Sidestepping Darwin: horizontal gene transfer from plants to insects

https://doi.org/10.1016/j.cois.2023.101035Get rights and content

Highlights

  • Recent HGT detection workflows enable large-scale studies of HGT among eukaryotes.

  • At least 14 insect species belonging to 6 orders contain plant-derived genes.

  • Many plant-derived genes have putative functions involved in plant-parasite interactions.

  • The impact of plant-to-insect HGT on insect evolution remains to be characterized.

Horizontal transfer of genetic material (HT) is the passage of DNA between organisms by means other than reproduction. Increasing numbers of HT are reported in insects, with bacteria, fungi, plants, and insects acting as the main sources of these transfers. Here, we provide a detailed account of plant-to-insect HT events. At least 14 insect species belonging to 6 orders are known to have received plant genetic material through HT. One of them, the whitefly Bemisia tabaci (Middle East Asia Minor 1), concentrates most of these transfers, with no less than 28 HT events yielding 55 plant-derived genes in this species. Several plant-to-insect HT events reported so far involve gene families known to play a role in plant-parasite interactions. We highlight methodological approaches that may further help characterize these transfers. We argue that plant-to-insect HT is likely more frequent than currently appreciated and that in-depth studies of these transfers will shed new light on plant-insect interactions.

Introduction

Darwin proposed that evolution occurs through natural selection of intraspecific variations transmitted across generations [1]. But he was unable to provide a satisfactory explanation for the origin of these variations and the mechanism underlying their transmission. Darwin and Mendel were contemporaries, but they never met and Mendel’s work was ignored by Darwin [2]. About 50 years after Darwin and Mendel died, Darwin’s natural selection and Mendelian inheritance, which posits that individuals inherit a combination of alleles from their parents, became two pillars of the modern synthesis. Remarkably, observations made in bacteria as early as 1928 — that is, before the modern synthesis was initiated — suggested that genetic information could also be transmitted between individuals through horizontal transfer (HT), that is, through means other than vertical, parent-to-offspring, inheritance [3]. In the second half of the 20th century, it became apparent that HT of genes was rampant in prokaryotes and that it was a major source of bacterial innovation [4]. The first hint that HT of genetic material was not restricted to prokaryotes but could also occur in eukaryotes may correspond to the discovery of endogenous retroviruses in vertebrate genomes during the late 1960s and early 1970s [5]. It was then suggested that the endosymbiotic origin of eukaryotes was accompanied by the relocation (through HT) of many organellar genes to the nuclear genome [6], and that transposable elements (TEs) 7, 8, as well as nonorganellar genes 9, 10 could be acquired horizontally in these taxa. These pioneering works were followed by the observation that the genome of phagotrophic single-cell eukaryotes contained many genes captured from their prokaryote and microbial eukaryote preys 11, 12, 13. Today, the importance of HT of genes in recent eukaryote evolution remains a matter of debate 14, 15, 16, 17, 18. But as a matter of fact, we are witnessing an increasing number of HT reports in both uni- and multi-cellular eukaryotes, largely fueled by the many high-quality new whole genome sequences that are deposited on a daily basis in public databases 19, 20, 21, 22, 23, 24. Importantly, many of these transfers likely facilitated the adaptation of the receiving species to a new ecological niche 25, 26, 27. In multicellular eukaryotes, most HT of genes reported so far involve genes of bacterial, fungi, or viral origin 23, 25, 28, 29, 30, 31••. Aside from HT of TEs, which are not rare [32], relatively few HT of genes between multicellular eukaryotes have so far been uncovered. This trend is seemingly changing in plants, in which numerous recent cases of plant-to-plant HT have been characterized 33, 34, 35, 36. In vertebrates, a single such event is known so far, which involves transfer of a gene coding an antifreeze protein between the Atlantic herring and the rainbow smelt [37]. Here, we provide a comprehensive account of another type of eukaryote-to-eukaryote HT, namely plant-to-insect HT, highlight methodological challenges inherent to the detection of such transfers, and discuss the possible mechanisms underlying these HT as well as their impact on insect genome evolution and plant insect interactions.

Section snippets

How many genes of plant origin in insect genomes?

The first claim of plant-to-insect HT was published in a 2015 article in which hundreds of transcripts from the mosquito Anopheles culicifacies were reported to encode proteins 100% identical to proteins found in plants [38]. However, using plant proteins listed in Supplementary Table 1 of Sharma et al. (2015) [38], we were unable to recover plant-derived genes in the genome of A. culicifacies, which is now available in Genbank (accession number: AXCM00000000.1). Two cases of TE transfer

Methodological challenges to detect horizontal gene transfer

Inferences of horizontal gene transfer (HGT) are plagued by methodological issues and several hypotheses alternative to HGT must be considered before HGT is favored 44•, 47, 48. It is, for example, essential to check that what looks like a horizontally acquired gene is not instead a contaminant. This may be done using fluorescent in situ hybridization, as in Dunning Hotopp et al. (2007) [49] or PCR as in Li et al. (2022) [31]. Another way to discard the possibility of contamination is to find

Functional impact of plant genes in insects

Only one experimental study characterized the function of a plant-derived gene in insect [43]. Together with the predicted function of all plant-derived genes in B. tabaci, it suggests that much like bacteria-to-insect HGT [54], plant-to-insect HGT was a source of important new functions to insects, which may have facilitated adaptation to their environment. Ref. [43] showed that the protein encoded by the BtPMaT1 plant-derived gene in B. tabaci has malonyl-transferase activity, that is, it

How can plant DNA be transferred to insects?

The mechanisms underlying HT in eukaryotes remain poorly understood. That most foreign genes so far reported in eukaryotes are from prokaryotes (this is especially true for insects 31••, 66) may in part be due to the capacity of several bacteria to transfer their DNA to eukaryotic cells through conjugation [67]. Furthermore, many arthropod and other metazoan species harbor obligate or facultative intracellular symbionts [68], some of which are in close contact with the host germline genome,

Conclusions and outstanding questions

The first plant-to-insect HGT was reported recently [41] and since then 156 plant-derived genes have been found in 14 insect species from six orders. The reasons why the whitefly B. tabaci concentrates most of these genes, as well as most nonplant foreign genes among insects, are unknown. Based on a comparison between two recent studies 31••, 44•, we contend that the number of horizontally acquired genes in insects, including those acquired from plants, is likely strongly underestimated. In

Declaration of Competing Interest

None.

Acknowledgements

CG is supported by a grant from Agence Nationale de la Recherche (ANR-18-CE02-0021-01 TranspHorizon).

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