Institut de Génétique et Microbiologie, Université Paris-Sud, Orsay, France
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Abstract |
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Introduction |
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More recent studies have used new tools such as fingerprinting with repeated sequences (usually transposable elements), proven to be valuable for several fungal species, including Magnaporthe grisea (Hamer et al. 1989
; Dobinson, Harris, and Hamer 1993
; Farman, Taura, and Leong 1996
), Mycosphaerella graminicola (McDonald and Martinez 1990
), Erisyphe graminis (O'Dell et al. 1989
), Cryphonectria parasitica (Milgroom, Lipari, and Powell 1992
), and F. oxysporum. In this species, fingerprinting allowed researchers to distinguish formae speciales (Namiki et al. 1994
), to track the origin of new infestation (Mouyna, Renard, and Brygoo 1996
), to detect a given forma specialis (Fernandez et al. 1998
), and to identify races within a forma specialis (Chiocchetti et al. 1999
). Moreover, PCR assays based on several transposable element insertion sites provided a useful diagnostic tool for quickly identifying formae speciales and races.
Transposable elements appear especially abundant within F. oxysporum that exhibit a high degree of genetic variability. This is illustrated by numerous transposon families (about 17) characterized thus far, representing the major classes of retroelements and DNA transposons (Julien, Poirier-Hamon, and Brygoo 1992
; Daboussi and Langin 1994
; Mouyna, Renard, and Brygoo 1996
; Okuda et al. 1998
; Gomez-Gomez et al. 1999
; Hua-Van et al. 2000
; Mes, Haring, and Cornelissen 2000
). One of these active DNA transposon families, named impala, is composed of few (810) elements and is typically 1,280 bp long with 37-bp inverted terminal repeats (ITRs). Impala contains a single open reading frame encoding a transposase of 340 amino acids (aa). This transposase is related to those found in elements belonging to the widespread Tc1-mariner superfamily (Langin, Capy, and Daboussi 1995
; Hua-Van et al. 1998
). In strain FOM24 (herein called M24), in which impala was first identified, about 10 different impala copies have been characterized. Three subfamilies, named E, D, and F, have been detected (Hua-Van et al. 1998
). The E and D subfamilies are represented by several copies, which are autonomous, inactive, or truncated (Hua-Van et al. 1998
; Hua-Van et al. 2001
). Within each subfamily, nucleotide divergence between the full-length elements is relatively low (around 1%), while the truncated elements are more polymorphic. The F subfamily contains only one full-length-but-inactivated element. These three subfamilies differ by as much as 20% at the nucleotide level (Hua-Van et al. 1998
). This result is intriguing when compared with the 0.3%5% polymorphism observed within the F. oxysporum complex for the nia and EF1
genes and internal transscribed sequence or intergenic sequence of ribosomal DNA (Avelange 1994
; Appel and Gordon 1996
; O'Donnell et al. 1998
). Two non-mutually-exclusive hypotheses may be proposed to explain the evolutionary origin of impala subfamilies. First, the presence of different subfamilies in a genome might be the result of ancestral polymorphism. The subfamilies present in the common ancestor would then be expected to be present in genetically diverse strains associated with diversification of these pathogens. Another possibility is the occurrence of one or more horizontal transfers. Such events have been described for other transposable elements (Kidwell 1992
; Robertson and Lampe 1995a
), notably for mariner elements, for which horizontal transfer appears to have played a major role in evolution (Garcia-Fernandez et al. 1995
; Lohe et al. 1995
; Robertson and Lampe 1995b
). In this case, the foreign impala element(s) might be expected to be present in a small number of related strains, all derived from the same ancestor in which the transfer occurred.
In order to understand the dynamics of impala within the complex, a collection of F. oxysporum strains with different host specificities were analyzed by Southern blot, PCR, and sequencing. This analysis showed that the impala family is widespread within F. oxysporum strains. A total of five subfamilies were identified, and most of these were present in several strains with different host specificities. On several occasions, similar inactive copies with unique sequence characteristics were detected in strains with various host specificities. Relationships of these strains were inferred through phylogenetic analysis of translation elongation factor (EF1) gene sequences. This revealed that strains containing very similar impala copies are usually closely related. The implications of these results for the evolutionary origin of strains and the use of impala as a tool are discussed.
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Materials and Methods |
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Polymerase Chain Reaction and Primer Sequences
Three pairs of primers were used to specifically amplify elements of the E subfamily (SpE5 [AGAACACAACCCTGCCACGG] and SpE3 [TCCGGGCCGTATGCACAGAG]) or the D subfamily (SpD5 [AAGGGCTTACGCACTCACAG] and SpD3 [CACGGGCAGTGTGAACAGAC]) or any impala elements (NS5 [CGATGCCTCGAGGCAAGGAA] and NS3 [TCTCTGCCTTCATCAACGCCC]). Elements at particular locations were amplified using primers nested in the flanking regions, about 100 bp from either side of the elements: SFA5 (TTGCCCCCACTTTGTGTCTG) and SFA3 (TATGCGACTTAGAAGTCGGC) for impA, SFC5 (ACCACTTGTTAGATGCTCGG) and SFC3 (ATCTAAACAAGGGGTGCGGC) for impC, and SFD5 (ATCGTGTGTATTCCTGATCC) and SFD3 (ACAGCCCGTTTCCCTCACGC) for impD. For impB and impG amplifications, a primer in the flanking region and an internal primer were used: SFB5 (CAATTCATTGCAGCCCACTG) and SpE3 for impB, or SFG3 (TCTGAGGAAGAAACTGATC) and SpG5 (TCCTGTTGAATGTTGGAGGG) for impG. The latter primer primes on the solo-LTR Han, inserted in impG (Hua-Van et al. 2000)
. Amplification of the EF1
fragment was conducted using primers EF-1 and EF-2 described in O'Donnell et al. (1998)
. Amplifications were done using standard procedures in a PTC100 thermocycler (MJ Research, Waldham, Mass.) using the following program: 30 cycles of 1 min at 94°C, 30 s at 60°C, and 1 min 30 s at 72°C, followed by a final extension of 10 min at 72°C.
Inverse PCR
To determine if deleted copies or ripped copies originated from the same event, the insertion points of these copies were cloned by Inverse PCR in strain MK, following a procedure adapted from Gloor et al. (1993)
. One hundred nanograms of genomic DNA was digested with restriction enzyme for 30 min at room temperature in a total volume of 20 µl. After 10 min inactivation at 65°C, 3 µl was used in a ligation experiment (10 µl final volume with Promega ligase and buffer; 30 min at room temperature). The ligation product inactivated for 10 min at 65°C was used in a PCR experiment using the following PCR program: 2 cycles of 95°C for 1 min, 58°C for 15 s, and 72°C for 5 min; 35 cycles of 95°C for 15 s, 58°C for 15 s, and 72°C for 3 min; and 72°C for 10 min.
For deleted copies, we used the restriction enzyme XbaI and primers DDV5 (AAAACGCGTGCCTAATCGGG) and DDV3 (CTCGGGCTAGACCGATCAGTC). For ripped copies, enzymes PstI and HindIII and primers RIPK5OUT (ATAACCAGCACGCCATAATTCG) and RIPK5IN (TTAAACACGAAGAAAAACGCGG) allowed amplification of 5' flanking sequences. We designed primers SF3-Del (CAAACAGAGCTTAACCTCAACCGC) and SF5-RIP (TCACTTGCTGTTCTCCCCAG), located in these flanking sequences, and used them along with a primer specific for impala (SpD5 or RIP5OUT, respectively) in a direct PCR experiment. An amplification product of the expected size was obtained in all strains containing these deleted or ripped copies (MK, L15, RL28 and MK, L15 and Ci).
Cloning and Sequencing
Impala PCR products were cloned using the Promega pGEMT-easy kit. For each strain, several individual clones were sequenced using the ABI PRISM Dye-Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems) on an ABI373 Automated DNA sequencer (Applied Biosystems). Sequencing primers corresponded to M13 forward and M13 reverse primers. EF1 sequencing was performed either after cloning as described above or directly on PCR products using primers EF-1 and EF-2. The nucleotide sequences reported in this paper are deposited in GenBank under accession numbers AF363407AF363439 (impala) and AF363394AF363406 (EF1
).
Phylogenetic Analysis
Multiple DNA alignments were obtained with the Clustal V program (Higgins and Sharp 1988
). Maximum-parsimony analyses were performed using the heuristic algorithm and default options of PAUP 4.0 (Swofford 2000)
. We carried out 100 or 1,000 bootstrap replications of maximum parsimony with a full heuristic search and default options.
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Results |
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Sequence Variation and Phylogenetic Analysis
The different PCR products obtained with the NS primers were cloned, and some of these clones were completely sequenced. A phylogenetic tree deduced from these sequences by maximum parsimony is shown in figure 3
. The clades corresponding to the known subfamilies E, D, and F were strongly supported by bootstrapping (Hua-Van et al. 1998
). The E subfamily (100% bootstrap) is composed of several groups of highly similar elements (around 4% nucleotide divergence; divergence can reach 12% for more divergent members), except for elements RL4-110, M11-6, and impB, which are supported by long branches. The D subfamily (100% bootstrap) is also very homogeneous in sequence (2.3% sequence divergence) but is characterized by the presence of several internally deleted elements. The F subfamily (98% bootstrap), for which only one element from strain M24 had been described, was also found in two other strains and appeared less homogeneous (14% nucleotide divergence).
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Active Versus Inactive Elements
Potentially active elements (i.e., containing no stop codons or frameshift mutations over the 800 bp sequenced) were found within the E and D subfamilies (fig. 3
), similar to those described previously from strain M24 (Hua-Van et al. 1998
). The present study also revealed the existence of such elements in the F subfamily but not in the K and P subfamilies.
Most of the sequences represented inactive copies, as deduced from the presence of stop codons and/or frameshifts. They were found in every subfamily. Among these, we identified two particular types of inactive elements. The first type was characterized by internal deletions. Three sequences with deletions, RL2822, L15
5, and MK
208 (belonging to the D subfamily), were identified in three different formae speciales (fig. 3
). Surprisingly, each of these possessed the same 327-bp deletion, and these truncated elements were highly similar at the nucleotide level. The deletion occurred within a 7-bp motif present at each deletion point in full-length elements (fig. 4
). Translations revealed that the reading frame was maintained in two of these copies. Using inverse PCR, we determined that all three copies were inserted at the same genomic position. Thus, these copies result from vertical transmission of an ancestral deleted copy.
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Discussion |
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Diversity Among Subfamilies
Potentially active elements (with no interruption in the sequenced coding frame) have been identified in subfamilies E, D, and F. Inactive elements were found in all subfamilies and represent the majority of the sequences. Inactivity mainly results from stop codons and frameshift mutations. However, we detected other alterations resulting from large deletions or a high rate of transitions. All of these data suggest that the impala family is genetically diverse.
Three elements, containing the same internal deletion, were identified in three strains with different host specificities. These elements were located at the same chromosomal position and clearly arose by vertical transmission from a common ancestor that contained this deleted copy. Location of the deletion between two repeats of 7 bp suggests mechanisms similar to those put forward for several other deleted transposable elements (O'Hare and Rubin 1983
; Streck, MacGaffey, and Beckendorf 1986
; MacRae and Clegg 1992
). One is homologous recombination between short repeats, from one element or from copies on sister chromatids (Streck, MacGaffey, and Beckendorf 1986
). Another is interruption of the gap repair mechanism that takes place after excision of the element (Kurkulos et al. 1994
; Hsia and Schnable 1996
; Rubin and Levy 1997
).
Diversity among subfamilies is also illustrated by the identification of several highly mutated elements in the E and K subfamilies. Alterations (CG-to-TA transitions) resemble those associated with RIP, a mutational process described in N. crassa (Selker et al. 1987
). This process acts on duplicated sequences in the same nucleus during the sexual phase. RIP-like processes have also been identified in other ascomycetous fungi, Aspergillus fumigatus (Neuvéglise et al. 1996
), M. grisea (Nakayashiki et al. 1999
), and Podospora anserina (Hamann, Feller, and Osiewacz 2000)
. Aspergillus fumigatus, like F. oxysporum, is an asexual fungus. Although the type of alteration is the same, the RIP processes in all of these species differ in target preference. In N. crassa, C-to-T transitions occur with decreasing frequencies in CpA > CpT > CpG > CpC (Cambareri et al. 1989
). C-to-T transitions are found mainly in (A/T)pCp(A/T) in M. grisea. In F. oxysporum mutations into CpA and CpG were preferred, and we also observed in the 5' flanks of mutated C's a preference for A, T, and, to a lesser extent, C. The de-RIPped sequences confirmed that RL4-110 and M11-6 belong to the E subfamily (99.8% and 98% identity with impE, respectively). The de-RIPped copy Ci-16(dRIP) still showed 7% nucleotide divergence from Ci-36, suggesting that Ci-16 is not a ripped version of Ci-36 and comes from another copy, not identified during this work. This putative element could be a divergent member of the K subfamily or a member of another new subfamily. Taking into account that subfamilies usually diverge from each other by 20%30%, the three ripped elements can be considered to belong to the K subfamily. Whereas the distributions of RIP in copies impB, RL4-110, and M11-6 are different, impB and its homologs, as well as the three copies in the K subfamilies, share nearly identical mutational patterns. In these two cases, the mutational process appears to have occurred in a common ancestor of the strains, since all copies homologous to impB are located at the same genomic position, as are the three ripped copies of subfamily K. Ripped copies appear to be the only remnant of impala in strains M11 and RL4 (see hybridization results in fig. 2B
). Strains M24 and Ci contain ripped and nonripped elements from the same subfamily. At least in these strains, the RIP-like process may have acted transiently, with a possible reinvasion of impala.
Impala Evolution and Phylogenetic Relationship Within the F. oxysporum Complex
The presence of highly similar impala elements in strains belonging to different formae speciales raised the question of the evolutionary origin of these strains. We constructed a phylogeny with the nuclear gene EF1, chosen because of its demonstrated utility for phylogeny reconstruction within this complex (O'Donnell et al. 1998
). We showed that except for strain MK, discussed below, strains containing impala elements at the same genomic position are genetically related on the basis of the EF1
gene tree. This result provides evidence that strains may be more closely related than assumed by their host specificities. For instance, the group of strains related to M24 exhibits pathogenic specificities to a wide range of plants. This suggests that pathogenicity shifts are relatively frequent and raises questions concerning the genetic bases of such a versatile pathogenic behavior. The polyphyletic origins of some formae speciales, notably of melonis (O'Donnell et al. 1998
), were also confirmed in this study. Strain MK was previously found to be different from other melonis strains based on VCG and mtDNA haplotype analysis (Jacobson and Gordon 1990
). We showed here that this strain, collected in Mexico, is actually closely related to strain L15, a pathogen of tomato collected in North Africa.
The phylogenetic data help clarify the evolutionary history of the impala family. The presence of copies at the same genomic location in closely related strains strongly suggests that these copies were inserted in a common ancestor. Absence of these copies in other related strains might then indicate that they were lost, either by excision (for impA and impE) or by deletion or rearrangement of the region (for impD). Stochastic loss is also suggested by the fact that some strains lack some subfamilies and by the fact that some rare strains appear to be devoid of impala. However, the existence of impala elements belonging to more widely divergent subfamilies is not completely excluded. Too-divergent copies would be undetectable in standard Southern experiments or by PCR amplification.
Another mechanism that may play a role in transposable element evolution is horizontal transfer. This is suggested for several transposable elements, with the most convincing examples being illustrated by the P element from Drosophila (Daniels et al. 1990
; Clark and Kidwell 1997
; Silva and Kidwell 2000
) and by the widely spread mariner element (Lohe et al. 1995
; Robertson and Lampe 1995b
). Members of this family have been found to be more similar among distantly related species than within a species. In the absence of strong phylogenetic support, horizontal transfer is not easily demonstrated. The widespread distribution of the different subfamilies is likely the result of an ancestral polymorphism. The horizontal transfer of one or more subfamilies is not excluded, but investigations on closely related species will be required for assessment of this question. Within the F. oxysporum complex, the distribution of different elements (ripped, deleted, or at a given position) is also suggestive of a vertical transmission, except in the case of impG in strain MK. This strain does not appear to be closely related to the other melonis strains on the basis of the EF1
analysis. Nevertheless, it contains the copy impG, detected only in a small group of melonis strains. Moreover, this strain contains a molecular marker (the sfo gene, homologous to the yeast SUR1 gene; Hua-Van et al. 2000)
, which has thus far been detected only in melonis strains (unpublished data). This gene is absent in all non-melonis strains, even those closely related to M24, and it is located 10 kb upstream of impG in M24. The presence of this gene and impG in MK suggests that the whole region could be conserved between MK and M24. However, this region, which is extremely rich in repeated sequences, is characterized by several apparent recombination events and is apparently subject to rapid reorganization (Hua-Van et al. 2000)
. Therefore, the possibility that the entire region surrounding impG in M24 could be present in MK seems rather surprising and raises the possibility of the genetic transfer of a large piece of DNA from the M24 group to MK. However, further analyses are required to test this hypothesis.
Impala as a Marker of Genetic Relationships
Identification of closely related elements (by their sequences or by their genomic positions) in different strains raises the question of whether impala could be used as a marker for inferring genetic relationships. The study of specific fixed impala elements appears to be a good strategy to detect close relationships. However, the example of strain MK indicates that some exceptions can occur. Therefore, the use of impala as a marker for genetic relationships can be very helpful in detecting unsuspected relationships, but it has to be used along with, or confirmed by, other markers, such as single-copy nuclear genes.
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Acknowledgements |
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Footnotes |
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1 Present address: Institut de Biotechnologie des Plantes, Université Paris-Sud, Orsay, France.
2 Keywords: transposable element
filamentous fungi
Fusarium oxysporum
Tc1-mariner superfamily
evolution
repeat-induced point mutation
3 Address for correspondence and reprints: Marie-Josée Daboussi, Institut de Génétique et Microbiologie, Université Paris-Sud, 91405 Orsay cedex, France. daboussi{at}igmors.u-psud.fr
.
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