Important characteristics for diversity and evolutionary success appear to have direct origins in DNA obtained by plant ancestors at least 600 million years ago
Alexandre Affonso / Revista Pesquisa FAPESP
Genes important for the processes of plant growth and cell division appear to have migrated from other groups of living beings, without any ancestral genetic relationship. The DNA fragments seem to have been acquired through unknown methods at least 600 million years ago, by charophyte algae, the group of green algae that gave rise to land plants. Research at the Federal University of Minas Gerais (UFMG) revealed the donor organisms, as reported in an article published at the end of February in the science journal New Phytologist.
The clue that pointed to the possibility of genes being appropriated from outside a direct genetic lineage appeared accidentally. While investigating the gene sequences of enzymes that degrade carbohydrates in plant cell walls, the researchers realized that certain genes appeared suddenly on the evolutionary path — charophyte algae possess the genes but other related algae do not. “Since the chance of them having appeared by chance, through random mutations, is minimal, we decided to look in more distant species,” says geneticist Luiz Eduardo Del Bem, from UFMG.
The team then obtained genetic data from every species of living being other than plants (from bacteria to rhinos), available in the genome bank of the National Center for Biotechnology Information (NCBI), in the United States. After months of searching and comparing, they found the same genes that code for enzymes in particular species of fungi and bacteria. The finding is an example of the biological phenomenon known as horizontal gene transfer.
Another result caught the Minas Gerais researchers’ attention. Over time, and with the evolution of plant lineages, the genes acquired by horizontal transfer underwent a series of duplications (from 20 initial genes to 400 in some current plant groups) and a radical change in the role their enzymes played. Originally responsible for digesting carbohydrates as a source of energy in the cells of microorganisms, today these enzymes act both in remodeling plant cell walls during cell replication and protecting against fungi and pathogens, by digesting the chitin these invaders are made up of.
Alexandre Affonso / Revista Pesquisa FAPESP
Because the cell wall is directly involved in plants’ growth and structural support, its emergence was essential for the transition from life in water to living on land. For this reason, Del Bem believes that genetic acquisitions resulting from exchanges between microorganisms have been a critical factor in the course of evolution and biological diversity that we see today. “These are fundamental impacts in the history of the diversification of species that conduct photosynthesis and, therefore, also in all ecosystems and terrestrial life forms that depend on photosynthesis.”
Horizontal gene transfer challenges the notion that life evolves in a branching, or tree shape — as postulated by Charles Darwin (1809–1882) — with characteristics passing from one generation to the next within the same lineage. Transmission between different groups of organisms would best be illustrated in the form of an interconnected web. Although a decade ago gene exchange was seen as a rare exception and almost always typified by cases of viruses and bacteria passing genetic material to their hosts, today examples are increasingly found in more complex and distantly related species.
Most of the time it is not a random gene transfer since it involves some contact between the organisms outside the context of reproduction. Biologist Suzana Alcantara, from the Federal University of Santa Catarina (UFSC), who researches plant diversification, cites one case: the whitefly (Bemisia tabaci), which, during its evolution took possession of plant genes that allowed it to neutralize the toxins the plants used to defend themselves against insects. Another example, says geneticist Nathalia de Setta, from the Federal University of ABC (UFABC), is snake genes that were incorporated by the ancestors of modern-day bovines through contact with ticks. And there is even evidence of the passage of genes from snakes to frogs in Madagascar, most likely also through transmission by parasites they had in common. In both cases, there is the element of transposition, in that when replicating itself the gene installs itself in different parts of the genome, providing genetic variability and the possibility that new functions may arise.
For both researchers, the increasing store of whole genome sequences in databases over recent years and the ease of access to this data are behind the growing acceptance within the scientific community regarding the importance of this phenomenon in the evolutionary process. De Setta was surprised to identify “imported” genes in the drosophila flies she was studying for her doctorate, which had not been the initial objective of her research. Still, she argues that other possibilities should be exhausted before pointing to horizontal gene transfer to explain the presence of an unexpected gene.
Molecular clock The comparison method that the UFMG researchers used also allowed them to calculate when genetic incorporation most likely occurred. About 23 different genes, of both bacterial and fungal origin, became part of the DNA of charophyte algae between 750 million and 550 million years ago, during the Precambrian. The terrestrial environment during this period can be imagined as being rocky, without vegetation or animals, and inhabited by communities of microorganisms. For Del Bem, these micro-forests, formed by bacteria, algae, protozoa, and unicellular fungi, would have been the pioneers in colonizing the out-of-water environment and provided ideal conditions for genetic transfers, since, for this to occur, cells need to be physically close.
With daily, close contact with other organisms in the intestine, mucous membranes, and skin — whether they are beneficial or disease agents — gene exchanges between human cells and the cells of these organisms may be frequent. “This reinforces the view that genetic material is much more horizontally fluid than we imagined,” emphasizes Alcantara. “The extent to which this affects the evolution of genetic lineages is a point that could still be better understood, especially if we consider this constant interaction between organisms.”
Alexandre Affonso / Revista Pesquisa FAPESP
Being close to each other is the primordial condition, but the exact mechanisms of how—in each of these cases—the genetic material ended up in another organism remain unknown. There are known methods observed in nature (which even inspired the first techniques for producing transgenics), with bacteria and viruses acting as vehicles for DNA or RNA fragments. Other possibilities include exchanges that occur between mitochondria and the cell nucleus, or the direct absorption of genetic material released into the environs by the death of a cell.
American botanist Pamela Soltis, curator at the Florida Museum of Natural History, is internationally recognized for her research into the patterns of life that generate biological diversity. Soltis believes that taking into consideration the impacts of horizontal gene transfer is important in studies of plant evolution. “It’s a really fascinating process, because the new genetic material provides potentially valuable opportunities for adaptations in the receiving species,” she reflects, in an email interview with Pesquisa FAPESP. However, she emphasizes the importance of exploring how they occurred in the cases that continue to be discovered.
Soltis points out that, after the gene transfer, other evolutionary factors come into play that are also essential to understanding a certain characteristic in a species. “For example, both the duplications and the change in function that fungal and bacterial genes underwent after incorporation by algae contributed to the diversification of plants in the terrestrial environment,” she concludes.
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