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:
sunyi692003@yahoo.com.cn
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-
Sun and Sun 295
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
296 Int. Res. J. Plant Sci.
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
Sun and Sun 297
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-
298 Int. Res. J. Plant Sci.
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.
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