MINIREVIEW PROLOGUE
Light Minireview Series*

Robert D. SimoniDagger and Arthur R. Grossman§

From the Dagger  Department of Biological Sciences, Stanford University, Stanford, California 94305-5020 and § Department of Plant Biology, Carnegie Institution of Washington, Stanford, California 94305



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Light as an energy source in photosynthesis was recognized by the end of the 18th century with observations reported by Joseph Priestly that plants exhibit light-dependent evolution of oxygen. Theodore de Saussure, in a remarkably insightful use of Lavoisier's law of conservation of mass, argued that the sum of the mass produced by plants as organic matter, including the oxygen evolved, was more than the weight of the CO2 consumed. He concluded that water too must be included in the equation of photosynthetic carbon fixation. Later Julius Mayer reported that not only is mass conserved but energy too, as the energy of light is converted into chemical energy.

Although the basic equations of photosynthesis have been known for 100-200 years, the interaction of plants, algae, and bacteria with light has remained one of the most fascinating and complex problems in biology, chemistry, and physics. However, light is involved in more than just driving photosynthetic electron transport. Plants, algae, and bacteria have learned to see and respond to their environment through the absorption of light by a number of different chromophorylated molecules. Among these absorbing species are protein-associated linear or cyclic tetrapyrroles, flavins, and carotenoids. This minireview series on light includes three articles, each focusing on fundamental aspects of the interaction of plants and bacteria with light, both as an energy source and as a regulator.

The first of the series, "Tracking the Light Environment by Cyanobacteria and the Dynamic Nature of Light Harvesting" by Arthur R. Grossman, Devaki Bhaya, and Qingfang He, describes some of the many ways that Cyanobacteria cope with different light conditions. Because light conditions (both intensity and wavelength) can vary widely, all plants have adaptive, regulatory responses to the dynamic character of their light environment.

The specific focus of the first minireview concerns the structure and molecular flexibility of the large light-harvesting complexes of Cyanobacteria that are known as phycobilisomes and the ways in which these complexes accommodate changing light conditions. Phycobilisomes are critical in partitioning absorbed excitation energy to the photosynthetic reaction centers of photosystems I and II in a process called "state transitions." This process may be important for balancing excitation of the photosystems, modulating the ratio of ATP production and CO2 fixation to accommodate environmental conditions, and dissipating excess absorbed light energy. Possible mechanisms involved in controlling state transitions are discussed.

In certain Cyanobacteria, phycobilisomes can change pigment-protein composition in an adaptive response to changes in wavelengths of light that are being absorbed by the cells in a phenomenon known as "complementary chromatic adaption" or CCA. This subject is explored in the context of the structural components of the phycobilisome and the ways in which the activities of genes encoding phycobilisome polypeptides are modulated by light quality. The use of molecular approaches, especially with respect to the generation and complementation of mutants for CCA, has been powerfully exploited to elucidate regulatory elements and their role in this acclimation process.

Finally, this first minireview summarizes recent advances in our understanding of the ways in which Cyanobacteria acclimate to high light intensities and the integration of cues elicited as a consequence of alterations in nutrient availability with light signals. The overall picture that emerges emphasizes the need for a "holistic" approach to the understanding of a very highly integrated system of responses that have evolved for optimal growth and survival.

The second minireview of this series, "The Phytochromes, a Family of Red/Far Red Absorbing Photoreceptors" is by Christian Fankhauser and focuses on a family of photoreceptors of red and far red light known collectively as the phytochromes. These photoreceptors are not directly involved in light energy conversion but provide critical regulatory responses to changing light conditions. It has long been recognized that the phytochrome family of proteins is involved in many aspects of plant development and morphogenesis including seedling germination, chloroplast development and seedling de-etiolation, inhibition or promotion of cell growth, neighbor perception and avoidance, and induction of flowering. Many of these responses may reflect both changes in intracellular ion fluxes and gene expression.

The use of molecular genetics, particularly in Arabidopsis, has been key to developing an understanding of the many roles played by the phytochromes and their mechanism of action. Analysis of various mutants of the phytochrome apoproteins, chromophores, and signaling molecules has highlighted the roles of phytochromes in sensing light quality, intensity, and duration.

The molecular features of the phytochromes are also discussed, including the biosynthesis and integration of the chromophore. Mutagenesis studies have been used to dissect regions of the protein(s) responsible for various functions. In addition, prokaryotic phytochromes are described, which provide a phylogenetic origin of the vascular plant versions of this photoreceptor and clues as to mode of function.

Finally, the signaling pathways triggered by photoperception are discussed and once again invoke the complex, integrated networks of G-proteins, Ca2+, and other familiar signaling molecules that often ultimately alter gene expression. Interestingly, one of the most well defined branches of phytochrome signaling involves import of the phytochrome molecule into the nucleus and its interactions with members of the bHLH class of transcription factors.

The third minireview, "Blue Light Sensing in Higher Plants" by John M. Christie and Winslow R. Briggs describes the two known blue light photosensory systems, the cryptochromes and the phototropins. Knowledge of these systems, similar to the phytochrome system, depends heavily on the isolation and analysis of photoregulatory mutants in Arabidopsis.

Interestingly, the two members of the cryptochrome family of blue light receptors, cry1 and cry2, have significant homology to bacterial DNA photolyases. DNA photolyases are enzymes that catalyze light-dependent repair of DNA damaged by UV light. Like photolyases, the cry proteins bind flavin adenine dinucleotide, FAD, as a chromophore, but they have no DNA lyase activity. cry1 and cry2 are also associated with a pterin, which serves as an antennae chromophore and transfers absorbed excitation energy to FAD.

The cryptochrome family of polypeptides is ubiquitous throughout the plant kingdom and is involved in growth control, anthocyanin synthesis, flowering, and entrainment of the circadian clock to the daily light/dark cycle. Although the mechanism(s) of cryptochrome signaling is not well understood, these molecules may mediate blue light-induced changes in gene expression by directly interacting with DNA. Some studies also suggest that blue light induces a rapid transient depolarization of the plasma membrane of hypocotyl cells, suggesting a mechanism for regulation of hypocotyl growth.

Studies of phototropism, an adaptive process whereby plants bend toward the light, has led to the discovery of another class of blue light receptors called the phototropins. This class of photoreceptor seems to be capable of autophosphorylation in response to blue light.

Genetic studies have identified the NPH1 gene. Null mutants for nph1 mutants lack phototropic curvature, and the blue light stimulated phosphorylation of a 120-kDa plasma membrane protein. This and other biochemical data suggest that the NPH1-encoded protein is the blue light receptor. Curiously, although nph1 is associated with the plasma membrane when isolated from several species, the amino acid sequence lacks obvious hydrophobic potential transmembrane sequences, suggesting that membrane association may depend on other factors. The protein has several domains including LOV domains, which are found in proteins regulated by light, oxygen, or voltage. In addition, nph1 binds flavin mononucleotide, FMN, and undergoes light-dependent autophosphorylation, suggesting that it functions as a photoreceptor kinase. Recent results suggest that the photochemistry associated with the nph1 control of phototropic curvature involves the formation of a flavin cysteinyl adduct, which is not very common in flavin biochemistry.

The authors and editors hope that this minireview series on light will serve to remind us all of the critical and complex role that light plays in the biosphere.


    FOOTNOTES

* This minireview will be reprinted in the 2001 Minireview Compendium, which will be available in December, 2001.

Published, JBC Papers in Press, February 16, 2001, DOI 10.1074/jbc.R100009200


Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.



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