Fungi Shed Light on Deep Biological Mysteries

Fungi are among the least studied and least understood organisms.  Elevated from plants to their own kingdom in 1969, they are extremely diverse yet difficult to observe, since many species cannot be grown in the lab.  The gaps in our knowledge of the fungi are being filled by new efforts to catalog them, but one of the most interesting findings may come from analysis of their genomes.  A new study shows that introns (intragenic regions) are more dynamic than previously thought.

How do you pronounce fungi?  Everyone knows the singular fungus, but the plural gets a variety of pronunciations.  Dictionary.com allows for either fun•jie or fun•guy as appropriate; David Attenborough usually says fun•ghee.  Take your pick; they are still fun to look at (see cute mushrooms at Flickr.com) – but no fun if you eat the wrong ones.  Never eat a mushroom in the wild!  Every healthy, safe mushroom has a look-alike that is poisonous.  The diversity of fungi is astonishing.  Some even glow in the dark.

Fungi are extremely important to the whole biosphere.  The BBC News said that “fungi, which fall between plants and animals on the tree of life, are the hidden helpers of our environment: they recycle waste and dead matter, and provide plants with water and nutrients.”  Dr. Martyn Ainsworth, a fungus researcher at the Royal Botanic Gardens at Kew, said, “They are absolutely fundamental to ecosystems. Fungi are really the behind-the-scenes team that are doing all the work.”  But as we know, humans have to deal with economic downsides of unwanted fungi like rusts, molds and blights.  The BBC article said that some of the most interesting findings are coming from genetics.

An example was just published in Current Biology.¹  Torriani et al. announced “Evidence for Extensive Recent Intron Transposition in Closely Related Fungi.”  Introns are non-coding DNA found between the “exons” – the coding parts that have to be spliced together after transcription from DNA to make messenger RNA.  Why are these introns, like spacers, transcribed, only to be clipped out?  Why does intron density vary by three orders of magnitude among eukaryotes?  These have long been mysteries.  Torriani et al. studied three closely-related species of fungi and found “74 intron positions showing intraspecific presence-absence polymorphisms (PAPs) for the entire intron.” 

Even more mystifying, they believe their analysis “showed that intron gain or loss was very recent.”  They didn’t say how recent, but one instance they identified as “very recent,” i.e., not millions of years.  Variations of the word “recent” appeared 22 times in their paper.  Further, they found “direct support for extensive intron transposition among unrelated genes.”  They found a case of intron gain, and cases of intron loss.  Apparently, introns are moving around and showing ongoing changes. Their abstract dropped this bombshell: “The large number of intron positions in transient phases of either intron gain or loss shows that intron evolution is much faster than previously thought and provides an excellent model to study molecular mechanisms of intron gain.”  How can this be, if fungi were among the first in evolutionary theory to appear, and have been evolving for billions of years?  A host of new questions arise if this is true.  How can genomes maintain stability in the face of dynamic intron gains and losses?  Is this dynamism true just for fungi, or is it characteristic of other eukaryotes?  What are the introns doing?  What mechanisms create, alter or remove them?

Unfortunately, we have more questions than answers at this time.  Torriani et al. did not discuss the functions of these introns; their goal was just to identify the dynamics; “the origins of introns are poorly understood,” they said.  For example, “The frequency of intron PAP at locus ID-54115 was highly variable, ranging from 0% to 90% among M. graminicola populations, but was fixed in both S1 and S2 (Figure 1C). This example illustrates a rapid intron loss, because half of the sampled populations completely lacked the intron.”    Other examples of “rapid transitions” and “rapid introgression” were described in the paper, yet other PAPs can persist in populations for a long time.

The closest thing to a theory they presented was in a section entitled, “Intron Transposition Is a Major Mechanism Generating New Introns.”  While some introns remain fixed, others vary.  The authors struggled with multiple hypotheses for their data.  “The large families of highly similar intron sequences found in these genomes suggest that certain intron sequences are much more likely to be transposed than others and that specific sequence patterns may promote transposition,” they said, recalling theories of mutational hotspots.  In another instance, “intron gains can result from recombination in the intron-flanking regions among paralogs.”  Comparing intron PAPs in paralogous and duplicate genes is adding to our knowledge, but not necessarily our understanding.  Here’s a sample of the confusion:

A previous study analyzing distantly related fungi revealed that some genes were hotspots for IGLs over evolutionary time [30]. Five genes in M. graminicola showed multiple intron PAPs (Table S1). To our knowledge, this is the first report of multiple intron PAPs occurring simultaneously within a single gene of a species. For all five genes, the most parsimonious explanation for multiple intron PAPs within a gene is the retention of ancestral sequences within the locus. Incomplete lineage sorting is frequent within the studied fungal clade [26] and provides a previously unrecognized mechanism for the retention of intron PAPs within species. This contrasts with multiple independent intron gains at the same intron position that were reported in Daphnia [5].

What can we conclude at this point?  “We present direct evidence of gains through intron transposition and intron transfer among paralogs,” they said, but that is like observing a process without understanding it.  Their findings at this point are only “suggesting that transient stages in the gain or loss of introns may be much more common than previously thought from the comparison of evolutionarily distant genomes.”  Other than assuming evolution and “evolutionary time,” the authors had little to say about evolution.

1. Torriani, Stuckenbrock, Brunner, McDonald and Croll, “Evidence for Extensive Recent Intron Transposition in Closely Related Fungi,” Current Biology, 17 November 2011, doi. 10.1016/j.cub.2011.10.041.

It’s unwise to be dogmatic about ideas for a phenomenon under investigation like introns, but what seems highly unlikely is that these dynamic changes have been going on for billions of years.  “Living fossils” show that animals and plants can maintain their outward morphology for whatever periods of time you believe in.  Does it make sense to think that rapid changes in intron gain and loss have been going on for billions of years?  The longer the time, the more scrambled a genome would become.  If not unscrambled for all that time, that would provide evidence that introns are being regulated by a mechanism that prevents scrambling.  Either way, the idea of unguided evolution loses credibility.

By bringing to the table the assumption that introns are purposeful and functional, intelligent design scientists can offer two benefits to the study of introns in fungi.  (1) A design-theoretic outlook on the problem.  As an example, they could look at introns as elements of a to-be-understood storage network system.  Previous work has shown introns as essential components of alternative splicing (5/06/2010, 4/5/2010, 2/06/08) .  In his new book The Myth of Junk DNA (Discovery Institute, 2011, available from Amazon.com) intelligent-design molecular biologist Jonathan Wells devoted a whole chapter to possible functions of introns: among them, regulators of gene expression during embryonic development, regulators of alternative splicing, storage regions for micro-RNA enhancers, and timers for transcription.  (2) A design-theoretic outlook on the ecological role of fungi.  ID scientists would not look at fungi in isolation, wasting time looking for common ancestors in some pre-vertebrate world, but see fungi as part of a grander purpose in a functional biosphere.  They would view the world as an ecological system, seeing the fungi as providers of essential services for the whole, including man – the only organism on Earth actively sequencing genomes and wondering how they work.