GRASSES CHALLENGE DARWIN’S THEORY OF NATURAL SELECTION BY BORROWING GENES

Lateral Gene Transfer (LGT), synonymous with Horizontal Gene Transfer has been a well-known concept, especially in prokaryotes, contributing to their evolution and genetic diversity considering their asexual duplication. 

Frederick Griffith

Lateral Gene transfer was first introduced by Frederick Griffith in 1928 by his renowned experiments with virulent Streptococcus pneumoniae and further clarified by Avery, MacLeod, and McCarty. Since then it has been the talk of the town and often called “Nature’s gene editing”. Although the concept was first confined to prokaryotes, later on, researchers started observing LGT in single-celled eukaryotes and even between single-celled organisms and complex multicellular organisms. Related to the latter aspects, Phytologists from the University of Sheffield, UK suspect  LGT to be a major contributor to the long history of genetic evolution within a Grass Lineage. 

The ability of LGT goes far and beyond, For example, organisms causing infections throughout 1930 to 1945 treated with the first three classes of antibiotics had gained resistance to them by 1955 through LGT, which is rather faster than any other way of genetic evolution. In the present day, many dangerous multi-drug resistant organisms such as VRSA and MRSA have emerged due to their evolution by LGT rendering the majority of the classes of antibiotics useless. Though LGT is a key process in evolution, it is not always advantageous to the organism, some may even have deterring effects, thus such acquired genes are lost along the way. Therefore it is challenging to identify all the acquired genes in an organism since a significant part of them are lost.

LGT was extensively studied and was confined to prokaryotes, LGT in eukaryotes was even considered controversial. The development of high-throughput sequencing and phylogenetic studies eventually uncovered LGT in eukaryotes, especially in plants, a multicellular organism, LGT has been prevalent in parasitic relations. In previous studies, LGT in grasses has been observed and among them, a single Australian Alloteropsis semialata (Paniceae tribe of Panicoideae subfamily) accession has been said to have gained most genes by LGT (about 59 laterally acquired genes were investigated from nine different donors 20 to 40 million years apart) leading to several sub-species. A.semialata is said to have originated in Africa where one of its divergent genetic variants, A.angusta is still found. 

The study from the University of Sheffield generated the complete reference genome for three accessions for A.semialata, one for A.angusta  and along with the original A.semialata reference genome previously published (therefore compiling 5 reference genomes in total), compared and identified all the protein-coding laterally acquired genes (LAG). They have also surveyed the whole genome sequence of an additional 40 diploid Alloteropsis to investigate the distribution of the identified laterally acquired genes in them and map them in a time-calibrated phylogeny, estimate LAG gains and losses, compare intraspecific gene variation in LAG and amount of variation in native genes to estimate the contribution of LGT in pangenomes.   

The phytologists detected a total of 168 acquired genes from the 5 reference genomes but only two were shared by all the five. They evaluated the rate of acquisitions to be 6 to 28 genes per mega annum and predicted that about 11 to 24% of them are lost per mega annum, and also that it differed significantly among lineages. They also estimated that LAGs were lost faster than that of vertically acquired genes (genes acquired from parents traditionally) by 0.02 to 0.8% per mega annum. They suggest that these numbers indicate a high turnover number, i.e., more than 20 foreign genes enter the recipient every million years, and about half of them are lost every 3 to 6 mega annum. Further investigation of the distribution of genes in the 45 Alloteropsis individuals showed a few ancient acquisitions and many recent acquisitions restricted to sublineages. 

Alloteropsis 

The analysis of these acquired genes revealed that they serve a wide range of functions, including roles related to C4 photosynthesis, disease resistance, and tolerance to abiotic stresses like environmental factors (e.g., temperature, and salinity). The phytologists also conducted a Gene Ontology (GO) enrichment analysis, which is a way to categorize genes based on their functions. In the analysis, they found four categories that were significantly overrepresented: cellulose biosynthetic process, cellulose synthase (UDP-forming) activity, pre-mRNA 3′-splice site binding, and ribonuclease P activity. These categories are indicative of specific gene functions within the organism. They infer that these categories are less noticeable when all the genes are considered at once, because “hitchhiker” genes, i.e. neighboring genes might have also transferred along with the advantageous genes simply because they were physically attached, and would have diluted the prominence of the advantageous gene functions in the overall analysis. Hitchhiker genes might not have any particular biological relevance to the organism. They conclude by stating that further research is needed to separate the hitchhiker genes from the advantageous ones to understand the selection of genes after they have been transferred. 

The phytologists also say that the detected LAGs are only the tip of an iceberg, and the rest could have been deleted in the evolutionary process, the reason behind this is predicted to be the relevance of the function of a LAG, for example, some resistance-providing genes could be retained only during the threat of the disease and might lose them after it subsides, whereas the other categories of genes integrated into essential pathways, like core C4 photosynthetic genes acquired by A.semialata, might be retained for longer periods even replacing native genes. 

The phytologists further remark that although their models suggest a constant rate of acquisitions and subsequent losses, this is not the case. They say that LGTs depend on various factors such as the method of reproduction of the grasses (selfing would cause fewer LGTs than vegetative propagation), the presence of potential donors in close contact, population size, mechanism of transfer, and the retention of LAGs depending on the demography of the recipient species. The mechanism of LGT is still unknown, several previous publishings suggest that it could be due to illegitimate pollination, repeated pollination, or pollen tube pathway-mediated transformation where the reproduction pathway is contaminated with a third DNA. These plant transformations could occur naturally just by wind pollination and would not need any human intervention. In the same context, the study states that the ZAM1505 lineage has accumulated a notably higher number of acquired genes than the other lineages, and provided a few speculative reasons that it could be because ZAM1505 comes from a region in Zambia where A. semialata is frequently found forming clumps with some known donor species. This clumping behavior may have provided more opportunities for lateral gene transfer (LGT). In clumps, plants are in close proximity to one another, potentially facilitating the exchange of genetic material, and other reasons such as large and constant populations, and proximity to the center of origin of the species were also suspected.

The study has also estimated that the LAGs contribute to less than one percent of the overall genome of any given accession of Alloteropsis and therefore have a major influence on the pangenome of A.semialata and the joint pangenome of A. semialata and A. angusta. Since the LAGs create significant changes in the recipient from the expression of genes to the catalytic actions of encoded enzymes creating a large diversity within the species and largely influencing evolution, these LAGs are considered crucial contributors to the pangenome. 

Finally, the phytologists conclude that the ability of these LAGs to be subsequently introgressed among related species and to provide novelty to the recipient’s genome, increases the adaptability of grasses to changing environmental conditions and challenges, thus enabling rapid adaptation.

Hence, We could say that these grasses have survived and challenged Darwin's theory of Natural Selection with a smart loophole: Borrowing Genes. 

References:

Find the study here: 

1. Raimondeau, P. et al. (2023) ‘Lateral gene transfer generates accessory genes that accumulate at different rates within a grass lineage’, New Phytologist [Preprint]. doi:10.1111/nph.19272. 

Supporting material:

2. Pereira, L., Christin, P. and Dunning, L.T. (2022) ‘The mechanisms underpinning lateral gene transfer between grasses’, PLANTS, PEOPLE, PLANET, 5(5), pp. 672–682. doi:10.1002/ppp3.10347. 

3. Sieber, K. (2017) Lateral gene transfer between prokaryotes and eukaryotes, www.sciencedirect.com. Available at: https://doi.org/10.1016/j.yexcr.2017.02.009 (Accessed: 21 October 2023).