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INVITED REVIEWS AND META-ANALYSES

The impact of transposable elements in environmentaladaptation

ELENA CASACUBERTA and JOSEFA GONZ �ALEZ

Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig Maritim de la Barceloneta 37-49, Barcelona 08003,

Spain

Abstract

Transposable elements (TEs) play an important role in the responsive capacity of their

hosts in the face of environmental challenges. The variety of mechanisms by which

TEs influence the capacity of adaptation of the host is as large as the variety of TEs

and host genomes. For example, TEs might directly affect the function of individual

genes, provide a mechanism for rapidly acquiring new genetic material and dissemi-

nate regulatory elements that can lead to the creation of stress-inducible regulatory

networks. In this review, we summarize recent examples that are part of an increasing

body of evidence suggesting a significant role of TEs in the host response to an ever-

changing environment, both in prokaryote and in eukaryote organisms. We argue that

in the near future, the increasing availability of genome sequences and the develop-

ment of new tools to discover and analyse TE insertions will further show the relevant

role of TEs in environmental adaptation.

Keywords: bursts of transposition, environmental adaptation, gene expression, horizontal

transfer, transposable elements

Received 21 November 2011; revision received 1 November 2012; accepted 2 November 2012

Introduction

Organisms are continuously challenged by their chang-

ing environments. Variation in climatic factors such as

temperature and humidity, interactions with other

organisms, resource availability, and presence of toxins

or other chemicals, among other biotic and abiotic fac-

tors, are likely to produce new selective pressures on

populations that can challenge their survival. Organ-

isms can respond to these changing environmental con-

ditions by shifting their geographical distribution,

through phenotypic plasticity or undergoing adaptive

evolution to the new local conditions (Chevin et al.

2010; Hoffmann & Sgr�o 2011). Of these three mecha-

nisms, adaptative evolution is argued to play the most

important role in determining the fate of species chal-

lenged by changing environmental conditions (Visser

2008).

Adaptive evolution occurs by natural selection when

individuals better able to survive and reproduce

pass on more genes to the next generation. As a

consequence, the genetic variants that confer a fitness

advantage increase in frequency in the population.

Mutation is the ultimate source of genetic variation and

different types of mutations, such as point mutations or

whole genome duplications, play a major role in adap-

tation. Transposable elements (TEs; see Box 1) are also

likely to play a relevant role in adaptation because of

their ability to generate mutations of great variety and

magnitude, and their capacity to be responsive and sus-

ceptible to environmental changes (Biemont & Vieira

2006; Schmidt & Anderson 2006; Oliver & Greene 2009;

Hua Van et al. 2011).Correspondence: Josefa Gonz�alez, Fax: +34 93 2211011;

E-mail: [email protected]

© 2013 Blackwell Publishing Ltd

Molecular Ecology (2013) 22, 1503–1517 doi: 10.1111/mec.12170

Box 1

Types of eukaryotic transposable elements

Transposable Elements (TEs) are DNA sequences that have the ability to move around in the genome by generat-

ing new copies of themselves. TEs are abundant, ancient, and active components of genomes. They are classified in

class I and class II elements according to the presence or absence of an RNA transposition intermediate. Within

each class, TEs are further subdivide in orders, based on their insertion mechanism, structure, and encoded pro-

teins; in superfamilies, based on their replication strategy; and in families, based on sequence conservation (Wicker

et al. 2007; Kapitonov & Jurka 2008).

Class II

Class I

Class II

SINEs (Alu)

AAAAA

Class I

MavericksIntegrase ATPase Protease Polymerase

DNA transposonTransposase

MITEs

HelitronsReplicase helicase

LTR retrotransposonGAG POL

Dark blue arrows represent direct or inverted repeats, blue boxes represent coding sequences and white boxes represent non-coding sequences.

Non-LTR retrotransposon

AAAAA

TEs can also be classified according to their self-sufficiency. TEs that are capable of producing the proteins neces-

sary for their transposition are classified as autonomous elements, while TEs that depend on other TEs to trans-

pose, such as SINEs and MITEs, are classified as nonautonomous elements. Nonautonomous elements are often

deletion derivates of autonomous elements although sometimes they have only limited sequence similarity to their

autonomous counterparts.

Transposable element-induced mutations range from

subtle regulatory mutations to gross genomic rear-

rangements often having complex phenotypic effects.

Box 2 includes a detailed description of the different

types of mutations generated by TEs, actively by de

novo insertion and retrotranposition, and passively by

Class I elements (retrotransposons) replicate using a RNA intermediate and areverse transcriptase. Each complete replication cycle produces new TE copies.As a consequence, retrotransposons are often the major contributors to therepetitive fraction in large genomes. Types of Class I elements include longterminal repeat (LTR) elements and non-LTR elements, such as LongInterspersed Nuclear Elements (LINEs) and Short Interspersed Nuclear Elements(SINEs). LTR elements have partly overlapping open reading frames (ORFs),GAG and POL closely related to retroviral proteins, flanked in both ends byLTRs with promoter capability. LINE elements consist of a 50 UntranslatedRegion (UTR) with promoter activity, two ORFs and a 30 UTR with a poly-A tail,a tandem repeat or merely an A-rich region. SINEs are nonautonomous elements,they rely on LINEs for transposition, that originate from accidental retrotrans-position of various polymerase III (Pol III) transcripts. Unlike retro-pseudogenes,SINEs possess an internal Pol III promoter allowing them to be expressed. Alus,the most common SINE in the human genome, consist of two CG-rich fragments,the left and right Alu, connected by an A-rich linker and ended in a poly-A tail.Class II elements do not require a reverse-transcription step to integrate into thegenome. DNA transposons encode a transposase that recognizes the terminalinverted repeats (TIRs) excises the TE out and then integrates the TE into a newsite in the genome. The gap that is left at the position where the TE was originallyinserted can be filled with a copy of the transposon by gap repair mechanisms.Alternatively, DNA transposons can increase in number by transposing duringchromosome replication from a position that has already been replicated toanother that has not been replicated yet. Miniature Inverted Repeats (MITEs)have no ORFs and also have TIRs. Two newly identified DNA transposons,Helitrons and Mavericks duplicate differently. Helitrons used a rolling-circlemechanism and do not have TIRs, while Mavericks, also known as polytons,probably replicate using a self-encoded DNA polymerase and have TIRs.Helitrons often carry gene fragments that have been captured from the hostgenome.


1504 E. CASACUBERTA and J . GONZ �ALEZ

acting as substrates for ectopic recombination. As well

as being vertically transferred, from parent to off-

spring, TEs can also be horizontally transferred, from

one species to another, potentially causing the multi-

tude of effects summarized in Box 2 in the new host

species. Additionally, TEs can also act as vectors facili-

tating the horizontal transfer of new genetic content

(Ochman et al. 2000; Frost et al. 2005). Whether they

do or do not transfer genes, horizontal transfer of TEs

is a source of raw genomic variation, and at times of

biological innovation, that influences the ability of the

organism to adapt to changes in its environment, and

to colonize new ecological niches (Schaack et al. 2010).

Box 2TEs generate a great variety of mutations

TEs can have a myriad of effects when they insert into new locations (Feschotte 2008; Goodier & Kazazian 2008;

Gogvadze & Buzdin 2009). These effects vary depending on where exactly the TE inserts and on the sequence of

the TE itself. When a TE inserts into the 5′ region of a gene, it can add new regulatory regions leading for example

to gene overexpression (a) or can disrupt existing regulatory regions and inactivate the gene in a particular tissue

or developmental stage (b). When a TE jumps into an exon it can disrupt the gene for example by altering the

reading frame, or by introducing a stop codon (c). A TE that inserts in the 3′UTR of a gene can disrupt the regula-

tory sequences in that UTR and/or it can add new ones, for example it can add miRNA-binding sites (d). A TE

can disrupt the 5′UTR of a gene leading to, for example, gene inactivation (e). When a TE inserts into an intron it

can: (f) be incorporated as a new exon, (g) introduce a STOP codon leading to a truncated transcript, (h) introduce

new splice sites creating new alternative spliced variants, (i) drive antisense transcription that could interfere with

the sense transcript of the same gene, (j) spread epigenetic silencing leading to gene inactivation.

(j) Gene silencing

(h) Alternative splicing

(g) Premature end

(i) Anti-sense transcription

(f) Exonization

Gene silencing

Cis disruption

5’ UTR disruption

Gene disruption

miRNA targeting

Alternative splicing

Premature end

Anti-sense transcription

Cis addition Exonization

gene structure mRNA

Pentagons represent cis-regulatory regions, grey boxes are UTRs, red boxes represent exons and blue boxes represent TEs.

(a) (f)

(g)

(h)

(i)

(j)

(b)

(c)

(d)

(e)

TEs are also involved in the duplication of genes and exons that may contribute to the generation of new genes

(Marques et al. 2005; Xing et al. 2006). TE-encoded genes can be exapted to perform cellular functions (Volff 2006).

Finally, TEs are also passive generators of mutations. TEs that belong to the same family of elements and are

located in different regions of the genome can act as substrates for ectopic recombination events generating rear-

rangements such as inversions, translocations or duplications (Schwartz et al. 1998; Hill et al. 2000; Bailey et al.

2003).


TEs IN ENVIRONMENTAL ADAPTATION 1505

TEs are also responsive and susceptible to environ-

mental changes. Stress-activated TEs might generate the

raw diversity that species require over evolutionary time

to survive stressful situations. The first person to present

this idea was Barbara McClintock through her extensive

work in the maize transposons Ac and Ds (McClintock

1984). This idea seemed overly optimistic for other

researchers that thought that activation of TEs is due to

the disruption of the host mechanisms that suppress

transposition in normal conditions. One of the clearest

cases of TE activation due to the breaking down of

repression mechanisms is hybrid dysgenesis in

Drosophila. Hybrid dysgenesis is a sterility syndrome

caused by very high rates of transposition of normally

inactive TE families (Bingham et al. 1982; Bucheton et al.

1984; Petrov et al. 1995). Activation of TEs could be the

consequence of the relaxation of epigenetic control

induced by environmental changes (Slotkin &

Martienssen 2007; Zeh et al. 2009; Rebollo et al. 2010).

However, the many examples providing solid grounds

for the activation of specific TEs in response to some

specific stress conditions indicates that the link between

TE activation and stress response is by far more complex

than the simple release of regulation (Wessler 1996;

Grandbastien et al. 1997; Capy et al. 2000; Schmidt &

Anderson 2006; Fablet & Vieira 2011).

In this review, we investigate the evidence for the role

of TEs in environmental adaptation. Because the litera-

ture on this topic is extensive, we do not attempt to

review every known case of environment-related

TE-induced adaptation, but rather focus on the most

recent examples from diverse organisms that illustrate

the variety of molecular mechanisms and phenotypic

effects of TE-induced mutations. We start with site-spe-

cific insertions of TEs that result in adaptation to the

environment. We then focus on the most recent evidence

for environmental adaptation mediated by horizontal

transfer of TEs. Finally, we review cases in which TEs are

activated by, or in response to, environmental stresses.

TE-induced mutations involved inenvironmental adaptation

TE-induced mutations have been frequently associated

with adaptation to the environment. Below, we briefly

describe some of the most compelling examples of indi-

vidual TE-induced environmental adaptations docu-

mented recently. These examples highlight the variety

of molecular mechanisms and adaptive phenotypic

effects of TEs, from bacteria to mammals.

Bacteria insertion sequences (IS) have long been associ-

ated with environmental adaptation. In early studies, it

was unclear whether the IS element was the causal muta-

tion responsible for the adaptive phenotypic change (e.g.

Naas & Nordmann 1994; Schneider et al. 2000; de Visser

et al. 2004). In recent years, however, a cause–effect rela-

tionship has been established between IS elements and

adaptation to several environmental challenges such as

adaptation to high osmolarity (Stoebel et al. 2009; Stoebel

& Dorman 2010), tolerance to toxic organic solvents (Sun

et al. 2009), metal-limited conditions (Chou et al. 2009)

and nutrient-limited conditions (Gaff�e et al. 2011). The

molecular mechanisms underlying these IS-induced

adaptive mutations are diverse, some insertions affect

gene expression (up-regulation, down-regulation, and

inactivation of nearby genes) while other insertions gen-

erate rearrangements leading to deletions. Although the

same adaptive phenotypes may arise in strains lacking IS

elements (Stoebel & Dorman 2010), the studies men-

tioned previously show that IS elements play an impor-

tant role in environmental adaptation.

In plants, adaptation to local environments has been

repeatedly associated with TE-induced mutations. For

example, in soybean, the disruption by a TE insertion

of GmphyA2, one of the two paralogs encoding phyto-

crom A, is associated with adaptation to high latitudes

as showed by phenotypic experiments and allelic distri-

bution analyses (Liu et al. 2008; Kanazawa et al. 2009).

In Arabidopsis, light-regulation of gene expression is

associated with FAR1 and FHY3 that have been co-

opted from an ancient Mutator-like transposase (Lin

et al. 2007). Lin et al. (2007) experimentally showed that

these proteins increase gene expression by directly

binding to the promoter regions of target genes. The

authors argue that the domestication of FAR1 and

FHY3 might have contributed to Arabidopsis adapta-

tion to changing light environments. In wheat, several

TE-induced mutations in vernalization genes are

responsible for changes in the growth habit that enables

wheat to adapt to a wide range of environments (Yan

et al. 2006; Chu et al. 2011).

Adaptation to local environments is also linked to

TE-induced mutations in Drosophila (Gonz�alez et al.

2008, 2010; Gonz�alez & Petrov 2009a). We carried out

the first genome-wide screen for recent adaptive TE

insertions in Drosophila melanogaster and we discov-

ered several TE insertions involved in local adaptation

(Gonz�alez et al. 2008, 2009b). In a follow-up study, we

showed that a substantial proportion of the identified

TE insertions are specifically adaptive to temperate

environments, and that the frequency of some of

these insertions correlates with environmental vari-

ables such as temperature and rainfall (Gonz�alez et al.

2010). We estimated that the already identified muta-

tions only represent a subset of the total number of

TE-induced adaptive mutations suggesting a wide-

spread role of TEs in environmental adaptation in

Drosophila.



Besides adaptation to local environments, TE inser-

tions in Drosophila have also been involved in

resistance to viral infection and resistance to insecti-

cides. Resistance to viral infection has been associated

with a TE insertion in the protein coding sequence of

CHKov1 (Magwire et al. 2011). The TE insertion trun-

cates CHKov1 creating four different altered transcripts,

none of which contain all four exons of the wild-type

gene. This insertion was previously shown to confer

resistance to insecticides, although the authors already

noted that the allele containing the insertion had been

evolving in the populations for a long time before insec-

ticides started to be used (Aminetzach et al. 2005). It

turns out that the allele carrying the insertion would

initially have played a role in defending flies against

viral infection. However, flies carrying this particular

TE insertion found themselves pre-adapted to the intro-

duction of insecticides in the middle of last century.

Magwire et al. (2011) also provide evidence that

CHKov1 alleles carrying duplications of the gene region

containing the insertion, resulted in further resistance to

viral infection. Similar to the CHKov1 allelic series, the

region containing a Cyp6g1 allele previously shown to

confer resistance to pesticides (Daborn et al. 2002), has

also suffered duplications and additional TE insertions

that increased resistance to pesticides (Schmidt et al.

2010). These two examples support the view that alleles

of large effect may sometimes reflect the accumulation

of multiple mutations of small effect at key genes. Other

than in Drosophila, a clear role for TE insertions in

insecticide resistance has also been demonstrated in

mosquitos (Darboux et al. 2007). The binary toxin pro-

duced by Bacillus sphaericus is used as an insecticide

against the mosquito Culex pipiens. Resistance to this

toxin is due to the insertion of a TE into the coding

sequence of the toxin receptor. The insertion induces a

new mRNA splicing event that creates a shorter tran-

script. This new transcript encodes an altered receptor

unable to interact with the toxin resulting in resistance

to this insecticide (Darboux et al. 2007).

Our last example connecting individual TE-induced

mutations and environmental adaptation comes from

paleogenomic studies in mammals (Santangelo et al.

2007; Franchini et al. 2011). Pomc, a gene involved in

stress response and regulation of food intake and

energy balance, has two functionally overlapping enh-

ancers that originated from ancient unrelated TE inser-

tions. In multicellular organisms, the presence of two

enhancers capable of guiding similar patterns in spatio-

temporal expression is common to several developmen-

tal genes. Rather than being redundant, the presence of

the two enhancers is required to overcome the chal-

lenges imposed by critical environmental conditions

such as changes in temperature (Frankel et al. 2010;

Perry et al. 2010). Possibly, the presence of these two

enhancers has been key to evolution of mammals

through the periods of abrupt climate change. Given

the abundance of TEs in mammalian genomes, the

authors concluded that it is conceivable that sequential

exaptation of TEs leading to analogous cell-specific

enhancers could be a more generalized phenomenon

than previously anticipated (Franchini et al. 2011).

Horizontal Transfer of TEs (HTT) and horizontalgene transfer (HGT) mediated by TEs

Besides being transferred from parent to offspring, TEs

can also be horizontally transferred between species. A

horizontally transferred TE (HTT) can generate in the

new host species the same battery of mutations

described for vertically transferred TEs (see Box 2).

Additionally, TEs can also act as vectors facilitating the

horizontal transfer of new genetic content (Ochman

et al. 2000; Frost et al. 2005). This phenomenon has

been extensively demonstrated in prokaryotes. In

eukaryotes, although TEs are capable of capturing and

transferring genes at a high frequency within a species

(Jiang et al. 2004; Morgante et al. 2005; Schaack et al.

2010) they have not yet been found to transfer host

genes between different species. Although horizontal

gene transfer (HGT) can also occur independent of TE

movement, in this review, we focus on TE-mediated

HGT events.

HTT and HGT in prokaryote environmentaladaptation

There is no doubt that prokaryotes increase their

genetic variation by HGT (Ochman et al. 2000; Aminov

2011). This mechanism rapidly integrates ‘foreign’ DNA

that gives the new host the opportunity to acquire new

functions, and to colonize extremely diverse habitats

(Wiedenbeck & Cohan 2011). This phenomenon is of

such importance in bacteria that the vast majority of

species-specific DNA sequences that differ between two

given species have been the result of different events of

horizontal transfer (Levin & Bergstrom 2000). The

mechanisms by which TE- induced HGT can take place

in prokaryotes are diverse and depend on which TE is

involved. HGT events often involve operons and gene

cassettes because horizontally transferred genes have a

better chance to be functional in the new host genome

if they are transferred with their flanking sequences.

Box 3 briefly describes the main TE sequences often

involved in HGT between prokaryote organisms. Addi-

tionally, a recent review is available to the readers inter-

ested in the mechanistic details of HGT in prokaryotes

(Toussaint & Chandler 2012).



Box 3Horizontal transfer in prokaryotes

The genetic content of an organism is received by vertical inheritance, leaving most organisms with a finite toolbox

to face all eventualities along their life and limiting their possibilities to explore new ecological niches. Neverthe-

less, in some occasions, evolution provides an alternative mechanism for rapidly acquiring new genetic material:

horizontal gene transfer. Below, we briefly described several types of prokaryotic transposons that have facilitated

the horizontal transfer of genes.

tpase

TIR

IS IS Structural genes

Composite transposon Insertion Sequence: IS

TIR: Terminal Inverted Repeat. tpase: transposase

TIR

Conjugative transposition Donor

Acceptor

Excision of circular intermediate

Transfer of a single strand of the circular intermediate

Replication

Integration

Composite transposons. In a composite transposon, two Insertion Sequences (ISs) flank one or more genes such as

Tn10 composed of two IS10 elements flanking the tetracycline resistance gene, or Tn5, two IS50 elements flanking a

three-resistance gene operon: streptomycin, bleomycin and kanamycin (Ochman et al. 2000). Composite transposons

can be mobilized between distantly related bacteria having a great impact on the adaptive capacity of the genome

that hosts them. ISs are also involved in creating modular assemblies of genes, the simplest being concatenation

within compound transposons. A good example is the 221 kb virulence megaplasmid of Shigella flexneri, pW100;

(Buchrieser et al. 2000; Venkatesan et al. 2001). In this megaplasmid, ISs represents 46% of the DNA content includ-

ing 26 full-length ISs and an extensive array of IS fragments indicative of ancestral rearrangements.

Insertion Sequence Common Regions (ISCR). ISCR are often associated with resistance and virulence genes. ISCR

resemble ISs but lack terminal inverted repeats and are thought to transpose by a rolling-circle mechanism. ISCR

impact on shuffling antibiotic resistance genes among bacteria is remarkable: they have been involved in horizontal

transfer events of resistance genes of every single class (Toleman et al. 2006).



Box 3 Continued

Conjugative transposons. Conjugative transposons encode their own ability to move from one bacterial cell to another

via cell-to-cell contact. Conjugative transposons have a surprisingly broad host range, and they probably contribute

as much as plasmids to the spread of antibiotic resistance genes in some genera of disease-causing bacteria. Many

conjugative transposons can mobilize co-resident plasmids, and some of them can even excise and mobilize

unlinked integrated elements.

Mobile Integrons (‘quantum leap’ evolution). Integrons are genetic elements able to acquire and rearrange open read-

ing frames (ORFs) embedded in gene cassette units and convert them to functional genes by ensuring their correct

expression. An Integron by itself is nonmobile and its basic functional units are the intI gene and the attI recombina-

tion site. intI encodes a site-specific tyrosine recombinase that recognizes the attI site (Collis et al. 1993; Collis & Hall

1995). intI is responsible for the integration and excision of the different genetic cassettes that compose the Integron.

A promoter often embedded inside the intI gene or the attI sequence drives the expression of the Integron.

When Integrons are associated with transposons they can be mobilized in conjugative plasmids and can be trans-

ferred to individuals of the same or different species. Through their life in different genomes, integrons can acquire

gene cassettes from different origin and be successful in different species thanks to the flexibility of the codon usage

of the harboured genes. Intriguingly, most gene cassettes associated with mobile integrons are composed by antibi-

otic resistance genes (Naas et al. 2001), although a few genes of unknown function have also been identified (Cam-

bray et al. 2010). Integrons have the capacity to harbour many gene cassettes as in the famous case of the Vibrio

cholerae super-integron with 179 gene cassettes (Mazel 2006). The impact of the integration of a mobile unit with

such high number of genes could be considered as a ‘quantum leap’ for the evolution of the new host.

int attI

Pc P2

Pint

Constant Variable

Int

int: integrase gene. attI: sequencesinvolved in recombinationPc, P2: Promoters for the acquired genes Pint: integrase promoter

Integron with exogenous genes

Integron basic structure to acquire genes and build gene cassettes:

.

Several instances of TE-induced HGT are related to

adaptation to different environmental conditions (Och-

man et al. 2000; Hacker & Carniel 2001; Toleman et al.

2006; Cambray et al. 2010; Aminov 2011). In this section,

we will focus on recent examples of HTT and HGT that

play a role in (i) the acquisition of new catabolic and

metabolic properties, (ii) detoxification, and (iii) patho-

genicity and virulence.

1 New catabolic and/or metabolic properties: We have

chosen a recently described example that illustrates

how the acquisition of new catabolic capacities has

allowed a host bacterium to better adapt to harsh

environmental conditions. Cupriavidus metallidurans is

a b-proteobacterium adapted to live in environments

that contain heavy metal pollution (Mijnendonckx

et al. 2011). A recent genome-wide analysis revealed



that there are 57 IS elements in this species, three of

which show 100% identity with IS elements of a

number of other bacteria: Ralstonia pickettii, Burkholde-

ria vietnamiensis, Delftia acidovorans and Comamonas

testosteroni. All these bacteria live in similar environ-

ments suggesting recent interactions and HTT events

between these strains. These horizontally transferred

TEs have been associated with genomic islands and

with gene inactivation that affect the autotrophic

growth capacity of C. metallidurans. Furthermore, one

of the horizontally transferred TEs is also associated

with stress response (Mijnendonckx et al. 2011). The

previous example demonstrates the crucial role that

TEs can have both directly and indirectly in the adap-

tive capacity of bacteria to harsh and polluted envi-

ronments.

2 Detoxification: The catabolic capacities of bacteria are

not only directly linked to their own chances to sur-

vive in a changing environment, but also often con-

tribute to the survival of other organisms that share

the same, often contaminated, environment. Wei and

collaborators showed that the gene methyl parathion

hydrolase, mph, involved in the degradation of organo-

phosphorus compounds, was part of a typical com-

posite transposon (Tnmph; see Box 3) flanked by two

IS6100 sequences in Pseudomonas sp (Wei et al. 2009).

The Tnmph composite transposon was successfully

transferred in the laboratory to a wide range of bacte-

rial species, including some phylogenetically distant

ones. These results suggest that Tnmph may contrib-

ute to the wide distribution of mph-like genes and the

adaptation of bacteria to organophosphorus com-

pounds (Wei et al. 2009). The possibility of manipu-

lating bacteria that live in our everyday environments

with composite transposons including genes like the

mph, expands the already available possibilities to

counteract some of the effects of contamination using

microorganisms (Wu et al. 2012).

3 Pathogenicity: Clostridium perfringens is a pathogenic

bacterium that causes serious illness in different live-

stock animals. The different isolates of C. perfringens

are classified based on which of four lethal toxins

they produce (Sayeed et al. 2010). Type B isolates are

the most virulent because they are able to produce

two different toxins: beta-toxin and epsilon-toxin.

Molecular characterization of type B isolates, demon-

strated that these isolates contain not just one, but

three different plasmids with virulence genes. The

identification of IS elements (IS1151) as well as genes

involved in conjugative transposition (tcp; see Box 3),

strongly suggested that both circular and conjugative

transposition may have been involved in the HGT of

these large virulence platforms (Sayeed et al. 2010).

This is another example of a case in which a series of

HGT caused by HTT has resulted in a better adapta-

tion. In this case, pathogenicity may increase the

chances of wider spread and therefore increase the

likelihood of survival of the host bacterium.

HTT and HGT in eukaryote environmental adaptation

Horizontal Transfer of TE events have been reported in

eukaryotic species as diverse as Drosophila, yeast and

fungi (Hall et al. 2005; Loreto et al. 2008; Gilbert et al.

2010; Schaack et al. 2010). These events may have evolu-

tionary relevance only if the newly inserted TE is able to

transpose, increase in copy number, or provide a new

cellular function. The capacity to transpose and increase

in copy number in a new invaded genome has been

reported for Helitrons (Box 1) in several organisms

including mammals, reptiles, fish, invertebrates and

insect viruses (Thomas et al. 2010). There is also evidence

for the generation of new cellular functions after an HTT

event for P-elements in Drosophila (Pinsker et al. 2001)

and SPIN elements in mouse (Pace et al. 2008). Therefore,

HTT could be an important evolutionary force shaping

eukaryotic genomes, although evidence for a specific role

in environmental adaptation has yet to be found.

As in prokaryotes, HGT has had an important role in

eukaryote genome evolution (Keeling & Palmer 2008;

Syvanen 2012). The evidence for HGT in diverse

eukaryotes is expanding rapidly in organisms such as

nematodes (Haegeman et al. 2011) and fungi (Fitzpa-

trick 2012). Many of the reported HGT events are

related to environmental adaptation. For example, the

ability of distantly related unicellular eukaryotes to live

in anaerobic environments (Loftus et al. 2005) or the

transfer of antifreeze proteins in fish (Graham et al.

2008) are due to HGT events. Although there is no evi-

dence yet of HGT mediated by TEs (Schaack et al.

2010), some authors predict that it will be soon discov-

ered (Keeling & Palmer 2008). For example, Helitrons

have a rolling-circle mechanism of transposition that

makes them especially prone to take adjacent 3′ unre-

lated DNA along (Feschotte & Wessler 2001) and there-

fore are strong candidates to play a major role in HGT

between eukaryotic species.

TE activation triggered by or in response toenvironmental stress

As we mentioned in the introduction, Barbara McClin-

tock was the first to propose that the activation of TEs

in response to stress induces mutations that could help

the organism adapt to new environmental conditions

(McClintock 1984). TEs would therefore play a key role



in translating changes in the external environment into

changes at the genomic level. Indeed, TEs respond

directly to some specific stress situations and in some

cases the specific TE sequences responsible for the

stress response have been identified. This is the case of

several Long Terminal Repeat (LTR) retrotransposons

that contain cis-regulatory elements in their 5′ LTR that

trigger transposon expression in response to a particu-

lar stimulus (Kumar and Bennetzen 1999). These regula-

tory sequences are similar to the well-characterized

motifs required for the activation of stress-responsive

genes (Grandbastien et al. 2005). The possibility of

acquiring changes in the cis-regulatory elements entails

the opportunity to respond to new and different envi-

ronmental factors. Examples of TEs containing these

cis-regulatory elements are abundant and are very well

represented in the literature. In Box 4 we describe some

of the classical examples, such as Tnt1 and Bare1 in

tobacco and barley, respectively.

Box 4

The U3 Box of LTR Retrotransposons

The 5′ LTR works as a promoter containing the sequences that drive, specify, and signal for termination of tran-

scription, and the capping signal. The LTR is subdivided in the U3, R and U5 domains. Different specific DNA ele-

ments in the U3 region (B boxes) have been identified in relation to specific molecules that signal for different

stress responses, such as phytohormones and elicitors. See some examples in the table below and text and refer-

ences for further details.

LTR Retrotransposon Specific molecule or stress situation

Tnt1A, N.tabacum (Beguiristain et al. 2001) Jasmonic acid, cryptogein

Tnt1C, N.tabacum (Beguiristain et al. 2001) Salicylic acid and auxin

Tto1, N.tabacum (Takeda et al. 1999) Jasmonic acid (JA)

OARE1, Hordeum vulgare (Kimura Y et al. 2001) Salicylic acid

BARE-1, Hordeum vulgare (Suoniemi et al. 1996) AcidAbscisic (ABA)

Tdt1, Triticum durum L. (Woodrow P. et al. 2010) Light and salinity

Tlc1, Solanum chilense (Salazar et al. 2007) Phytohormones

5’ LTR

U3 R U5

B boxes

.

Although the specific sequence that responds to stress

has not been identified, for other LTR retroelements it

has been shown experimentally that the LTR is suffi-

cient in itself to activate TE transcription in response to

stress. This, for example, is the case of the activation

under nitrate starvation stress of the Blackbeard

retrotransposon in the marine diatom Phaeodactylum

tricornutum (Maumus et al. 2009). Because LTR elements

are very abundant in this diatom genome, the authors

suggest that their massive activation may probably con-

tribute to major genome rearrangements that would

allow this organism to respond rapidly to changing

environmental conditions (Maumus et al. 2009). Further-

more, the authors show that the retroelement is hy-



pomethylated in response to nitrate starvation, which

provides a link between environmental stress and chro-

matin remodelling in diatoms.

Besides being present in the 50LTR, transcriptional

regulatory sequences are also located in the open read-

ing frames of some LTR retrotransposons (Servant et al.

2008, 2012). This is the case for the LTR retrotransposon

Ty1 of Saccharomyces cerevisiae. The transcription of the

Ty1 retrotransposon is induced, among other specific

stress conditions, by a shortage of adenylic nucleotides

(Todeschini et al. 2005). A recent study by Servant and

collaborators identifies the mechanism of activation of

this TE (Servant et al. 2012). It turns out that severe ade-

nine starvation activates the expression of the transcrip-

tion factor TYE7. TYE7 binds to the E-boxes, located

downstream of the transcription start site of the TYA

gene, and alters Ty1 antisense transcription. As a conse-

quence, there is an increase in sense Ty1 mRNA that

leads to retrotransposition of this element and coactiva-

tion of the expression of genes adjacent to Ty1 inser-

tions (Servant et al. 2008, 2012).

Other than LTR retrotransposons, class II elements

such as Miniature Inverted-repeat Transposable Ele-

ments (MITEs) have also been shown to respond specif-

ically to some stress conditions. This is the case, for

example, for the mPing MITE in rice. In some rice

strains mPing has amplified from c. 50 to 1000 copies

(Naito et al. 2006). The analyses of the insertion sites in

the strains that have undergone this burst of transposi-

tion revealed that under normal growth conditions

mPing elements have a modest impact on the host

because of highly evolved targeting mechanisms that

minimize the effects on host gene expression (Naito

et al. 2009). However, mPing is able to confer a stress-

inducible state to the nearby genes regardless of

whether the TE is inserted at their 5′ or the 3′ region,

suggesting its potential to act as an enhancer element.

Although a specific sequence inside the mPing element

has not been defined, it is clear that mPing is able to

provide the surrounding genes the capacity to respond

to certain stress situations but not others (e.g. cold and

salt but not drought). Because of the high copy number

of mPing in rice genomes, its specific transcription and

transposition could result in new gene regulatory net-

works of coordinated expression that would contribute

to a fine-tuned response of this organism to specific

stress factors. The creation of such regulatory networks

in response to certain stresses could be a widespread

phenomenon in nature since evidence for rapid and

massive amplification of MITEs has been found in

virtually all sequenced eukaryotic genomes and even in

some prokaryote ones (Naito et al. 2009).

The case of mPing illustrates how the integration site

of some TEs may confer stress-inducibility to nearby

genes. However, the opposite is also true: some TEs

specifically integrate close to stress-responsive genes.

Tf1, an LTR retrotransposon from Schizosaccharomyces

pombe, shows a tendency to integrate in a 500 bp win-

dow upstream of ORFs (Behrens et al. 2000; Bowen et al.

2003). Guo & Levin (2010), further demonstrate that in

different activation experiments the newly integrated

Tf1 elements insert close to RNAPol II promoters but

interestingly, there was no correlation with the level of

transcription of the targeted promoters. Instead, Tf1 had

a strong preference for promoters that are induced by

specific stress conditions, such as genes induced by

cadmium and heat. The targeting of Tf1 to stress-

induced promoters represents a unique response that

may function to specifically alter expression levels of

stress response genes (Guo & Levin 2010).

Activation of TEs is not always directly triggered by

a specific stress but the effects that such stress causes

in other cellular mechanisms allow a rapid activation

of some particular TE copies (Dai et al. 2007; Coros

et al. 2009). An interesting example to illustrate this

kind of secondary response is the activation of the Ty5

retrotransposon in Sacharomyces subject to starvation

stress. Ty5 in Sacharomyces preferentially integrates

into heterochromatic regions. This pattern of integra-

tion is directed by the interaction between the Ty5 in-

tegrase targeting domain (TD) and the heterochromatic

protein Sir4 when Ty5 is phosphorylated (Zhu et al.

2003; Dai et al. 2007). When Sacharomyces is faced

with starvation, numerous signal transduction path-

ways, among them the protein kinase A pathway, are

affected. When the TD of Ty5 is not phosphorylated,

there is no interaction with Sir4 and the pattern of

integration of this retrotransposon changes radically.

Under such conditions Ty5 becomes a potent endoge-

nous mutagen that integrates randomly throughout the

genome, including into gene-rich regions. This change

in the pattern of integration of Ty5 is observed in

response to some specific stress conditions (e.g. starva-

tion stress) and not others (e.g. heat-shock, DNA dam-

age, osmotic shock or oxidative stress). The regulation

of Ty5 phosphorylation by stress, demonstrates that

TEs provide the cell with a prewired mechanism to

reorganize the genome in response to environmental

challenge (Dai et al. 2007).

Finally, we will highlight two of the several recent

examples from the literature indicating that noncoding

and small interfering RNAs are also another possible

path by which TEs respond to stress (Hilbricht et al.

2008; Mariner et al. 2008; Lv et al. 2010; Yan et al. 2011;

McCue et al. 2012). Possibly one of the best-studied

stress responses in eukaryotes is the one triggered by

heat-shock. However, the exact mechanisms by which

most organisms subject to a heat-shock manage to



repress the transcription of most genes are still

unknown. Mariner and collaborators discovered one

mechanism of response to heat-shock involving TEs in

humans (Mariner et al. 2008). Alu elements function as

cell stress genes: different stress conditions cause an

increase in the expression of Alu RNAs, which rapidly

decreases upon recovery from stress (H€asler & Strub

2006). Alu RNA has been implicated in regulating

several aspects of gene expression such as alternative

splicing, RNA editing, translation and miRNA expres-

sion and function (H€asler & Strub 2006; H€asler et al.

2007). In humans, Alu elements but not other Pol III

transcribed genes are activated by heat stress. Mariner

et al. (2008) demonstrated that the mRNA of the Alu

element block transcription by binding RNApol II and

entering the repressor complexes that will be loaded

onto the promoters of the repressed genes. Interestingly,

in mouse cells the SINE B2 element activated upon

heat-shock is also able to repress transcription of many

genes using a similar mechanism. Although the B2

SINE derived from tRNA from mouse, and the human

Alu derived from 7SL-like precursor, do not have

sequence identity or similar RNA secondary structures,

their similar effects on the host heat–shock response

suggest that these two SINE elements have converged

to the same biological function.

An additional example reveals how siRNAs gener-

ated by a retrotransposon confer the capacity to

respond to desiccation to the callus of the plant Cratero-

stigma plantagineum (Hilbricht et al. 2008). CDT-1 was

first identified as a plant desiccation tolerant gene and

later recognized as being a TE, although it is still pend-

ing classification. Hilbright and collaborators reported

that while no translation from this element is needed

for the desiccation tolerance response, the transcription

and the posterior production of related siRNAs from

CDT-1 is essential to induced expression of desiccation-

inducible genes.

Overall, the examples described previously strongly

suggest a role of TEs in the ability of the host to respond

to changes in the environment. The evidence that only

some specific TE families, and not all the TEs in the gen-

ome, are activated in response to stress and the evidence

that these TEs respond to some specific stress conditions

and not others, strongly suggest that activation of TEs

by stress is not only a byproduct of genome deregula-

tion. The consequences of TE activation in response to

stress are diverse. Stress-activated TEs: (i) contribute to

major genomic rearrangements (Maumus et al. 2009), (ii)

confer nearby genes the capacity to respond to stress

(Guo & Levin 2010; Servant et al. 2012), which may lead

to the creation of new regulatory networks (Naito et al.

2009; Ito et al. 2011) and (iii) alter the genome randomly

through insertion of the newly generated copies (Dai

et al. 2007). Therefore, containing a certain number of

potentially active TEs may increase the genome ability

to cope with environmental changes.

Concluding remarks

Given the opportunistic nature of evolution, the capac-

ity of TEs to generate mutations of great variety and

magnitude suggests that TEs are important players in

genome evolution. Some authors may consider that the

capacity of TEs to create genetic diversity that might

result beneficial for the host genome has not been

exploited often, nor has it necessarily been subject to

positive selection. In this review, we argue that there

are many examples that provide solid grounds for the

beneficial effect of TEs in host genome evolution in gen-

eral and in host environmental adaptation in particular.

Note that several of the works summarized in this

review (e.g. Gonz�alez et al. 2008; Naito et al. 2009; Fran-

chini et al. 2011) strongly suggest that the particular

cases described may represent the tip of the iceberg.

Moreover, identifying TE insertions involved in envi-

ronmental adaptation depends ultimately on our ability

to identify a given nucleotide sequence as a TE or a TE

remnant. As such, we are still likely underestimating

the role of TEs in environmental adaptation just because

of our limitations to identify TE insertions. We antici-

pate that in the next years increased availability of gen-

ome sequences, the development of new tools to

accelerate the discovery of TE insertions (Fiston-Lavier

et al. 2011; Flutre et al. 2011; Makalowski et al. 2012)

and the increased knowledge about which genes and

traits are relevant for adaptation will further support

the prevalent role of TEs in environmental adaptation.

Acknowledgements

We thank Anna-Sophie Fiston-Lavier, Lain Guio, Ruth Hersh-

berg, Lidia Mateo, Dmitri A. Petrov and Alfredo Ruiz for

critically reading the manuscript. This work was supported by a

grant from the Spanish Ministry of Science and Innovation

BFU2009-08318/BMC awarded to E.C. and by a Ramon y Cajal

grant (RYC-2010-07306), a Marie Curie CIG grant (PCIG-GA-

2011-293860) and a National Programme for Fundamental

Research Projects grant (BFU-2011-24397) awarded to J. G.

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E.C. is a functional evolution researcher interested in

the role of TEs in the evolution of eukaryote genomes.

J.G. leads the Evolutionary and Functional Genomics

research group which focuses on elucidating the

molecular process and the functional consequences of

adaptation.



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