Responses of ferns to red light are mediated by an unconventional photoreceptor

Abstract

Efficient photosynthesis is essential for plant survival. To optimize photosynthesis, plants have developed several photoresponses. Stems bend towards a light source (phototropism), chloroplasts move to a place of appropriate light intensity (chloroplast photorelocation) and stomata open to absorb carbon dioxide. These responses are mediated by the blue-light receptors phototropin 1 (phot1) and phototropin 2 (phot2) in Arabidopsis (refs 1-5). In some ferns, phototropism and chloroplast photorelocation are controlled by red light as well as blue light. However, until now, the photoreceptor mediating these red-light responses has not been identified. The fern Adiantum capillus-veneris has an unconventional photoreceptor, phytochrome 3 (phy3), which is a chimaera of the red/far-red light receptor phytochrome and phototropin. We identify here a function of phy3 for red-light-induced phototropism and for red-light-induced chloroplast photorelocation, by using mutational analysis and complementation. Because phy3 greatly enhances the sensitivity to white light in orienting leaves and chloroplasts, and PHY3 homologues exist among various fern species, this chimaeric photoreceptor may have had a central role in the divergence and proliferation of fern species under low-light canopy conditions.

Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy

“…15, we see the signature of this third fern radiation in the Cretacaeous beginning soon after the rise of flowering plants. This radiation was likely an ecological opportunistic response to the establishment of more complex angiosperm-dominated ecosystems and, based on our current findings, was at its inception almost entirely restricted to niches on the forest floor, the occupation of which was possibly facilitated by the evolution of a unique photoreceptor in polypods (18). In this study, however, we also find evidence for what we interpret as a fourth leptosporangiate radiation in the Cenozoic, which appears to be driven by the evolution of epiphytism and the subsequent invasion of the angiosperm-dominated canopies of modern tropical rain forests soon after their origin.…”

“…But why were leptosporangiates able to flourish as other nonflowering vascular plant lineages floundered? In part, their success may be linked to acquiring a unique photoreceptor that enhanced their sensitivity to light (in orienting leaves and chloroplasts) (18) and likely allowed them to better occupy the shady floors of angiosperm-dominated forests (15). Traits associated with the evolution of epiphytism-a capacity to reside on an above-ground plant surface while not extracting water or nutrients from the host plant or the ground (19)-may also have played an important role.…”

Targeted knockout in Physcomitrella reveals direct actions of phytochrome in the cytoplasm

“…This is intriguing with respect to recent findings in the fern Adiantum (39). Here an unusual phytochrome-related protein, Adica;PHY;3, a phytochromephototropin chimera, mediates R-induced phototropism and chloroplast photorelocation.…”

Evolution of the Stomatal Regulation of Plant Water Content

“…Extant lycophyte and fern stomata have the capacity to open rapidly in the light (Mansfield and Willmer, 1969;Doi and Shimazaki, 2008;McAdam and Brodribb, 2012), with lycophyte stomata possessing both photosynthetically driven stomatal opening in red light-as well as blue light-triggered opening, while leptosporangiate ferns (which comprise more than 96% of fern specific diversity; Palmer et al, 2004) have lost blue light stomatal signaling (Doi et al, 2015). The reason behind this loss of blue light stomatal signaling in derived ferns is, as yet, unknown, but may be due to a chimeric red-blue photoreceptor, an adaptation associated with photosynthesis in low light environments (Kawai et al, 2003).…”