Review articles
Transposons in filamentous
fungi—facts and perspectives
Frank Kempken and Ulrich Kück*
Summary
Transposons are ubiquitous genetic elements discovered so far in all investigated
prokaryotes and eukaryotes. In remarkable contrast to all other genes, transposable elements are able to move to new locations within their host genomes.
Transposition of transposons into coding sequences and their initiation of chromosome rearrangements have tremendous impact on gene expression and genome
evolution. While transposons have long been known in bacteria, plants, and
animals, only in recent years has there been a significant increase in the number of
transposable elements discovered in filamentous fungi. Like those of other eukaryotes, each fungal transposable element is either of class I or of class II. While class
I elements transpose by a RNA intermediate and employ reverse transcriptases,
class II elements transpose directly at the DNA level. We present structural and
functional features for such transposons that have been identified so far in
filamentous fungi. Emphasis is given to specific advantages or unique features
when fungal systems are used to study transposable elements, e.g., the evolutionary impact of transposons in coenocytic organisms and possible experimental
approaches toward horizontal gene transfer. Finally, we focus on the potential of
transposons for tagging and identifying fungal genes. BioEssays 20:652–659,
1998. r 1998 John Wiley & Sons, Inc.
Introduction
Transposable elements were first discovered in maize during
the late 1940s by Barbara McClintock. Since then, an evergrowing number of transposons were detected in bacteria,
plants, and animals.(1,2) There are numerous examples of
mutations and other types of genetic variations associated
with the activity of transposons. This includes insertions into
(i) exons, (ii) regulatory regions, (iii) introns, and (iv) the
mediation of recombinations.(3) Aside from the effect of transposons on genomic variation, evolutionary considerations
mainly regard transposons as genetic parasites.(4) However,
a number of recent observations suggest coadaptations to
mitigate reduced host fitness in some cases, e.g., (i) host
regulation of copy number, (ii) insertion bias of transposons
Lehrstuhl für Allgemeine Botanik, Ruhr-Universität Bochum, Bochum,
Germany.
*Correspondence to: Ulrich Kück, Lehrstuhl für Allgemeine Botanik,
Ruhr-Universität Bochum, D-44780 Bochum, Germany. E-mail:
ulrich.kueck@ruhr-uni-bochum.de
652
BioEssays 20.8
for noncoding regions or (iii) self-regulation of copy number.(3)
Finally some data even suggest benefits from the presence of
transposons in a host: (i) a repair mechanism for doublestranded DNA breaks in yeast,(5,6) or (ii) the replacement of
damaged telomers in Drosophila.(7) Quite recently, transposable elements were also discussed to be involved in processes leading to aging, which is often associated with
genetic instability.(8) While the mutational character of transposons is a well-established fact, their evolutionary relevance
and particularly their potential benefit for their hosts are still
controversial. This is often because of difficulties in establishing experimental test systems in more complex organisms,
such as plants and animals. Some of these difficulties may be
circumvented by the use of filamentous fungi as experimental
organisms. The first hints of the presence of transposable
elements in fungi came from conventional genetic studies
with unstable spore color mutants of Ascobolus immersus.(9,10) However, it was not until 1989 that the first molecular
analysis of a transposon from a filamentous fungus was
reported—the Tad element from Neurospora crassa.(11) Since
then, the scientific community has witnessed an enormous
BioEssays 20:652–659, r 1998 John Wiley & Sons, Inc.
Review articles
increase in the number of cloned and sequenced fungal
transposable elements(12)(Table 1).
It is the aim of this review to describe the main strategies
for identifying new transposons in fungi. Furthermore, we
present data on distribution and classification of fungal
transposons and most importantly to point out specific advantages of fungal experimental systems. Finally, we describe
first steps toward the development of gene tagging systems
in filamentous fungi.
Strategies to identify fungal transposons
Four strategies have been employed to identify previously
unknown transposons. (1) Use of heterologous probes for
Southern hybridization experiments (e.g., ref. 13). However,
this strategy requires appropriate probes and detects only
transposons of known type. (2) Transposon traps. In most
cases, transposons were identified by insertion into a gene,
such as the nitrate reductase (niaD) gene (e.g., ref. 14)
leading to a change in phenotype. The niaD gene is particularly suitable for this approach, as here it is possible to select
both for transposon integration and excision. By contrast,
transposon Tad was isolated by insertion mutation in the
Neurospora crassa am gene.(11) Transposons may be easily
identified by polymerase chain reaction (PCR) amplification
of such mutants. This method is suitable to identify elements
with rather high excision and insertion frequencies. (3) Identifying repeated DNA sequences by differential hybridization.
In this approach, a fungal gene library is probed with fungal
genomic DNA and, in parallel, with a rDNA probe. Then
non-rDNA, repeated sequences are the subject of further
analysis.(15–17) This approach is particularly suitable for identifying transposons with high copy number, regardless of
whether they are active. (4) PCR with oligonucleotides
representing conserved motifs of reverse transcriptases,(18–
20) which are encoded by most class I transposable elements
(see below). This method is particularly useful for identifying
class 1 elements and permits rapid screening of a large
number of organisms.
Structure and function of transposable elements
Unlike most bacterial transposons, which carry genes conferring a selective advantage to the host, for example antibiotic
resistance, eukaryotic transposable elements, including those
from fungi,(1,2) carry no selectable genes. Fungal transposons, like other eukaryotic transposons, can be divided into
two classes. Class I elements transpose via an RNA intermediate employing a reverse transcriptase.(21) By contrast, most
class II elements transpose at the DNA level by excision from
a donor site and reintegration elsewhere in the genome.
Approximately one-half of all identified fungal transposons
belong to class I (Table 1). So far three types of class I
elements are known in filamentous fungi:
1. Retrotransposons: These elements carry long terminal
repeats (LTR) and encode gag (viral coat proteins) and pol
(reverse transcriptase, RNase H, integrase, and protease)
genes (Fig. 1A). Retrotransposons have been identified in
a number of plant pathogens, e.g., Cft-1 in Cladosporium
fulvum (22) and Skippy from Fusarium oxysporum.(23) Although there is no apparent correlation between the
genomics location of these elements and the pathogenity
of their host, retrotransposons represent useful genetic
markers for strain identification. Remarkably, all but two
are members of the gypsy retrotransposon subfamily, with
only two (MARS2 and MARS3)(24) being a copia like
retrotransposon. The two subfamilies differ in the order of
their pol genes (Fig. 1A).
2. Retroposons, or LINE-like retroelements: These elements
usually possess poly-A-tails but no LTRs (Fig. 1A). LINE
elements were originally identified in mammals (for literature, see ref. 1); intact retroposons of this type also carry
gag and pol genes. Fungal members of this group include
MARS1 from Ascobolus immersus(18) and the Tad element
from N. crassa.(11) Tad has some interesting features, as it
occurs in a fungus that usually inactivates repeated DNAs
by a mechanism known as ‘‘RIP’’ (see below).
3. SINE-like elements: These elements are derived from
RNA polymerase III transcripts. They do not possess
special structural features or gag or pol genes (e.g., ref.
25). Instead it is believed that they are trans-activated by
reverse transcriptases provided by LINE-like elements or
retrotransposons.
Class II elements in fungi are mostly Fot1/Pogo-like or belong
to the Tc1/mariner superfamily.(26,27) Tc1/mariner-like elements were named according to their prototypes found in
nematodes and insects,(28,29) while Fot1/Pogo elements (Pogo
transposon from Drosophila) are a recently established distantly related branch.(27) As shown in Figure 1B, both types of
elements possess short terminal inverted repeats and cause
a 2-base pair (bp) target site duplication with the sequence
‘‘AT’’ upon integration in the host genomic DNA. However,
they encode different types of transposases. Typical examples for these transposon families are the Fot1 and Impala
elements from F. oxysporum, respectively.(14,30) It is unknown
why this class II transposon family is predominant in fungi.
However, since transposon traps were used to identify most
of these transposons, the Fot1/Pogo and Tc1/mariner-like
elements may simply represent a very active type of transposon that may have been more successful than others in
spreading by horizontal gene transfer. Indeed there is evidence for horizontal gene transfer of Fot1 elements in
different Fusarium species.(31) Members of other families
have also been detected in fungi. First, the hAT transposon
family (Fig. 1B) includes the maize Activator (Ac), snapdragon Tam3, and the Hobo elements from Drosophila.(32)
BioEssays 20.8
653
Review articles
TABLE 1. Class I and II Transposons from Hyphal Fungi
Host name
Class I
Ascobolus immersus
Aspergillus fumigatus
Botrytis cinerea
Cladosporium fulvum
Colletotrichum gloesporioides
Erysiphe graminis f.sp. hordei
Fusarium oxysporum
Podospora anserina
Magnaporthe grisea
Nectria haematococca
Neurospora crassa
Class II
Acobolus immersus
Transposon
name
Size
(kb)
Hideaway
MARS1
MARS2
MARS3
MARS4
MARS5
Afut1
Boty
Cft-1
CgT1
EGH24-1
Eg-R1
Foret-1
Palm
Skippy
Repa
Fosbury
Grasshopper
Maggy
MGR583
Mg-SINE
MGSR1
Nrs1
Pogo
Tad1-1
2.5 to 9.4
1.8c; 2.4c
1.5c; 1.7c
1.4c
0.43c
4.4c
6.9
?
7.0
,5.7
0.9
0.7
10b
Ascot-1
Tascot
Aspergillus nidulans
F2P08
Aspergillus niger
Ant1
A.n. var. awamori
Tan
Vader
Beauveria nivea ATCC42437
Restless-d1
Botrytis cinerea
Flipper
Cochliobolus carbonum
Fcc1
Fusarium oxysporum
Fot1
Fot2
Impala
Hop
Magnaphorthe grisea
MGR586
M.g. AVR2-YAMO
Pot3
Pot2
Nectria haematococca
Nht1
Neurospora crassag
Guest
Phanerochaete chrysosporium
Pce1
Puccinia sorghi
PSR
Tolypocladium inflatum ATCC34921 Restless
b
TSD
[bp]
i
i
i
i
i
i
5
i
5
13
13
i
Copy
no.
15–20
60
40
60
20
b
.10
1–38d
25
.10
a
,50
i
b
i
b
b
7.8
5
0.3
5
,10
i
b
,5.5 kbb
8.0
5
.10
5.6
5
0–100
i
.7.5c
40–50b
i
0.47
,100
i
0.8
,40
i
0.5
11
1.6
3
5–10
6.9
14–17
,40
b
0.4f
8
b
3.6
8
i
,1.5
?
4, 8
2
1
i
1.7
1
0.4
2
,15
1.9
None
1
i
1.7
,20
i
1.8
.10
i
1, 9
4–100
i
2, 1
,100
1, 3
2
6
b
3, 5
7
1.86
2
0–.50
i
b
?
1, 9
2
,100
2.2
2
0–100
0.1d (1.3)
3
,25
1.7
2
1–5
0.5h
5
,100
4.1
8
15–20
Type
Retrotransposon-like?
16, 52
LINE-like
24
Retrotransposon-like (copia)
Retrotransposon-like (copia)
Retrotransposon-like
i
Retrotransposon
Retrotransposon
Retrotransposon
LINE-like
SINE-like
SINE-like
Retrotransposon
LINE-like
Retrotransposon
Single LTR
Retrotransposon
Retrotransposon
Retrotransposon
LINE-like
SINE-like
SINE-like
SINE-like
Retrotransposon
LINE-like
69
70
22
71
25
72
73
74; cited as retroelement in 12
75
76
77
78
79
15; cited in 80
81
82
83
84
11, 85
hAT-like
hAT-like
Fot1/Pogo-like
Tcl/Mariner-like
Fot1/Pogo-like
Fot1/Pogo-like
Ac-like (hAT family)
Fot1/Pogo-like
Fot1/Pogo-like
Fot1/Pogo-like
Fot1/Pogo-like
Tc1/Mariner-like
?
Fot1/Pogo-like
Fot1/Pogo-like
Fot1/Pogo-like
Fot1/Pogo-like
mini transposonb
Tc1-mariner-likeb
34
EMBL accession Y07695
86
58
87
75
57
88
89
14
26
30
26
90
i
Ac-like (hAT family)
TSD, target site duplication.
aVery high copy number.
bUnknown; generally, copy numbers differ largely between strains and are often difficult to estimate.
cLength of sequenced DNA fragment.
dNumber of lambda clones containing the element.
eSize of largest transcript is 7.5 kb.
fNo open reading frame.
gAn active Fot1/Pogo-like element named Punt from N. crassa (see ref. (12)).
hLarger copies present; LTR-retrotransposons are of gypsy type if not stated otherwise.
iUnknown, not determined.
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BioEssays 20.8
Reference
13
91
36
92
93
33
Review articles
Figure 1. Genetic maps of eukaryotic
transposable elements. A: Class I transposable elements. B: Class II transposable
elements. hAT and Tc1/Mariner families
are easily distinguished by different encoded transposases. In addition Tc1/
Mariner elements have always target site
duplications of the sequence ‘‘AT.’’ Fot1/
Pogo elements also have ‘‘AT’’ TSDs, but
encode a different kind of transposase.
PBS, primer binding site; gag, gene for
structural proteins; pol, gene for transposition; PR, protease; Int, Integrase; RT, reverse transcriptase; (TAA)n poly-A-tail (not
all eukaryotic retroposons possess poly-Atails). LTR, long terminal (direct) repeat;
TIR, terminal inverted repeat; TSD, target
site duplication.
They possess very short inverted repeats and cause an 8-bp
target site duplication. So far, three transposons of this group
have been found in fungi: The transposon Restless from the
cyclosporin C producing fungus Tolypocladium inflatum is an
active element that has some unusual features, such as
alternative splicing of its transposase mRNA,(33) a deleted
hAT-like element (Ascot),(34) and a sequence from A. immersus (Tascot) recently submitted to the EMBL database
(Y07695), also seems to be a hAT transposon. However,
phylogenetic analysis shows that the fungal hAT transposons
are distantly related only.(35) Second, a deletion fragment of a
transposon (Guest; Fig. 1b) was found in N. crassa,(36) which
is only 98 bp in size. However, there are larger copies of
Guest scattered in the genome(36) (P.J. Yeasdon and D.E.A.
Catcheside, personal communication). Elements of similar
size (named Tourist) are also known from higher plants,(37)
and it is believed that they are important for the generation of
transcriptional cis-acting sequences. It is not yet known
whether Guest has a similar function.
Specific advantages to be gained from studying
the transposons of filamentous fungi
Since transposition in plants, animals, and bacteria has been
studied intensively at the molecular level over the past
decade or so (for literature, see refs. 3,38,39), why study
them in fungi?
1. Fungi have relatively small genomes in the order of about
30–40 Mb, and chromosomes can be separated on a
single gel by pulsed-field gel electrophoresis (for literature, see refs. 41,42). Such analysis can be extended
using rare cutting restriction enzymes.(42) As a result, fungi
are particularly favorable for addressing questions such
as how transposable elements contribute to the evolution
of genomes and whether they are responsible for the
remarkably high degree of karyotype variability observed
in some species (e.g., refs. 43–45). Studies done with
plant transposable elements Activator and Dissociation
suggest a high probability for transposons arranged in
tandem to cause chromosome breakage and rearrangement (reviewed in ref. 46). The availability of detailed
genetic maps for some fungi (e.g., N. crassa) should
greatly facilitate more detailed studies of such phenomena
in fungi.
2. Many fungi have developed mechanisms to inactivate
repeated sequences prior to or during sexual recombination. Prime examples are the ‘‘RIP’’ phenomenon in N.
crassa, and the ‘‘MIP’’ phenomenon in A.immersus. While
C-to-T transitions are generated at high frequency in
repeated sequences as a consequence of ‘‘RIP’’ (47–49),
‘‘MIP’’ causes methylation of cytosine residues in repeated
DNA sequences (reviewed in ref. 50) and is known to
effect certain transposons in A. immersus as well.(24) The
efficiency of these mechanisms in destroying invading
transposons is not yet known in detail, but the N. crassa
transposon Tad is clearly subject to ‘‘RIP’’ if cloned into a
Tad free strain. There is also evidence of ‘‘ripped’’ Tad
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655
Review articles
elements in a number of N. crassa strains.(51) Yet, the
introduction of a foreign transposable element into these
species may provide a simple analytical approach to
establish if and how transposons can survive in fungi
exhibiting ‘‘RIP’’ and ‘‘MIP.’’ The Ascot element from A.
immersus may be too small to be subject to ‘‘MIP,’’(34) and
other transposons may exist in only one copy that does not
trigger the inactivation mechanism. Another clue to this
question comes from recent research, where a retroelement like sequence found inserted within the rDNA cluster
of Ascobolus immersus does not seem to be affected
much by ‘‘MIP,’’ although it is present in many additional
copies in the genome.(52) Similarly, for Tad a strategy to
avoid inactivation by the host is discussed.(51)
3. Filamentous fungi differ from most other eukaryotes in
having a coenocytic organization in which a large number
of nuclei exist in a single cytoplasmic compartment. This
alters the expected impact of transposition events for the
organism. Although transposition events are rare, they
occur usually at higher rates than normal mutations. This
is particularly true for class II elements, which may
account for 80% of spontaneous mutations in some
organisms (e.g., Drosophila).(53) It is reasonable to assume a single transposition event in each 1,000–10,000
nuclei. A large mycelium will harbor millions of nuclei with
transposons inserted at numerous positions, each in a few
nuclei only. While transposition events must usually be
detrimental to mononuclear cells in most eukaryotes, they
can survive in a coenocytic organism as a heterokaryon.
This ability to retain nuclei in which essential genes are
inactive may have had a large impact on the evolution of
fungal genomes.
4. Regulation of transposition is poorly understood in most
experimental systems. The discovery of alternative splicing of mRNA derived from the fungal Ac-like transposon
Restless(33) may lead to the understanding how transposition is regulated. Restless has a long open reading frame,
interrupted by a short intron and may encode a 803-aa
polypeptide. Alternative splicing occurs at a second 38
splice site, separated only 4 nt from the first. As a
consequence, a frame shift occurs in the RNA, which after
translation will result in a polypeptide of 157 amino acid
residues. This peptide may play a role in regulation of
transposition, since it carries a amino acid sequence
similar to a zinc finger and may resemble a DNA binding
motif. Further studies are under way to examine the
biochemical functions of both polypeptides and to elucidate host encoded factors involved in alternative splicing.
5. The transposition mechanism of class II elements is not
well known. In general transposition may be replicative;
i.e., a new transposon copy integrates elsewhere in the
genome with the old copy remaining at its previous
location. Alternatively, a transposon may excise from its
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BioEssays 20.8
genomic site and integrate at a new one as it is assumed
for most eukaryotic class II transposons. Aspects of this
mechanisms are yet to be elucidated, such as the time and
mode of excision. The availability of a large number of
mitotic and meiotic mutants in Aspergillus and Neurospora
provides the means to address these questions. We
recently succeeded in isolating circular, extrachromosomal copies of Restless,(54) similar to those found for the
Tc1 transposon.(55) These circular molecules consist of
Restless elements fused at their terminal inverted repeats,
but separated by genomic DNA of different size. These
molecules may be intermediates of the transposition
mechanism.
6. Gene transfer between species is always a controversial
subject, although such horizontal transfer has undoubtedly occurred for some transposons, e.g., the P element
from Drosophila melanogaster.(56) Studies of transposons
in closely related strains or species may support this
concept. For transposon Fot1 sequence comparisons
suggest horizontal transfer to be relevant within the genus
(31)
Fusarium. In our laboratory we have found single active
or nonactive truncated transposons in closely related
Beauveria strains that may be the result of recent horizontal gene transfer.(57) A transposon from Aspergillus niger,
the Ant1 element carries a piece of the genomic DNA from
that fungus,(58) opening the possibility for transfer of host
sequences to other fungi by horizontal transfer. Because
fungi readily form anastomoses, it is possible to test for
horizontal transfer in the laboratory, using approaches
similar to those used for plasmids.(59–61) The mechanism of
transfer to different nuclei may involve RNA intermediates
or extrachromosomal transposon copies. Kinsey(62) reported the transfer of Tad between nuclei in heterokaryons, and the plasmid-like copies of Restless(54) may be
transferred to other nuclei as well.
Toward a transposon based gene tagging system
in fungi
Gene tagging is a method for identifying unknown genes
using transposable elements. It is based on the inactivation of
a gene by integration of the transposon into the promoter or
coding region. This may lead to a new phenotype, permitting
recognition of the transposition event and physical tagging of
the mutated gene. The gene can then be identified by
isolating the transposon and flanking regions from the genomic DNA of the mutant. For this purpose, specific vectors
were developed e.g. for use in higher plants, but endogenous
transposons may also be used (for literature, see ref. 63). The
maize Activator element has been widely used, because it is
active in a variety of monocotyledons and dicotyledons (e.g.,
refs. 64,65). A number of laboratories have begun the
Review articles
Figure 2. Proposed gene tagging vectors for use in filamentous fungi. A: Simple
vector with a transposable element inserted between promotor (prom.) and selectable gene (select. gene) The vector
carries a second selectable gene for selection of transformants. Transposition of the
transposon is favored and can be monitored by selective pressure on the first
selectable gene. B: A more sophisticated
vector with the transposase gene replaced
by a selectable gene. An engineered transposase gene can be activated by an inducible promotor (ind. prom.). term., terminator of transcription.
development of transposon tagging systems for filamentous
fungi (e.g., refs. 16,26,66). Class II elements, such as Impala
from Fusarium or Restless from Tolypocladium, appear to be
ideally suited as a basis for transposon tagging. Since
Restless is related to the broad host range transposon
Activator,(46) it may well be useful in many different hosts
which would greatly facilitate gene tagging in fungi. Prototypes of vectors to be used in such an approach are shown in
Figure 2. These vectors basically consist of a reporter
gene disrupted by a transposon, which is localized between
promoter and open reading frame. This vector design is
reminiscent of the first plant tagging vectors.(67) Vectors
carrying the Restless transposon were introduced into the
plant pathogen Botrytis cinerea as well as in N. crassa and
Sordaria macrospora and analysis of activity of the transposable element Restless in its new hosts is in progress (currently investigated). We already have chown that Restless is
able to tag a gene involved in the regulation of nitrogen
metabolism in T. inflatum, the original host of the transposon.(68)
The usefulness of developing transposon tagging for fungi
can be questioned, as other techniques are available, such
as vector-based gene tagging or restriction enzyme-mediated integration. Transformation is inefficient in many fungi,
making each tag dependent on a successful transformation
event. However by employing a transposon-tagging system,
a single fungal clone carrying a vector with a transposable
element could be turned into a cornucopia of transposoninduced mutations.
Conclusions
We have now reached a point where several transposons are
characterized, some of them ideally suited to address important questions about the biological role of transposons and
their mechanisms of movement. Fungal experimental systems have a variety of advantages, with regard to other
eukaryotic systems, and they may permit the solution of
problems that are difficult to resolve in other organisms.
Future studies of transposons in fungi should and will focus
on three main areas: (i) the ability of host organisms to
inactivate invading transposons and ways to avoid that
inactivation; (ii) horizontal transfer between different species,
which is apparently much easier to approach experimentally
in fungi; and (iii) the unique environment for transposons in
coenocytical organisms, which is different from almost all
other eukaryotic cells. This last point in particular may provide
very interesting clues for the genome evolution in fungi.
Finally, transposon tagging in fungi will provide an excellent
tool for gene identifications. This is of particular interest with
respect to genome sequencing projects, which are currently
in progress in a number of fungal genomes, e.g., Aspergillus
or Neurospora.
Acknowledgments
We thank Drs. J. Clarkson and David E.A. Catcheside for
their comments on the manuscripts.
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