Department of Plant Pathology, University of California, Riverside
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Abstract |
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Introduction |
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The molecular biology of oomycetes began to be investigated only recently, but an interesting finding has been that their genomes are larger than those of most lower eukaryotes and contain substantial repetitive DNA. Most studies have involved Phytophthora, in which genomes vary in size from 6.2 x 107 to 2.4 x 108 bp and contain 50% or more repetitive DNA (Tooley and Therrien 1987
; Mao and Tyler 1991
). A survey in P. infestans indicated that some repeated DNA contains reverse transcriptase motifs, suggesting that this repeated DNA evolved from retroelements (Judelson and Randall 1998
).
To identify factors that have shaped the evolution and genetics of Phytophthora, we are characterizing the nature of its transposable elements. It is also anticipated that this will lead to the development of new molecular tools and an understanding of the phenotypic instability of isolates, in which sectoring for growth rate, morphology, virulence, and other traits are reported (Stamps 1953
; Buddenhagen 1958
; Erwin et al. 1963
). Transposable elements are known to be a major source of spontaneous variation and mutation in many eukaryotes (Bennetzen 2000
). In addition, transposable elements may alter chromosome structure by expanding the size of genomes through amplification and by providing regions of homology for illegitimate recombination (Sanmiguel et al. 1998
). This may be a driving force in speciation (Loennig and Saedler 1997
; Hurst and Schilthuizen 1998
). Indeed, comparing the phylogenies of transposable elements and their hosts is useful for analyzing the evolutionary characteristics of both (Kossida et al. 2000
).
This study describes a family of repeated DNA within Phytophthora that resemble the Ty3/Gypsy group of retrotransposons, which were detected in 29 of 37 species tested. The family appears to have been a major force in the evolution of Phytophthora chromosomes, representing a miniscule part of the genome in some taxa and as much as 25% in others. Distinct evolutionary lineages of the retroelementlike sequence were identified, showing significant intraspecific and interspecific variation. Some relationships between lineages matched phylogenies of species within the genus, whereas others represented either basal lineages predating speciation within Phytophthora or horizontal transfer events. Most elements appeared to be defective.
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Materials and Methods |
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DNA Hybridization
Gel blots of genomic DNA, and replicas of colonies from a bacterial artificial chromosome (BAC) library (Randall and Judelson 1999
), were prepared on nylon membranes as described (Judelson and Fabritius 2000
). Dot-blots were made by placing genomic DNA (100 µg/µl) or appropriate standards in a microtiter dish in 10 x SSPE (SSPE is 0.18 M NaCl, 10 mM NaH2PO4, 1 mM EDTA) plus 0.1 µg/ml SybrGold (Molecular Probes, Eugene, Ore.). These were spotted to replicate membranes using a slotted, surfactant-treated 96-pin tool designed to deliver 0.5 µl (V&P Scientific, San Diego, Calif.). To correct for errors in initial DNA quantitations, bound DNA was quantitated under long-wave UV light using a Fluor-S camera and QuantityOne software for Macintosh (Biorad, Richmond, Calif.). Membranes were prepared for hybridization by soaking each membrane for 10 min in 0.4 M NaOH followed by 3 x SSPE, hybridized as described (Judelson and Fabritius 2000
), and washed at 50°C in 1 x SSPE, 0.3% sodium dodecyl sulfate, 0.1% sodium pyrophosphate. Signals were detected by phosphorimager analysis and quantified using QuantityOne software (Biorad).
Sequencing of PCR Products and BAC Clones
Retroelement fragments obtained by PCR were cloned into pGEMT-EZ (Promega, Madison, Wis.) and sequenced using T7 and SP6 primers. A region of genomic DNA cross-hybridizing with the retroelement was isolated from a BAC clone and subcloned as HindIII and XbaI-BglII fragments in pBS-KS2+ (Stratagene, La Jolla, Calif.), which were sequenced in both directions by primer walking. Sequences were assembled using Seqman for Macintosh (DNASTAR, Madison, Wis.). Sequences were deposited in GenBank under accession numbers AF490269AF490339.
Alignments and Phylogenetic Analysis
Preliminary studies were performed using the Alignment program of Vector NTI (Informax, Bethesda, Md.). Data were then reformatted and analyzed using programs from the PHYLIP 3.57c package for Macintosh (distributed by J. Felsenstein, Department of Genetics, University of Washington, Seattle). For DNA-based phylogenies, a consensus tree was developed from 1,000 bootstrapped data sets using DNADIST followed by NEIGHBOR (Neighbor-Joining option) and CONSENSE. Protein phylogenies were developed from 1,000 bootstrapped data sets analyzed using the PROTDIST program (PAM matrix) followed by CONSENSE.
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Results |
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Alternatives were tested for amplifying the region from the nine species recalcitrant to PCR with RetroA and RetroB. This included using RetroA, RetroB, and other specific primers at reduced annealing temperatures, or degenerate primers. Success was realized only for P. lateralis, using degenerate primers. That the DNA from the eight remaining refractory species was suitable for amplification was confirmed by PCR using random amplified polymorphic DNA and ITS primers.
Relationships Between Family Members
The evolution of the retroelementlike family within Phytophthora was examined by comparing 75 clones. These generally included two to three elements for each of the 29 species. The sequences were aligned and a phylogenetic tree was developed (fig. 1
).
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Whereas retroelementlike sequences generally did not cluster with those from the same species, the phylogram revealed strong relationships between related species. This was most obvious for sequences from P. infestans, P. mirabilis, and P. phaseoli, which are shown at the bottom of figure 1
. These species reside in Group IV of the Waterhouse scheme, and analyses of ITS and other loci confirmed their close association (Moeller, De Cock, and Prell 1993
; Tooley, Carras, and Falkenstein 1996
). To help explore the relationship between these three species, 23 retroelementlike sequences were analyzed. All 23 intermingled within the phylogram, reflecting the evolution of lineages predating the radiation of the three species from their common ancestor. That distinct sublineages were already present in such an ancestor is suggested by the low bootstrap values obtained for many nodes. These sequences did not have affinity with the retroelementlike sequences from another Group IV species, P. colocasiae, and other Group IV members such as P. ilicis and P. hibernalis were negative in PCR. This confirms ITS-based data that contend that the P. infestanslike group (ITS clade 1c) is poorly related to such other Group IV taxa, which lie in ITS clades 2 and 3 (Cooke et al. 2000
).
Other clusters were also evident, such as between members of Waterhouse Groups II and III (including ITS clades 2 and 5) and between Groups V and VI (ITS clades 7a and 8a). Exceptions to such patterns were also noted. For example, the P. erythroseptica 340 sequence (Group VI) clustered with Group V and VI sequences, whereas P. erythroseptica 6180 resided in a clade largely from Groups II and III. This latter clade includes two additional Group VI sequences (P. vignae 7825 and P. cambivora 6412), suggesting that it may represent a retroelement lineage that predates radiation of the Group II-III and Group V-VI clades, or which underwent horizontal transfer. That such observations were not an artifact of isolate misidentification was shown by ITS analyses.
Nature of Differences Between Family Members
Several molecular phenomena distinguish the different retroelementlike lineages. A combination of base changes, insertions, and deletions were observed. These changes, and particularly the insertions and deletions, support many conclusions drawn from the phylogram. For example, a cluster of five sequences from P. infestans, P. mirabilis, and P. phaseoli, presumed to represent a lineage predating radiation of those species, was supported by the observation that they each contained the same novel deletions and insertions (not shown). Excluding gaps, the mean nucleotide divergence was 16.7%.
The potential translation products of the sequences were determined and compared with that of functional reverse transcriptase polyproteins. Nearly all contained frameshifts or stop mutations. This indicated that most were obtained from defective elements.
Copy Number of Element
Extraordinary divergence in the abundance of the retroelement sequence in different species of Phytophthora was revealed using dot-blot assays (fig. 2
) and blots of gels of genomic DNA (not shown). For the dot-blots, genomic DNA and standards for copy number were spotted on a membrane that was hybridized at low stringency with a 32P-labeled "average" retroelement probe. This probe and the copy number standard were made by pooling DNA from 24 sequences representing each subclade in figure 1
.
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The values shown in figure 2
represent only estimates of copies per genome for two reasons. Firstly, the calculations invoke a 108-bp genome, which was selected on the basis of the Phytophthora species measured to date which include P. infestans at 2.4 x 108 bp (Tooley and Therrien 1987
), P. porri at 1.2 x 108 bp (F. Mauch, personal communication), and P. sojae at 6.2 x 107 bp (Mao and Tyler 1991
). Secondly, not all of the 24 sequences in the probe may have hybridized to all potential targets at maximum efficiency. Nevertheless, copy values from the dot-blot approach were similar to values from alternative methods. For example, whereas the dot-blots indicated that P. infestans contained 32 copies per genome (correcting for its known genome size), a value of 25 copies was calculated from the fraction of colonies from a BAC library that hybridized to the probe. Secondly, the value calculated for P. cinnamomi from dot-blots hybridized with the 24-sequence probe was only 24% less than that obtained using a P. cinnamomiderived probe (not shown).
The enormous interspecific variation in copy number was confirmed by analyzing blots of electrophoresed genomic DNA (not shown). Using the 24-sequence probe, for example, massive hybridization was observed against P. cinnamomi, P. cambivora, and P. iranica which were calculated from dot-blots to have >6,000 copies each. In contrast, very low hybridization was recorded against P. infestans, P. megasperma, and P. porri, which were calculated to have 35 copies. This intensity difference was not an artifact of some bias caused by using the 24-sequence probe. For example, a probe based on P. infestans sequences showed much greater hybridization against DNA from P. iranica than against DNA from P. infestans. These blots also confirmed the absence of cross-hybridizing sequences in the species negative in PCR including P. humicola, P. ilicis, P. macrochlamydospora, P. quininea, and P. richardiae.
Distribution of Family in P. infestans
The retroelementlike family appeared to be dispersed throughout the genome of P. infestans, based on the patterns of hybridization observed in blots of genomic DNA restricted with different enzymes plus analyses of BAC clones isolated by hybridization with the 24-sequence probe. In genomic blots, for example, the pattern observed was consistent with a dispersed pattern or a localized array of highly variable sequences (fig. 3
, left). The dispersed pattern seemed more likely, however, because only single bands were observed in restriction digests of the BACs (fig. 3
, right).
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Detailed Analysis of Individual Family Members in P. infestans
The majority of elements in P. infestans appeared defective, based on sequencing portions of the retroelementlike loci from the 12 BAC clones. Eleven loci were quickly shown to have frameshift or nonsense mutations. The remaining clone first appeared to contain an intact retroelement on the basis of the presence of >1 kb of an intact reading frame and was therefore analyzed in detail. However, subsequent data showed that it also contained frameshift and nonsense mutations and was truncated (fig. 4
).
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To test for activity of the retroelementlike family, both the 24-sequence pooled probe and the one derived from six P. infestans elements were hybridized to blots of DNA of 20 genetically and geographically diverse isolates of P. infestans. Patterns in HindIII and PvuII digests were monomorphic, consistent with a lack of recent transposition (not shown). Nevertheless, a weak 5-kb transcript was detected in RNA blots, and relatives were present in an expressed sequence tag database (EST) of P. infestans (not shown). Also, possible historical transposition activity was revealed by observing that the 5' end of the right-facing element bordered a truncated version of a sequence in the EST database (94% identity). The data were consistent with a deletion of the 3' two-thirds of a gene that predated the retroelement at the locus, as shown in figure 4 .
The P. infestans elements were compared with those from other organisms by generating a phylogram incorporating reverse transcriptasecontaining viruses and retrotransposons (fig. 5
). The two P. infestans retroelementlike sequences, labeled as PIRETA and PIRETB, had the strongest affinity with the Ty3/Gypsy group and especially those of plant origin defined as class B plant elements by Marin and Llorens (2000)
. The sequence closest to PIRETA and PIRETB fell into the Tma subfamily of Ty3/Gypsy elements from Arabidopsis (Marin and Llorens 2000
). It is consequently proposed that PIRETA and PIRETB had evolved from a long terminal repeat (LTR) retroelement, even though LTRs were absent from the copies that were sequenced.
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Discussion |
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The groupings of the retroelement sequences analyzed in this study cannot be used to unambiguously infer species phylogenies within Phytophthora because of the propensity of such elements for horizontal transfer and their multicopy nature. Moreover, for each species, only two or three retroelement sequences were analyzed; therefore, a full sampling of their diversity remains to be performed. Nevertheless, the retroelement data are generally congruent with most conclusions of the ITS-based phylogenies (Cooke et al. 2000
; Förster, Cummings, and Coffey 2000
). This includes their disagreement with some of the Waterhouse classifications, although in fairness it should be noted that Waterhouse recognized that her scheme might not always reflect true phylogenies (Waterhouse 1963
).
The spread of the element within the Phytophthora groups may have involved both vertical and horizontal transmission. Vertical distribution explains the similar phylogenies of many elements and host species, as illustrated by the cluster of P. infestans-P. mirabilis-P. phaseoli sequences. In contrast, those sequences from Group VI species that were close to Groups II and III may reflect horizontal transfer. Many Phytophthora species share the same environmental niche, facilitating horizontal transfer. In fact, there are examples of new species formed by natural interspecific hybridization (Man In't Veld et al. 1998
; Brasier, Cooke, and Duncan 1999
).
Interspecific variation in the copy number of the element was striking. At one extreme, PCR and hybridization assays identified species lacking the element. This was less surprising for P. insolita, P. macrochlamydospora, and P. richardiae than for P. humicola and P. ilicis because Cooke et al. (2000)
placed the first three in clades 9 and 10, far from other Phytophthora taxa (clades 18). Although there are contradictory data on this placement (Förster, Cummings, and Coffey 2000
), the ancestral retroelement may have inserted in the progenitor of the main Phytophthora clade, bypassing the P. insolita cluster. The absence of the element in P. humicola and P. ilicis, by contrast, is harder to reconcile because both are well rooted with element-containing species in both the Waterhouse and ITS phylogenies. The element could have been eliminated, before substantial amplification had occurred, by the loss of a chromosome arm, ectopic excision, or recombinational editing (Wichman et al. 1993
).
At the other extreme, species such as P. iranica and P. cactorum contained about 10,000 copies of the retroelementlike sequence. If the entire element were in the 5-kb range, this would likely account for >25% of their genomes. Cooke et al. (2000)
clustered these species in clades 1a and 1b; the much lower abundance in clade 1c species like P. infestans (2030 copies) helps fix the stage at which a burst of amplification likely occurred. The hypothesis that amplification was blocked in species like P. infestans is consistent with the truncations, frameshift mutations, and other defects found by this study. In species such as P. iranica, the Gypsy-like retroelement family possibly includes both full-length and truncated copies, as seen in organisms in other kingdoms (Marin and Llorens 2000
).
This study has presented the first comprehensive analysis of a family of transposable elementlike sequences distributed throughout Phytophthora. Besides the Gypsy relative revealed by this study, a copia-like sequence was previously reported from P. infestans (Tooley and Garfinkel 1996
). Additional types of retroelements likely reside within Phytophthora. Twelve distinct families of LTR retrotransposons exist in C. elegans, for example (Bowen and McDonald 1999
). Whether all transposable elements in Phytophthora are retroelements also remains to be determined. In yeast, retrotransposons are the only class of transposable elements (Sandmeyer 1998
), whereas plants contain elements replicating through either RNA or DNA intermediates (Bennetzen 2000
). Considering the taxonomic placement of oomycetes, it will be interesting to learn which paradigm best fits their genomes.
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Acknowledgements |
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Footnotes |
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Keywords: Gypsy
Phytophthora
oomycete
speciation
evolution
repeated DNA
Address for correspondence and reprints: Department of Plant Pathology, University of California, Riverside, California 92521. howard.judelson{at}ucr.edu
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