgaris . [22]

Chromoviruses contain an additional chromodomain (chromatin organization modifier domain) at the C-terminus of their integrase protein. [23] [24] They are widespread in plants and fungi, probably retaining protein domains during evolution of these two kingdoms. [25] It is thought that the chromodomain directs retrotransposon integration to specific target sites. [26] According to sequence and structure of the chromodomain, chromoviruses are subdivided into the four clades CRM, Tekay, Reina and Galadriel. Chromoviruses from each clade show distinctive integration patterns, e.g. into centromeres or into the rRNA genes. [27] [28]

Ogre-elements are gigantic Ty3-retrotransposons reaching lengths up to 25 kb. [29] Ogre elements have been first described in Pisum sativum . [30]

Metaviruses describe conventional Ty3-gypsy retrotransposons that do not contain additional domains or ORFs.

The Sushi family of Ty3 long terminal repeat retrotransposons were first identified in teleost fish and Sushi-like neogenes were subsequently identified in mammals. [31] Mammalian retrotransposon-derived transcripts (MARTs) cannot transpose but have retained open reading frames, demonstrate high levels of evolutionary conservation and are subject to selective pressures, which suggests some have become neofunctionalized genes with new cellular functions. [31] Retrotransposon gag-like-3 (RTL3/ZCCHC5/MART3) is one of eleven Sushi-like neogenes identified in the human genome. [31]

BEL/pao family

The BEL/pao family is found in animals. [32]

Endogenous retroviruses (ERV)

Although retroviruses are often classified separately, they share many features with LTR retrotransposons. A major difference with Ty1-copia and Ty3-gypsy retrotransposons is that retroviruses have an envelope protein (ENV). A retrovirus can be transformed into an LTR retrotransposon through inactivation or deletion of the domains that enable extracellular mobility. If such a retrovirus infects and subsequently inserts itself in the genome in germ line cells, it may become transmitted vertically and become an Endogenous Retrovirus. [6]

Terminal repeat retrotransposons in miniature (TRIMs)

Some LTR retrotransposons lack all of their coding domains. Due to their short size, they are referred to as terminal repeat retrotransposons in miniature (TRIMs). [33] [34] Nevertheless, TRIMs can be able to retrotranspose, as they may rely on the coding domains of autonomous Ty1-copia or Ty3-gypsy retrotransposons. Among the TRIMs, the Cassandra family plays an exceptional role, as the family is unusually wide-spread among higher plants. [35] In contrast to all other characterized TRIMs, Cassandra elements harbor a 5S rRNA promoter in their LTR sequence. [36] Due to their short overall length and the relatively high contribution of the flanking LTRs, TRIMs are prone to re-arrangements by recombination. [37]

Related Research Articles

<span class="mw-page-title-main">Genome</span> All genetic material of an organism

A genome is all the genetic information of an organism. It consists of nucleotide sequences of DNA. The nuclear genome includes protein-coding genes and non-coding genes, other functional regions of the genome such as regulatory sequences, and often a substantial fraction of junk DNA with no evident function. Almost all eukaryotes have mitochondria and a small mitochondrial genome. Algae and plants also contain chloroplasts with a chloroplast genome.

<span class="mw-page-title-main">Retroposon</span>

Retroposons are repetitive DNA fragments which are inserted into chromosomes after they had been reverse transcribed from any RNA molecule.

<span class="mw-page-title-main">Transposable element</span> Semiparasitic DNA sequence

A transposable element (TE), also transposon, or jumping gene, is a type of mobile genetic element, a nucleic acid sequence in DNA that can change its position within a genome, sometimes creating or reversing mutations and altering the cell's genetic identity and genome size.

<span class="mw-page-title-main">Retrotransposon</span> Type of genetic component

Retrotransposons are mobile elements which move in the host genome by converting their transcribed RNA into DNA through reverse transcription. Thus, they differ from Class II transposable elements, or DNA transposons, in utilizing an RNA intermediate for the transposition and leaving the transposition donor site unchanged.

Metaviridae is a family of viruses which exist as Ty3-gypsy LTR retrotransposons in a eukaryotic host's genome. They are closely related to retroviruses: members of the family Metaviridae share many genomic elements with retroviruses, including length, organization, and genes themselves. This includes genes that encode reverse transcriptase, integrase, and capsid proteins. The reverse transcriptase and integrase proteins are needed for the retrotransposon activity of the virus. In some cases, virus-like particles can be formed from capsid proteins.

Pseudoviridae is a family of viruses, which includes three genera.

Lentivirus is a genus of retroviruses that cause chronic and deadly diseases characterized by long incubation periods, in humans and other mammalian species. The genus includes the human immunodeficiency virus (HIV), which causes AIDS. Lentiviruses are distributed worldwide, and are known to be hosted in apes, cows, goats, horses, cats, and sheep as well as several other mammals.

Simian foamy virus (SFV), historically Human foamy virus (HFV), is a species of the genus Spumavirus that belongs to the family of Retroviridae. It has been identified in a wide variety of primates, including prosimians, New World and Old World monkeys, as well as apes, and each species has been shown to harbor a unique (species-specific) strain of SFV, including African green monkeys, baboons, macaques, and chimpanzees. As it is related to the more well-known retrovirus human immunodeficiency virus (HIV), its discovery in primates has led to some speculation that HIV may have been spread to the human species in Africa through contact with blood from apes, monkeys, and other primates, most likely through bushmeat-hunting practices.

Exon shuffling is a molecular mechanism for the formation of new genes. It is a process through which two or more exons from different genes can be brought together ectopically, or the same exon can be duplicated, to create a new exon-intron structure. There are different mechanisms through which exon shuffling occurs: transposon mediated exon shuffling, crossover during sexual recombination of parental genomes and illegitimate recombination.

Group-specific antigen, or gag, is the polyprotein that contains the core structural proteins of an Ortervirus. It was named as such because scientists used to believe it was antigenic. Now it is known that it makes up the inner shell, not the envelope exposed outside. It makes up all the structural units of viral conformation and provides supportive framework for mature virion.

<span class="mw-page-title-main">Long interspersed nuclear element</span>

Long interspersed nuclear elements (LINEs) are a group of non-LTR retrotransposons that are widespread in the genome of many eukaryotes. LINEs contain an internal Pol II promoter to initiate transcription into mRNA, and encode one or two proteins, ORF1 and ORF2. The functional domains present within ORF1 vary greatly among LINEs, but often exhibit RNA/DNA binding activity. ORF2 is essential to successful retrotransposition, and encodes a protein with both reverse transcriptase and endonuclease activity.

<span class="mw-page-title-main">Short interspersed nuclear element</span>

Short interspersed nuclear elements (SINEs) are non-autonomous, non-coding transposable elements (TEs) that are about 100 to 700 base pairs in length. They are a class of retrotransposons, DNA elements that amplify themselves throughout eukaryotic genomes, often through RNA intermediates. SINEs compose about 13% of the mammalian genome.

Human Endogenous Retrovirus-W (HERV-W) is a family of Human Endogenous Retroviruses (HERVs).

<span class="mw-page-title-main">RTL6</span> Human protein

Retrotransposon Gag Like 6 is a protein encoded by the RTL6 gene in humans. RTL6 is a member of the Mart family of genes, which are related to Sushi-like retrotransposons and were derived from fish and amphibians. The RTL6 protein is localized to the nucleus and has a predicted leucine zipper motif that is known to bind nucleic acids in similar proteins, such as LDOC1.

Metavirus is a genus of viruses in the family Metaviridae. They are retrotransposons that invade a eukaryotic host genome and may only replicate once the virus has infected the host. These genetic elements exist to infect and replicate in their host genome and are derived from ancestral elements unrelated from their host. Metavirus may use several different hosts for transmission, and has been found to be transmissible through ovule and pollen of some plants.

Semotivirus is the only genus of viruses in the family Belpaoviridae. Species exist as retrotransposons in a eukaryotic host's genome. BEL/pao transposons are only found in animals. Semotivirus is the only genus currently recognized, the genus description corresponds to the family, Belpaoviridae description.

<span class="mw-page-title-main">ZCCHC18</span> Protein-coding gene in the species Homo sapiens

Zinc finger CCHC-type containing 18 (ZCCHC18) is a protein that in humans is encoded by ZCCHC18 gene. It is also known as Smad-interacting zinc finger protein 2 (SIZN2), para-neoplastic Ma antigen family member 7b (PNMA7B), and LOC644353. Other names such as zinc finger, CCHC domain containing 12 pseudogene 1, P0CG32, ZCC18_HUMAN had been used to describe this protein.

<i>Ortervirales</i> Order of viruses

Ortervirales is an order that contains all accepted species of single-stranded RNA viruses that replicate through a DNA intermediate and all accepted species of double-stranded DNA viruses that replicate through an RNA intermediate . The name is derived from the reverse of retro.

Retrozymes are a family of retrotransposons first discovered in the genomes of plants but now also known in genomes of animals. Retrozymes contain a hammerhead ribozyme (HHR) in their sequences, although they do not possess any coding regions. Retrozymes are nonautonomous retroelements, and so borrow proteins from other elements to move into new regions of a genome. Retrozymes are actively transcribed into covalently closed circular RNAs and are detected in both polarities, which may indicate the use of rolling circle replication in their lifecycle.

Cer6 is a LTR retrotransposon that is described from sequencing data in the chromosome III of C. elegans.

References

  1. ↑ Grohme, Markus Alexander; Schloissnig, Siegfried; Rozanski, Andrei; Pippel, Martin; Young, George Robert; Winkler, Sylke; Brandl, Holger; Henry, Ian; Dahl, Andreas; Powell, Sean; Hiller, Michael; Myers, Eugene; Rink, Jochen Christian (January 2018). "The genome of Schmidtea mediterranea and the evolution of core cellular mechanisms". Nature. 554 (7690): 56–61. doi:10.1038/nature25473. hdl: 21.11116/0000-0003-F5F3-6 . ISSN   1476-4687.
  2. ↑ Baucom, RS; Estill, JC; Chaparro, C; Upshaw, N; Jogi, A; Deragon, JM; Westerman, RP; Sanmiguel, PJ; Bennetzen, JL (November 2009). "Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome". PLOS Genetics. 5 (11): e1000732. doi: 10.1371/journal.pgen.1000732 . PMC   2774510 . PMID   19936065.
  3. ↑ McCarthy EM, McDonald JF (2004). "Long terminal repeat retrotransposons of Mus musculus". Genome Biol. 5 (3): R14. doi: 10.1186/gb-2004-5-3-r14 . PMC   395764 . PMID   15003117.
  4. ↑ "OSF". osf.io. Retrieved 2022-11-04.
  5. ↑ Copeland CS, Mann VH, Morales ME, Kalinna BH, Brindley PJ (2005). "The Sinbad retrotransposon from the genome of the human blood fluke, Schistosoma mansoni, and the distribution of related Pao-like elements". BMC Evol. Biol. 5 (1): 20. doi: 10.1186/1471-2148-5-20 . PMC   554778 . PMID   15725362.
  6. 1 2 Wicker T, Sabot F, Hua-Van A, et al. (December 2007). "A unified classification system for eukaryotic transposable elements". Nat. Rev. Genet. 8 (12): 973–82. doi:10.1038/nrg2165. PMID   17984973. S2CID   32132898.
  7. ↑ Sandmeyer, Suzanne B; Clemens, Kristina A (2010). "Function of a retrotransposon nucleocapsid protein". RNA Biology. 7 (6): 642–654. doi:10.4161/rna.7.6.14117. ISSN   1547-6286. PMC   3073325 . PMID   21189452.
  8. ↑ Wicker, Thomas; Sabot, François; Hua-Van, Aurélie; Bennetzen, Jeffrey L.; Capy, Pierre; Chalhoub, Boulos; Flavell, Andrew; Leroy, Philippe; Morgante, Michele (December 2007). "A unified classification system for eukaryotic transposable elements". Nature Reviews. Genetics. 8 (12): 973–982. doi:10.1038/nrg2165. ISSN   1471-0064. PMID   17984973. S2CID   32132898.
  9. ↑ GAO, XIANG; HAVECKER, ERICKA R.; BARANOV, PAVEL V.; ATKINS, JOHN F.; VOYTAS, DANIEL F. (December 2003). "Translational recoding signals between gag and pol in diverse LTR retrotransposons". RNA. 9 (12): 1422–1430. doi:10.1261/rna.5105503. ISSN   1355-8382. PMC   1370496 . PMID   14623998.
  10. ↑ "What is Transposon's Target Site Duplication (TSD)?". 22 May 2019.
  11. ↑ Wicker, T; Keller, B (July 2007). "Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families". Genome Research. 17 (7): 1072–81. doi:10.1101/gr.6214107. PMC   1899118 . PMID   17556529.
  12. ↑ Llorens, C; Muñoz-Pomer, A; Bernad, L; Botella, H; Moya, A (2 November 2009). "Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees". Biology Direct. 4: 41. doi: 10.1186/1745-6150-4-41 . PMC   2774666 . PMID   19883502.
  13. ↑ Laten, HM; Majumdar, A; Gaucher, EA (9 June 1998). "SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein". Proceedings of the National Academy of Sciences of the United States of America. 95 (12): 6897–902. Bibcode:1998PNAS...95.6897L. doi: 10.1073/pnas.95.12.6897 . PMC   22677 . PMID   9618510.
  14. ↑ Bousios, A; Kourmpetis, YA; Pavlidis, P; Minga, E; Tsaftaris, A; Darzentas, N (February 2012). "The turbulent life of Sirevirus retrotransposons and the evolution of the maize genome: more than ten thousand elements tell the story". The Plant Journal. 69 (3): 475–88. doi: 10.1111/j.1365-313x.2011.04806.x . PMID   21967390.
  15. ↑ Kapitonov, VV; Jurka, J (1999). "Molecular paleontology of transposable elements from Arabidopsis thaliana". Genetica. 107 (1–3): 27–37. doi:10.1023/a:1004030922447. PMID   10952195. S2CID   27249664.
  16. ↑ Weber, B; Wenke, T; Frömmel, U; Schmidt, T; Heitkam, T (February 2010). "The Ty1-copia families SALIRE and Cotzilla populating the Beta vulgaris genome show remarkable differences in abundance, chromosomal distribution, and age". Chromosome Research. 18 (2): 247–63. doi:10.1007/s10577-009-9104-4. PMID   20039119. S2CID   24883110.
  17. ↑ Miguel, C; Simões, M; Oliveira, MM; Rocheta, M (November 2008). "Envelope-like retrotransposons in the plant kingdom: evidence of their presence in gymnosperms (Pinus pinaster)". Journal of Molecular Evolution. 67 (5): 517–25. Bibcode:2008JMolE..67..517M. doi:10.1007/s00239-008-9168-3. PMID   18925379. S2CID   28629941.
  18. ↑ Bousios, A; Minga, E; Kalitsou, N; Pantermali, M; Tsaballa, A; Darzentas, N (30 April 2012). "MASiVEdb: the Sirevirus Plant Retrotransposon Database". BMC Genomics. 13: 158. doi: 10.1186/1471-2164-13-158 . PMC   3414828 . PMID   22545773.
  19. ↑ Pélissier, T; Tutois, S; Deragon, JM; Tourmente, S; Genestier, S; Picard, G (November 1995). "Athila, a new retroelement from Arabidopsis thaliana". Plant Molecular Biology. 29 (3): 441–52. doi:10.1007/bf00020976. PMID   8534844. S2CID   8296300.
  20. ↑ Wright, DA; Voytas, DF (June 1998). "Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins". Genetics. 149 (2): 703–15. doi:10.1093/genetics/149.2.703. PMC   1460185 . PMID   9611185.
  21. ↑ Wright, DA; Voytas, DF (January 2002). "Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses". Genome Research. 12 (1): 122–31. doi:10.1101/gr.196001. PMC   155253 . PMID   11779837.
  22. ↑ Wollrab, C; Heitkam, T; Holtgräwe, D; Weisshaar, B; Minoche, AE; Dohm, JC; Himmelbauer, H; Schmidt, T (November 2012). "Evolutionary reshuffling in the Errantivirus lineage Elbe within the Beta vulgaris genome". The Plant Journal. 72 (4): 636–51. doi: 10.1111/j.1365-313x.2012.05107.x . hdl: 11858/00-001M-0000-000E-F0B9-B . PMID   22804913.
  23. ↑ Marín, I; Lloréns, C (July 2000). "Ty3/Gypsy retrotransposons: description of new Arabidopsis thaliana elements and evolutionary perspectives derived from comparative genomic data". Molecular Biology and Evolution. 17 (7): 1040–9. doi: 10.1093/oxfordjournals.molbev.a026385 . PMID   10889217.
  24. ↑ Gorinsek, B; Gubensek, F; Kordis, D (May 2004). "Evolutionary genomics of chromoviruses in eukaryotes". Molecular Biology and Evolution. 21 (5): 781–98. doi: 10.1093/molbev/msh057 . PMID   14739248.
  25. ↑ Novikova, O; Smyshlyaev, G; Blinov, A (8 April 2010). "Evolutionary genomics revealed interkingdom distribution of Tcn1-like chromodomain-containing Gypsy LTR retrotransposons among fungi and plants". BMC Genomics. 11: 231. doi: 10.1186/1471-2164-11-231 . PMC   2864245 . PMID   20377908.
  26. ↑ Gao, X; Hou, Y; Ebina, H; Levin, HL; Voytas, DF (March 2008). "Chromodomains direct integration of retrotransposons to heterochromatin". Genome Research. 18 (3): 359–69. doi:10.1101/gr.7146408. PMC   2259100 . PMID   18256242.
  27. ↑ Neumann, P; Navrátilová, A; Koblížková, A; Kejnovský, E; Hřibová, E; Hobza, R; Widmer, A; Doležel, J; Macas, J (3 March 2011). "Plant centromeric retrotransposons: a structural and cytogenetic perspective". Mobile DNA. 2 (1): 4. doi: 10.1186/1759-8753-2-4 . PMC   3059260 . PMID   21371312.
  28. ↑ Weber, B; Heitkam, T; Holtgräwe, D; Weisshaar, B; Minoche, AE; Dohm, JC; Himmelbauer, H; Schmidt, T (1 March 2013). "Highly diverse chromoviruses of Beta vulgaris are classified by chromodomains and chromosomal integration". Mobile DNA. 4 (1): 8. doi: 10.1186/1759-8753-4-8 . PMC   3605345 . PMID   23448600.
  29. ↑ Macas, J; Neumann, P (1 April 2007). "Ogre elements--a distinct group of plant Ty3/gypsy-like retrotransposons". Gene. 390 (1–2): 108–16. doi:10.1016/j.gene.2006.08.007. PMID   17052864.
  30. ↑ Neumann, P; Pozárková, D; Macas, J (October 2003). "Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced". Plant Molecular Biology. 53 (3): 399–410. CiteSeerX   10.1.1.551.7542 . doi:10.1023/b:plan.0000006945.77043.ce. PMID   14750527. S2CID   13412101.
  31. 1 2 3 Ball, Hope C.; Ansari, Mohammad Y.; Ahmad, Nashrah; Novak, Kimberly; Haqqi, Tariq M. (November 2021). "A retrotransposon gag-like-3 gene RTL3 and SOX-9 co-regulate the expression of COL2A1 in chondrocytes". Connective Tissue Research. 62 (6): 615–628. doi:10.1080/03008207.2020.1828380. ISSN   1607-8438. PMC   8404968 . PMID   33043724.
  32. ↑ Llorens, Carlos; Soriano, Beatriz; Navarrete-Muñoz, Maria A.; Hafez, Ahmed; Arnau, Vicente; Benito, Jose Miguel; Gabaldon, Toni; Rallon, Norma; Pérez-Sánchez, Jaume; Krupovic, Mart (2021). "Reverse-Transcribing Viruses (Belpaoviridae, Metaviridae, and Pseudoviridae)". Encyclopedia of virology (Fourth ed.). Amsterdam. pp. 653–666. doi:10.1016/B978-0-12-809633-8.21514-8. ISBN   978-0-12-814516-6. S2CID   243337524.{{cite book}}: CS1 maint: location missing publisher (link)
  33. ↑ Witte, Claus-Peter Le, Quang Hien Bureau, Thomas Kumar, Amar (2001). "Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes". Proceedings of the National Academy of Sciences of the United States of America. 98 (24). The National Academy of Sciences: 13778–13783. Bibcode:2001PNAS...9813778W. doi: 10.1073/pnas.241341898 . OCLC   678730241. PMC   61118 . PMID   11717436.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  34. ↑ Antonius-Klemola, Kristiina; Kalendar, Ruslan; Schulman, Alan H. (2006-01-11). "TRIM retrotransposons occur in apple and are polymorphic between varieties but not sports". Theoretical and Applied Genetics. 112 (6): 999–1008. doi:10.1007/s00122-005-0203-0. ISSN   0040-5752. PMID   16404583. S2CID   7035882.
  35. ↑ Gao, Dongying; Li, Yupeng; Abernathy, Brian; Jackson, Scott (2014-10-29). "Landscape and evolutionary dynamics of terminal-repeat retrotransposons in miniature (TRIMs) in 48 whole plant genomes" (PDF). doi:10.1101/010850. S2CID   10238180 . Retrieved 2020-10-03.{{cite journal}}: Cite journal requires |journal= (help)
  36. ↑ Kalendar, R.; Tanskanen, J.; Chang, W.; Antonius, K.; Sela, H.; Peleg, O.; Schulman, A. H. (2008-04-11). "Cassandra retrotransposons carry independently transcribed 5S RNA". Proceedings of the National Academy of Sciences. 105 (15): 5833–5838. Bibcode:2008PNAS..105.5833K. doi: 10.1073/pnas.0709698105 . ISSN   0027-8424. PMC   2311327 . PMID   18408163.
  37. ↑ Maiwald, Sophie; Weber, Beatrice; Seibt, Kathrin M; Schmidt, Thomas; Heitkam, Tony (2020-10-03). "The Cassandra retrotransposon landscape in sugar beet (Beta vulgaris) and related Amaranthaceae: Recombination and re-shuffling lead to a high structural variability". Annals of Botany. 127 (1): 91–109. doi: 10.1093/aob/mcaa176 . ISSN   0305-7364. PMC   7750724 . PMID   33009553.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.