Final Report Summary - HYLIFE (Exploiting hybrids between annual and perennial plant species to identify genes conferring agronomically important traits)
Plant species differ tremendously in their life span. Perennials live for many years, flowering and producing seeds each year. By contrast, annual species only reproduce once in their life time and may survive for only a few weeks. During evolution of flowering plants these different life cycles have diverged independently many times and can arise in short evolutionary time spans. However, little is known of the genetic and molecular basis of the divergence of annual and perennials. We use the Crucifer family as a model system to study this problem, and particularly focus on the sister species perennial Arabis alpina and annual Arabis montbretiana. We generated high quality reference genome sequences of these and related species, and found that annuals typically have smaller more compact genomes. These differences are largely due to the presence of many more active transposable elements in the perennial genome. We then hybridized these species and generated a population of perennial Arabis alpina harbouring segments of the genome of annual Arabis montbretiana. Using this population, we identified genes that contribute to differences in behavior between the annual and perennial. A striking difference between these species is that perennials delay reproduction and flowering until they have acquired a greater shoot mass, whereas annuals flower rapidly as young plants. We showed that this difference occurs in the Crucifers because perennials such as Arabis alpina flower exclusively through a regulatory pathway whose activity is repressed by a small non-coding RNA. This small RNA is reduced in abundance at the apex of the plant and in the apices of branches as these become older. Therefore, as these apices age the small RNA abundance falls allowing expression of its target transcription factors, which promote flowering. Strikingly, this pattern can explain why different branches of the perennial flower at different times and how some branches are prevented from flowering until the following year. By contrast, the annual plant can flower flexibly either through the age-dependent pathway or through an independent pathway that induces flowering in response to day length and bypasses the requirement for the age-dependent pathway. Activity of this day-length pathway therefore allows annual plants to flower at a young age. We showed that we can switch the behavior of the perennial to that of the annual by introgressing a single floral regulatory gene from the annual. This gene is differentially expressed in the annual and perennial, and in the perennial acts as a repressor of the day-length pathway. The difference in expression pattern of this gene between the annual and perennial is sufficient to confer the difference in age-dependent flowering. In a second example, we showed that introgression of a single annual gene encoding another transcription factor is sufficient to promote early flowering of the perennial. When introgressed into the perennial, the annual gene is expressed earlier in development than the perennial allele. Our work shows that characteristic differences in behavior of annual and perennial plants are often caused by differences in transcription of key regulatory genes. We also find that in independent cases of annual and perennial divergence, the same differences in expression have arisen independently. Our work provides a genetic and molecular understanding of divergence of the reproductive behaviours of annual and perennial species. Most crop plants are high yielding annuals, and the exploitation of herbaceous perennials as crops is limited by their lower yields. Our work demonstrates how transfer of single annual genes into perennials can alter their reproductive patterns and increase their productivity.