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