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Seeking the Lineage of Plants

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In biology, we learn that there are two major groups of organisms: eukaryotes and prokaryotes. The simplest summary of the difference between the two is that eukaryotes have cells with nuclei and organelles, while prokaryotes do not. This means that prokaryotic cellular function is not isolated into particular areas of the cells. There are additional, important, differences between the two, such as DNA structure and function.
One of the important questions relevant to the origin of life is how the first prokaryotic and eukaryotic cells formed. Alternatively stated, where did the complicated organelles come from?
From what we know now, eukaryotes have cells that look like small factories where different organelles function like departments within that factory. This is a highly organized system, so from an evolutionary standpoint, it must have evolved from a simpler system. Proponents of endosymbiosis theory believe that they evolved from the “simpler” prokaryotes.
Endosymbiosis theory argues that eukaryotic organelles formed when one prokaryote engulfed another prokaryote. For a detailed analysis of this theory, see Jonathan M.’s article here.
In brief, endosymbiosis tends to overemphasize the similarities between organelles and prokaryotic organisms while de-emphasizing the not-so-minute differences. It also seems to downplay prokaryotic complexity and the evolutionary leaps that must occur for a prokaryotic organism to become integrated into another cell and start functioning as a type of proto-organelle.
In a recent Science article, Price et al. report their studies that look at the origins of plastids, major organelles within certain plant cells, in order to confirm a certain plant phylogeny. Plastids are found in plant and algae cells. The most familiar examples are chloroplasts, which are involved in photosynthesis, and are found in green plants. However there are a number of other types of plastids.
Plastids are thought to have formed from endosymbiosis, and the authors of this article take this event as factual rather than merely hypothetical, despite its being, in fact, unconfirmed:

Eukaryote evolution has largely been shaped by the process of primary endosymbiosis, whereby bacterial cells were taken up and over time evolved into double membrane-bound organelles, the plastid and the mitochondrion.

Price et al. look at plastids that were supposedly derived from cyanobacteria. These plastids all contain certain features that are similar to cyanobacteria, and those organisms that contain them are therefore thought to be along the same phylogenetic lineage. They include Glaucophyta, Rhodophyta, and green algae, along with their plant descendants.

These three lineages are postulated to form the monophyletic group Plantae (or Archaeplastida), a hypothesis that suggests the primary cyanobacterial endosymbiosis occurred exclusively in their single common ancestor.

Unfortunately, as the authors point out, phylogenies based on other features, such as genetics, do not support the cyanobacteria- and plastid-derived phylogeny.
Also, glaucophytes, a type of freshwater algae that is in the Archaeplastida family, have unique features indicative of less evolved cyanobacteria, or ancestral cyanobacteria, meaning that they may have evolved differently. Their study seeks to determine “the evolutionary history of key algal and land plant traits and to test Plantae monophyly…” by considering the glaucophyte Cyanophora paradoxa (C. paradoxa).
The authors experimentally replicated the genome of C. paradoxa and compared it to a genome database. Using this comparison, they generated phylogenetic trees showing a relationship between glaucophytes and red and green algae. They wanted to find the “footprint” of cyanobacterium-derived features in the Plantae genomes by looking at nuclear genes.

Plylogenetic analysis of the predicted C. paradoxa proteins showed 274 to be of cyanobacterial provenance. This constitutes [approx]6% of proteins in the glaucophyte that have significant BLASTp hits…as found in other algae. Of the proteins that may be destined for the plastid, 80% were derived from cyanobacteria.

Furthermore, the authors accounted for horizontal gene transfer which is a source of foreign genes that is not from endosymbiosis.
They found that the mitochondrial analyses of C. paradoxa and another distantly related glaucophyte confirms relatedness within Plantae plastids and “places glaucophytes very close to the divergence point of red and green algae.”
The authors then analyzed C. paradoxa for traits similar to those associated with plastid endosymbiosis. These include 1) sugar-phosphate transporters, 2) protein-conducting channels, 3) light-harvesting complex proteins, 4) anaerobic capabilities, and 5) carbohydrate metabolism enzymes. C. paradoxa lacks 1 and 3, but the authors found similarities that suggest a work-around for C. paradoxa‘s apparent lack in these key features.
The authors conclude that their genetic analysis of C. paradoxa unambiguously supports Plantae lineage based on cells that were derived from cyanobacteria through endosymbiosis.

Analysis of the gene-rich C. paradoxa genome unambiguously supports Plantae monophyly…laying to rest a long-standing issue in eukaryote evolution. Plantae share many genes with an EGT [endosymbiosis] or HGT [horizontal gene transfer] origin that have essential functions such as photosynthesis, starch biosynthesis, plastid protein import, plastid solute transport, and alcohol fermentation.

The authors point out the possible alternative to the Plantae linage which is worth noting in its entirety:

The alternative explanation of a polyphyletic Plantae would require the unlikely combination of a large number of independent HGT events in its major phyla followed by gene loss in all (or many) other eukaryotes. Consolidation of the Plantae allows insights into the gene inventory of their common ancestor. It is now clear that the Plantae ancestor contained many of the key innovations that characterize land plant and algal genomes, including extensive EGT from the cyanobacterial endosymbiont and retarding of plastid-destined proteins, the minimal machinery required for plastid protein translocation, and complex pathways for fermentation and starch biosynthesis.”

The authors also conclude that C. paradoxa is not an anomaly to the Plantae family, “[r]ather, the C. paradoxa genome contains a unique combination of ancestral, novel, and ‘borrowed’ (e.g. via HGT) genes, similar to the genomes of other Plantae.”
The authors reject the alternative explanation because multiple, independent horizontal gene transfer events are less likely than their proposed scenario. However, the scenario they propose, which on the surface seems simpler and therefore much more likely, is not. The authors offer no mechanism or process by which these cyanobacteria incorporated into another prokaryote and eventually became an organelle of a plant cell working in concert with the other organelles within the cell to make a fully functional, replicating cell.
This is the crux of endosymbiosis theory. It is a large leap from one prokaryotic organism engulfing another to an interactive cellular complex. Furthermore, if this did occur early on in the evolutionary timeline, then there is the significant issue of just how long it would take for this “unique combination of ancestral, novel, and ‘borrowed’ genes” events to occur.

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