The importanceof horizontal gene transfer in plant

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It should be recognized that, at least in land plants, gene transfer between ... ability to accept foreign DNA and integrate it into the genome. Thus, we ... genetic material, usually from a distantly related species. ... While the HGT primarily associated with prokaryotic ... transfer (LGT), is any process in which an organism.

International Research Journal of Plant Science (ISSN: 2141-5447) Vol. 2(10) pp. 294-298, October, 2011 Available online http://www.interesjournals.org/IRJPS Copyright © 2011 International Research Journals

Review

The importance of horizontal gene transfer in plant evolution and its implications for our view of genetically modified plants Yi Sun1* and Danqiong Sun2 1*

Biotechnology Research Center,Shanxi Academy of Agri. Sci., Taiyuan, 030031 China. 2 Gladstone Institutes, University of California-San Francisco, CA 94158 USA. Accepted 28 September, 2011

The ability to move genes between species by transformation methods is very useful for basic research to evaluate the role of a gene in explaining the phenotypic differences between species and for applied research to introduce a desirable gene into a crop plant. However, some people have expressed concern that transformation experiments are unnatural. By implication, the unnaturalness of transformation is often taken to suggest that it is hazardous to the environment and health of human and animals. We will show that horizontal gene transfer, a natural version of transformation, has been occurring throughout evolutionary history. It should be recognized that, at least in land plants, gene transfer between taxonomically different species by conventional sexual reproduction (introgression, hybridization, such as triticale – a cross between wheat and rye) is more common than the transfer of pieces of DNA by non-sexual means (e.g., viruses, bacterial plasmids, or uptake and integration of naked DNA). However, increasing evidence suggests that horizontal gene transfer certainly occurs when one species comes into an intimate contact with another. Numerous examples of horizontal gene transfer from bacteria or fungi to plants and between plants have been published, proving that plants have a natural biological ability to accept foreign DNA and integrate it into the genome. Thus, we conclude that although interspecific transformation experiments, like all other genetic manipulations, should be reviewed for possible adverse environmental or health impacts, there is no reason to assume that more risk arises from transformation experiments than other common genetic and breeding methods. Keywords: Plant evolution, horizontal gene transfer, genetic transformation. INTRODUCTION In plant molecular biology, genetic modification is the genetical alteration of a variety or a line through the uptake, genomic incorporation, and expression of exotic genetic material, usually from a distantly related species. Studies on genetically-modified (GM) plants have gone on for three decades, and this year is the 17th year of the first commercialization of a GM crop (FlavrSavr tomatoes, released in 1994). Genetic modification is not only used to produce elite crop varieties, which may help enhance and stabilize agriculture production, but is also a powerful tool for scientists who are interested in studying gene function. Genetic modification has been criticized as being

*Corresponding Author E-mail:

[email protected]

unnatural and hazardous by certain groups (Dale, 2005; Batalion, 2009). Here we review the evolutionary history of non-human-mediated transformation of plants. We show that transformation has been pervasive at several different scales: from examples involving a few or single genes/operons, to whole chromosomes, or whole genomes. Furthermore, we show that these examples are not just similar to GM technology in terms of the outcome – foreign genes integrated into a recipient genome - but the molecular mechanisms underlying transformation in nature closely resemble the methods used by scientists that introduce foreign genes into genomes. Finally, we illustrate the important roles of horizontal gene transfer (HGT) in plant evolution. We conclude that, since transformation has been occurring throughout the history of life on earth, argu-

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ments against the use of GM technology unnaturalness of transformation are unfounded.

as

Mono or oligo-gene transformation in plant evolution While the HGT primarily associated with prokaryotic species (Johnsborg et al., 2007; Scudellari 2011), the phenomenon also occurs in land plants (Woloszynska, 2005; Richardson and Palmer, 2007; Bock 2010), and it appears that the exchange of genetic information across eukaryotic species lines is far more pervasive and more radical in its consequences than we could have guessed just a decade ago (Keeling and Palmer 2008; Zhaxybayeva and Doolittle, 2011). It is reported that horizontal transfers occur between plants’ mitochondrial genes (Richardson and Palmer, 2007). One well-documented case involves gene transfer from host plants in the Vitaceae to endoparasites of the Rafflesiaceae (Davis and Wurdack, 2004). Similarly, there is evidence of gene transfer from the plastid genome of an unidentified plant to the mitochondrial genome of a Phaseolus species (bean) (Woloszynska et al., 2005). Interestingly, horizontal transfer of mitochondrial genes has been found to sometimes involve multiple genes. For example, Amborella trichopoda, a rare shrub in New Caledonia, has been argued to have acquired 26 mitochondrial genes from other land plants (Bergthorsson, 2004; Richardson and Palmer, 2007). Likewise, Won and Renner (2003) provide evidence of the transfer of nad1 intron 2 and adjacent exons from an angiosperm in the asterid clade to Gnetum, a gymnosperm. Additionally, it was reported recently that the genome of Striga hermonthica, the eudicot parasite witchweed, contains a nuclear gene that is widely conserved among grass species but is not found in other eudicots. Phylogenetically, these gene clusters with sorghum, the monocot host of the parasite, suggesting that nuclear genes can be captured by parasitic weeds in nature (Yoshida et al. 2010). In addition to gaining genes from other plants, plants appear to have acquired genetic material from fungi, with which they have had close symbiosis, ever since plants first invaded land. Indeed, fungi may have helped early plants adapt to the stresses of the terrestrial realm (Heckman et al. 2001). A recent study discovered that acquisition of phenylalanine ammonia lyase (PAL) pathway through horizontal gene transfer from fungi to the ancestor of land plants might have been a crucial step in the invasion of land (Emiliani et al., 2009). Whole genome transformation via endosymbiosis Horizontal gene transfer, also known as lateral gene transfer (LGT), is any process in which an organism incorporates genetic material from another organism

without being the offspring of that organism. By contrast, vertical inheritance occurs when an organism receives genetic material from its parents. Most genetic studies have been focused on vertical inheritance, but there are increasing evidence that horizontal gene transfer plays an important role in organism evolution, especially among single-celled organisms. HGT is abundantly documented among living prokaryotes (Woese, 1998; Griffiths,2007; Richards and Talbot, 2007), and there is every reason to assume that it was also rampant in the archeozic era in the prokaryotic grade ancestors of modern eukaryotes. Thus, land plants (embryophyta) and all other living organisms have a deep history of HGT, which played a role in contributing to the genome content of all modern organisms. In addition to gene-by-gene HGT, plant ancestry includes at least two events of endosymbiosis (Margulis, 1970), which can be equated with whole-genome horizontal gene transfer. The first of these endo-symbiositic events yielded an aerobic eukaryote with a mitochondrion derived from an engulfed alpha-proteobacterium. Then, a heterotrophic eukaryote acquired the genome of a cyanobacterium through endosymbiosis, resulting in a primary plastid, which is now found in all land plants. This second engulfment event gave the cell the capacity to trap energy for itself from the sunlight (McFadden 2001; Archibald, 2005; Archibald 2009). It was this transformation that allowed for the eventual invasion of land by multicellular embryophytes, making green the most prominent color on terra firma million years later. It could be argued that endosymbiosis is not really an instance of genetic modification but just two genomes living and reproducing in close (very close!) contact. This perspective would, however, not reduce the amount of genetic transformation that has occurred, since many genes have subsequently been transferred from organelles to the nuclear genome, or vice versa (Brouin et al., 2008; Blanchard and Lynch, 2000; Woodson and Chory,2008). It has been estimated that ca. 4,500 of the 24,990 genes (accounts for ≈18% of the protein-coding genes) in the Arabidopsis nuclear genome came from the plastid (Martin et al. 2002). Furthermore, such a number appears to be an underestimate of the extent of transformation of the nuclear genome by organellar DNA because most organellar genes that have historically been stably inserted into the nuclear genome were quickly lost. This is because, until gene products evolved a novel function or acquired an appropriate signal sequence so as to be transported back to the source organelle, the gene would not be maintained by the selection process. Thus, we can be sure that vascular plant genomes have, during their history, been transformed many thousands of times by DNA from the plastids or mitochondria. This has been illustrated by the discovery of several entire plastid genomes inserted in the nuclear genome of Arabidopsis thaliana (Stupar et al., 2001) and the large chloroplast DNA fragment in that of rice (Yuan

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et al., 2002). Whole genome transformation via allopolyploidy Allopolyploidization, resulting from the fusion of unreduced gametes from relatively distantly-related parents, is known to be an important phenomenon in plant evolution. We would argue that allopolyploids can be viewed as examples of whole genome transformation. Many plants that are important in our daily life are allopolyploids including bread wheat, oat, cotton, tobacco, cabbage, leek, apple, strawberry, kiwifruit, and chrysanthemum, to name just a few (Gaut et al., 2000; Smedmark, 2003; Soltis et al., 2004; Adams and Wendel, 2005; Meyers and Levin, 2006). Allopolyploidization has conferred on plants broad adaptability, fixed heterosis, and consequently opportunities to evolve into new species and/or to successfully colonize new environments (Ni et al, 2009). Allopolyploidization brings together two formerly isolated genomes into intimate contact in much the same way as genetic transformation brings a single gene (or a small number of genes) into a foreign genetic background. In both cases novel genetic and epigenetic interactions occur. This is well documented in allopolyploids where rapid changes in cytosine methylation patterns, silencing or activating certain genes, or activation of transposable genetic elements may occur (Liu and Wendel, 2002; Liu and Wendel, 2003;Adams, and Wendel, 2005; Ma and Gustafson,2005). Once allopolyploids are established, other more long-lasting effects can occur. These can include differential gene loss, subfunctionalization, or neofunctionalization, which may be viewed as “normal” evolutionary changes. However, some changes are more readily understood as instances of “genetic modification.” For example homeologous gene conversion (Wendel et al. 1995), or translocation of a genomic region from one parental chromosome into a region that derives from the other parent. Thus, while allopolyploid hybridization is not usually included within the rubric of genetic modification, because genome contact is initially via sexual reproduction, we would argue that at the molecular level this frequent and important phenomenon closely resembles genetic transformation. Molecular mechanisms of plant transformation in nature It is worth noting that the mechanisms implicated in the natural transfer of DNA into plant genomes do not appear so much different to those used in human-mediated genetic modification. Sometimes the suspicion is that close physical contact between DNA from two species, such as occurs between an endoparasite and its host (Barkman et al., 2007), may allow naked DNA of one

species to enter a cell of another species. When this happens, the foreign DNA can occasionally be integrated into the recipient’s genome (if it happens to have suitable flanking sequences). This phenomenon resembles biolistic and sonication-based methods for transforming plants in the laboratory in that all that is needed is the introduction of foreign DNA into the nucleus for recombination and stable transformation to occur. In other cases, HGT is likely due to microbial vectors such as viruses and plant pathogenic bacteria. For example, a recent study suggested that the genes that some Chlorella species use to synthesize chitin cell wall probably originated in fungi and were probably introduced into the alga by large DNA viruses (Blanc et al. 2010). The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. The most widely used laboratory approach exploits the transfer DNA (abbreviated T-DNA) sequences of the tumor-inducing (Ti) plasmid in Agrobacterium tumefaciens. This bacterium possesses mechanisms that reliably transfer DNA fragments flanked by T-DNA into the host plant's nuclear DNA genome (Schell and Montagu, 1977). Molecular biologists modified this natural plasmid, resulting in Agrobacterium-mediated T-DNA transfer now being a widely-used tool for genetic engineering in plants. While less widely used for stable transformation, viruses such as Tobacco Rattle Virus, are also able to introduce foreign genes into a plant nuclear genomes. There is every reason to assume that some of the many cases in which genes have been acquired horizontally during plant evolution used T-DNA or viral vectors just like those employed by laboratory scientists. The relevance of natural transformation for the GMO debate As we have shown, natural transformation has been a pervasive force that has had a great impact on the features of living plant species. But, how should this observation affect one’s opinions on the naturalness and safety of genetically modified organisms? Let us start with natural issues and then turn to safety concerns. A basic argument against genetically modified organisms is that they are created by unnatural means and are therefore unacceptable. This argument flounders on the data we have cited, which show that transformation is natural, being a process that has occurred innumerable times in the history of crop plants. A more nuanced position would be to argue that the problem is not that the process is unnatural, but that humans have the temerity to try and control the process so as to yield desirable agronomic traits. This argument proves itself unsatisfactory as well, when one considers the history of plant (and animal) breeding. Agriculture arose multiple times in different parts of world when humans learned to save seeds for growing in successive

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seasons (Rindos,1987; Allard, 1999; Hancock, 2004). Early farmers likely had imposed inadvertent selection (e.g., for loss of dispersal abilities and synchronized germination) as well as more directed artificial selection by choosing to store seed from better-looking plants. In addition to acting on preexisting variation, farmers’ practices enhanced genetic variation through interspecies hybridization. Even if we assume that early farmers did not intentionally cross species, by altering plant ecology and introducing crops into new areas where they could hybridize with wild relatives, farming certainly altered the gene pool of many crop species. This level of human shaping of the genetic composition of crop species continued until the 20th century, when plant breeders developed new methods to induce mutations (with radiation, mutagenic chemicals and produce the “Clearfield” rice variety), improved techniques for combining different lines and selecting elite hybrids, and developed strategies to exploit heterosis and cytoplasmic male sterility in breeding designs. In all cases, the techniques used in plant breeding involved controlling and accelerating natural processes, not creating totally artificial processes. As discussed above, the same is true for transgenic techniques. As with conventional breeding, transformation technologies simply accelerate and direct natural processes to more rapidly introduce desirable traits into our crops. Given this, it is very difficult to see why GM crops but not crops derived from scientific plant breeding programs should be judged unnatural. What about safety? Is there more chance of accidentally creating a new crop that is toxic to humans or harmful to the environment by transgenic methods than by conventional scientific plant breeding? Since transformation is a natural process, we can see no biological reason why GM crops should necessarily pose more hazards than crops created using other natural processes (e.g., mutagenesis and wide introgression). The only argument we can see is that GM methods may be more effective at permitting humans to achieve ill-conceived goals. If a company had the idea to make a tomato that expressed the peanut allergen, they could probably fulfill their aim quicker using transgenic methods than with conventional breeding. But the problem here is not the technique but the ill-conceived goal and the inattention to risk when developing any new product. Thus we think that the risks of GM crops should be evaluated case by case rather than with blanket suspicion. For instance, the sources and characteristics of isolated genes should be examined carefully to predict potential hazards. That being said, similar precautions should also be taken for new elite varieties developed by “conventional” breeding techniques. Similarly, basic research that generates transgenic plants should be subjected to similar regulatory oversight as research that involves generating hybrids between distantly related species, for example. The basic hazards are the same for

conventional and transgenic approaches to crop improvement and research and, as we have been at pains to stress, both approaches adapt and accelerate natural processes. The production of GM crops offers many potential benefits to agriculture and the perpetual challenge of producing enough, high quality foods to feed an ever growing human population. Most importantly, genetic modification allows one to introduce useful genetic variation into a recipient species. For example, GM techniques allow for the creation of crops that are intrinsically more resistant to pathogens and more able to grow with lower inputs of fertilizers and pesticides. As we more fully appreciate the environmental impacts of pesticides (even “organic” ones such as BT) and fertilizers, both local impacts on the environment, and global impacts in terms of the carbon cycle, the case for using GM technology to introduce “green” traits only gets stronger. It would be refreshing if more environmentalists came to recognize that GM technology is their friend. By looking at the abundance of genetic transformation in the history of plant evolution we have shown that genetic modification is a natural process, or at least as natural as other methods used in plant breeding but well targeted on certain genes we so desire, and basic plant genetic research. While there is a tendency to react viscerally to GM crops as human creations, they are really no more artificial than any other elite crop variety. Nature has blessed plants with diverse genetic capabilities that have allowed them to diversify and thrive in nature and also to be highly malleable under the concerted efforts of plant breeders. Indeed, we would go so far as to say that failing to explore and develop all available methods for crop improvement, including transgenic ones, would equal to have their own hands and feet tied when trying to meet the major environmental and productivity challenges of 21st century agriculture. CONCLUSION Plants were created by the nature, and evolved with the changes made and selected by the nature. We live on the nature generosity and have acquired our breeding skills by imitating what nature does. We have shown here that many interactions (many more are unexpected and undetected) occur among various plant genomes, and between plant genomes and those of other organism kingdoms, that have made our planet so colorful and thriving. Both vertical and horizontal gene transfers are indispensible to the plant evolution. As stated by Margulis and Sagan (2001), "Life did not take over the globe by combat, but by networking". GM is one of the most precious gifts our generous nature grants to us. We are grateful to the great nature that have shown us the power of genetic transformation in the long run of both the earth and plant evolution, and taught us the marvelous techno-

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logy of genetic transformation. We have no reason not to use it to make the planet more peaceful and harmony. ACKNOWLEDGEMENT Authors are grateful to Professor David Baum, Department of Botany, University of Wisconsin-Madison, USA for his thoughtful and enlightening comments. This work was supported by the grants from the Major Projects for Breeding Genetically Modified Organisms from the China Agriculture Ministry. REFERENCES Adams KL, Wendel JF (2005). Polyploidy and genome evolution in plants. Curr. Opin. Plant. Biol. 8: 135-141. Allard RW (1999). Principles of Plant Breeding. John Wiley and Sons Inc. New York, Chichester, Weinheim, Brisbane, Singapore, Toronto. Archibald JM (2005). Jumping genes and shrinking genomes—Probing the evolution of eukaryotic photosynthesis with genomics. IUBMB Life 57: 539–547. Archibald JM (2009). Genomics: green evolution, green revolution. Science 324: 191-192. Barkman TJ, McNeal JR, Lim SH, Coat G, Croom HB, Young ND, de Pamphilis CW (2007). Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol. Biol. 7: 248. Batalion N (2009). 50 Harmful effects of genetically modified (GM) foods. http://www.raw-wisdom.com/50harmful. Bergthorsson U, Richardson A, Young G, Goertzen L, Palmer J (2004). Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella, PNAS. 101: 17747-17752. Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A, Lindquist E, Lucas S, Pangilinan J, Polle J, Salamov A, Terry A, Yamada T, Dunigan DD, Grigoriev IV, Claverie JM, Van Etten JL(2010). The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22: 2943–2955. Blanchard JL, Lynch M (2000). Organellar genes: why do they end up in the nucleus? Trends Genet. 16: 315–20. Bock R (2010). The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci. 15: 11-22. Brouin G, Baoud H, Xia J (2008). Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol. Phylogenet Evol. 49: 827-831. Dale PJ (2005). Where science fits into the GM debate? Page 1-15 In Gene Flow from GM Plants. Poppy GM and Wilkinson MJ, eds. Blackwell Publishing Ltd. Davis CC, Wurdack KJ (2004). Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales, Science 305: 676–8. Emiliani G, Fondi M, Fani R, Gribaldo S (2009). A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biol. Direct 4:7 Griffiths G (2007). Cell evolution and the problem of membrane topology, Nat. Rev. Mol. Cell Biol. 8: 1018–24. Hancock JF (2004). Plant Evolution and the Origin of Crop Species. CABI Publishing. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001). Molecular evidence for the early colonization of land by fungi and plants. Science 293: 1129–1133. Johnsborg O, Eldholm V, Håvarstein LS (2007). Natural genetic transformation: prevalence, mechanisms and function. Res. Microbiol. 158: 767-778.

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