Horizontal gene transfer in plants

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See Horizontal gene transfer, Mobile DNA and Gene transfer for broader discussions.
See also Transgenic plant for discussion in the context of horizontal gene transfer in plants via pollen, and artificial horizontal gene transfer methods used in biotechnology.

Horizontal gene transfer (HGT), also called lateral gene transfer (LGT) is any process in which an organism transfers genetic material (i.e. DNA) to another cell that is not its cellular offspring, as distinct from vertical gene transfer where genes are inherited from parents or ancestors in a lineage of cellular organisms.

Natural gene transfer between plants that do not cross-pollinate

Natural movement of genes between different plant species and from other kingdoms (Monera, Fungi) into plants occurs by gene transfer mediated by natural agents such as microrganisms, parasites, epiphytes, viruses or mites and by direct cell to cell transfer. Such transfers occur at a frequency that is low compared with the hybridization that occurs during pollination, but can be frequent enough to be a significant factor in genetic change of a chromosome on evolutionary time scales [1] [2]. The mitochondrion of plants is a frequent staging ground for gene movement.

One frequent suggestion for the movement of mobile DNA is a horizontal transfer of mobile element DNA or RNA, either as a naked nucleic acid or within a virus. These types of transfers are thought to occur quite commonly into damaged tissues (e.g. insect feeding sites), given the tendency of eukaryotic cells to take up and incorporate foreign mobile DNAs into their genomes. It should be noted that in multicellular organism such a transfer would rarely occur in tissues that would give rise to gametes and be transmitted to the next generation. Thus it has been suggested that a greater number of transposable elements and a tendency towards larger genomes might be observed in plant species that reproduce asexually [3].

Mitochondria and gene transfer

Mitochondria are thought to have arisen as bacterial endosymbionts, and contain their own circular chromosome which has all the hallmarks of a bacterial origin.

This mitochondrial chromosome is a dynamic genetic reservoir which, during the course of natural evolution, frequently incorporates new from genes plastid and nuclear chromosomes (that is from the nucleus rather than another organelle) via intracellular gene transfer[4] [5].

In addition a large number of discoveries of horizontal gene transfer of mitochondrial genes of land plants have recently been discovered, mostly the result of transfer of a mitochondrial gene from one flowering species to another, but also including transferred moss genes, and flowering plant transfer to gymnosperms[6].

Chloroplasts and gene transfer

Less commonly, horizontal gene transfer involves the chloroplast and nuclear genomes of plants.

The first recognized horizontal gene transfer into chloroplasts was of a bacterial gene into red agae. This first discovery is an ancient transfer of the rubisco genes that concerned with carbon dioxide fixation (rbcL and rbcS) from a bacterium into the common ancestor of red algal plastids and their derivatives [7]

A second known horizontal gene transfer into chloroplasts concerns a large ribosomal subunit bacterial protein gene (rpl36) which has transferred into the ancestor of the algal protist cryptophyte and haptophyte plastids (chloroplasts), and which was detected in Guillardia theta.

This rpl36 gene is distantly related to a rpl36 gene normally found in other chloroplasts, and is similar to an essential gene found most bacteria. In this case a bacterial rpl36 has completely replaced the native rpl36 gene to the very end of the gene by an unusual and ill-understood mechanism [8]

Transfer of genes involving nuclear chromosomes

In the sheep's fescue Festuca ovina, a gene for the enzyme phosphoglucose isomerase appears to have been transferred from the distantly related Poa genus. Such horizontal gene movement of a nuclear gene may follow from a non-standard fertilization with more than one pollen grain, or a direct horizontal gene transfer mediated by a plant virus.[9]

Mobile genetic elements in plants

This natural gene movement between species has been widely detected during genetic investigation of various natural mobile DNA, such as transposons, and retrotransposons that naturally transfer to new locations in a genome, and often move to new species host over an evolutionary time scale. There are many types of natural mobile DNAs, and they have been detected abundantly in food crops such as rice [10].

These various mobile or jumping genes play a major role in dynamic changes to chromosomes during evolution [11], [12], and have often been given whimsical names, such as Mariner, Hobo, Trans-Siberian Express (Transib), Osmar, Helitron, Sleeping Princess, MITE and MULE, to emphasize their mobile and transient behavior.

Such genetically mobile DNA constitutute a major fraction of the DNA of many plants, and the natural dynamic changes to crop plant chromosomes caused by this natural transgenic DNA mimics many of the features of plant genetic engineering currently pursued in the laboratory, such as using transposons as a genetic tool, and molecular cloning. See also transposon, retrotransposon, integron, provirus, endogenous retrovirus, heterosis [13].

There is large and growing scientific literature about natural transgenic events in plants, such as the creation of shibra millet in Africa, and movement of natural mobile DNAs called MULEs between rice and millet [14]. An article about natural MULE gene movement between rice and millet is worth describing fully:

Jumping genes cross naturally between rice and millet

PLoS biology 234x60.GIF

In the early 1950s, legendary plant geneticist Barbara McClintock found the first evidence that genetic material can jump from one place to another within the genome. The variegated kernels of her maize plants, she determined, resulted from mobile elements that had inserted themselves into pigment-coding genes, changing their expression. McClintock's mobile elements, or transposons, moved over generations within a single species. More recently, another form of genetic mobility has been discovered—genetic information can sometimes be transferred between species, a process called horizontal gene transfer. While horizontal genetic transfer occurs most commonly in bacteria, it has been detected in animals as well. Most transfers between higher animals involve the movement of transposons. Horizontal transfer can also occur between the mitochondrial DNA of different plant species. Until now, however, no one had found evidence for horizontal transfer in the nuclear DNA of plants.

In a new report, Xianmin Diao, Michael Freeling, and Damon Lisch studied the genomes of millet and rice, two distantly related grasses that diverged 30–60 million years ago. While the two grasses show significant genetic divergence from accumulating millions of years of mutations, they carry some transposon-related DNA segments that are surprisingly similar. The authors conclude that these sequences were transferred horizontally between the two plants long after they went their separate ways.

Transposons of the class identified by Diao et al. typically consist of a variable length of DNA that codes for one or more enzymes flanked by repeating sequences called terminal inverted repeats (TIRs). These repeats can bind to each other to form a 'lollipop' that is easily excised from the DNA strand, carrying the rest of the transposon along with it. Plant genomes are rife with transposons, many of which are relatively passive. Transposons from the 'Mutator' family in maize, however, are especially active, frequently causing mutations as they insert themselves into new positions in the genome. They perform this jump with assistance from the two proteins they code for, a transposase and a helper gene.

DNA from many species of plants contains several families of cousins of the Mutator transposons. These 'Mutator-like elements', or MULEs', code for a protein similar to the transposase, as well as the TIR sequences. Diao et al. identified 19 distinct MULEs in the DNA of various species of millet (genus Setaria), and compared these with the rice genome sequence, which was published in 2002. They compared the sequence similarity of these MULEs to that of other proteins that are also conserved in the same species for which sequences are available. Strikingly, they observed much higher sequence similarity between the MULEs from millet and rice than is typical for transposons. The greater similarity of the MULE DNA is easily explained if it jumped somehow, horizontally, between the species, but there could be alternative explanations. The match could have arisen without horizontal transfer, for example, if the MULE DNA had been under positive selection, as typically happens for protein-coding genes that confer some survival or reproductive benefit. In such cases, natural selection tends to preserve the integrity of these sequences.

To test for signs of selection, the researchers looked at regions of the MULE DNA that don't appear to code for protein. The similarity between these non-coding regions in millet and rice MULEs was just as high as for the coding regions, even though selection probably doesn't influence them. Even within the coding sections, 'synonymous' mutations—which don't change the protein sequence and so are not prone to selection—showed few differences between these elements.

Another explanation for the low divergence of the rice and millet MULE sequences could be that they occur within a genomic region that, for whatever reason, experienced lower than average mutation rates. If this were the case, sequences adjacent to the elements should also show reduced variation. The authors tested this alternative hypothesis with the help of maize, which has more genomic sequence available than millet, by comparing genes flanking MULE regions in rice with evolutionarily conserved sequences in maize. The sequences did not show the similar degree of reduced variation predicted for below-average mutation rates.

Since neither selection nor low mutation frequency can explain the similar DNA between the grasses, the authors conclude, a transposon must have carried it between millet and rice long after these species diverged. Interestingly, the authors also found similar sequences in bamboo, raising the question of how common horizontal transfer may be between plant species. Given that plant mitochondrial genes appear “particularly prone to horizontal transfer,” the authors note, “it is remarkable that these results represent the first well-documented case of horizontal transfer of nuclear genes between plants.” But as researchers begin to explore the growing databases of plant genomic sequences, they can determine whether this finding constitutes an anomaly—or points to a significant force in plant genome evolution. —Don Monroe

Citation: (2006) Jumping Genes Cross Plant Species Boundaries. PLoS Biol 4(1): e35 DOI:10.1371/journal.pbio.0040035 Published: December 20, 2005

Copyright: © 2005 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Epiphytes and parasites as a bridge for gene flow between diverse plant species

Pathways for horizontal gene transfer between plants and parasitic or epiphyte plants that grow on them are now well established.

Epiphytic and parasitic plants are common in the tropical rain forests of New Caledonia in which the flowering shrub Amborella grows. Amborella leaves and stems are often covered with epiphytes, including mosses. Ulfar Bergthorsson and co-workers have suggest that this could readily promote direct, plant-to-plant horizontal gene transfer, and they have implicated the mitochondrial chromosome of Amborella to be more heavily in horizontal gene transfer than even most free-living bacteria. 20 of its 31 known mitochondrial protein genes from other land plants, mostly from other angiosperms but including six striking cases of transfer from moss donors. [15]

In 2004 it was also discovered that three species of plantains, have a normal functioning copy of the mitochondrial gene (atp1) plus a second defective copy. This second copy resembles the atp1 gene in parasitic dodder plants (genus Cuscuta) that grow on plantains, and details analysis indicate dooder to plantain horizontal gene transfer has occurred. Dodders are parasites have no chlorophyll twine around host stems and send in roots to intimately penetrate their host's cells, enabling DNA to be transferred.[16].

The converse gene transfer, host plant to parasitic plant has also been detected. In this case the parasites are Rafflesiaceae endophytic plants which lack leaves, stems, and roots, and rely entirely on their host plants for their nutrition. When flowering they producing the largest flowers in the world, which mimic rotting flesh — as an enticement to the flies that pollinate them. [17].

General implications of horizontal gene transfer in plants

A flurry of research over the last decade has shown that gene movement between distantly related plants (such as flowering plants and mosses or gymnosperms) is a fact of natural evolution, and the research has revealed plant epiphytes and parasites as one vehicle for this movement. Natural transfer of genes between fungi, bacteria and plants is also established (see Horizontal gene transfer).

These biological insights are emerging at a time when artificial transfer of genes into food crops remains controversial and often resisted with the claim [18] that it would never occur in nature (See plant breeding, transgenic plants, Biotechnology and plant breeding).

Accurate knowledge of this facet of plant evolution is relevant to the ongoing debate about transgenic plants produced by biotechnology.

References

  1. Syvanen, M. and Kado, C. I. Horizontal Gene Transfer. Second Edition. Academic Press 2002.
  2. Richardson AO, Palmer JD. (2006) Horizontal gene transfer in plants.J Exp Bot. 2006 Oct 9; [Epub ahead of print]
  3. Bennetzen, J. L., (2000) Transposable element contributions to plant gene and genome evolution. Plant Molecular Biology 42: 251–269, 2000.
  4. Burger G, Gray MW, Lang BF: Mitochondrial genomes: anything goes.Trends Genet 2003, 19:709-716.
  5. Koulintchenko M et al. (2003) Plant mitochondria actively import DNA via the permeability transition pore complex EMBO J 22:1245-1254
    • Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective Curr Genet 46:123-139
  6. Cho Y et al. (1998) Explosive invasion of plant mitochondria by a group I intron Proc Natl Acad Sci USA 95:14244-14249
  7. Delwiche CF, Palmer JD (1996) Rampant horizontal transfer and duplication of Rubisco genes in eubacteria and plastids. Mol Biol Evol 1996, 31:873-882.
  8. Rice DW, Palmer JD. (2006) An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters.BMC Biol. 2006 Sep 6;4:31.
  9. Ghatnekar L et al.(2006) The introgression of a functional nuclear gene from Poa to Festuca ovina Proc Biol Sci 273:395-9
  10. DNA-binding specificity of rice mariner-like transposases and interactions with Stowaway MITEs
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  13. Gene duplication and exon shuffling by helitron-like transposons generate intra species diversity in maize.
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  15. Bergthorsson U et al. (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella Proc Natl Acad Sci USA 101:17747-17752
    • Richardson AO Palmer JD (2006) Horizontal gene transfer in plants J Exp Bot 2006 Oct 9; [Epub ahead of print]
  16. Mower JP et al. (2004) Plant genetics: gene transfer from parasitic to host plants. Nature 432: 165–166.
  17. [Charles C et al. (2004) Host-to-Parasite Gene Transfer in Flowering Plants: Phylogenetic Evidence from Malpighiales Science 305:676 - 678
  18. What is genetic engineering?