Another Notable Explosion: Has Darwin's "Abominable Mystery," the Origin of Flowering Plants, Been Solved? - Evolution News & Views

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Another Notable Explosion: Has Darwin's "Abominable Mystery," the Origin of Flowering Plants, Been Solved?

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We've had a lot to say in the past year about the Cambrian explosion, the subject of Stephen Meyer's book Darwin's Doubt. But that's not the only explosive event in the fossil record that disturbed Charles Darwin.

Recently Google News highlighted a story in Design & Trend magazine that trumpeted about how "DNA of Oldest Flowering Plant 'Solves' Darwin's 'Abominable Mystery'." That's pretty major exposure for a story about ancient flowers. Indeed the writer makes it sound like Darwinian theory has just come into a real windfall:."Scientists have newly sequenced the genome of the Amborella plant, one of the two oldest lineages of flowering plants, for the first time, potentially addressing Charles Darwin's 'abominable mystery' -- the question why flowers suddenly thrived on Earth millions of years ago."

An article article in Science echoes this:

Darwin famously characterized the rapid rise and early diversification of flowering plants (angiosperms) in the fossil record as an "abominable mystery." Identifying genomic changes that accompanied the origin of angiosperms is key to unraveling the molecular basis of biological innovations that contributed to their geologically near-instantaneous rise to ecological dominance.

("The Amborella Genome and the Evolution of Flowering Plants")

Well, did the study in fact identify molecular pathways from other types of plants that led to specific traits of flowering plants that have made them more successful? Or to put it another way, did the researchers identify any specific, adaptive molecular changes that might help to resolve Darwin's "abominable mystery"? No, they didn't. Rather, by comparing DNA sequences in angiosperms to other plants, they found "1179 gene lineages (orthogroups) first appeared in angiosperms" and "The new gene lineages in flowering plants may have led to gene functions specific to angiosperms and crucial for their diversification and success." In other words, a lot of crucial genes for producing flowers in angiosperms don't seem to have orthologues (i.e., homologous genes) in other types of plants. This was contrary to Darwinian expectations.
The large number of orthogroups first appearing in angiosperms suggests that a diverse collection of novel gene functions was likely associated with the origin of flowering plants. Analyses of GO [gene ontology] annotations for genes in angiosperm-derived orthogroups revealed the origin of orthogroups with functions associated with key innovations defining the flowering plant clade (table S16) (17). GO annotations related to reproduction (flower development, reproductive developmental process, pollination, and similar terms), including MADSbox gene lineages, were overrepresented in this set of orthogroups. Genes with roles in Arabidopsis floral development are included in 201 orthogroups, 18 of which were evolutionarily derived in the MRCA [most recent common ancestor] of angiosperms. Significant enrichments were also observed for several classes of regulatory genes (transcription, regulation of gene expression and of cellular, biochemical, and metabolic processes) as well as genes involved in various developmental processes. These include genes involved in carpel development, endosperm development, stem cell maintenance in meristems, and flowering time, suggesting that they might be key components underlying the origin of the flower.

("The Amborella Genome and the Evolution of Flowering Plants")

It seems that the "rapid rise and early diversification of flowering plants (angiosperms) in the fossil record" is now also supported by genomic studies, since a lot of novel genes were "associated with the origin of flowering plants."

The reason why Amborella is important to understanding the MRCA of angiosperms is because it is thought to have branched off very early in the angiosperm tree. Thus by sequencing its genome, they hoped to gain a better understanding of early flowering plants. Instead, what they found is that the mitochondrial genome in Amborella seems to be a mish-mash or conglomerate of many different sources, including both other angiosperms and non-flowering plants. And that is extremely hard to explain within a Darwinian framework. According to a news piece in Science Daily:

"The Amborella mitochondrial genome is huge, and most of its DNA is foreign, acquired from the mitochondrial genomes of other plant species," Alverson said. "We've never seen horizontal gene transfer at this scale. It's not acquiring genes or bits of genes in a piecemeal way. It's been swallowing up whole genomes. One of our main tasks was to determine the ancestry of its several hundred 'extra' genes."
Of course what they call "foreign" DNA just means that Amborella's mitochondrial genome has unique elements, and other elements that resemble other plants, including mosses, green algae, and a wide variety of other angiosperms including Oxalidales, Santalales, Fagales, and Ricinus. Because the some sections of Amborella's mitochondrial DNA resembles these species, they're considered "foreign."

If what you want to do is tell a nice, neat story of descent with modification, the evolution of Amborella's mitochondrial genome presents a severe problem. It seems especially odd to find such similarities between Amborella and other angiosperms if Amborella branched off early in the history of angiosperms, long before other angiosperm species evolved. Perhaps Amborella incorporated these other mtDNA elements much later in its history.

The authors never for a second admit that, under their Darwinian evolutionary view, these findings are odd. Instead, to explain how Amborella ended up with all these phylogenetically unexpected genomic similarities in its mitochondrial DNA, they simply invoke "horizontal gene transfer."

To help recover the evolutionary spin, the researchers speculate that Amborella's mitochondrial genomes are largely non-functional "junk" DNA:

The plant's mitochondrial genome is unusual for at least three reasons. ... "One of the really interesting things about Amborella is that although it is loaded with all of this extra DNA, most of it is junk," Alverson said. "The genes are degenerated and nonfunctional. Amborella is a hoarder. Its genome is a museum of dead DNA." ... "The Amborella mitochondrial genome is like the old lady in the song who swallows a fly, and then a spider, a bird, a cat, etc., all the way to a horse, at which point, finally, 'she's dead of course,'" Palmer said. "Likewise, the Amborella genome has swallowed whole mitochondrial genomes, of varying sizes, from a broad range of land plants and green algae. But instead of bursting from all this extra, mostly useless DNA, or purging the DNA, it's held on to it for tens of millions of years. So you can think of this genome as a constipated glutton, that is, a glutton that has swallowed whole genomes from other plants and algae and also retained them in remarkably intact form for eons."
But why would this DNA remain "remarkably intact" if it were merely useless junk that didn't perform any function? Indeed, consider this statement from another Science paper on the Amborella genome:
To gain insight into the causes and consequences of HGT [horizontal gene transfer] in mitochondrialDNA (mtDNA), we sequenced the mitochondrial genome of Amborella trichopoda because polymerase chain reaction-based sampling had shown it to be rich in foreign genes.

("Horizontal Transfer of Entire Genomes via Mitochondrial Fusion in the Angiosperm Amborella")

The reason they became intrigued with Amborella is because it's supposedly "rich in foreign genes" -- entirely functional genes, not junk DNA, apparently involved in the polymerase chain reaction. How do they then turn around and claim that all that foreign DNA which was supposedly "swallowed" from "other plants and algae" was "junk"? Well, the reason they think "the great majority of the foreign mitochondrial genes in Amborella are unlikely to be functional" is because they are thought to be "pseudogenes." Most don't appear to produce transcripts, and among those that do produce transcripts, they seemed to be "not expressed properly" or "poorly edited." Yet that results in a strange conundrum, as the paper explains:
In typical angiosperm mtDNAs, comparably old and large tracts of largely nonfunctional DNA would be expected to have mostly been lost by now, and what remained to be more highly rearranged.
In other words, all these pseudogenes in Amborella's mitochondrial DNA have remained, in the authors' own words, "remarkably intact" and "surprisingly intact with respect to overall sequence content and arrangement," despite the fact they are supposedly "nonfunctional." Normally, useless DNA would tend to be lost, either by chance or perhaps even by selection, over long periods of time. So why did Amborella not lose the non-functional "junk" DNA in its mitochondrial genome? Why has it remained, again in the paper's own words, in "remarkably intact form for ages"? It's simple, the paper concludes: "Amborella mtDNA seems, however, less prone to lose and rearrange DNA." So all this mitochondrial DNA doesn't do anything, but it's remained "remarkably intact," as if it is doing something, despite the fact that we know that it must be "junk."

In fact, it's known that pseudogenes can yield functional RNA transcripts, functional proteins, or perform a function without producing any transcript. A 2012 paper in Science Signaling noted that although "pseudogenes have long been dismissed as junk DNA," recent advances have established that "the DNA of a pseudogene, the RNA transcribed from a pseudogene, or the protein translated from a pseudogene can have multiple, diverse functions and that these functions can affect not only their parental genes but also unrelated genes." The paper concludes that "pseudogenes have emerged as a previously unappreciated class of sophisticated modulators of gene expression." Likewise, a 2012 paper in RNA Biology states that "pseudogenes were long considered as junk genomic DNA" but "pseudogene regulation is widespread in eukaryotes."

Is it possible these authors have prematurely inferred that this phylogenetically bizarre mitochondrial DNA is "junk" -- when in fact it's performing important functions? If this DNA isn't junk, that would certainly explain why it remains "remarkably intact" and "surprisingly intact with respect to overall sequence content and arrangement."

Photo credit: @Doug88888/Flickr.