The first paper on HGT in plants (1971)

The first descriptions of what we now call horizontal gene transfer (HGT) started appearing in the middle of last century (Freeman 1951; Lederberg et al. 1951), although what appears to be the first account was mistakenly attributed to sexual recombination (Lederberg & Tatum 1946). Shortly thereafter, experimental work was published concerning mechanisms for the transfer of genetic material between micro-organisms via what we now call transduction (Zinder & Lederberg 1952; Stocker et al. 1953).

The possibility was soon considered that the asexual transfer of genetic units may be of more general occurrence (Ravin 1955). However, it was not really until molecular sequencing became available in the 1980s that biologists started presenting anecdotal evidence for gene transfer among eukaryotes (Shilo & Weinberg 1981; Singh et al. 1981; Buslinger et al. 1982; Hyldig-Nielson et al. 1982; Engels 1983), although Benveniste & Todaro (1974) may have been the first to do so. Unfortunately, most of these suggestions turned out to be spurious, once more evidence accumulated (Smith et al. 1992; Syvanen 1994).

So, it was not until this century that HGT among eukaryotes started to be taken seriously (Bergthorsson et al. 2003, 2004; Won and Renner 2003), although in the first case the evidence presented is rather doubtful. Since the advent of the genome sequencing era, HGT has become an important discussion point for eukaryote evolution (see reviews by Bock 2010; Boto 2010; Renner & Bellot 2012).

All of this work seems to have ignored a speculative, but very prescient, paper published by Frits Went in 1971, based on morphological and anatomical data rather than on gene sequences (ie. phenotypic rather than genotypic evidence). This seems to be a classic example of molecular research being disconnected from the literature on whole-organism biology. Note that, of course, all of the early papers about HGT in bacteria were also based on phenotypic data, although in those cases it was experimental rather than descriptive data.

Went's "suggested mechanism for parallel development [is] by transfer of chromosome fragments carrying groups of genes of proven adaptive competence". Here are some extracts from the Discussion, showing that he was explicitly considering HGT among plants:

The development of parallel morphological characters suggests that in each case closely similar sequences of cell division and cell differentiation occur, which thus lead to similar forms. This in turn suggests that similar sets of genes are involved. It is known in a number of cases (except when too many chromosomal translocations have occurred such as in Drosophila) that genes involved in development of individual organs are frequently located together in chromosome segments. This almost forces us to assume that these parallel forms are due to the presence of similar chromosome segments. According to this view, the similarities did not arise by identical series of mutations in all plants with parallel forms (which would have resulted in whole series of intermediate forms), but by a one-time transfer of the same chromosome segment.

The transfer of a particular chromosome segment between different families has to be non-sexual of course. Non-sexual transfer of genetic material has now been demonstrated in a number of cases. Transduction in bacteria is a prime example. There is also the transfer of viruses, which are either RNA or DNA, and which can occur between completely unrelated families (tobacco mosaic can infect more than a dozen different families).

In consequence I suggest that 1) particular chromosome segments, containing gene sequences for the development of specific forms, exist in certain geographical areas. And, 2) these chromosome segments can be transmitted from one plant to another. This can occur sexually within one genus ... or a-sexually between genera or families ...

Is it possible to accept the existence of gene-group transfer between families? The morphological, anatomical, and biochemical examples presented speak for it. Transduction provides a basis. Interfamiliar virus transfer is possible. Is there perhaps an insect vector for this interfamiliar chromosome transfer? Or does it occur during fertilisation, when anyway at least 2 complete nuclei are transferred, and when perhaps part of a third nucleus could move as well?

Went was principally a plant physiologist, although he also worked in plant ecology, and was apparently an avid anti-reductionist, who was concerned about the increasing dominance of genetics in biology. Possibly, he would not have been impressed by the molecular revolution that lead ultimately to the widespread study of HGT in plants. He preferred (Went 1974) "presently neglected fields which may not find their solution in DNA or RNA. Excessive preoccupation with this subject presently so popular has impoverished biology as a whole."

References

Benveniste RE, Todaro GJ (1974) Evolution of C-type viral genes: inheritance of exogenously acquired viral genes. Nature 252: 456-459.

Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197–201.

Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proceedings of the National Academy of Sciences of the USA 101: 17747-17752.

Bock R (2010) The give-and-take of DNA: horizontal gene transfer in plants. Trends in Plant Science 15: 11-22.

Boto L (2010) Horizontal gene transfer in evolution: facts and challenges. Proceedings of the Royal Society B: Biological Sciences 277: 819-827.

Busslinger M, Rusconi S, Birnstiel ML (1982) An unusual evolutionary behaviour of a sea urchin histone gene cluster. EMBO Journal 1: 27-33.

Engels WR (1983) The P family of transposable elements in Drosophila. Annual Review of Genetics 17: 315-344.

Freeman VJ (1951) Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. Journal of Bacteriology 61: 675-688.

Hyldig-Nielson, JJ, Jensen EØ, Paludan K, Wiburg O, Garrett R, Jørgensen P, Marcker KA (1982) The prnmary structures of two lehemoglobin genes from soybean. Nucleic Acids Research 10: 689-701.

Lederberg J, Lederberg EM, Zinder ND, Lively ER (1951) Recombination analysis of bacterial heredity. Cold Spring Harbor Symposium on Quantitative Biology 16: 413-443.

Lederberg J, Tatum EL (1946) Gene recombination in Escherichia coli. Nature 158: 558.

Ravin AW (1955) Infection by viruses and genes. American Scientist 43: 468-478.

Renner SS, Bellot S (2012) Horizontal gene transfer in eukaryotes: fungi-to-plant and plant-to-plant transfers of organellar DNA. Advances in Photosynthesis and Respiration 35: 223-235.

Shilo BZ, Weinberg RA (1981) DNA sequences homologous to vertebrate oncogenes are conserved in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 78: 6789-6792.

Singh L, Purdom IF, Jones KW (1981) Conserved sex chromosome-associated nucleotide sequences in eukaryotes. Cold Spring Harbor Symposium on Quantitative Biology 45: 805-813.

Smith MW, Feng D-F, Doolittle RF (1992) Evolution by acquisition: the case for horizontal gene transfers. Trends in Biochemical Science 17: 489-493.

Stocker BAD, Zinder ND, Lederberg J (1953) Transduction of flagellar characters in Salmonella. Journal of General Microbiology 9: 410-433.

Syvanen M (1994) Horizontal gene transfer: evidence and possible consequences. Annual Review of Genetics 28: 237-261.

Went FW (1974) Reflections and speculations. Annual Review of Plant Physiology 25: 1-26.

Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proceedings of the National Academy of Sciences of the USA 100: 10824-10829.

Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. Journal of Bacteriology 64: 679-699.