Hopeful monsters

17 May 2013 by Malcolm Campbell, posted in Biology

Monsters are tragic beings. They are born too tall, too strong, too heavy. They are not evil by choice. That is their tragedy." Ishirō Honda (1911-1993)

Sometimes monstrous things lurk at our feet.

As proof positive, while I was gazing down the other day, I spotted a monstrously large dandelion flower right where I stood.

Now, dandelions are quite commonplace at this time of the year. Mild temperatures and moist soil have promoted an explosion of blooms. Parklands and lawns are festooned with rather unassuming smatterings of dandelion yellow.

Given the preponderance of dandelions, perhaps it shouldn’t be surprising that some extraordinary variant might emerge from time to time. Even natural variation within a population might yield some individuals at the extreme of a given scale. In the case of growth, for example, one might expect some large flowers and some small flowers. The thing was, the flower I saw fell outside the extremes of normal variation. It was “extra-ordinary” in the original sense of the word.

The floral head of the monstrous dandelion was double the size of the regular flower. It was as though two flower heads had fused. In keeping with this, the underlying floral stem was at least double the thickness of a regular stem. In botanical terms, the plant I had found is said to be fasciated. Fasciated plants are characterised by an enlarged shoot apex, accompanied by thickening of related organs, such as flowers and stems.

As someone who has spent much of their adult life either looking at or looking for mutants, my reflex reaction when finding something of the sort of the unusual dandelion is to think it might be a mutant. This is not an unreasonable supposition.

Mutants, of course, are common in nature. As their name implies, mutants are the products of mutations, heritable changes to the DNA code. Mutations arise periodically through a variety of mechanisms. This includes the normal process of DNA replication, which can incorporate errors into genes. If such errors occur in the DNA of cells that give rise to eggs or sperm, the mutations are then transmitted from one generation to the next.

Most mutations are benign, and create no visible trait. What’s more, most mutations are said to be recessive. A mutation is recessive when any trait arising from the mutation is only visible when all copies of the gene in a cell must have the mutation. For humans, and most plants, where there are generally two copies of the every gene in most cells of the body, both copies must carry the mutation to see the trait, if the mutation is recessive. In some rare circumstances, the mutation may be dominant, where only one mutated copy of the gene is necessary to produce a mutant trait.

Fasciated mutants are well known across many plant species, including tomatoes, tobacco, soybean and maize. The best-characterised fasciated mutants are found in thale cress. Thale cress, also known as Arabidopsis, is the laboratory rat of plant biology.

There are many different fasciated mutants of Arabidopsis. Of these, the most thoroughly understood are the clavata mutants. The clavata mutants are products of recessive mutations in any one of three different CLAVATA genes, named CLAVATA1, CLAVATA2 and CLAVATA3.  [It’s worth noting the use of italics and letter case here. Generally speaking, for plant biologists, italics are used when referring to a gene or a mutant. Similarly, generally speaking, lower case letters indicate a recessive mutation; whereas, the upper case letters indicate the normal, generally dominant, un-mutated version of a gene.]

The CLAVATA genes encode components of a signalling system that functions at the apex of a plant stem. The apex contains all the cells that will give rise to the plant body. The cells in the apex are the plant equivalent of animals’ stem cells. Think of them as stem cells that literally reside in a stem. Plant size is dependent, in large part, to the activity of these cells. They function as little cell division factories, giving rise to all the cells that will differentiate to become different parts of the plant body – stems, leaves, and flowers.

The CLAVATA genes encode a little circuit that ensures that the rate of apex cell proliferation is precisely what is needed by the plant. If the plant carries two copies of a mutation in any one of the three CLAVATA genes, so that one of these genes is not functional, then apex cell proliferation is not held in check, and the plant produces more cells, and larger organs. In this way, you end up with a fasciated mutant.

When I spied the dandelion variant, my first assumption was that it was likely a mutant, something like an Arabidopsis clavata mutant. Given the number of dandelions in the field where I stood, it seemed reasonable to suspect that one might be a mutant.

We know that mutations of this sort are the raw material of evolution. The periodic, random appearance of mutations provides material upon which natural selection acts. If the mutant trait confers a reproductive advantage under the prevailing conditions, the mutant will proliferate, and eventually be the predominant representative of the species. This domination may proceed to the point where the mutant defines the species. Evolution in action!

The fasciated dandelion at my feet represented such a remarkable possibility for evolution. It was, in the parlance of the last century, a “hopeful monster” – a mutant variant with large differences in a trait that could confer a strong selective advantage. The large flower, could, in theory, produce larger numbers of seeds than the regular dandelions. Over time, assuming the trait was heritable, the mutant’s lineage would overwhelm those plants that produced regular amounts of seed. Eventually, this “hopeful monster” would dominate. It would be the species. Such are the immediate thoughts of a biologist standing with an extraordinary dandelion in a field of blossoms.

Fortunately, sober second thoughts prevailed. The first thought was that the likelihood of my being the sole person on Earth to ever encounter a fasciated mutant dandelion was pretty low. Given this, why hadn’t other “hopeful monster” dandelions prevailed and become a new species? While not a fatal blow, my hypothesis already looked like it was on shaky ground.  In fact, my “hopeful monster” hypothesis was itself looking like a “hopeful monster” – an interesting new idea to me, but one that was unlikely to survive the selection pressure imposed by further examination.

The hypothesis was further undermined by the basic biology of dandelions. Like some plant species, dandelions have a rather interesting genetic composition. You and I, and organisms as diverse as poplar trees, polar bears and fruit flies, all have two copies of each gene in most of our cells. Dandelions have three.  As most mutations are recessive, including the known fasciation mutations, this means that dandelions must have mutations in all three copies in a given gene for a trait to arise. While not impossible, the likelihood of this is very low. In fact, the likelihood is low enough so as to undermine the possibility that I had discovered a mutant. Given this, what was the likely cause of my fasciated dandelion?

No less remarkable than a mutation, it turns out that fasciated dandelions can arise through a variety of environmental factors. As we considered above, fasciation occurs when the plant’s apex cells don’t function properly. Consequently, any environmental factor that disrupts normal apex activity has the potential to cause fasciation. Key amongst these is damage to the apex. Damage can occur through mechanical means – when an insect or other herbivore munches on the apex, for example. Alternatively, the apex may be damaged by harsh conditions such as frost.  Both types of damage are known to cause fasciation.

Some plant pathogens are also known to induce fasciation. Some viruses and bacteria have been cited as inducers of fasciation. One bacterium is so known for its ability to cause fasciation that it carries this trait in its name, Rhodococcus fascians. Rhodococcus fascians is a fascinating bacterium that has evolved a mechanism to specifically induce fasciation. Rhodococcus fascians carries a suite of genes that induce fasciation. One gene that encodes an enzyme that synthesises a plant hormone. This hormone is a natural inducer of fasciation.

In light of the fact that multiple environmental factors, from frost to bacteria, could induce fasciation, it seemed that my remarkable little discovery was more likely the product of environment, than of genetics.

Score one for sober second thoughts over “hopeful monster” hypotheses!

This underscores an important point – one that applies equally to the evolution of organisms as it does to the evolution of ideas.  From time to time, on both biological and intellectual landscapes “hopeful monsters” do appear. Sometimes these are large, truly novel changes that are transmitted, proliferate, and eventually dominate. On other occasions, these hopeful monsters are the merely the product of the environment. The prevailing conditions create the hopeful monster, but the change is contingent on those conditions, is not transmitted, and disappears as quickly as it appeared.

I can’t help but think that some notions about what science is, and what science isn’t, fit in the category of an environmentally-induced hopeful monster. Preoccupation with economic growth and/or recovery has created a unique intellectual environment. This environment has induced some policy makers to question the value of basic science – unless science has some obvious applied benefit to the economy, or to society more generally, it is deemed devoid of value. Consequently, some policy makers propose prioritising science that is directed toward application – backing that science with some sort of commercial outcome. This thinking seems an environmentally-induced hopeful monster.

When considered in the context of the broader scope of human history, the nature of scientific discovery, and the way in which innovation emerges from discovery, the notion that applied science is the only science to be valued is seen for what it is – a product of the times – not worth transmitting, promulgating, or allowing to dominate. Like my hopeful monster dandelion hypothesis, this is a monstrosity that really must die.

References:

Chouard T (2010) Revenge of the hopeful monster. Nature 463: 864-867

Clark SE  et al. (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119: 397-418

Crespi M et al. (1994) The fas operon of Rhodococcus fascians encodes new genes required for efficient fasciation of host plants. Journal of Bacteriology 176: 2492-2501

Laufs P et al. (1998) Cellular parameters of the shoot apical meristem in Arabidopsis. The Plant Cell 10: 1375-1389

Leyser HO & Furner IJ (1992) Characterisation of three shoot apical meristem mutants of Arabidopsis thalianaDevelopment 116: 397-403

Rojo E et al. (2002) CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. The Plant Cell 14: 969-977

Images: All photographs by Malcolm M. Campbell.

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2 Responses to “Hopeful monsters”

  1. Jim Woodgett Reply | Permalink

    Lovely piece. No need for mutations in all three genes if a mutant allele is dominant, although that is a rarer effect. Love the journey from monster dandelion to political trends to applied science. Even the UK Science Advisor, Mark Walport, claims his role is to ensure scientific knowledge is translated into economic growth: http://www.guardian.co.uk/commentisfree/2013/may/14/oxford-university-takes-shell-funding

    Will our advisors soon be telling artists than the only art worth creating is that which is useful (or makes money)?

    • Malcolm Campbell Reply | Permalink

      Thanks for the very kind feedback, Jim. I fear that you are correct about the direction that government funding of both the arts and the sciences may take - at least in the near term. The "return on investment" trajectory has been adopted by many governments worldwide, with "return" defined as some sort of near-term economic benefit. This is, of course, a facile way to ascribe value to arts and sciences. The arts and sciences certainly do have near term tangible economic benefits - but they also have longer term tangible economic benefits, collateral economic benefits, and a swath of substantial benefits that are neither economic nor material. What value do we ascribe to knowing, understanding, sharing and connecting? These things have immense value, but one that gets lost in the current valuation process. That is something worth fixing.

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