MiRNA Control of Vegetative Phase Change in Trees

Abstract

After germination, plants enter juvenile vegetative phase and then transition to an adult vegetative phase before producing reproductive structures. The character and timing of the juvenile-to-adult transition vary widely between species. In annual plants, this transition occurs soon after germination and usually involves relatively minor morphological changes, whereas in trees and other perennial woody plants it occurs after months or years and can involve major changes in shoot architecture. Whether this transition is controlled by the same mechanism in annual and perennial plants is unknown. In the annual forb Arabidopsis thaliana and in maize (Zea mays), vegetative phase change is controlled by the sequential activity of microRNAs miR156 and miR172. miR156 is highly abundant in seedlings and decreases during the juvenile-to-adult transition, while miR172 has an opposite expression pattern. We observed similar changes in the expression of these genes in woody species with highly differentiated, well-characterized juvenile and adult phases (Acacia confusa, Acacia colei, Eucalyptus globulus, Hedera helix, Quercus acutissima), as well as in the tree Populus x canadensis, where vegetative phase change is marked by relatively minor changes in leaf morphology and internode length. Overexpression of miR156 in transgenic P. x canadensis reduced the expression of miR156-targeted SPL genes and miR172, and it drastically prolonged the juvenile phase. Our results indicate that miR156 is an evolutionarily conserved regulator of vegetative phase change in both annual herbaceous plants and perennial trees. The existence of discrete juvenile and adult phases of vegetative development in plants was first recognized in trees, in which these phases are usually prolonged and quite stable. Annual plants also undergo changes in vegetative morphology during shoot development, but the relationship between this process and vegetative phase change in trees is unclear. This is because both the timing and the nature of the morphological changes that mark these transitions are different in these groups of plants. Here we show that the expression pattern of miR156—a master regulator of vegetative phase change in Arabidopsis and maize—is conserved in woody plants with well-defined juvenile and adult phases, and we show that over-expression of this microRNA prolongs the expression of the juvenile phase in the tree Populus x canadensis. Our results indicate that the mechanism of the juvenile-to-adult transition is likely conserved throughout flowering plants.