Partial penetrance facilitates developmental evolution in bacteria

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Abstract
Geneticists have long known that individuals with exactly the same genetic make-up can differ from one another in their development and resulting phenotype, but the developmental and evolutionary significance of the phenomenon are not clear. The nature of this 'partial penetrance', whereby the effects of a mutation are observed only in some individuals, even in an isogenic population, has been studied using Bacillus subtilis sporulation as a model developmental system. The results suggest how mutations affecting DNA replication and cell division may act in synergy to facilitate the evolution of twin sporulation as a new trait, through progressive increases in its penetrance. Individuals with exactly the same genetic make-up can differ from one another in their development and resulting phenotype when the genome contains a mutation — a phenomenon called 'partial penetrance'. Exploration of the genetic and stochastic factors controlling the proportion of abnormal 'twin' spores in mutant populations of the bacterium Bacillus subtilus now reveals how mutations affecting DNA replication and cell division may act in synergy to significantly increase the penetrance of twin sporulation. Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fates of individual organisms differently1,2,3,4. This phenomenon, known as partial penetrance, has been observed in diverse developmental systems. However, it remains unclear how the underlying genetic network specifies the set of possible alternative fates and how the relative frequencies of these fates evolve5,6,7,8. Here we identify a stochastic cell fate determination process that operates in Bacillus subtilis sporulation mutants and show how it allows genetic control of the penetrance of multiple fates. Mutations in an intercompartmental signalling process generate a set of discrete alternative fates not observed in wild-type cells, including rare formation of two viable ‘twin’ spores, rather than one within a single cell. By genetically modulating chromosome replication and septation, we can systematically tune the penetrance of each mutant fate. Furthermore, signalling and replication perturbations synergize to significantly increase the penetrance of twin sporulation. These results suggest a potential pathway for developmental evolution between monosporulation and twin sporulation through states of intermediate twin penetrance. Furthermore, time-lapse microscopy of twin sporulation in wild-type Clostridium oceanicum shows a strong resemblance to twin sporulation in these B. subtilis mutants9,10. Together the results suggest that noise can facilitate developmental evolution by enabling the initial expression of discrete morphological traits at low penetrance, and allowing their stabilization by gradual adjustment of genetic parameters.