ARTICLE: Tension and Resolution

Tension and resolution: dynamic, evolving populations of organelle genomes within plant cells
IG Johnston
Molecular Plant 12 764 (2019)

Mitochondria and chloroplasts are compartments in cells that power complex life. Both started out billions of years ago as independent organisms with complete genomes, that were acquired by ancestral cells. Since these endosymbioses, the genomes of mitochondria (mt) and chloroplasts (cp) have become stripped down. Modern mt and cp have lost lots of genes either completely or the “host” cell nucleus. Mt and cp now exist in dynamic populations within the cells of modern organisms. In plants and algae, the two co-exist, sharing responsibility for the energy balance of the organism – and hence ultimately powering and feeding life, including the human population.

Plant mt and cp populations are weird. Different plants and algae have very different mt and cp genomes – some huge (many megabases, several chromosomes in the case of some mt) and some tiny. Unlike the more familiar animal (and human) case, plant mt genomes readily recombine, mixing up their structures and genetic content within the cell. Both mt and cp move around plant cells rapidly – we’re not sure why, particular for mt. Again, unlike animal mt, neither plant mt not cp are particularly prone to meet up and fuse into big networks – they usually stay as individual compartments, except for short interactions. We do know that if we perturb the physical or genetic dynamics of organelles, the plant suffers – which we can sometimes exploit in breeding efficient crops.

 Populations of mitochondria (A green, B) and chloroplasts (A blue, C) moving in the plant cell

In a recent review article here in Molecular Plant, we reviewed current knowledge about these dynamics and speculated about what principles these populations of mt and cp may be responding to. We first asked why mt and cp may retain different sets of genes in different species – a question we’ve touched upon before here (blog). Retaining more genes in organelles may have the “pro” of making individual organelles more independent, and better at responding to demands (see John Allen’s CoRR hypothesis, e.g. here). But there’s the “con” that organelles are dangerous places, and genes retained there may be more subject to damage than in the safe haven of the nucleus. So individual plants may choose to retain mt and cp genes for dynamism, or shift them to the nucleus for robustness. Neither extreme is perfect – there are always pros and cons – leading to a tension to which different plants have selected different resolutions.

Pursuing this line, we next speculated that because plants are immobile (and hence unable to move away from challenging conditions), they may favour the “dynamism” side over the “robustness” side. This would explain why they often retain more organelle genes than motile organisms, but would also predict that they face a double challenge: (i) more organelle genes and (ii) exposure to more challenging environments, both of which may lead to genetic damage. This could be a reason why plant organelles undergo recombination – as a way of ameliorating genetic damage. But again, there are pros and cons: the “pro” of fixing genetic damage is balanced by the “con” of recombination mixing and confusing genetic structure. Perhaps this is why the physical behaviour of plant organelles is different to that in animals – keeping mt and cp separate may limit the amount of recombination that can take place, allowing the plant to control this second pro-con tradeoff.

 

(left) the proposed tension between robustness (i) and dynamism (ii). Perhaps plants are more (ii)-like because they need to respond to fluctuating conditions... because of their immobility (right) with hypothesised knock-on consequences.

All of these ideas are presented as hypotheses, and we proposed some ways that a combination of new experiment and theory can help make progress understanding these complex, vital systems in future. Watch this space! Iain