Evidence Linking miR156, a Master Regulator of Phase Change, to Heterochrony in Eucalyptus

Heterochrony – a change in the timing or rate of developmental events throughout ontogeny – is a major evolutionary process in plants and animals.  It has been argued that just a few changes in genes which regulate developmental events might produce markedly different morphologies in descendants and provide a means of rapid adaptive evolution.  In plants, such changes are particularly significant when they involve the timing of developmental events such as vegetative phase change in heteroblastic species.  The Australian forest tree Eucalyptus globulus is strikingly heteroblastic, with clear differences in the morphology and orientation of juvenile and adult leaves, but also differences in leaf anatomy, physiology, chemical composition and resistance to pests and diseases.  We studied the genetic basis of ecotypic differentiation between a coastal population of E. globulus with precocious vegetative phase change and populations in which the timing of vegetative phase change is more characteristic of ‘normal’ E. globulus.  Recent research has implicated two microRNAs (miR156 and miR172) as master regulators of vegetative phase change across a diverse range of plants, but a link between polymorphism in this regulatory network and adaptation in natural populations remains to be demonstrated.  Here, we present multiple lines of evidence (QTL, genome scans and expression analyses) that link major differences in phase change phenotype between precocious and normal ecotypes of E. globulus to variation in a single miR156 gene.  Our findings highlight the evolutionary importance of this regulatory network and a mechanism by which heterochrony could cause rapid differentiation and speciation in plants.