Trends in Ecology & Evolution
OpinionReducing the genome size of organelles favours gene transfer to the nucleus
Section snippets
The unidirectional transfer hypothesis
The unidirectional transfer hypothesis suggests that genes can move only from organelles to the nucleus, because one or more of the steps described in Box 1 are more likely to occur in one direction (towards the nucleus) than in the other. For example, Step 1 (sequence transfer to the nucleus) could be unidirectional: organelles would be unable to import nucleic sequences, perhaps because transfer is more frequent from a multicopy genome to a single copy genome than the reverse 10. A slightly
Free radical and Muller's ratchet hypotheses
Once the genetic redundancy following Step 2 is established, any copy can be lost (Box 1). Repeated sequence transfers, followed by random loss at Step 3, could lead to gene transfer (the ‘gene transfer ratchet’) 12. However, the expression of the new nuclear copy is likely to be less accurately regulated and less adapted to (eco)physiological needs than that of the original organelle copy 9: why then does it survive? A role for selection at this step can be addressed by evaluating the outcome
Selection for small genome size as an alternative explanation
Loss of organelle genes could be favoured if, in intracellular life forms, there is selection for smaller organelle genomes. The size of the eukaryotic host genome is less constrained 40, as shown by the presence of noncoding sequences. No selective pressure specifically favours nuclear loss and asymmetric gene loss could be selected after genetic redundancy has been achieved by gene transfer (Fig. 1b) or gene substitution (Fig. 1a). There is a long-recognized trend towards genome size
Organelle genome compactness
Selection for small genomes also accounts for organelle genome compactness. Pseudogenes are uncommon in organelle genomes and intergenic spacers are rather short. Unnecessary genes often undergo deletions; for example, the fast elimination of photosynthetic genes from nonphotosynthetic plastids of Epiphagus (a parasitic angiosperm of recent origin 29) and Plasmodium (the causal agent for malaria, which possesses a highly derived plastid 16) (Table 1). Note that the loss of pseudogenes in
Selection pressures acting on organelle genome size
Selective pressure for small size is probably not continuous, but it might act at some stages of the life cycle, mainly those requiring fast division. Some limited stages, such as the zygotic bottleneck 36 or gametogenesis 49, can be of major importance for cytoplasmic organelle populations. Similarly, accumulation of deleted mitochondria during ageing varies among human tissues 50, indicating different selection pressures.
The pressure might not even be constant at the phylogenetic level and
Conclusions
Selection for small genomes, through replicative advantage and/or increased metabolic efficiency, contributes to the genetic reduction of endosymbionts, independently of their eukaryotic or prokaryotic origin, either through gene transfer or through substitution of nuclear genes (Fig. 1). Combined, it leads to the increasing control of organelles by the nucleus. Acquisition of new genes by organelles, although genetically and cytologically possible, is greatly hampered by this selection in most
Acknowledgements
We wish to thank A. Atlan, G. Dujardin, A. Rötig, P. Saumitou-Laprade and B. Sears for helpful discussions, and S. Loiseaux-De Goër for help in preparing Table 1. We also acknowledge two anonymous referees for their comments on this Opinion.
Glossary
- Biolistic methods
- experimental genetic transformation using tungsten bullets and a gun to enhance DNA penetration in the cells.
- Coenocytic
- cell with numerous nuclei within a single cytosolic space.
- Endosymbiosis
- mutually beneficial association of two organisms, with one living in the cells of the other. [Primary endosymbiosis: symbiotic engulfment of a bacterium by a eukaryotic cell. It can lead to organelles surrounded by two membranes (the outer one deriving from the phagocytotic membrane).
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