Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants
© Barkman et al; licensee BioMed Central Ltd. 2007
Received: 30 May 2007
Accepted: 21 December 2007
Published: 21 December 2007
Some of the most difficult phylogenetic questions in evolutionary biology involve identification of the free-living relatives of parasitic organisms, particularly those of parasitic flowering plants. Consequently, the number of origins of parasitism and the phylogenetic distribution of the heterotrophic lifestyle among angiosperm lineages is unclear.
Here we report the results of a phylogenetic analysis of 102 species of seed plants designed to infer the position of all haustorial parasitic angiosperm lineages using three mitochondrial genes: atp1, coxI, and matR. Overall, the mtDNA phylogeny agrees with independent studies in terms of non-parasitic plant relationships and reveals at least 11 independent origins of parasitism in angiosperms, eight of which consist entirely of holoparasitic species that lack photosynthetic ability. From these results, it can be inferred that modern-day parasites have disproportionately evolved in certain lineages and that the endoparasitic habit has arisen by convergence in four clades. In addition, reduced taxon, single gene analyses revealed multiple horizontal transfers of atp1 from host to parasite lineage, suggesting that parasites may be important vectors of horizontal gene transfer in angiosperms. Furthermore, in Pilostyles we show evidence for a recent host-to-parasite atp1 transfer based on a chimeric gene sequence that indicates multiple historical xenologous gene acquisitions have occurred in this endoparasite. Finally, the phylogenetic relationships inferred for parasites indicate that the origins of parasitism in angiosperms are strongly correlated with horizontal acquisitions of the invasive coxI group I intron.
Collectively, these results indicate that the parasitic lifestyle has arisen repeatedly in angiosperm evolutionary history and results in increasing parasite genomic chimerism over time.
The parasitic lifestyle has evolved repeatedly in nearly every major lineage of life, and in the broad sense includes brood parasitism, social parasitism, genomic parasitism, and nutritional parasitism [1, 2]. Among plants, nutritional parasites obtain water and nutrients directly from their photosynthetic host plant through a specialized feeding structure, the haustorium, which is attached to either host shoots or roots . These plants include both hemiparasites (parasites with the ability to photosynthesize) and holoparasites (those that cannot photosynthesize) . While both hemi- and some holoparasites grow largely exterior to the host, certain holoparasites grow nearly completely embedded within the host plant tissues as endoparasites, emerging only during sexual reproduction [3, 4]. Though most parasites can be classified according to their photosynthetic status and the nature of their interactions with their hosts, insight into the evolution of parasitic traits has been hampered by the lack of a broad phylogenetic perspective.
The parasitic lifestyle is thought to have evolved 8  to 11  times in flowering plants, but comprehensive phylogenetic analyses have never been performed to investigate the evolutionary frequency and pattern of the shift to heterotrophy in angiosperms. The lack of a robust phylogenetic hypothesis for parasitic angiosperms has also hampered studies of genome evolution  and the inference of ancestral conditions that may have promoted the evolution of the haustorial parasitic lifestyle. Furthermore, although considerable progress has been made towards the molecular systematics of many parasitic plants [5, 7–12], several parasites have obscure positions within angiosperm phylogeny, accounting for 7 of 18 unplaced taxa in the recent molecularly-based ordinal classification of flowering plants .
Classifying parasitic plants using morphological characters has long been difficult because of the extreme reduction or alteration of vegetative and floral morphology that occurs in holoparasitic lineages [3, 14]. The primary challenge associated with inferring the phylogenetic placement of many parasites using molecular data in a global angiosperm context is spurious long-branch attraction  caused by their highly divergent DNA sequences [5, 11]. Furthermore, the apparent loss of photosynthetic and other genes that have been commonly used to study flowering plant phylogeny [5, 6, 16] has prevented the inclusion of many parasites in otherwise comprehensive studies [13, 17, 18]. A possible solution to these phylogenetic problems is through the study of plant mtDNA, which is retained regardless of photosynthetic ability and has proven useful for determining the phylogenetic affinities of some parasitic plants [10–12]. To infer the number of origins and distribution of parasitism in a global angiosperm phylogenetic context we used three mtDNA genes:atp1, coxI, and matR.
While mtDNA may offer several advantages for the study of parasitic plants, its use necessitates careful consideration of the possibility of horizontal gene transfer (HGT) [19–26]. Of particular relevance to our study are reports that mitochondrial genes may be horizontally transferred between hosts and parasites [21, 23, 25, 27]. Also, the invasive mitochondrial coxI group I intron (which is lacking from most plants) has been independently, horizontally acquired from unknown vectors in various flowering plants . One consequence of such transfers is that parasites may appear closely related to their hosts, thereby obscuring their true phylogenies; however, if such occurrences are relatively uncommon, the majority of loci should correctly predict the phylogenetic positions of most parasites. Our multigene approach coupled with broad angiosperm ordinal sampling will allow us to estimate the number of parasitic plant origins in flowering plant phylogeny, interpret potential horizontal transfers of foreign mtDNA into parasitic plant genomes and discern whether parasites are more likely to horizontally acquire DNA than non-parasites.
Phylogenetic placement of parasites
Within this phylogenetic framework, it appears that haustorial parasitism has arisen at least 12 independent times as indicated by the orange (mostly hemiparasitic) and red (holoparasitic) branches (Fig. 1). It is not clear whether parasitism arose once in the ancestor of Balanophoraceae + Santalales or if the parasitic lifestyle independently evolved in the two lineages because the earliest diverging branches of Santalales are not parasitic and it is unlikely that parasitism is a reversible trait . Thus, it is possible that there are actually 13 origins of parasitism implied by this tree (Fig. 1). Because some parasite phylogenetic positions did not receive high bootstrap support, we attempted to discern whether a hypothesis of fewer than 12 origins of parasitism could be rejected. Trees that constrained Apodanthaceae + Cynomoriaceae + Santalales + Balanophoraceae to be monophyletic in any of the three positions shown in Fig. 1 were rejected by the S-H test as significantly worse than the unconstrained tree of Fig. 1 (P < 0.05 in all cases). Trees that constrained the position of Apodanthaceae as sister to Cynomoriaceae or Santalales were significantly worse than the optimal tree of Fig. 1 (P < 0.05). Trees constraining the position of Santalales + Balanophoraceae with Apodanthaceae were significantly worse than the optimal tree (P < 0.05) while a position sister to Cynomoriaceae could not be rejected. Finally, trees that constrained the position of Cynomoriaceae-only to be sister to either Apodanthaceae or Santalales + Balanophoraceae were not significantly different from the optimal tree shown in Fig. 1. Thus, these data suggest that there were as few as 11, or as many as 13, origins of parasitism in angiosperm evolutionary history.
The phylogenetic tree shown in Fig. 1 also reveals a surprising feature of parasite evolution: endoparasitism has arisen in four independent lineages. These four lineages, marked by an "E" in Figure 1, include Apodanthaceae, Rafflesiaceae, Cytinaceae, and Mitrastemonaceae (hereafter referred to as "endoparasites"). Because these four endoparasite families have traditionally been included in Rafflesiaceae it was previously assumed that endoparasitism was uniquely derived , although several recent studies have shown that these families are not closely related [11, 21, 23, 31]. Figure 1 clearly indicates that the endoparasites are not monophyletic. In fact, trees that constrained the endoparasite clade to be monophyletic in any of the four positions shown in Fig. 1 were rejected by the S-H test as significantly worse than the unconstrained tree of Fig. 1 (P < 0.05 in all cases).
Putative horizontal transfer of atp1
coxI intron acquisition in parasitic plants
Phylogenetic aspects of parasitism
The pattern of evolution of haustorial parasitism in angiosperms is striking in several regards. First, it appears that parasitism has evolved repeatedly in many major groups of flowering plants from magnoliids to derived eudicot lineages, and most of these lineages (8 of 11–13) now consist entirely of nonphotosynthetic parasites. However, monocots, campanulids, and caryophyllids (ca. 22%, 12%, and 7% of angiosperm diversity, respectively) have never evolved parasitism or else retain no extant parasitic representatives. In contrast, within lamiids alone (ca. 12% of angiosperm diversity), parasitism has independently evolved 3 times including both shoot (Cuscuta) and root (Orobanchaceae and Lennoaceae) parasites, although this may not be statistically different from zero. Why some lineages have a propensity to become parasitic is not clear; however, the strong correlation of the distribution of the coxI intron (which, at the ordinal level, is also rare in monocot and campanulid orders, but rich throughout rosid and lamiid orders) with the independent origins of parasitism (Fig. 1 and 6) is tantalizing and will be discussed below. Second, the highly specialized trait of endoparasitism , in which most of the vegetative portion of the parasite lives inside of its host with emergence occurring during sexual reproduction, has evolved independently in at least 4 lineages, Mitrastemonaceae, Cytinaceae, Rafflesiaceae, and Apodanthaceae. Furthermore, although not studied here, Arceuthobium (Santalales) is endoparasitic . Evolutionary convergence of the endoparasitic lifestyle in one-third of the parasitic angiosperm lineages and only in the most derived species of Santalales suggests this may be a common adaptive peak of parasite-host relationships. As in animals, a selective advantage of the endoparasitic mode for plants may be to avoid predators (herbivores) and live in a homeostatic environment . Third, this ordinal level-placement of all parasitic angiosperms (except Cynomorium), corroborates other recent studies and together resolve many long-standing taxonomic questions. Thus, revisions of existing classifications are needed to include many of these parasites in orders they have not been placed in previously. This is particularly true of Rafflesiaceae, Mitrastemonaceae, Cytinaceae, and Apodanthaceae. Further work is required to refine the positions of most parasitic plants within their orders. However, use of mtDNA will require cognizance of the possibilities of HGT from host-to-parasite  and also from parasite-to-host [25, 27]. Surprisingly, in spite of the conflicting nature of atp1 relative to coxI and matR in the endoparasites Rafflesiaceae and Mitrastemonaceae, confident placements were obtained in the combined analyses. In contrast, the position of Cynomorium is obscured by the conflicting phylogenetic positions implied by matR (Saxifragales) and coxI + atp1 (Sapindales). This conflict could suggest possible horizontal transfer (HGT) of matR or both coxI and atp1 in Cynomorium; however, neither Sapindalean nor Saxifragalean hosts have been described in the literature to our knowledge. A placement of Cynomorium with Saxifragales has been suggested by 18S as well as matR .
Multiple Horizontal Gene Transfers of atp1
One of the major predicted consequences of long-term parasitic interactions is that genetic transfer will occur between host and parasite [1, 2, 38]. Although evidence to support this hypothesis has been scarce in eukaryotes, the phylogenetic evidence we present from atp1 of endoparasitic plants is consistent with this prediction. While HGT is plausible from host-to-parasite, it is not clear that such transfers should be advantageous to recipients. One possibility in parasites is that if their native mt loci were degenerate but could have been replaced by a highly conserved copy, then transfer should be strongly selected for because it would help ensure efficient metabolism in these extreme holoparasites. Yet, there is no statistical evidence for this hypothesis in the chimeric atp1 sequences of Pilostyles because the retained portions of the presumably older caesalpiniod xenolog (regions I) are not divergent at nonsynonymous sites relative to photosynthetic plants. Regardless of any potential selective advantage of HGT, it appears that atp1 is mobile because of the multiple transfers that we and others have reported [19, 23, 27]. Because atp1 appears to be located near sites of recombination in some plants , its mobility may be facilitated. Further support for HGT in parasitic plants may come from surveys of other genes, particularly from the nuclear genome of these parasites.
The close phylogenetic relationships of atp1 between endoparasites and their hosts, the statistically significant phylogenetic conflict of atp1 relative to matR + coxI, and the differential evolutionary dynamics of atp1 relative to coxI and matR, suggest that atp1 has been acquired horizontally in Rafflesia + Rhizanthes, Pilostyles, and Mitrastema from their respective host lineages. The possibility of HGT of plant mtDNA, including atp1, has been raised in other angiosperms [19–23] and seems a likely explanation for our results for several reasons. First, the horizontal transfer of macromolecules, including RNA, from host plant to parasitic plant has been shown to occur experimentally [40, 41]. Second, these parasites (Rafflesia, Rhizanthes, Pilostyles, and Mitrastema) are wholly endoparasitic angiosperms; they vegetatively grow completely embedded within their hosts to enhance the acquisition of water, nutrients, and complex macromolecules. Third, because reproductive tissues arise from the endophytic vegetative tissue in these species, cells that carry horizontally acquired host DNA are likely to give rise to reproductive meristems and transmit the new DNA to future generations of the parasitic plant. Future studies should aim to determine if a native copy of atp1 still exists in these parasites and characterize the genomic location and flanking sequence of putatively transferred sequences.
coxI intron invasion and genomic chimerism
Although there have been multiple horizontal acquisitions of the homing coxI intron throughout angiosperm history , it is clear that this invasive sequence is more prone to invade some angiosperm lineages than others (eg. lamiids and parasites). While the source of the intron is unclear in the parasites (and angiosperms in general ), the acquisition of foreign DNA has been predicted to be a key event in the evolution of parasitic angiosperms , and this intron could represent a marker of a genomically more widespread historical transformation. This is a particularly interesting possibility because the coxI intron in angiosperms is most closely related to those known from fungi and the evolution of haustorial parasitism has been hypothesized to have occurred via a mycoheterotrophic antecedent relationship . Recently, genomic comparisons have revealed that the shift to parasitism in nematodes may have been facilitated by the recent acquisition of foreign DNA from bacteria . Whether the acquisition of foreign DNA was a key step in the evolution of parasitism in plants awaits genomic studies of these parasites.
Genomic chimerism among angiosperms is probable given that there have been multiple origins of parasitism throughout flowering plant history and that HGT is possible from host to parasite  and vice versa . Although some parasitic lineages are highly host specific, many others have a broad range of potential host species (Fig 7), and host shifting is to be expected through the history of individual parasite lineages [1–3]. Therefore, even if HGT between plant parasites and their hosts is very rare, through time this could result in plant genomes that are complex chimeras of horizontally as well as vertically acquired sequences.
We sampled representatives of at least one family from 44 of 45 orders from the recent ordinal classification of angiosperms . In total, 102 seed plant species from 92 angiosperm families were represented in addition to every major parasitic plant group [3, 5]. Three gymnosperms, Pinus, Ginkgo, and Zamia, were included as outgroups to root phylogenetic estimates. Although we attempted to use the same DNA for all gene isolation, some composite taxa were used in our analyses (see Additional file 1). In the case of one of our samples of Malpighiales, Euphorbia milli was used for matR and Croton alabamensis for coxI and atp1. In the case of Malvales, Alcea rosea was used for matR and Althaea officinalis for coxI and atp1. In the rest of the cases, we isolated the 3 genes from the same DNA or different species of the same genus (see Additional file 1).
General molecular methods, including DNA extraction, PCR, and DNA sequencing were performed as previously described [11, 43]. The basic RNA extraction and RT-PCR procedures followed published methods . Great care was taken to limit the possibility of host plant or other contamination of the parasitic plant DNA samples, including careful dissection of tissues distal to the host-parasite interface as well using multiple independent isolations from two laboratories and/or related species or genera. Furthermore, we also sampled the host plant individuals of the holoparasites, Rafflesia pricei (Tetrastigma diepenhorstii), Mitrastema yamamotoi (Quercus subsericea), and Pilostyles thurberi (AZ) (Psorothamnus emoryi) so they could be directly compared. This is a critical aspect of our study and is absolutely necessary in order to discriminate between putative cases of horizontal gene transfer and contamination or the presence of phloem-mobile nucleic acids taken up by parasites. Please see Additional files 1 and 2 for the voucher numbers and GenBank accession numbers for all of the sequences included in this study. In total, 188 new mtDNA sequences were generated.
ClustalX  was used to produce preliminary sequence alignments followed by minor manual adjustments. Regions of uncertain alignment from all three genes, coxI intron sequences , and known RNA editing sites for atp1 and coxI were excluded prior to analysis . Modeltest v3.06  was used to determine the best-fit model of nucleotide substitution for each data set analyzed; these models were implemented during maximum likelihood (ML) analyses with PAUP*4.0 . ML heuristic searches used 10 random addition sequences and TBR swapping. Support values could not be determined using ML because of the large computation time required, so bootstrap support (BP) values were obtained using GARLI  from 100 replicates using an automated stopping criterion set to 5,000 generations. Bayesian analyses were performed using MrBayes v3.0b4 . Five chains were simultaneously run for one million generations and these were sampled every 100 generations. The first 10,000 generations were discarded as the "burn-in" period because of convergence lnL after this point and posterior probabilities (PP) for individual clades were then obtained from the remaining samples. Corrected pairwise divergences were calculated using the optimal models of nucleotide substitution determined by Modeltest for each gene separately. The S-H test  was used to test for statistically significant differences among competing topological hypotheses. Putative gene conversion events were identified using GeneConv . The concentrated changes test  was used to test for non-random association between parasitism and the presence of the coxI intron by first tracing the intron distribution onto the tree in Fig. 1 or Fig. 6. We tested the null hypothesis that gains and losses of parasitism are randomly distributed over the angiosperm phylogenetic tree. Probabilities for the 10 gains and 0 losses of parasitism occurring in lineages that possess the coxI intron were then determined by 1,000 simulations.
The authors thank J. Leebens-Mack and D. Cowan for valuable discussion, and K. Mat Salleh, D. Goldman, John La Duke, Billie Turner, Beryl B. Simpson, R. A. Smith, D. Olmstead, L. Musselman, G. Yatskievych, J. Hoder, K. Steiner, D. Nickrent, Siam Lakasa, Jamili Nais, Tony Omeis and the Biology Greenhouses at Penn State University, Missouri Botanical Gardens and the Berkeley Botanical Gardens for plant materials. This work was supported by the Faculty Research and Creative Activities Support Fund of Western Michigan University (to T.J.B.), a grant from the National Science Foundation (to C.W.D. and N.D.Y.) and the Department of Biology of Penn State University.
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