# On the coevolution of transposable elements and plant gnomes

Peter Civan, Pavol Hauptvogel

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## To cite this version:

Peter Civan, Pavol Hauptvogel. On the coevolution of transposable elements and plant gnomes. American Journal of Botany, 2011, 2011, pp.1-9. 10.1155/2011/893546. hal-02642867

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## Review Article

# On the Coevolution of Transposable Elements and Plant Genomes

Peter Civáň,<fnref n="1" /> Miroslav Švec,<fnref n="1" /> and Pavol Hauptvogel<fnref n="2" />

Correspondence should be addressed to Peter Civáň, civan@fns.uniba.sk

Received 1 June 2011; Revised 23 August 2011; Accepted 6 September 2011

Academic Editor: Curtis C. Daehler

Copyright © 2011 Peter Civáň et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Plant genomes are unique in an intriguing feature: the range of their size variation is unprecedented among living organisms. Although polyploidization contributes to this variability, transposable elements (TEs) seem to play the pivotal role. TEs, often considered intragenomic parasites, not only affect the genome size of the host, but also interact with other genes, disrupting and creating new functions and regulatory networks. Coevolution of plant genomes and TEs has led to tight regulation of TE activity, and growing evidence suggests their relationship became mutualistic. Although the expansions of TEs represent certain costs for the host genomes, they may also bring profits for populations, helping to overcome challenging environmental (biotic/abiotic stress) or genomic (hybridization and allopolyploidization) conditions. In this paper, we discuss the possibility that the possession of inducible TEs may provide a selective advantage for various plant populations.

## 1. Transpositional Strategies, Distribution, and Regulation of TEs

Transposable elements (TEs) comprise a palette of immensely diverse DNA structures that can be unified by the following definition: they all are (or have been) able to insert themselves (or new copies of themselves) into new locations within genome. According to their mechanism of transposition, TEs can be classified [1] into class I elements (retroelements) transposing through an RNA intermediate, and class II elements (DNA transposons) moving only via DNA. The major superfamilies of class I are *Ty1-copia* and *Ty3-gypsy* retrotransposons, while class II is represented by TIR (terminal inverted repeat) elements and *Helitrons*, which are sometimes classified separately [2]. Among both retrotransposons and transposons, nonautonomous forms (e.g., MITEs, SINEs, and LARDs) are quite prevalent [3], utilizing the transpositional machinery of autonomous TEs.

A significant portion of plant genomes is constituted by class I elements (specifically LTR retrotransposons, with direct long terminal repeats at both ends), which replicate in a "copy-and-paste" manner. In brief (according to [3, 4]), the genomic DNA copy of a retroelement is transcribed into mRNA that enters the cytosol, similarly to standard

DNA transcripts. The information of the mRNA is translated, typically creating a structural protein GAG and a polyprotein POL. These protein products associate with other retroelement mRNA copies and pack them into virus-like particles. Within these structures, dimerized mRNA copies are reversely transcribed into cDNA and the whole complex enters the nucleus, where the new cDNA copy integrates at a new site. This mode of transposition, if not suppressed, allows retroelements to massively increase their copy numbers, resulting in a rapid expansion of genome size.

Compared to retrotransposons, class II elements are anticipated to have a smaller potential of increasing their copy number. Owing to their "cut-and-paste" insertional mechanism mediated by transposases, multiplication arises only when a transposon from a recently replicated genomic region is transposed to a region about to undergo replication [5] or in cases when the excision site is repaired by gene conversion, using the sister chromatid as a template [4]. Nevertheless, short DNA transposons like MITEs (minia-ture inverted-repeat TEs) can be remarkably effective in increasing their copy numbers each generation [6, 7]. In the genome of *Lotus japonicus*, the copy number of detected MITEs is similar to, or higher than, the copy numbers of major LTR retrotransposon superfamilies [8], and the overall

<footnote n="1">¹Department of Genetics, Faculty of Natural Sciences, Comenius University, Mlynská dolina B1, 842 15 Bratislava 4, Slovakia</footnote>

<footnote n="2">²Plant Production Research Center, Gene Bank of Slovak Republik, Bratislavská cesta 122, 921 68 Piešťany, Slovakia</footnote>
contribution to the genome size is smaller only because of the
short length of MITEs (200–500 bp).

For most of the TEs in plant genomes, a certain balance
between TE proliferation and minimal damage to the host
has evolved. This balance is widely achieved by epigenetic
silencing, an important feature of which is its reversibility
[9]. Epigenetic suppression of TEs are realized on dif-
ferent levels—from general transcriptional control by TE-
unspecific histone modification and siRNA-directed DNA
methylation [10–12], to posttranslational processes, like the
species-specific control of nuclear localization of transposase
[13, 14]. Silencing of TEs can be immensely effective. For
example, LTR retrotransposons constitute a large part of
the *Gossypium* genome, but almost no transcripts were
found in the *Gossypium* EST database [15]. Interestingly, a
variety of LINE-like transcripts have been found in the same
EST libraries, suggesting different levels of suppression for
particular TE classes. But attenuation of TEs is not irre-
versible. Disruption of epigenetic silencing patterns and con-
sequent derepression and proliferation of TEs are thought
to be associated with two natural phenomena—interspecific
hybridization [16–18] and biotic/abiotic stress [19–23].

TEs are not evenly distributed along chromosomes. DNA
transposons are overrepresented in gene-rich or euchromatic
regions [7, 24], avoiding exons [7], while class I elements
concentrate in gene-poor, heterochromatic regions around
centromeres [24–28]. Exceptions to this general pattern are,
for example, *copia* retroelements of maize overrepresented
in euchromatin [29], or the FIDEL retrotransposon absent
from heterochromatin in *Arachis* [30]. Authors frequently
suppose the existence of yet unknown mechanisms of region-
specific TE targeting. However, the uneven distributions of
class I and class II elements across the genomes might be sat-
isfactorily explained by probabilistic principles (as follows),
without the need to hypothesize any targeting mechanism.

DNA transposons in heterochromatic regions may be less
likely to be transposed because of the DNA topology inac-
cessible for transposases. On the contrary, DNA transposons
in euchromatic or genic regions are being transposed fre-
quently, and owing to the transposition strategy, the excised
element is prone to reinsert at a nearby genomic location,
which is likely to be euchromatic too (the shorter the distance
between the original and novel position, the higher the
probability that the two loci are in the same condition). The
passive copies in the heterochromatin are eventually removed
from the genome while only the active copies have chances to
multiply, and thus colonize the euchromatin. Transpositions
into exons are mostly filtered out by natural selection, so the
majority of DNA transposons is observed in introns, or 5'
and 3' adjacent regions. The less severe consequences of short
TE insertions for splicing might be the reason why MITEs
predominate in introns over other elements.

The situation is different for LTR retrotransposons.
New copies of class I elements are generated outside the
nucleus—in the cytosol, thus the probability for a new
copy to reintegrate in the proximity of the maternal ele-
ment is extremely low. Without any targeting mechanism,
retroelements integrate randomly across the whole genome,
and the observed uneven distribution can be attributed to

the following factors: (i) the majority of transpositions
within or near genes is filtered out by selection because of
the usually deleterious effects; and (ii) LTR retrotransposons
(or TEs in general) are removed more efficiently from highly-
recombining regions because the mechanisms of removal
are recombination dependent [31–33]. This hypothesis is
supported by the finding that *Sorghum* LTR retrotransposons
younger than 10,000 years appear to be randomly distributed
along chromosomes [34]. Distribution patterns of TEs are
therefore likely to be a function of the transpositional strat-
egy and age of the individual TE family, affected by methyla-
tion [35] and some genomic particularities of the host species
(e.g., gene density and recombination landscapes).

## 2. Effects of Transposable Elements on Plant Genomes

2.1. *Genome Size.* The most obvious effect of TE existence in plants is their impact on the genome size. TE fraction can be as low as ~15% in small plant genomes, and as high as >70% in large plant genomes (Table 1) while the number of genes remains roughly constant [36] (of course, the latter does not hold true for polyploids). The correlation between the proportion of TEs—specifically LTR retrotransposons—and the physical length of the genome is so evident in the examined plant species [36, 37] that the genome size can be generally regarded as a linear function of TE content, and the dynamics of LTR retrotransposons as the major contributor to 1C-value differences among plants.

To answer the question what is the “typical” TE con-
tribution to the length of plant genome, one needs some
factual idea of a “typical” plant 1C-value. For this purpose,
Tenaillon et al. [37] use an arithmetic mean of the 1C-values
provided by Bennett and Leitch [38]. Their Plant DNA C-
value database currently comprises 6,287 and 204 entries for
angiosperms and gymnosperms, respectively; mostly based
on Feulgen microdensitometry and flow cytometry data.
Although this dataset probably cannot be considered a repre-
sentative sample of all land plants (e.g., monocots being over-
represented), as the most comprehensive one it still provides
informative insights into plant genome size variation. The
average genome size (1C) of angiosperms (flowering plants)
and gymnosperms sampled in this database is 5.809 Gbp
and 18.157 Gbp, respectively. However, the distribution of
1C-values, especially in angiosperms, shows strong positive
skewness (Figure 1), with the data unevenly distributed
around the mean (72.3% of the examined angiosperm
species having smaller genomes than the mean value of
the dataset). For such distributions, the median is a better
indication of central tendency than the arithmetic mean.
The median values of the angiosperm and gymnosperm
genome size data sampled in the Plant DNA C-value
database are 2.401 Gbp (1.416 Gbp for eudicots; 5.746 Gbp
for monocots) and 17.506 Gbp, respectively. In other words,
half of the examined flowering plants has genome sizes
below 2.4 Gbp. Surprisingly, the interval 0.4–0.6 Gbp rep-
resents here the modal category for angiosperm 1C-values,
comprising 8.38% of examined species (Figure 1(b)). Hence,
*Oryza sativa*, *Lotus japonicus*, *Medicago truncaluta*, *Vitis*
<table><caption>TABLE 1: Known TE proportions in plant genomes when various authors provide different values, the range is given. Inconsistent estimates of TE content result from incomplete genomic representation and/or varying bioinformatical approaches. Examination of complete genomes and application of the same TE discovery pipeline is therefore essential for comparative analyses on intra- and interspecies level. No data on TE content is available for gymnosperms, and angiosperms with large genomes (>2.4 Gbp) are underrepresented. In most genomes, *Helitrons* were not surveyed appropriately.</caption><thead><tr><th>Species</th><th>Predominant fertilization</th><th>Genome size (Gbp)</th><th>TE content (%)</th><th>DNA transposon content (%)</th><th>Retrotransposon content (%)</th><th>Genomic fraction examined</th><th>References</th></tr></thead><tbody><tr><td>Arabidopsis thaliana</td><td>S</td><td>0.125</td><td>6–15.36</td><td>2–3</td><td>4</td><td>Complete/draft genome</td><td>[12, 25, 32]</td></tr><tr><td>Arabidopsis lyrata</td><td>C</td><td>0.207</td><td>23.48</td><td>ns</td><td>ns</td><td>Complete/draft genome</td><td>[12, 73]</td></tr><tr><td>Brachypodium distachyon</td><td>S</td><td>0.272</td><td>26.17</td><td>4.77</td><td>21.4</td><td>Complete/draft genome</td><td>[74]</td></tr><tr><td>Carica papaya</td><td>C</td><td>0.372</td><td>51.9</td><td>ns</td><td>ns</td><td>Complete/draft genome</td><td>[75]</td></tr><tr><td>Cucumis melo</td><td>C</td><td>0.454</td><td>8.13</td><td>0.93</td><td>7.2</td><td>BAC clones (6.7 Mbp)</td><td>[76]</td></tr><tr><td>Oryza sativa</td><td>S</td><td>0.472</td><td>35</td><td>ns</td><td>17</td><td>Complete chr. 10; complete/draft genome</td><td>[24, 39]</td></tr><tr><td>Lotus japonicus</td><td>S</td><td>0.472</td><td>30.8</td><td>0.97–8.1</td><td>10.4–19.23</td><td>TAC clones (32.4 Mbp); 2/3 genome</td><td>[8, 77]</td></tr><tr><td>Medicago truncaluta</td><td>S</td><td>0.475</td><td>38</td><td>ns</td><td>9.6*</td><td>BAC clones (0.233 Mbp)</td><td>[40, 78]</td></tr><tr><td>Populus trichocarpa</td><td>C</td><td>0.485</td><td>42</td><td>2.5**</td><td>10.3**</td><td>Complete/draft genome</td><td>[79]</td></tr><tr><td>Vitis vinifera</td><td>S</td><td>0.487–0.505</td><td>21.5–41.4</td><td>1.98</td><td>20</td><td>Complete/draft genome</td><td>[41, 80, 81]</td></tr><tr><td>Brassica oleracea</td><td>C</td><td>0.6</td><td>20</td><td>6</td><td>14</td><td>Complete/draft genome</td><td>[32]</td></tr><tr><td>Sorghum bicolor</td><td>S</td><td>0.73</td><td>62.5–59</td><td>7.5/17</td><td>55/42</td><td>Complete/draft genome</td><td>[34, 82]</td></tr><tr><td>Glycine max</td><td>S</td><td>1.1</td><td>58</td><td>16</td><td>42</td><td>Complete/draft genome (3.42 Mbp)</td><td>[38, 83]</td></tr><tr><td>Gossypium herbaceum</td><td>S</td><td>1.667</td><td>52.1</td><td>&lt;0.1</td><td>52</td><td>Small insert genomic library (3.42 Mbp)</td><td>[84]</td></tr><tr><td>Zea mays</td><td>C</td><td>2.3</td><td>85</td><td>8.6</td><td>75</td><td>Complete/draft genome</td><td>[29]</td></tr><tr><td>Aegilops tauschii</td><td>S</td><td>4.988</td><td>68.2</td><td>13.3</td><td>53.5</td><td>Small insert genomic library (2.911 Mbp)</td><td>[38, 85]</td></tr><tr><td>Hordeum vulgare</td><td>S</td><td>5.7</td><td>88.1</td><td>ns</td><td>ns</td><td>BAC clones (0.44 Mbp)</td><td>[86]</td></tr><tr><td>Secale cereale</td><td>C</td><td>8.093</td><td>69.3</td><td>5</td><td>64.3</td><td>BAC clones (2.033 Mbp)</td><td>[38, 87]</td></tr></tbody></table>

S—self-pollination; C—cross-pollination; ns—not specified; * only full-length LTR retrotransposons analysed; ** only TEs with homology to known repeat elements considered.

vinifera, Brasica oleracea, and Populus trichocarpa have “typical” genome lengths (Table 1), therefore it can be implied that transposable elements typically constitute one-third of angiosperm genomes.

Genome size changes are not unidirectional. TE fragments and solo LTRs have been found to constitute a significant fraction of repetitive elements (e.g., [39–43]), and

are believed to be remnants of removed TEs [31]. There is evidence that transpositional bursts can be followed by DNA loss [44], and it has been reported that the removal of LTR retrotransposons can proceed with different efficiency in distinct species [33, 40, 42]. However, it should be noted that the estimations of a retroelements’ half-life assume constant removal rates for repetitive sequences, and rely on the
<figure><img src="image_3.png" /></figure>

FIGURE 1: Frequency distribution for *spermatophyta* 1C-values. The dataset consists of all angiosperm (6,287) and gymnosperm (204) entries in the Plant DNA C-value database [38] (retrieved 27/05/2011). (a) Comparison of angiosperm and gymnosperm 1C-value frequency distribution. Genomes of *spermatophyta* were split into categories with 1 Gbp intervals (X-axis); the proportion (percent) of each category (vertical axis) is shown separately for the two groups. Interestingly, angiosperms (mean = 5.809 Gbp, $s_x$ = 9.5287, median = 2.401 Gbp) and gymnosperms (mean = 18.157 Gbp, $s_x$ = 7.4496, median = 17.506 Gbp) do not display similar distributions. Despite the extreme range of 1C-values, 95% of flowering plants fall within 0–22 Gbp. The range of gymnosperm 1C-values is smaller; however, the overall genome size is higher, with 95% of species falling within 7–33 Gbp. (b) Higher resolution of angiosperm 1C frequency distribution. X-axis shows genome size categories with 0.2 Gbp increments and the vertical axis indicates the proportion of each category (percent). Mean and median values are indicated by the red and green line, respectively. The mean of the first half of the histogram (left to the median) is 1.049 Gbp; the mean of the second half is 10x larger (not indicated). Hence, the average “small” (<2.4 Gbp) and “large” (>2.4 Gbp) angiosperm genomes are ~1 Gbp and ~10 Gbp long, respectively. Modal interval (0.4–0.6 Gbp) includes 8.38% of flowering plants.

molecular clock principle; therefore, the revealed interspecies
differences in TE survival should be interpreted cautiously.

Disregarding the mutational effects of TEs at this point,
a dramatic increase of noncoding or repetitive fraction in
the genome theoretically raises the nutritional and time
requirements for DNA replication and maintenance in each
cell (leading to putative costs formulated as the “large
genome constraint hypothesis,” [45]). The higher nutritional
and time demands may lead to decreased fecundity and pro-
longed generation time, the two main constituents affecting
selective advantage [46]. While such changes are apparently
disfavouring in populations of unicellular organisms, the
growing genome size does not seem to impose an evident and
unambiguous selective disadvantage in *spermatophyta* (seed
plants) [45, 47].

Offering one intriguing example: phosphorus (P) is
known to be the limiting nutrient in most soils (reviewed
in [48]). As it is one of the basic components of nucleic
acids, plants with significantly larger genomes have higher
P demands for DNA synthesis, leaving lesser amounts for
other essential cell processes (e.g., ATP or phospholipid
dependent). Therefore, it seems natural to anticipate that
plants with large C-values should lose the ecological
competition against the plants whose genomes are several-
fold smaller. Despite that, genome sizes in examined land
plants range 2056-fold [49], with *Genlisea margaretae* (1C =
63.4 Mbp = 0.0648 pg) [50] and *Trillium hagae* (1C =
132.5 pg) [51] on the opposite poles. Relatively large, almost
22-fold differences in 1C-values have also been reported for
members of a single genus (*Eleocharis*) at the same ploidy
level [52].

If we reject the unlikely possibility that such enormous
genome size variation in plants is attributable to stochastic
processes only, the question arises as to why some plants
maintain relatively small genomes (Figure 1) while others
sink into genomic obesity [53]. In theory, there are two
possible causes that may allow transposable elements, and
thus genomes to expand extensively: (i) deficiency in the
mechanisms of suppression and/or removal of TEs from the
genome and (ii) selective advantage that favours individuals
and/or populations with high TE activity.

In relation to the former possibility (i), Weil and
Martienssen [9] compare the interaction of TEs and host
genomes to resistance to pathogens, and hypothesize that
as transposons evolve ways around host silencing, host
organisms evolve new genes for silencing, perhaps through
duplication and subfunctionalization. This idea is supported
by the discovery of positive selection acting on some LTR
retrotransposons in the rice genome [54]. On rare occasions,
mutant variants of retroelements can escape host recognition
and rapidly amplify, leading to what is commonly observed
as bursts of amplification. Consequently, the detected vari-
ability in TE activity in time and taxa can be attributed to
different phases of the “host-parasite” interaction. The occa-
sional escape of TEs from the host suppression via random
mutations and positive selection seems plausible; however,
such events should exhibit roughly the same periodicity in all
genomes, assuming similar substitutional rates of repetitive
DNA among species. Therefore, this “red queen race” in itself
can hardly explain the enormous differences in plant genome
sizes. Moreover, the host-pathogen analogy also implies
that the species with below-average performance in TE
suppression are evolutionary disadvantaged to those species who have successfully prevented transpositional bursts of parasitic retroelements. Comparing the plant species with small and large genomes, we lack any direct evidence for such generalization.

The above-mentioned conflicts direct the attention to the latter alternative (ii), which suggests plant genome size variation to be caused by a differential selective advantage of TE possession acting in distinct species or populations (i.e., the presence and activity of transposable elements might be beneficial in some species/populations while detrimental in others). Testability of this hypothesis depends on identifying the nature of such advantage; therefore, other effects of TEs on plant genomes need to be carefully considered (see below).

2.2. *Mutability.* The discovery of transposable elements was accompanied by the observation of their mutability [55], which unlike the growing genome size, can often have a phenotypic manifestation. Transpositions into the coding regions of genes are usually deleterious; however, those transpositional events that passed through the sieve of selection can induce a variety of genetic changes, including interrupting host genes, creating different expression forms, changing intron length, and affecting expression levels of adjacent genes [56]. Downregulation of genes may be caused not only by TE insertions disrupting the promoters, but more likely by siRNA-guided DNA methylation, which is primarily directed to suppress the TE activity but affects the expression of nearby genes too [35]. Whole-genome differences in TE-siRNA interactions have such dramatic effects on expressional patterns that they may contribute to speciation [12]. Among recently reported TE-induced mutations are cluster-shaped somatic variation in grapevine caused by the insertion of *Hatvine1-rrm* DNA transposon in the *VvTFL1A* gene promoter [57]; flower color gene mutation caused by *TgmExpress1* transposition into the intron 2 of *F3H* gene in soybean [58]; or transposon-induced DNA methylation of *CmWIP1* promoter leading to sex determination in melon [59].

Comprehensive and genome-wide analyses of TE muta-
bility have been accomplished on the fully sequenced genome
of rice. According to [39], while LTR retrotransposons
constitute ~17% of the rice genome, 22% of these sequences
lie within putative or established rice genes. Within the genic
regions, fragmented elements have been predominantly
identified, and full-length elements are rare [39]. Available
genomic sequences of the two rice subspecies—*japonica*
and *indica*—provide a powerful resource for comparative
and functional genomic analyses, which has been utilized
by Huang et al. [56] to study transposon insertion poly-
morphisms (TIPs). Interestingly, more than 10% of TIPs
between Nipponbare and 93-11 rice cultivars were located
in expressed gene regions. Roughly half of those TIPs
occurred in introns, often resulting in alternative splicing,
and more than a third were found in [-1, -250] regions,
relative to the transcription start site. Effects of TE insertions
within the promoters are particularly impressive in the case
of two genes, causing 18-fold upregulation and 23-fold

downregulation of gene expression [56]. In another study
[7], high-throughput sequencing was utilized to determine
1,664 insertion sites of *mPing* transposon in a population of
24 rice plants. Subsequent comparative microarray analysis
concluded that the vast majority of TE insertions either have
no impact, or preferentially enhance transcription under
normal conditions. However, seven out of ten loci, unaffected
by *mPing* insertion under normal conditions, were inducible
by salt and cold stress. Scanning *mPing* sequences for cis-
acting plant regulatory elements resulted in identification
of 96 putative regulatory motifs, one-third of which were
stress responsive. These experiments demonstrate that the
*mPing* transposon, resembling a mobile gene enhancer,
provides new binding sites for transcription factors or other
regulatory proteins, and may actually benefit the host by
creating potentially useful allelic variants and novel, stress-
inducible regulatory networks [7].

Among the most intriguing features of transposable
elements is the ability of certain classes to capture gene
fragments. The potential to contribute to gene evolution by
combining genes, exons, and introns into novel functional
units is most apparent in *Helitrons*. Although these elements
were initially challenging to identify due to the absence of
typical TE structural features [60, 61], an effective structure-
based program has been developed recently, leading to the
detection of thousands *Helitrons* in several plant genomes
[61]. The frequency of the gene capture is particularly
striking in the genome of maize [62, 63]. For example,
Morgante et al. [62] randomly selected nine genic insertions
polymorphic in maize inbred lines and demonstrated that
eight of them are nonautonomous *Helitrons*, each containing
between one and seven different fragments of host genes.
Yang and Bennetzen [63] have shown on a genome-wide
scale that 60% of maize *Helitrons* contains captured frag-
ments of nuclear genes, 4% of which are under purifying
selection, and another 4% exhibiting apparent adaptive
selection, which suggests beneficial effects for the host or
*Helitron* transposition/retention. Although the vast majority
of the genes captured by *Helitrons* are incomplete, defective
copies of conserved functional genes (including exons and
also introns), a fraction of those gene fragments may serve as
the template for interfering RNAs or new gene functions via
exon shuffling, expanding the repertoire of mutable changes
provided by TEs.

The last significant mutable effect of TEs to be mentioned
is the macrotransposition, that is, a transposition involving
two physically close, interacting elements, and an inter-
vening chromosomal segment. Such transposon pairs may
produce other complex rearrangements, including deletions,
inversions, and reshuffling of the intertransposon segment
[64], thus macrotransposition can be another contributor to
genome divergence and speciation.

**3. From Individuals to Populations:**
*From Junk to Treasure*

In the study of coevolution of TEs and plant genomes,
two different populations affected by inconsistent selection
forces should be recognized—the population of transposable
elements within the genomic niche of an individual, and the
population of diverse individuals within an ecological niche.
In this section, the term population refers to the latter one.

Since the early work of Barbara McClintock, the presence
and action of transposable elements in the host genomes has
been studied from the perspective of an individual. Because
the mutational consequences of TE activity on genes and
their expression patterns (see above) are undirected by the
host and principally random, it has become apparent that
the uncontrolled TE transposition or expansion is, in the
vast majority of cases neutral, detrimental, or lethal for an
individual. The absence of evident benefits of the possession
of transposable elements for an individual led to TEs being
regarded as an archetype of selfish or parasitic DNA, whose
only functional aim is to reproduce itself, regardless of
the effect on the host genome. The large genomic regions
occupied by ancient, suppressed, or still active transposable
elements have acquired a label “junk DNA”—an unnecessary
burden for cell and organism.

The individual-based viewpoint in the TE research was
needed, because a fundamental description of TE diversity,
prevalence, and *modus operandi* was required, and also
understandable, because the technical possibilities to study
TE dynamics on the population level were unavailable until
recently. However, evolution acts on populations, not on
individuals. Some recent studies have drawn the attention
to population processes related to TEs [37, 65–67], and it
is becoming clearer that to answer the questions about the
origin, evolution, function, and importance of transposable
elements in plant genomes, it is necessary to move the
research focus from individuals to populations.

Environmental stresses are known initiators of TE activ-
ity [20–23, 68], and diverse effects of transpositional events
on the expression of adjacent genes have been reported [7, 35,
56, 57, 59, 68]. Although the mutational impact of TE bursts
is likely to be detrimental for an individual, TE activity cre-
ates new variability in the population, providing raw material
for selection forces. An illustrative example of how effective
the TEs can be in generating genetic diversity is provided
by the activity of the *mPing* DNA transposon in some rice
strains. With roughly 40 new transpositions of *mPing* per
plant per generation, even small populations contain thou-
sands of new insertions, a large portion of which upregulates
genes in their vicinity under stress conditions [6, 7].

Hence, TE activity may actually help the population
to overcome changing environmental conditions and adapt
to new ecological settings. Under diversifying selection,
this ability of quick adaptations is likely to outbalance
the costs of decreased fitness of some individuals, or the
possible large genome constraint. From this perspective, the
escape of TEs from the silenced state resembles more a
regulated response to cope with stress on population level
rather than an undesired side effect of stress exposure,
an idea initially hypothesized by McClintock [55] as the
“response to genomic shock.” Possession of a mechanism
that can boost the evolutionary changes and be switched on
and off depending on the situation might be the decisive
factor for the survival or extinction of a population in
changing environments. It is suggestive to hypothesize that

transposable elements might represent such a tool and were
actually “invented,” or at least modified by eukaryotes to fulfil
this function. And if plants possess and use an autonomous
mechanism to control TE proliferation, it means they also
have a basic control over their own genome size.

The hypothesis of transposable elements as intrinsic
tools for increasing genetic variability has some testable
implications (i)–(iii). For example, (i) TE-driven stimulation
of variability could be especially beneficial for species, pop-
ulations, or genomic regions exposed to strong diversifying
selection (e.g., host-pathogen systems). Such entities would
be therefore expected to possess more transposable elements
and their TE dynamics to be more responsive to stress
conditions. Interestingly, Nielen et al. [30] have found LTR
retrotransposon FIDEL associated with conserved *Arachis*
genes less frequently than what was expected by chance, but
its presence close to fast-evolving NBS genes (resistance gene
analogues) was in agreement with random distribution.

(ii) Asexually reproducing organisms and self-pollinating
plants, which lack the opportunity to recombine their genetic
material, might profit from the enhanced diversity sustained
by the TEs, as suggested for rice by Naito et al. [7].
However, the outcrosser *Arabidopsis lyrata* shows 2-3 times
higher TE content than the selfer *A. thaliana* (Table 1). The
relationship between the mating system and TE dynamics
for these two relatives has been studied [68, 69], and among
the possible causes are differences in effective population
size and related stochastic processes, or more deleterious
consequences of the accumulation of recessive mutations in
self-pollinating plants. Self-pollinators might also be more
efficient in suppressing TEs owing to more rapid fixation of
epigenetic silencing patterns.

On the other hand, Bestor [70] assumes that the
aggressiveness of transposons in self-fertilizing sexuals is
self-limited comparing to outcrossing sexuals, where the
transposon fixation is nearly certain provided that the
coefficient of selection imposed by the transposon is less
than 0.5 when there is one or more transposition events per
generation. It implies that self-pollinators are not expected
to have higher transposon content than related outcrossers,
unless the TEs provide some net benefits to the host.
While *Triticeae* seems to be an interesting tribe for such
comparisons (Table 1), more comprehensive data on the TE
content is required.

(iii) Taxa adapted to environmentally stable niches, such
as ocean depths or high altitudes, would be expected to
contain significantly less TEs comparing to the organisms
from more unstable environments, which supposedly over-
came multiple bursts of TE activity. An excellent opportunity
to study these expectations is provided by three diploid
sunflower species. *Helianthus anomalus*, *H. deserticola*, and
*H. paradoxus* are independently derived via hybridization
events between the same two parental taxa, *H. annuus* and
*H. petiolaris*. The three hybrid taxa encountered a rapid,
retrotransposon-mediated genome expansion [71, 72], and
all of them occupy habitats considered abiotically extreme
relative to either parental species. *H. anomalus* and *H.
deserticola* inhabit arid desert-like environments whereas
*H. paradoxus* occurs exclusively in saline environments.
Interestingly, the scale of copy number increase for *copia* LTR retrotransposons differs considerably among the three sunflower hybrid species, with a 3.7-fold increase in copy number in the genome of *H. paradoxus* (relative to the average parental species value) versus a lower 1.7-fold and 2.2-fold increase for *H. anomalus* and *H. deserticola*, respectively [72]. The copy number increase of *gypsy* LTR retrotransposons is even more stunning, with 5.6- to 23.6-fold multiplication in the hybrid taxa, compared to parental populations (which did not differ significantly) [71]. Ungerer et al. [71] suggest that hybridization, abiotic stress, or both may have been involved in this extensive retrotransposon proliferation. In either case, it is tempting to hypothesize that this is an example of TE proliferation being “switched on” by the host regulatory mechanisms (possibly coevolving with the TEs) as an action to elicit mutational consequences potentially helpful in adapting to new environments.

## 4. Conclusion

Genome-wide and population-based examinations of similar projections have the potential to illuminate the role of transposable elements in speciation, adaptation, and in the evolution of plant genomes, in general. Besides, a detailed knowledge of TE activity regulation is required to understand the coevolution of TEs and plant genomes, and the extent of consequential benefits utilizable by plants. During the past decades, the notion of TEs has varied from autotelic junk to valued tool of evolutional response. In the light of new evidence, the terms like “junk” or “selfish” DNA, and even “host genome” and “defence mechanisms for TE suppression” are becoming more misleading than ever. At present, comparative and functional genomic studies targeted on TE population dynamics and TE-cell interactions, supported by high-throughput technologies, are on the way to finalize this paradigm shift.

## Acknowledgments

The authors would like to thank two anonymous reviewers for helpful suggestions and constructive critique. This paper was supported by the Slovak Research and Development Agency under the Contracts no. APVV-0770-07 and no. APVV-0661-10.

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