In normal times, the genes peppered across a plant’s DNA function more or less according to the common metaphors of popular science. Here, they look very much like ‘instructions’ used to build the plant’s body and direct its behaviour. But when a plant encounters an unexpected circumstance, things get wild. The instruction metaphor breaks down, and a new insight into the interconnected nature of genes, organism and environment is revealed.
I will zoom in on one wild phenomenon here, to make the point. Forty years ago, cracks in the genes-are-instructions metaphor had already appeared with the discovery of ‘alternative splicing’ (Berget et al, 1977). Alternative splicing occurs when a gene gets transcribed differently than ‘usual’. One way to think about what this means is to imagine a gene to be a paragraph of text. Under normal circumstances, the gene is expressed by pulling specific words and sentences from the paragraph and putting them together to be read. But in certain conditions, some of those words or sentences might be omitted, or others put in. In language, this amounts to a change in meaning. In genetics, this means changed physiology and behaviour.
Gene transcripts are shuttled away to get translated into long stringy molecules called proteins. Different parts of proteins push and pull at each other, and the strings often fold into complex but very specific shapes that then specify how the protein interacts. A dizzying array of different protein shapes enable and participate in an equally dizzying array of functions. If alternatively spliced transcripts are translated, these proteins —known as protein isoforms— have a different shape than their regular counterparts, and so can interact differently.
Some protein isoforms seem like well-established alternatives that can be pumped into action in the face of common disturbances, such as drought. But not all alternative proteins are evolutionarily conserved ‘Plan Bs’ waiting idly in the toolkit (Mastrangelo et al. 2012). For better or worse, it appears the number and nature of protein isoforms is not prescribed. A door is opened for the creative role that chaos plays in plant life. Some isoforms turn out to be nonfunctional. They are quickly degraded and their building blocks re-used. Others wreak havoc in the form of deformity and disease. Still others end up assisting the plant in new ways.
It turns out that alternative splicing in plant genes is especially prolific when a plant is encountering a novel stress. Why would a plant bother creating all these variants, with nonfunctional or unpredictable effects, at a time that requires urgent coordinated response? The answer turns out to be exquisitely Darwinian: in precarious times, it may be advantageous to produce a lot of new possible solutions to a danger. To do so, it adopts a randomization strategy. In risky times, it pays to take risks. Doing so, the plant increases the odds of an adaptive response. By generating variations of its gene products, the plant is increasing its repertoire, brainstorming without a brain.
This is roughly the same thing that happens in species at the population level in the process known as ‘natural selection’ (Darwin 1859): diversity in a population of organisms increases the likelihood that when given an environmental disturbance, at least some organisms of that species will survive long enough to pass on their genes. At the organism level, alternative splicing increases the chance that some behavioural response to a stress will be beneficial for the plant’s survival.
So, plant genes are more likely to produce predictable proteins when living conditions are stable, but the plant quickly generates creative chaos out of its genes when it needs to. With this insight, what happens to the ‘instruction’ metaphor? It seems to me this: the plant regulates and deregulates its genes, streamlining their effects in some contexts, relaxing those constraints in others. When genes behave in a streamlined way, it looks like they are deterministically instructing the plant cells. But alternative splicing during stressful conditions shows that if such determinism sometimes exists, it is only because the plant is determining it. The instructor is the organism, shifting how it uses its cellular resources in response to its shifting environment. In some situations it relies on routine, in others on creativity.
Alternative splicing is common in all eukaryotes, not just plants. But because plants cannot escape threats by running, slithering or flying away, the capacity to generate novel possible solutions seems especially crucial to the way they make a living. Readers of this journal will know that the ‘secondary metabolism’ of a plant is the set of processes whereby plants generate those complex chemical orchestras that so define their unique contributions to ecology as much as to economy. Consider the deluge of alkaloids, polyphenols, and terpenes that plants bring into the world: it is these chemicals that are used to ward off pests and attract allies, but that are also concentrated into tinctures and suffuse our aromatherapies. Notably, the secondary metabolism of plants seems highly susceptible to alternative splicing. For instance, 75% of Solanum lycopersicum (tomato) genes associated with producing secondary metabolites undergo alternative splicing (Clark et al. 2019).
In humans, there are more genes getting alternatively spliced —and spliced in more different ways— in the brain than anywhere else in the body (Yeo et al 2004). Just as animals employ alternative splicing to increase the problem- solving versatility of their neurons, plants use it to improvise volatile variations on their favoured fragrant themes.
Welcome to jazz ecology.
(originally published in Herbology News)