- Research article
- Open Access
Transcriptional activity of PIF and Pong-like Class II transposable elements in Triticeae
© The Author(s). 2017
- Received: 15 January 2017
- Accepted: 26 July 2017
- Published: 3 August 2017
Transposable elements are major contributors to genome size and variability, accounting for approximately 70–80% of the maize, barley, and wheat genomes. PIF and Pong-like elements belong to two closely-related element families within the PIF/Harbinger superfamily of Class II (DNA) transposons. Both elements contain two open reading frames; one encodes a transposase (ORF2) that catalyzes transposition of the functional elements and their related non-autonomous elements, while the function of the second is still debated. In this work, we surveyed for PIF- and Pong-related transcriptional activity in 13 diploid Triticeae species, all of which have been previously shown to harbor extensive within-genome diversity of both groups of elements.
The results revealed that PIF elements have considerable transcriptional activity in Triticeae, suggesting that they can escape the initial levels of plant cell control and are regulated at the post-transcriptional level. Phylogenetic analysis of 156 PIF cDNA transposase fragments along with 240 genomic partial transposase sequences showed that most, if not all, PIF clades are transcriptionally competent, and that multiple transposases coexisting within a single genome have the potential to act simultaneously. In contrast, we did not detect any transcriptional activity of Pong elements in any sample.
The lack of Pong element transcription shows that even closely related transposon families can exhibit wide variation in their transposase transcriptional activity within the same genome.
- Transposable elements
- DNA transposon
- Class II
Triticeae is a pooid tribe with approximately 30 genera and 300–400 species , including wheat, barley, and rye. The tribe’s economic importance has made it the focus of many evolutionary and genetic studies over the last few decades. The Triticeae genome is large and complex, with approximately 70–80% composed of transposable elements (TEs) [2–7].
Eukaryotic TEs have been divided into two main groups based on their structure and transposition mechanism. Class I TEs (retrotransposons) transpose by reverse transcription of an RNA intermediate, while Class II TEs (DNA elements) transpose via a double-stranded DNA intermediate through a “cut and paste” mechanism whereby the element is excised and reinserted elsewhere in the host genome. These usually have terminal inverted repeats (TIRs) whose size and sequence are characteristic of the family or superfamily to which the element belongs. Autonomous Class II elements encode all functional products required for transposition, including a transposase gene (TPase) that catalyzes DNA cleavage and transposition. Non-autonomous elements are usually deletion derivatives of autonomous elements that only retain the terminal sequences necessary for recognition and activation by the transposition machinery of autonomous elements [8, 9]. All TE superfamilies contain both autonomous and non-autonomous elements .
Transposable elements are major contributors to genome size and variability, and gene evolution [11–16]. Their ability to move and amplify within a genome results in mutational activity that can alter gene structure and function [17, 18] through loss of genes [12, 14, 15], changes in expression levels , or evolution of new functions [20–22]. Once integrated in the genome, some TEs accumulate mutations and become transcriptionally and/or transpositionally inactive [23–26]. A fine balance between transcription, transposition, and host survival should be reached, and the host tightly controls the activity of TEs . However, despite mutation and cell control, some TEs remain transcriptionally and transpositionally active [28–34].
This work is focused on the transcriptional activity of a superfamily of Class II elements called PIF/Harbinger in the genomes of 13 diploid species from the wheat tribe, Triticeae. The PIF/Harbinger elements form a widespread superfamily of DNA transposons, which consists of PIF and Pong-like elements. PIF and Pong-like elements were first discovered in the maize  and rice  genomes, respectively, and they have since been detected in the genomes of many flowering plants, animals, and fungi [28, 35–38].
We have demonstrated that PIF and Pong elements in the genomes of diploid Triticeae species are abundant and highly variable, and represent multiple diverse lineages within genomes that appear to predate the origin of the tribe itself [45, 46]. To determine whether they are transcriptionally active, we screened 15 diploid individuals from 13 species for the presence of PIF and Pong-like transcripts, and we performed phylogenetic analyses of both genomic DNA and cDNA copies to establish whether the detected transcripts are produced by several or only few transposase lineages. We found that PIF-like transposases are actively transcribed in Triticeae and that most, if not all, transposase lineages that we previously identified are transcriptionally competent . In contrast to our evidence of PIF transcription, we did not detect any transcriptional activity of Pong elements in any sample.
List of Triticeae taxa included in PIF transcriptional analyses. Samples are represented with their names and collection numbers
genomic PIF a
Sample source and reference number
Sample source and reference number
Aegilops comosa Sibth. & Smith
Agropyron cristatum (L.) Gaertn.
Australopyrum velutinum (Nees) B.K.Simon
Crithopsis delileana (Schult.) Roshev.
Dasypyrum villosum (L.) P.Candargy
Eremopyrum bonaepartis (Spreng.) Nevski
Henrardia persica (Boiss.) C.E.Hubb
Heteranthelium piliferum (Banks & Sol.) Hochst.
Hordeum bogdanii Wilensky (1)
Hordeum bogdanii Wilensky (2)
Hordeum chilense Roem. & Schult.
Peridictyon sanctum (Janka) Seberg, Fred., & Baden
Psathyrostachys fragilis (Boiss.) Nevski
Psathyrostachys juncea (Fisch.) Nevski
Pseudoroegneria libanotica (Hack.) D.R.Dewey
Pseudoroegneria spicata (Pursh) Á.Löve
Pseudoroegneria tauri (Boiss. & Balansa) Á.Löve
Secale montanum Guss.
Taeniatherum caput-medusae (L.) Nevski (1)
Taeniatherum caput-medusae (L.) Nevski (2)
Thinopyrum bessarabicum (Săvul. & Rayss) Á.Löve
Triticum monococcum L.
Triticum urartu Tumanian ex Gandilyan
DNA, RNA extractions and cDNA synthesis
The DNA was extracted for previous phylogenetic studies from fresh or dried leaf material, using a CTAB-based method . RNA was extracted from fresh leaf material harvested from reproductively mature plants (Table 1). Plant tissue was snap-frozen in liquid nitrogen and total RNA was extracted using a commercial extraction kit (Promega), following the manufacturer’s instructions. Crude total RNA preparations were treated with TURBO DNA-free™ (Ambion) to remove residual DNA. RNA quality was inferred by running 5 μl on an agarose gel, and RNA concentrations were estimated using a NanoDrop Spectrophotometer (Thermo Fisher Scientific Inc., MA, USA). Prior to cDNA synthesis, the presence/absence of genomic DNA contamination was tested for all RNA preparations using PCR reactions with PIF and Pong primers known to work on genomic DNA, and an RT- control supplied with the cDNA synthesis kit. cDNA was generated from DNA-free total RNA using the Protoscript RT-PCR kit (NEB) using 2 μl of random and oligo-dT primers and following the manufacturer’s protocol. The cDNAs were used as templates in amplification reactions as described below.
Amplification of the PIF ORF2 conserved domain
Triticeae-specific degenerate primers (cPIF-for: GGAGCHWTNGATGGYACWCAC, cPIF-rev: AAGGTTGAAYAGCTCCYT) targeting a conserved portion of the PIF transposase were used for all PCR amplifications (Fig. 1b). These primers are anchored in two highly conserved amino acid residue motifs (GAMDGTH and RELFNL respectively) of the transposase gene, surrounding the “DD” portion of the “DDE” motif. The predicted TPases encoded by plant PIF transposons vary in length from 392 to 432 amino acids ; the amplified portion represents between 120 and 147 amino acids. The position of the “DD” transposase fragment was predicted by comparison of a reduced set of aligned Triticeae sequences to the corresponding portion of the “DDE” motif from a Zea mays PIF element (AY362811; Fig. 1b). All amplifications were carried out in a 10 μl reactions containing 50 ng of cDNA, 10× PCR buffer, 0.1 mmol/L of each primer, 0.5 units of Taq polymerase (Sigma), 0.2 mmol/L of each dNTP, and 1.5 mmol/L MgCl2. The PCR amplification conditions were: 5 min of DNA denaturation at 95 °C, followed by 35 cycles of 30 s at 95 °C, 45 s at 57 °C and 60 s at 72 °C for each cycle. The last cycle was followed by a 10 min final extension at 72 °C.
Amplification of the Pong ORF2 conserved domain
Degenerate primers (Pong-for: GGCWCCATYGAYTGTATGCAC, Pong-rev: YTCGTCYTCVACYATCATRTTGTG; ) were used for cDNA amplification of approximately one-third or 520 bp of conserved region of the Pong transposase domain, including the “DDE” motif. These primers are anchored in two highly conserved amino acid residue blocks (GTIDCMH and NMIVEDE) of the transposase gene (Fig. 1c) and were previously shown to work on genomic DNA [37, 46]. All amplifications were carried out as described in .
Cloning, sequencing and sequence alignment
PCR products were cloned prior to sequencing, and multiple clones from each species were sequenced to evaluate intra-individual transposase diversity. Three PCR reactions were run for each cloning reaction to counter the potential effects of PCR drift . PCR products from replicated reactions were isolated on 1% agarose gels, combined and purified on columns (Qiagen). Cleaned products were cloned into pGEM-T Easy vectors (Promega) and transformed into E.coli JM109 competent cells (Promega) according to the manufacturer’s instructions, except that all reactions were halved. Positive (white) colonies containing the insert were PCR amplified as described above. The resulting fragments were cleaned with 0.2 μl exonuclease and 0.4 μl shrimp alkaline phosphatase, and sequenced in both directions with the PCR primers. Sequencing was performed on an ABI 377 automated sequencer (Applied Biosystems). The nucleotide and inferred amino acid sequences of PIF-like transposases were aligned using CLUSTALW  with default parameters, and then manually adjusted in MacClade 4.08 (Maddison and Maddison). All alignments are available upon request.
Phylogenies were estimated using maximum parsimony (MP) and maximum likelihood (ML). Parsimony analyses and pairwise sequence distances were estimated with PAUP* v.4.0b10 . The parsimony bootstrap method, with 1000 replicates with heuristic search, was used to estimate the robustness of the clades  (tree not shown). For the ML analysis, the appropriate model of sequence evolution was determined by jModelTest [53–55] and the corrected Akaike information criterion . The selected models of evolution were implemented in the Mac OS X version of GARLI v.0.95  for analysis. Following the recommendations of the author, multiple (50) analyses with random starting tree topologies were performed for each data set. Runs were set for an unlimited number of generations, and automatic termination following 10,000 generations without a significant change in topology. Bootstrap support for each tree was estimated based on 100 ML bootstrap replicates with the same options used to generate the ML tree. All sequences were deposited in the NCBI GenBank database (accession numbers MF281799-MF281954).
Isolation and characterization of PIF cDNAs
We isolated, cloned, and sequenced 156 unique cDNA fragments from the conserved transposase domain of PIF-like TEs in 15 diploid Triticeae samples. As in our previous analysis of genomic PIF sequences, all fragments corresponded to the “DD” portion of the “DDE” transposase motif (Fig. 1b) . PCR amplifications yielded two bands of approximately 360 and 440 bp, labeled “S” (short) and “L” (long) in the PIF phylogenies (Figs. 2 and 3), for all samples except Eremopyrum bonaepartis, Triticum monococcum, and Agropyrum cristatum, in which only the longer fragments were detected. The 156 cDNA sequences revealed that the length difference between long and short fragments is explained by the retention of an intron during transcription by 112 PIF transposase fragments, ranging in size from 72 to 88 bp. The intron was located six residues upstream of the second D (Fig. 1b), and contained a stop codon in 85 of the sequences. Approximately 30 of the 156 products contained additional deletions and insertions of one or a few bases; thus, some apparently non-functional gene copies are being transcribed. Sequences showed 58.65–100% nucleotide identity, with the highest level of divergence (41.35%) found between E. bonaepartis 14L and Psathyrostachys juncea 8L. Identical ORF cDNA fragments were detected in different samples in four cases (marked with rectangles on Fig. 2): Pseudoroegneria libanotica 14L and Taeniatherum caput-medusae1 6L; P. libanotica 4L and Hordeum bogdanii2 17L; T. urartu 5S and T. caput-medusae2 2S; and T. caput-medusae2 17S, T. caput-medusae1 5S, and Crithopsis delileana 5S.
Triticeae contain transcriptionally active PIF, but not Pong elements
Our results show that PIF is actively transcribed in all samples. We did not detect any transcriptional activity for the closely related Pong elements, even though a previous study of Pong genomic sequences  showed that Pong sequences are, like PIF, widely dispersed within Triticeae, with multiple distinct and genetically diverse transposases coexisting within individual genomes. We do not think the lack of transcripts can be explained as a technical artifact due to poor amplification, because the amplification primers used here are the same ones used to successfully amplify a wide diversity of genomic Pong sequences from the same Triticeae species . The Pong results not only further highlight a difference in transcriptional activity between these otherwise very similar groups of elements, but they also served a practical purpose, as an additional control confirming the absence of genomic DNA contamination in all RNA preparations.
All phylogenetic analyses of the Triticeae PIF-like cDNAs were performed on a region of approximately 360 bp coding sequence; the intron was excluded because of alignment ambiguities. Maximum parsimony topologies (not shown) were in general accordance with the ML topologies, but there was more resolution and support in the ML trees. Given the difficulties of finding an outgroup while providing clarification of phylogenetic relationships between TEs, we used the mid-point rooting method  for all of the phylogenetic trees. Although PIF sequences from grass genera outside the wheat tribe are available, they are not appropriate as outgroups for the Triticeae elements because the PIF-like lineages within Triticeae appear to predate the tribe’s origin [i.e., some PIF elements from within the Triticeae are more closely related to grass elements from outside of the tribe than they are to other elements from within the tribe [; see also [38, 42]].
Phylogeny of PIF cDNA transcripts in Triticeae
This data set included all 156 cDNA fragments from all 15 accessions. (A phylogeny of 44 cDNA PIF transcripts with no intron is presented as an Additional file 1). The best topology (−lnL = 5,169.16730; Fig. 2) revealed three main groups of PIF cDNAs in Triticeae (I-III in Fig. 2). Psathyrostachys juncea 2L was sister (69% bootstrap support) to group I (100% bootstrap), which was the largest and the most complex group, and was further subdivided into two weakly supported subgroups. Group I contained sequences from all samples except E. bonaepartis. Within this group, P. libanotica 14L was identical to T. caput-medusae1 6L (indicated with rectangles on Fig. 2). Group II (weakly supported) was represented by sequences from all samples except H. bogdanii1 and T. monococcum. Within this group, three sets of sequences were identical: H. bogdanii2 17L and P. libanotica 4L; T. caput-medusae2 2S and T.urartu 5S; and C. delileana 5S, T. caput-medusae2 17S, and T. caput-medusae1 5S (indicated with rectangles on Fig. 2). Aegilops comosa 9S was sister to group II with bootstrap of 64%. Group III (100% bootstrap support) only included sequences from C. delileana, P. libanotica, and P. juncea. The small size of this group points to a combination of differences in element transcriptional activity, the loss of some lineages through stochastic events and natural selection, and/or random sampling artifacts. Crithopsis delileana and P. libanotica exhibited very broad distribution, with cDNA sequences in all of the main evolutionary lineages identified.
Phylogeny of genomic and cDNA PIF transposase fragments
This analysis included 156 cDNAs generated for this study along with 240 genomic PIF sequences from a previous phylogenetic study of PIF sequences in Triticeae  (Fig. 3). Of the 240 genomic sequences, 113 had frameshifting indels or stop codons, and thus are probably not functional. The best topology (−lnL = 11,008.92254; Fig. 3) revealed multiple distinct transposase cDNA fragments grouped with genomic sequences in well-defined and generally well-supported clades (Fig. 3). The wide distribution of cDNA sequences among the genomic sequences showed that they are derived from multiple evolutionary lineages, indicating that distinct transposases have retained transcriptional competence during the evolution of the tribe and have the potential to function simultaneously within a genome (Fig. 3).
Eight cDNAs were identical to genomic PIF fragments (indicated with green rectangles in Fig. 3), suggesting that they originated from identical or nearly identical transposase fragments (although only half of them are paired with genomic copies from the same species). Of these eight transcripts, seven were derived from transposases with no frameshifting indels or stop codons. The eighth, cH. bogdanii2 7L, is characterized by four single base pair deletions, resulting in a change of the reading frame, thus demonstrating that transcriptional activity does not necessarily indicate functional activity. Two pairs of genomic transposase sequences were identical (marked with pale blue rectangles on Fig. 3): gThinopyrum bessarabicum 8 and gP.libanotica 14; and gH. bogdanii 15 and gT. urartu 23.
Transcription is the first of several steps required for TE transposition . Autonomous elements (i.e. elements that encode all functional products required for transposition) have the potential to self-activate or regulate the activity of related non-autonomous versions, which are ubiquitous in grass genomes . To ensure the viability of their host, and therefore their own survival, optimized transmission and restricted transpositional activity are the hallmark of many TE families. Once integrated in the host genome, TEs rapidly accumulate small insertions, deletions, and rearrangements that alter their structural integrity and render them inactive [23, 25, 26]. Plant cells have also developed a variety of transcriptional and post-transcriptional regulatory mechanisms to protect their genomes against TE movement, including silencing by increased DNA methylation of promoter regions, histone modifications, or small RNA interference [19, 60–62].
Transcriptional activity of PIF and Pong-like TEs in Triticeae
Our work on the evolutionary dynamics of PIF and Pong transposase activity in Triticeae had two major goals. The first was to determine whether PIF and Pong are transcriptionally active in Triticeae, and the second was to assess the diversity of transcribed transposase lineages. We found that PIF-like transcripts are present throughout the Triticeae, indicating that they have remained transcriptionally active throughout of the long history of the tribe (13–25 mya; ). Phylogenetic analysis of both genomic DNA and cDNA revealed that the detected PIF transcripts belong to distinct clades, and that most, if not all transposase lineages have remained transcriptionally competent. In contrast, we did not detect any transcriptional activity of Pong elements in any sample, in spite of previous work  showing that the diversity of Pong elements in Triticeae genomes is comparable to that of PIF elements in the same species, with multiple distinct lineages coexisting within a single genome. Although this work is focused on TE transcriptional activity in mature leaf material only, the lack of Pong activity in the wheat tribe also contrasts with observations from other plant species; Pong elements have undergone recent amplification in Arabidopsis and Brassica , and are transcriptionally active in rice [30, 64–66]. One plausible explanation for the lack of Pong-related transcription within Triticeae genomes could be the failure of a related or unrelated TE, transposase gene, or mechanism to activate the transcription machinery of Pong elements in a common ancestor of Triticeae. It is highly unlikely that individual Pong copies have been transcriptionally inactivated separately due to natural selection and/or genetic drift. Based on our previous analyses of Pong elements within Triticeae genomes, their expansion seems to be recent , thus it is possible that the element is still active but another mechanism has failed to instigate its transcription and therefore activity.
Phylogeny of PIF cDNA transcripts
Genome-wide studies of transcriptional activity of 56 maize TE families, the PIF family included, have demonstrated that TE Expressed Sequence Tags (ESTs) are located only in a few clades of genomic sequences, indicating that few evolutionary branches of the TEs are transcriptionally active . However, in contrast to these findings, our results revealed that the majority of PIF lineages have retained transcriptional capacity.
The wide distribution of distinct taxa in groups I and II in Fig. 2 suggests that diverse ancestral lineages were vertically transmitted and have remained transcriptionally active during the evolution of the tribe (13–25 mya; ). Elements from groups I and II are missing from only a few individuals; this could be attributed either to loss from those genomes or to a sampling artifact. Group III (Fig. 2) is represented in far fewer individuals, which may be due to differential evolutionary success of this transposase lineage due to selection, and/or to stochastic losses. However, the presence of these transcripts in species derived from basal branches of the wheat tribe such as Psathyrostachys [68, 69] indicates this lineage was already present at the beginning of Triticeae radiation, and later lost from some of the descendants.
The presence of identical PIF transposase fragments shared across species boundaries suggests that recent or ongoing occasional horizontal transfer (HT) events have played a significant role in the complex distribution of PIF elements in Triticeae. This was also supported by our previous analysis of PIF dynamics in Triticeae , in which we identified two pairs of genomic PIF transposase gene fragments that exhibited extremely high nucleotide sequence identities (marked with pale blue rectangles on Fig. 3). Triticeae genera diverged 13–25 mya , and it is highly unlikely that their transposase sequences diverged at the same time as the hosts and maintained such high sequence similarity, even if they are under selective constraints . Here, the identification of identical pairs of cDNA and genomic transposase fragments provides further evidence that HT plays a role in the distribution of PIF elements among genera.
PIF and Pong-like elements are widely dispersed within the genomes of diploid Triticeae species. However, both TE families display unique features and vary considerably in their transposase transcriptional activity. No Pong-related transcripts were detected, while an abundance of diverse PIF-related transcripts were identified in all samples, indicating wide variations in the activity of closely related transposon families within the same genome. Multiple distinct transcriptionally competent PIF transposase clades were discovered, revealing that transcription of PIF elements in Triticeae is not restricted to few evolutionary lineages.
We appreciate the very helpful comments on the manuscript provided by three anonymous reviewers.
This work was supported by a National Science Foundation Grant (DEB-0426194) to Roberta J. Mason Gamer, and a Provost’s Award and an Elmer Hadley Research Award from the University of Illinois at Chicago to Dragomira N. Markova.
Availability of data and materials
All sequences are deposited in the NCBI GenBank database (accession numbers MF281799-MF281954).
DNM gathered the data and performed the analyses. DNM and RJMG conceived the study and wrote the manuscript. Both authors read and approved the final manuscript.
Ethics approval and consent to participate
Not applicable. No experiments or procedures involving animals were performed in this study.
Consent for publication
Both authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Löve A. Conspectus of the Triticeae. Feddes Repertorium. 1984;95:425–521.Google Scholar
- Charles M, Belcram H, Just J, Huneau C, Viollet A, Couloux A, Segurens B, Carter M, Huteau V, Coriton O, et al. Dynamics and differential proliferation of transposable elements during the evolution of the B and a genomes of wheat. Genetics. 2008;180(2):1071–86.View ArticlePubMedPubMed CentralGoogle Scholar
- Li W, Zhang P, Fellers JP, Friebe B, Gill BS. Sequence composition, organization, and evolution of the core Triticeae genome. Plant J. 2004;40(4):500–11.View ArticlePubMedGoogle Scholar
- Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C. Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J. 2006;48(3):463–74.View ArticlePubMedGoogle Scholar
- Wicker T, Taudien S, Houben A, Keller B, Graner A, Platzer M, Stein N. A whole-genome snapshot of 454 sequences exposes the composition of the barley genome and provides evidence for parallel evolution of genome size in wheat and barley. Plant J. 2009;59(5):712–22.View ArticlePubMedGoogle Scholar
- Mayer KF, Martis M, Hedley PE, Simkova H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, et al. Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell. 2011;23(4):1249–63.View ArticlePubMedPubMed CentralGoogle Scholar
- The International Barley Genome Sequencing Consortium. A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491(7426):711–6.Google Scholar
- Capy P, Bazin C, Higuet D, Langin T. Dynamics and evolution of transposable elements. TX: Landes Biosciences, Austin; 1998.Google Scholar
- Feschotte C, Jiang N, Wessler SR. Plant transposable elements: where genetics meets genomics. Nat Rev Genet. 2002;3(5):329–41.View ArticlePubMedGoogle Scholar
- Feschotte C, Wessler SR. Mariner-like transposases are widespread and diverse in flowering plants. Proc Natl Acad Sci U S A. 2002;99(1):280–5.View ArticlePubMedGoogle Scholar
- Jiang N, Feschotte C, Zhang X, Wessler SR. Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol. 2004;7(2):115–9.View ArticlePubMedGoogle Scholar
- Lai J, Li Y, Messing J, Dooner HK. Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci U S A. 2005;102(25):9068–73.View ArticlePubMedPubMed CentralGoogle Scholar
- Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, WR MC, Lavine K, Mittal V, May B, Kasschau KD, et al. Role of transposable elements in heterochromatin and epigenetic control. Nature. 2004;430(6998):471–6.View ArticlePubMedGoogle Scholar
- Ma J, Bennetzen JL. Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A. 2004;101(34):12404–10.View ArticlePubMedPubMed CentralGoogle Scholar
- Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet. 2005;37(9):997–1002.View ArticlePubMedGoogle Scholar
- Wang W, Zheng H, Fan C, Li J, Shi J, Cai Z, Zhang G, Liu D, Zhang J, Vang S, et al. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell. 2006;18(8):1791–802.View ArticlePubMedPubMed CentralGoogle Scholar
- Bennetzen JL. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. 2000;42(1):251–69.View ArticlePubMedGoogle Scholar
- Biemont C, Vieira C. Genetics: junk DNA as an evolutionary force. Nature. 2006;443(7111):521–4.View ArticlePubMedGoogle Scholar
- Lippman Z, Martienssen R. The role of RNA interference in heterochromatic silencing. Nature. 2004;431(7006):364–70.View ArticlePubMedGoogle Scholar
- Casacuberta E, Gonzalez J. The impact of transposable elements in environmental adaptation. Mol Ecol. 2013;22(6):1503–17.View ArticlePubMedGoogle Scholar
- Hayward A, Ghazal A, Andersson G, Andersson L, Jern P. ZBED evolution: repeated utilization of DNA transposons as regulators of diverse host functions. PLoS One. 2013;8(3):e59940.View ArticlePubMedPubMed CentralGoogle Scholar
- Majumdar S, Singh A, Rio DC. The human THAP9 gene encodes an active P-element DNA transposase. Science. 2013;339(6118):446–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Lampe DJ, Witherspoon DJ, Soto-Adames FN, Robertson HM. Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. Mol Biol Evol. 2003;20(4):554–62.View ArticlePubMedGoogle Scholar
- Silva JC, Loreto EL, Clark JB. Factors that affect the horizontal transfer of transposable elements. Curr Issues Mol Biol. 2004;6(1):57–71.PubMedGoogle Scholar
- Witherspoon DJ. Selective constraints on P-element evolution. Mol Biol Evol. 1999;16(4):472–8.View ArticlePubMedGoogle Scholar
- Silva JC, Kidwell MG. Evolution of P elements in natural populations of Drosophila Willistoni and D. Sturtevanti. Genetics. 2004;168(3):1323–35.View ArticlePubMedPubMed CentralGoogle Scholar
- Zilberman D, Henikoff S. Silencing of transposons in plant genomes: kick them when they're down. Genome Biol. 2004;5(12):249.View ArticlePubMedPubMed CentralGoogle Scholar
- Casola C, Lawing AM, Betran E, Feschotte C. PIF-like transposons are common in drosophila and have been repeatedly domesticated to generate new host genes. Mol Biol Evol. 2007;24(8):1872–88.View ArticlePubMedGoogle Scholar
- de Araujo PG, Rossi M, de Jesus EM, Saccaro NL Jr, Kajihara D, Massa R, de Felix JM, Drummond RD, Falco MC, Chabregas SM, et al. Transcriptionally active transposable elements in recent hybrid sugarcane. Plant J. 2005;44(5):707–17.View ArticlePubMedGoogle Scholar
- Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, SR MC, Wessler SR. An active DNA transposon family in rice. Nature. 2003;421(6919):163–7.View ArticlePubMedGoogle Scholar
- Lopes FR, Carazzolle MF, Pereira GA, Colombo CA, Carareto CM. Transposable elements in Coffea (Gentianales: Rubiacea) transcripts and their role in the origin of protein diversity in flowering plants. Mol Gen Genomics. 2008;279(4):385–401.View ArticleGoogle Scholar
- Ohtsu K, Smith MB, Emrich SJ, Borsuk LA, Zhou R, Chen T, Zhang X, Timmermans MC, Beck J, Buckner B, et al. Global gene expression analysis of the shoot apical meristem of maize (Zea Mays L.). Plant J. 2007;52(3):391–404.View ArticlePubMedPubMed CentralGoogle Scholar
- Vicient CM, Jaaskelainen MJ, Kalendar R, Schulman AH. Active retrotransposons are a common feature of grass genomes. Plant Physiol. 2001;125(3):1283–92.View ArticlePubMedPubMed CentralGoogle Scholar
- Walker EL, Eggleston WB, Demopulos D, Kermicle J, Dellaporta SL. Insertions of a novel class of transposable elements with a strong target site preference at the r locus of maize. Genetics. 1997;146(2):681–93.PubMedPubMed CentralGoogle Scholar
- Grzebelus D, Lasota S, Gambin T, Kucherov G, Gambin A. Diversity and structure of PIF/harbinger-like elements in the genome of Medicago Truncatula. BMC Genomics. 2007;8:409.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhang X, Wessler SR. Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis Thaliana and Brassica Oleracea. Proc Natl Acad Sci U S A. 2004;101(15):5589–94.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhong H, Zhou M, Xu C, Tang D-Q. Diversity and evolution of pong-like elements in Bambusoideae subfamily. Bio Syst Ecol. 2010;38(4):750–8.View ArticleGoogle Scholar
- Zhou M-B, Lu J-J, Zhong H, Liu X-M, Tang D-Q. Distribution and diversity of PIF-like transposable elements in the Bambusoideae subfamily. Plant Sci. 2010;179(3):257–66.View ArticleGoogle Scholar
- Ding Z, Gillespie LL, Mercer FC, Paterno GD. The SANT domain of human MI-ER1 interacts with Sp1 to interfere with GC box recognition and repress transcription from its own promoter. J Biol Chem. 2004;279(27):28009–16.View ArticlePubMedGoogle Scholar
- Mo X, Kowenz-Leutz E, Laumonnier Y, Xu H, Leutz A. Histone H3 tail positioning and acetylation by the c-Myb but not the v-Myb DNA-binding SANT domain. Genes Dev. 2005;19(20):2447–57.View ArticlePubMedPubMed CentralGoogle Scholar
- Sterner DE, Wang X, Bloom MH, Simon GM, Berger SL. The SANT domain of Ada2 is required for normal acetylation of histones by the yeast SAGA complex. J Biol Chem. 2002;277(10):8178–86.View ArticlePubMedGoogle Scholar
- Zhang X, Jiang N, Feschotte C, Wessler SR. PIF- and pong-like transposable elements: distribution, evolution and relationship with tourist-like miniature inverted-repeat transposable elements. Genetics. 2004;166(2):971–86.View ArticlePubMedPubMed CentralGoogle Scholar
- Rezsohazy R, Hallet B, Delcour J, Mahillon J. The IS4 family of insertion sequences: evidence for a conserved transposase motif. Mol Microbiol. 1993;9(6):1283–95.View ArticlePubMedGoogle Scholar
- Yuan YW, Wessler SR. The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proc Natl Acad Sci U S A. 2011;108(19):7884–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Markova DN, Mason-Gamer RJ. The role of vertical and horizontal transfer in the evolutionary dynamics of PIF-like transposable elements in Triticeae. PLoS One. 2015;10(9):e0137648.View ArticlePubMedPubMed CentralGoogle Scholar
- Markova DN, Mason-Gamer RJ. Diversity, abundance, and evolutionary dynamics of pong-like transposable elements in Triticeae. Mol Phylogenet Evol. 2015;93:318–30.View ArticlePubMedGoogle Scholar
- Kapitonov VV, Jurka J. Molecular paleontology of transposable elements in the Drosophila Melanogaster genome. Proc Natl Acad Sci U S A. 2003;100(11):6569–74.View ArticlePubMedPubMed CentralGoogle Scholar
- Doyle JJ. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem bull. 1987;19:11–5.Google Scholar
- Wagner A, Blackstone N, Cartwright P, Dick M, Misof B, Snow P, Wagner GP, Bartels J, Murtha M, Pendleton J. Surveys of gene families using polymerase chain reaction: PCR selection and PCR drift. Syst Biol. 1994;43:250–61.View ArticleGoogle Scholar
- Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22(22):4673–80.View ArticlePubMedPubMed CentralGoogle Scholar
- Swofford DL. Phylogenetic analysis using parsimony (*and other methods). Sunderland, Massachussets: Sinauer Associates; 2003.Google Scholar
- Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39(4):783–91.View ArticlePubMedGoogle Scholar
- Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25(7):1253–6.View ArticlePubMedGoogle Scholar
- Posada D. Selection of models of DNA evolution with jModelTest. Methods Mol Biol. 2009;537:93–112.View ArticlePubMedGoogle Scholar
- Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–8.View ArticlePubMedGoogle Scholar
- Posada D, Buckley TR. Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Syst Biol. 2004;53(5):793–808.View ArticlePubMedGoogle Scholar
- Zwickl DJ. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion: Ph.D. dissertation, University of Texas, Austin, Texas, USA. 2006.Google Scholar
- Farris JS. Estimating Phylogenetic trees from distance matrices. Am Nat. 1972;106(951):645–68.View ArticleGoogle Scholar
- Fedoroff N. Transposons and genome evolution in plants. Proc National Academy Sci. 2000;97(13):7002–7.View ArticleGoogle Scholar
- Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Carrington JC. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 2007;5(3):e57.View ArticlePubMedPubMed CentralGoogle Scholar
- Martienssen R, Lippman Z, May B, Ronemus M, Vaughn M. Transposons, tandem repeats, and the silencing of imprinted genes. Cold Spring Harb Symp Quant Biol. 2004;69:371–9.View ArticlePubMedGoogle Scholar
- Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA. Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol. 2008;6(12):2880–95.View ArticlePubMedGoogle Scholar
- Gaut BS. Evolutionary dynamics of grass genomes. New Phytol. 2002;154(1):15–28.View ArticleGoogle Scholar
- Jiao Y, Deng XW. A genome-wide transcriptional activity survey of rice transposable element-related genes. Genome Biol. 2007;8(2):R28.View ArticlePubMedPubMed CentralGoogle Scholar
- Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H, Inoue H, Tanisaka T. Mobilization of a transposon in the rice genome. Nature. 2003;421(6919):170–2.View ArticlePubMedGoogle Scholar
- Shan X, Liu Z, Dong Z, Wang Y, Chen Y, Lin X, Long L, Han F, Dong Y, Liu B. Mobilization of the active MITE transposons mPing and pong in rice by introgression from wild rice (Zizania Latifolia Griseb.). Mol Biol Evol. 2005;22(4):976–90.View ArticlePubMedGoogle Scholar
- Vicient CM. Transcriptional activity of transposable elements in maize. BMC Genomics. 2010;11:601.View ArticlePubMedPubMed CentralGoogle Scholar
- Escobar JS, Scornavacca C, Cenci A, Guilhaumon C, Santoni S, Douzery EJ, Ranwez V, Glemin S, David J. Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae). BMC Evol Biol. 2011;11:181.View ArticlePubMedPubMed CentralGoogle Scholar
- Mason-Gamer RJ, Orme NL, Anderson CM. Phylogenetic analysis of north American Elymus and the monogenomic Triticeae (Poaceae) using three chloroplast DNA data sets. Genome. 2002;45(6):991–1002.View ArticlePubMedGoogle Scholar