Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns.
Li FW., Villarreal JC., Kelly S., Rothfels CJ., Melkonian M., Frangedakis E., Ruhsam M., Sigel EM., Der JP., Pittermann J., Burge DO., Pokorny L., Larsson A., Chen T., Weststrand S., Thomas P., Carpenter E., Zhang Y., Tian Z., Chen L., Yan Z., Zhu Y., Sun X., Wang J., Stevenson DW., Crandall-Stotler BJ., Shaw AJ., Deyholos MK., Soltis DE., Graham SW., Windham MD., Langdale JA., Wong GK., Mathews S., Pryer KM.
Ferns are well known for their shade-dwelling habits. Their ability to thrive under low-light conditions has been linked to the evolution of a novel chimeric photoreceptor--neochrome--that fuses red-sensing phytochrome and blue-sensing phototropin modules into a single gene, thereby optimizing phototropic responses. Despite being implicated in facilitating the diversification of modern ferns, the origin of neochrome has remained a mystery. We present evidence for neochrome in hornworts (a bryophyte lineage) and demonstrate that ferns acquired neochrome from hornworts via horizontal gene transfer (HGT). Fern neochromes are nested within hornwort neochromes in our large-scale phylogenetic reconstructions of phototropin and phytochrome gene families. Divergence date estimates further support the HGT hypothesis, with fern and hornwort neochromes diverging 179 Mya, long after the split between the two plant lineages (at least 400 Mya). By analyzing the draft genome of the hornwort Anthoceros punctatus, we also discovered a previously unidentified phototropin gene that likely represents the ancestral lineage of the neochrome phototropin module. Thus, a neochrome originating in hornworts was transferred horizontally to ferns, where it may have played a significant role in the diversification of modern ferns.