W. Martin, "Molecular evolution: Lateral gene transfer and other possibilities" (2005)

"Heredity" June 2005, Volume 94, Number 6, Pages 565-566; http://www.nature.com/cgi-taf/DynaPage.taf?file=/hdy/journal/v94/n6/full/6800659a.html

>                       Molecular evolution: Lateral gene transfer and other possibilities

W Martin1

1The Institute of Botany, University of Düsseldorf, Germany
>                       Correspondence to: W Martin, e-mail: <a href="mailto:[email protected]">[email protected]<a>

Heredity (2005) 94, 565-566. doi:10.1038/sj.hdy.6800659
>                       Published online 30 March 2005

>                       Two recent reports suggesting that extensive lateral gene transfer occurs among higher plants clash with our view of evolution as Darwin understood
>                       it. The concept of descent with modification has proven exquisitely robust, with
>                       only two genuine mechanistic additions to Darwin's principles of natural selection operating on variation among progeny, having emerged over the
>                       last 150 years. One is endosymbiosis, where highly divergent lineages merge outright, such as the origin of chloroplasts from cyanobacteria or the origin
>                       of mitochondria from proteobacteria. The other is lateral, or horizontal, gene transfer (LGT), where disparate lineages occasionally exchange parts of
>                       their genetic fabric. Genome sequences have provided sound evidence that both endosymbiosis among eukaryotes, and LGT - among prokaryotes -
>                       are indeed real, although there is still much debate as to just how frequently either has occurred during evolution. That debate now continues.
>                       In 2003, Bergthorsson's team reported sequences homologous to plant mitochondrial DNA (mtDNA) from a variety of species, obtained using
>                       polymerase chain reaction (PCR) with conserved primers against protein-coding regions of plant mtDNA. As some sequences in the
>                       phylogenies branched in very unusual positions, the authors concluded that frequent lateral transfer of mitochondrial DNA between distantly related
>                       plants had caused this pattern. Viruses, bacteria, fungi, insects, pollen, even meteorites and grafting were suggested as vectors for this exchange
>                       (Bergthorsson et al, 2003). The authors provided a figure showing genes being laterally transferred not only between species but also from ancient
>                       lineages in the past to more recent lineages, interpretations that 'imply the existence of the transferred gene in an intermediate, unidentified
>                       vectoring agent or host plant for millions of years' (Bergthorsson et al, 2003) - yet without mutation, one should add. Several of the unsually
>                       branching sequences involved the shrubby flowering plant Amborella trichopoda, prompting a more extensive search among DNA samples from
>                       this species. That follow-up study on Amborella has now appeared (Bergthorsson et al,
>                       2004) and is no less eyebrow-raising. Conserved primers were designed for the 31 protein-coding genes typical of higher plant mtDNA. In total, 20 of
>                       the 31 primer pairs generated two or more different PCR amplification products with Amborella DNA as the substrate and these mutiple products
>                       branched in disparate parts of the trees. Bergthorsson et al (2004) interpreted this as evidence for 'massive' LGT from a myriad of higher plant
>                       donors, and concluded that Amborella mtDNA 'has sustained proportionately more HGT than any other eukaryotic, or perhaps even
>                       prokaryotic, genome yet examined'. If true, this would be an unprecedented situation for three reasons. First, plant mitochondrial genome
>                       sequences have not yet provided evidence for the acquisition of genes from other species (Bergthorsson et al, 2004). Second, the Amborella
>                       chloroplast genome sequence reveals no acquisitions from other species (Goremykin et al, 2003). Third, no reports of widespread lateral acquisition
>                       from various higher plant donors have emerged from any plant nuclear genome sequenced so far. Is there really something special about
>                       Amborella that makes it an LGT-haven? Is higher plant mtDNA hopping among species faster than we can sequence it? Or are there possible
>                       alternative interpretations of the observations other than LGT? If we exclude DNA contamination from other sources as a possible factor in
>                       their results, as Bergthorsson's team (2003, 2004) did, we can still ask what positive evidence there is that the sequences in question are indeed
>                       incorporated in the Amborella mtDNA or nuclear genome to substantiate the LGT case. Specific hybridisation and cloning of the noncoding regions
>                       flanking the amplified sequences would have offered the opportunity to see how and where the LGT candidate sequences were integrated in
>                       unequivocally endogenous Amborella DNA. Flanking sequences as specific probes are needed in the case of plant mtDNA because it evolves at an
>                       inexplicably slow rate: across the deepest comparisons of flowering plants, sequences of mtDNA coding regions are typically 95% identical or more at
>                       the nucleotide level and hence will crosshybridise. However, these studies only reported the conserved reading frame sequences, without any flanking
>                       regions or integration sites, leaving their chromosomal and intracellular location - mitochondrion or nucleus - open, although Bergthorsson and
>                       team (2004) favour a mitochondrial localisation. This could have been clarified by a complete mitochondrial genome sequence for Amborella,
>                       contiguous linkage between the LGT candidates and bona fide mtDNA isolated from organelles, or in situ hybridisation with specific probes.
>                       Indeed, the recently published mitochondrial genome sequence for tobacco (Sugiyama et al, 2005) revealed that several genes previously reported to
>                       have been lost from that genome and transferred to the nucleus are in fact present in the mtDNA, underscoring the value of complete genome data in
>                       assessing subcellular gene localisation. There is also the possibility that the unusual PCR products from Amborella
>                       stem from substrates somewhere in its genome, but that the unusual trees are not due to LGT. Those who study animal mitochondrial DNA have long
>                       known that nuclear pseudogenes of mitochondrial DNA often have unusual sequences (Bensasson et al, 2001). Such nuclear pseudogenes of mtDNA
>                       are called 'numts' and have been found in large numbers in most sequenced eukaryotic genomes, particularly among plants (Richly and Leister, 2004).
>                       Thalmann et al (2004) recently showed that numts in primates are a serious problem because they are readily, sometimes even preferentially, amplified
>                       over genuine mtDNA, even though the organelle copy is present in larger template numbers. Numts are extremely difficult to distinguish from bona
>                       fide mtDNA (Bensasson et al, 2001; Thalmann et al, 2004, 2005) and can produce very unusual branching patterns in phylogenetic trees causing
>                       primate species to apparently intermingle (Thalmann et al, 2004) in a pattern that would suggest rampant LGT, were the identity of the bona fide
>                       mtDNA and the numt not known. The levels of sequence differences between higher plant mtDNA from
>                       different orders are low, less than that observed between human and chimp mtDNAs. For example, the rps2 sequences representing the deeply
>                       diverging dicot orders Laurales and Magnoliales - separated by roughly 150 million years (Bergthorsson et al, 2003) - have only two nucleotide
>                       differences across 474 sites: G  T transversions at positions 89 and 263. The 1.2 kb-long atp1 sequences from the gymnosperm Ginkgo and the
>                       angiosperm Illicium, separated by about 300 million years (Kim et al, 2004), have only 6% nucleotide differences (Bergthorsson et al, 2004). By
>                       comparison, human and chimp sequences for the 1.8-kb long nad5 gene from mtDNA have nearly twice as much (11%) differences. The extremely
>                       low rate of substitution in higher plant mtDNA makes it amenable to using conserved primers (Bergthorsson et al, 2003, 2004), but low numbers of
>                       substitutions alone does not distinguish whether the PCR products obtained are mtDNA or numts (Bensasson et al, 2001; Thalmann et al, 2004).
>                       Adding to these uncertainties is the issue of RNA editing, the C  T changes of which affect over 20 codons each in 10 different reading frames
>                       of Arabidopsis mtDNA (Geige and Brennicke, 1999). Little is known about the prevalence and among-gene distribution of mitochondrial editing in
>                       other higher plant lineages. Other reports for plant-to-plant LGT have also appeared recently (Won and Renner, 2003) but they, too, involved
>                       exclusively mtDNA and very small numbers of remarkably distributed sequence differences. There is also the issue of current phylogenetic
>                       methods themselves, which are anything but error-free (Holland et al, 2004).
>                       None of this is to say that the mechanisms and amounts of LGT inferred in the recent findings from plant mtDNA cannot be true. However, the
>                       inferences of LGT via meterorites, LGT from the past to the present, and more frequent LGT among shrubs than among prokaryotes are rather
>                       surprising. It is prudent, therefore, to consider possible alternative explanations. After all, dinosaur bone DNA once caused quite a stir, but it
>                       turned out to be a numt (Zischler et al, 1995). Thus, it will be of interest to see this new LGT evidence corroborated by independent experimental
>                       approaches that circumvent PCR and to see its biological significance for the process of heredity among the organisms in question.

References

Bensasson D et al (2001). Trends Ecol Evol 16: 314-321. Article PubMed

Bergthorsson U et al (2003). Nature 424: 197-201. Article PubMed

Bergthorsson U et al (2004). Proc Natl Acad Sci USA 101: 17747-17752. Article
>                       PubMed

Geige P, Brennicke A (1999). Proc Natl Acad Sci USA 96: 15324-15329. Article
>                       PubMed

Goremykin VV et al (2003). Mol Biol Evol 20: 1499-1505. Article PubMed

Holland BR et al (2004). Mol Biol Evol 21: 1459-1461. Article PubMed

Kim S et al (2004). Am J Bot 91: 2102-2118.

Richly E, Leister D (2004). Mol Biol Evol 21: 1081-1084. Article PubMed

Sugiyama Y et al (2005). Mol Genet Genom 272: 603-615. Article

Thalmann O et al (2004). Mol Ecol 13: 321-335. Article PubMed

Thalmann O et al (2005). Mol Ecol 14: 179-188. Article PubMed

Won H, Renner SS (2003). Proc Natl Acad Sci USA 100: 10824-10829. Article
>                       PubMed

Zischler H et al (1995). Science 268: 1192-1193. PubMed

Sekcje

Narzędzia osobiste

W. Martin, "Molecular evolution: Lateral gene transfer and other possibilities" (2005)

Akcje Dokumentu