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Evolution of light perception networks in plants

Genetically identical plants develop rather differently depending on the light conditions in which they live. In the dark, the plant grows in length in order to reach the sunlight needed for photosynthesis. Exposed to light, the plant then switches to a different development programme, becomes green and assembles its photosynthesis machinery. Prof. Dr. Andreas Hiltbrunner from the Institute of Biology II at the University of Freiburg is interested in finding out how the light-induced switch between these two programmes is regulated. Working with systems biologist Prof. Dr. Christian Fleck from the University of Wageningen in the Netherlands and molecular biologist Prof. Dr. Enamul Huq from the University of Texas at Austin in the USA, Hiltbrunner is exploring how reactions to light have developed and enabled plants to grow. The project, which starts in autumn 2013, is funded under the Human Frontier Science Programme (HFSP) with funds totaling more than a million US dollars.

Arabidopsis thaliana, commonly known as thale cress, and Physcomitrella patens, a type of moss, are popular model organisms used in scientific research. © Prof. Dr. Andreas Hiltbrunner, University of Freiburg

Light is essential for the growth and development of plants. Depending on the brightness and spectral composition, light induces species-specific reactions in plants. Phytochromes A and B are plant proteins (i.e. pigments, photoreceptors) that perceive light and trigger reactions similar to those triggered by the human visual pigments. Prof. Dr. Andreas Hiltbrunner from the University of Freiburg and his colleagues are investigating how the model plant Arabidopsis reacts to light and transduces signals to control the activity of various genes. 

“We are specifically interested in phytochromes,” said the plant physiologist. “Researchers have recently found out that phytochromes are translocated into the nucleus after they have been activated by light.” The transfer of phytochrome A (PHYA) into the nucleus involves two proteins, i.e. FHY1 and FHY1-like, light-regulated proteins that accumulate in the dark and that are very similar to each other. Both of them have a binding site for phytochrome A and a nuclear localisation sequence. Without the two transporters, very little phytochrome A gets into the nucleus. The translocation of phytochrome B works differently: it is assumed that certain transcription factors, so-called PIFs (phytochrome interacting factors) assist in the translocation of phytochrome B into the nucleus where it can control the expression of certain growth genes, amongst other things.

Each photoreceptor has its specific absorption spectrum; it absorbs a specific light wavelength and hence colour as a maximum response to light perception – at least in theory. However, reality can be totally different: the spectrophotometric analysis of phytochrome A reveals that it has a maximum absorption capacity in the red light spectrum, but has maximal effect in the far-red light spectrum. 

Schematic showing the transduction of light after the incidence of light.<br />
Signal transduction after the incidence of light: active PHYA (Pfr) is transported into the nucleus by FHY1 (F). PIFs inhibit light-induced responses. HY5, HFR1 and LAF1, which have a positive effect on light-dependent responses, are degraded in the dark by a complex consisting of COP1 and SPA. In the light, PHYA interacts with nuclear PIFs, which are then degraded and responses to light can no longer be inhibited. At the same time, PHYA inactivates the COP1-SPA complex, which is why HY5, HFR1 and LAF1 are stabilised and enhance responses to light. © Prof. Dr. Andreas Hiltbrunner, University of Freiburg

HIR – a researcher’s dream – or rather nightmare?

High-irradiance response (HIR) is a phenomenon that has been known for a long time, but has nevertheless remained enigmatic. “As far as the photoreceptor is concerned, we would expect the strongest response to the red light spectrum,” says Hiltbrunner explaining that this is when the plant has reached the light and starts to develop leaves. “However, PHYA is essential for far-red high-irradiance responses, which are of particular ecological relevance as they enable plants to establish under shade conditions.” In the shade of other plants, the far-red light proportion is much greater than in the sunlight as the red light is absorbed by the chlorophyll of the leaves. In evolutionary terms, higher plants with PHYA have acquired the capability to react to far-red light and grow in shady areas, which can be an enormous selection advantage.

Hiltbrunner and his team are investigating the question as to why plants use a photoreceptor that has its absorption maximum in the light red spectrum. It has long been assumed that PHYA and its transport into the nucleus by way of FHY1 developed late in evolution and is characteristic of seed plants (spermatophytes). Moreover, the interaction of PHYB with the PIFs has been regarded as a relatively recent invention of nature. The reason for these assumptions is that crytpogams (mosses and ferns) do not possess the phytochromes A and B. However, the issue is not as simple as that: “Researchers found that the moss Physcomitrella also possesses a FHY1 protein, and that this also plays a role in whether phytochromes 1 and 3 (ed. note: red light receptors found in some ferns and mosses which prefer to grow under weak light) are transported from the cytosol into the nucleus.

The observation that Physcomitrella FHY1 has the same function as its counterpart in Arabidopsis is supported by the observation that FHY1 can compensate the fhy1 mutant of Arabidopsis. Hiltbrunner’s team is currently investigating whether Physcomitrella also possesses PIFs and whether they play a role in light-dependent signal transduction. According to Hiltbrunner, this might well be the case.

Juggling with key components

A central evolutionary question asked by Hiltbrunner is: Which came first? Phytochrome A or HIR? Nowadays there is increasing evidence that the shift of the pigment response into the far-red spectrum also occurs in Physcomitrella where no PHYA is present. How can this be explained? There are two potential answers: 1) The systems might have evolved twice and independently of one another. 2) There was one original phytochrome that was able to emit a high-irradiance response and that had to be transported into the nucleus by way of an FHY1. As mosses, ferns and seed plants diverged, phytochrome A and B developed in seed plants like Arabidopsis; phytochrome B lost its original properties and developed new ones. If the second assumption is true, Hiltbrunner assumes that HIR-like responses must have evolved in the last common ancestor of cryptogams and modern seed plants. This would mean that HIR signalling pre-dates PHYA.

From September 2013 onwards, Hiltbrunner will be working alongside plant biologist Prof. Dr. Enamul Huq and systems biologist Prof. Dr. Christian Fleck in order to elucidate these questions, using, amongst other things, mathematical models to identify the key components governing the evolution of species-specific reactions to light in plants. In their search for key components in the evolution and properties of photoreceptors, the researchers have found that many of these components are not only present in Arabidopsis, but also in the moss Physcomitrella. Hiltbrunner: “I would be surprised if the different responses of Arabidopsis and Physcomitrella to light are due to components that only one of them possesses, but not the other one. I think that the species-specific reactions to light are most likely due to differences in the interplay between phytochromes and other components.”

Systems biology provides insight into evolution

For his computer models, Hiltbrunner will use certain parameters which he has either already used in previous examinations or which he will determine in the future. These parameters will incude the phytochrome synthesis rate, its conversion into its active form or the time it takes to form a complex with FHY1 or dissociate from it. The inclusion of these parameters in virtual networks will enable the researches to simulate potential signalling pathways that lead to specific light responses. “We are trying to measure individual parameters, which will then be used by the mathematicians to build and test models,” Hiltbrunner explains. “In a second step, the models will be used to predict which components and interactions are particularly important and have changed during evolution.” With this knowledge, Hiltbrunner will carry out experiments with plants, generating mutations and examining their effect with the goal of finding out whether the model conforms with the real situation. He will particularly focus on the relationship between molecular biology and ecology, which is the level at which selection takes place. “If a mutant survives in the laboratory, this does not mean that it will also survive under ecologically relevant conditions,” said Hiltbrunner.

Further information:

Prof. Dr. Andreas Hiltbrunner
Institute of Biology II
University of Freiburg
Schänzlestr. 1
79104 Freiburg
Tel.: +49 (0)761/203 - 2709
E-mail: andreas.hiltbrunner(at)biologie.uni-freiburg.de


Website address: https://www.gesundheitsindustrie-bw.de/en/article/news/evolution-of-light-perception-networks-in-plants