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REGULATORS OF GROWTH | Photomorphogenesis
REGULATORS OF GROWTH / Photomorphogenesis
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level of Pfr present after far-red light is insufficient to lead to a response. If an increasing period of darkness is introduced between a red pulse and a far-red pulse there is an escape from reversibility. Such experiments provide information about the kinetics of phytochrome action. Analysis of mutants reveals that B-type phytochromes play an important role in this response mode of phytochrome action.
Cryptochrome
A blue/UV-A-absorbing photomorphogenic photoreceptor.
Etiolation
The strategy of dark growth.
Photochromic
A compound that exists in two forms that are interconvertible by light.
Photomorphogenesis
The responses of plants to the light environment about them.
Very Low Fluence Response (VLFR)
Photoreceptor
A protein with an attached chromophore that absorbs light.
Phototropin
The blue/UV-A-absorbing photoreceptor involved in phototropism.
Phytochrome
A red/far-red-absorbing photomorphogenic photoreceptor.
Skotomorphogenesis
The strategy of dark growth or etiolation.
Action spectra for these responses coincide with the absorption spectrum of the Pr form of phytochrome. They are incredibly sensitive and can be saturated by very low fluences of red light. It has been calculated that only one in a million molecules of Pr have to be excited. This means that these responses can be elicited by the green light often used as safelight for photomorphogenic studies and even by the low level of conversion of Pr to Pfr occurring in response to far-red light. Therefore, these responses can only be studied by growing plants in absolute darkness and they are obviously not reversible by far-red light. Examples of processes showing this kind of response are the stimulation of seed germination and regulation of gene expression. Analysis of mutants has revealed that phyA is active in this mode of phytochrome action. High Irradiance Responses (HIR)
In contrast, other responses require continuous irradiation for maximal effect and show an increase in response to irradiance. Such responses cannot be explained on the basis of the absence or presence of Pfr, but reflect the cycling between the two forms. This implies that phytochrome can act as a photon counter. Both phytochromes and cryptochromes can act as irradiance sensors. In the case of de-etiolation, far-red light has been shown to be very effective in de-etiolation and is consequently called the far-redHIR. Physiological analysis predicted that this was a labile phytochrome and type-specific mutants showed that it is the phyA pool that is involved in this response. Red-HIR responses have also been demonstrated. Under continuous irradiation with red light, the phyA pool is rapidly depleted and the phyB-type phytochrome family members act as irradiance sensors. By definition, where the cryptochromes are involved in photon counting it can be described as a blue-HIR response.
List of Technical Nomenclature Apoprotein
The protein part of a chromoprotein.
Chromophore
The part of a photoreceptor that gives it the capacity to absorb light.
See also: Regulators of Growth: Circadian Rhythms; Photomorphogenesis.
Further Reading Kendrick RE and Kronenberg GHM (eds) (1994) Photomorphogenesis in Plants, 2nd edn, p. 828. Dordrecht: Kluwer Academic Publishers. Lin C (2000) Photoreceptors and regulation of flowering time. Plant Physiology 123: 39–50. Neff MM, Fankhauser C, and Chory J (2000) Light: an indicator of time and place. Genes and Development 14: 257–271. Sage LC (1992) Pigment of the Imagination. A History of Phytochrome Research. San Diego: Academic Press. Smith H (2000) Phytochromes and light signal perception by plants – an emerging synthesis. Nature 407: 585–591.
Photomorphogenesis R E Kendrick, Wageningen University, Wageningen, The Netherlands J L Weller, University of Tasmania, Hobart, Australia Copyright 2003, Elsevier Ltd. All Rights Reserved.
Introduction Life on earth depends on the energy emitted as a result of nuclear fusion in the sun. This solar energy, which takes the form of electromagnetic radiation (Table 1), is initially fixed in the biosphere by the process of photosynthesis in plants and microorganisms. Photosynthesis is the main source of energy
1070 REGULATORS OF GROWTH / Photomorphogenesis Table 1 The visible spectrum and its flanking regions Region
Wavelength (nm)
UV UV-C UV-B UV-A
o280 280–320 320–400
Visible Blue Green Yellow Orange Red
400–480 480–550 550–590 590–650 650–700
Near infra-red Far-red
700–800
for the green plant, and the efficient use of the available photosynthetic radiation is the key strategy for plant survival. It is therefore not surprising that plants have evolved photosynthetic pigments that together can harvest light over the broad band of available radiation. The main photosynthetic pigments, the chlorophylls, are present at high concentration and absorb across a range of wavelengths from 400 to 700 nm. Within this range, their main absorption peaks are in the blue (BL) and red (R) regions of the spectrum. The less effective absorption by chlorophylls in the green region of the spectrum results in a preferential reflection and transmission of green light, which gives leaves their typical green color. Since light is the energy source for plants, they essentially compete with each other for access to it. Most green plants are sedentary and, unlike most animals, are unable to move in search of a more energy rich environment. Instead, plants can modify the way they grow, so that they can use the available energy in a more efficient way. Any modification of development that increases the plant’s ability to compete for light will provide a clear advantage, which can be acted upon by natural selection. A number of different developmental strategies have evolved, and any individual plant species may exhibit different strategies in different situations. For example, the plant may increase the efficiency of its light capture by modifying its photosynthetic structures. This may include modification of the chloroplasts, and of the shape, size, and thickness of leaves (i.e., they show shade tolerance). Other species compete directly for access to light by outgrowing their neighbors (i.e., they show shade avoidance). Arrangement of leaves may also be modified to minimize self-shading. Yet other species avoid competition by shifting their period of vegetative growth to a time of year when fewer other species are
Table 2 List of responses throughout the life cycle of a plant, which are collectively grouped under the title plant photomorphogenesis Regulation of seed germination Seedling establishment (de-etiolation) Responses to UV-B Phototropism Sun-tracking of flowers and leaves Shade avoidance and near neighbor detection Entrainment of the circadian clock Photoperiodic processes such as induction of flowering and dormancy mechanisms
present. In addition, plants often exhibit a growth bending toward the light (phototropism). These growth changes in response to light, which provide a clear selective advantage, can be clearly demonstrated by time-lapse photography. Another important developmental response to light is seen predominantly in seed plants. With the development of the seed habit it became necessary for seeds to germinate in a moist environment, often below the soil surface. This has resulted in the development of a seedling growth strategy in darkness or under very low light levels in which normal development of leaves is repressed and stem elongation is stimulated. Upon emergence into light, elongation dramatically slows down, and leaves begin to develop before the limited food reserves in the seed are exhausted. Collectively, modifications of plant development in response to light such as these are known as ‘‘photomorphogenesis’’ (from the Greek words ‘‘photo’’ meaning light and ‘‘morphogenesis’’ meaning development of form). Table 2 lists a number of processes that are encompassed by this term. In the related phenomenon of ‘‘photoperiodism,’’ processes such as flowering, bud outgrowth, and storage organ formation are regulated by daylength, rather than by just the quantity and quality of light. Finally, in addition to these developmental responses to light, some plants also show daily movements in response to light. Examples are the phenomena of sun tracking and sleep movements of leaves and flowers.
Photoreceptors in Photomorphogenesis Developmental responses to light do not depend on the highly abundant light harvesting pigments of photosynthesis, but on distinct photoreceptors, which provide information to the plant about the light conditions under which it is growing. However, given the importance of photosynthesis for plant growth, we could expect that wavelengths of light most appropriate to serve as developmental signals would also be those that are best for photosynthesis.
REGULATORS OF GROWTH / Photomorphogenesis
It is now known that there are several different families of photomorphogenic photoreceptors, which do predominantly absorb light in the R and BL regions of the spectrum. These include the phytochromes, which absorb principally in the R and far-red (FR) light regions, and several other photoreceptors that absorb in the BL/UV region, including the cryptochromes (see Regulators of Growth: Phytochromes and other Photoreceptors). These photoreceptors also vary in their sensitivity to other variables in the light environment, such as irradiance and duration. Thus, it seems that selective pressures have favored the development of a relatively sophisticated light sensing system, which allows the plant to respond in different ways to different competitive situations throughout its life cycle.
Action Spectra Unlike in animals, plant photoreceptors are not organized into specialized structures, but are distributed throughout the plant. Also, unlike the light harvesting pigments, photomorphogenic photoreceptors are generally present at very low levels, which means that they are not obvious to the naked eye. Their existence was first inferred from physiological experiments that determined the relative effectiveness of different wavelengths of light in the induction of a given photomorphogenic response. This relationship is known as an ‘‘action spectrum.’’ The light absorbing properties of many biological pigments derive from the interaction between the protein and an attached chemical group called a chromophore. Different chromophore groups have characteristic light absorbing properties, which determine their colors. Comparison of the action spectrum for a photomorphogenic response with absorption spectra of known pigments can therefore provide useful information about the general nature of the photoreceptor or photoreceptors regulating the response in question. In some cases, predictions made on the basis of action spectra have been remarkably accurate, as in the case of the discovery of phytochrome. However, the level of resolution in the measurement of action spectra is usually fairly low, relative to that of absorption spectroscopy. Action spectra are therefore of limited value in distinguishing the action of photoreceptors, which have only minor differences in their absorption spectra.
Germination A dormant seed is essentially in a state of suspended animation and must make the critical (all or none)
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decision of whether or not to germinate. This is particularly critical for small seeds with limited food reserves. It is clear that for small seeds buried in soil, it is a selective advantage to remain dormant until brought close to the soil surface (Figure 1). Otherwise, the germinating seedling risks expending all the energy reserve of the seed before reaching the full light conditions under which photosynthesis can begin. Light is known to regulate seed germination in several different ways, depending on the species. In some species, dormant seeds can be induced to germinate by incredibly small amounts of light. In these cases, the response does not depend on the wavelength of the light. It has been shown that very sensitive responses such as this are regulated by phytochrome A (phyA), a member of the phytochrome photoreceptor family (see Regulators of Growth: Phytochromes and other Photoreceptors). Such extreme sensitivity to light may represent a very early warning to buried seeds that they are near the soil surface. In other cases, the induction of germination requires higher amounts of light, and shows wavelength dependence more characteristic of phytochrome action. A typical example is provided by dormant lettuce (Lactuca sativa) seeds, which germinate if exposed to a few minutes of R after imbibition, but do not germinate if maintained in darkness. An irradiation with FR given immediately after the R negates the effect of the R. This R/FR reversibility of germination can be repeated many times, and the germination response is only dependent on the final irradiation. Observations such as this have led to the idea that phytochrome operates as a molecular switch, and is activated when it is converted from the R-absorbing form (Pr) to the FR-absorbing form (Pfr). In this response, as in others discussed below, phytochrome clearly detects the presence or absence of R. The significance of being able to monitor R is obvious when it is considered that photosynthetic pigments have an absorption maximum in the R. High levels of R are therefore a good indicator of an environment productive for photosynthesis, and linking germination to R is therefore a sensible strategy. But what is the significance of FR to the plant? The answer to this question appears to lie in the changing spectral quality of light in the natural environment. Under a dense vegetation canopy, the light is depleted in the R region of the spectrum, but is still relatively rich in longer FR wavelengths. A low R : FR photon ratio is thus a specific indicator of vegetational shade. Phytochrome, specifically phytochrome B, gives a
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FR> R R > FR
Germination
De-etiolation
Blue
FR>R
R> FR
Shade avoidance
Phototropism
Short days
Long days
Short - day plant
Long - day plant
Flowering Figure 1 Examples of photomorphogenic processes exhibited by plants throughout their life cycle.
seed the ability to monitor this ratio, and allows it to make an ‘‘informed decision’’ about whether or not to germinate (Figure 1). Phytochrome has also been implicated in other responses in which seed germination is actively inhibited by light. It is possible that these different modes of light responsiveness for germination may coexist in many species. Their relative prominence may also explain differences in the specific light requirements for germination among species.
Skotomorphogenesis (Etiolation) and Seedling Establishment (De-etiolation) Because the germinating seed has only a limited supply of energy, it is important that the emerging seedling reaches the light and becomes a selfsufficient photosynthetic green plant as quickly as possible. Seedlings germinating under the soil initially direct their energy into rapid, negatively geotropic elongation growth, and do not waste
REGULATORS OF GROWTH / Photomorphogenesis
energy in producing leaves. This strategy of growth has been called skotomorphogenesis or etiolation, and is generally seen wherever seedlings are germinated in darkness (Figure 1). The bean sprouts (Phaseolus aureus) eaten in Chinese restaurants provide a typical example of an etiolated seedling. These seedlings have an elongated hypocotyl and poorly developed primary leaves, which are devoid of chlorophyll. In addition, the shoot apex is protected by the formation of a characteristic hook structure. Once exposed to light, the whole developmental strategy of the plant rapidly changes. Stem elongation ceases, the apical hook opens, and the primary leaves expand to become photosynthetic. Protective pigments such as anthocyanin may also be produced. This process of seedling establishment in the light environment is called de-etiolation. Underlying the visible changes in the seedling are profound changes in the expression of many genes, e.g., the formation of the photosynthetically competent plastids. The genes that encode ribulose bisphosphate carboxylase/oxygenase, the key enzyme involved in the fixation of carbon dioxide in photosynthesis and the most abundant protein on earth, are inactive in etiolated seedlings, but rapidly become active after exposure to light. This is a tightly coordinated process involving the integrated action of both plastid and nuclear genomes. Inhibition of elongation growth results from a modification of cell wall properties, such as deposition of the cellulose microfibrils in the secondary cell wall. These processes could be mediated by changes in plant hormone metabolism and action. De-etiolation of the aerial parts of the plant is accompanied by enhanced growth and branching of roots below the soil surface. Both inhibition of elongation growth and expansion of leaves can result from photoconversion of Pr to Pfr by R, in the classical low fluence response mode of phytochrome action. However, other wavelengths are also clearly effective, particularly in the BL and FR regions of the spectrum. Unlike the response to R, which can be induced by a single pulse of light, responses to BL and FR generally require continuous exposure at high irradiance, and have therefore been termed high irradiance responses. Mutants deficient in specific phytochromes have shown that the FR high irradiance response is regulated by phyA, whereas R/FR-reversible responses are predominantly regulated by phyB. The basis for the differences in wavelength and irradiance requirements of these two phytochromes has yet to be satisfactorily explained.
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Phytochrome also absorbs BL and is also partially responsible for de-etiolation responses to this waveband. However, the existence of other, specific BL-absorbing photoreceptors for de-etiolation was postulated for a long time. Progress in identifying photoreceptors responsible for BL-mediated phenomena has been hampered by the fact that action spectra for BL-induced responses have several peaks of action in the BL/UV-A region of the spectrum. Flavins and carotenoids were long considered as two candidate pigments, but neither shows the full absorption profile predicted by action spectra. It is now known that the primary photoreceptors for BL-mediated photomorphogenic responses, the cryptochromes, each carry two chromophores: a pterin and a flavin. The stage of seedling establishment is a critical step in the life cycle of every plant, hence the very strong selection pressure for the use of multiple photoreceptors and cross-talk between them to signal this transition. It is obvious that at low light levels below the soil surface no individual photoreceptor will be saturated, and having a higher photoreceptor concentration would confer selective advantage. This would clearly favor the duplication of the phytochrome gene family in seed plants. This gives the seedling an early warning of proximity to the soil surface. Analysis of mutants for most photoreceptors involved in de-etiolation has shown that heterozygotes exhibit a partial loss of response particularly under low irradiances. This is termed haplo-insufficiency, and implies that light responses are limited by the photoreceptor abundance. During the evolution of seed plants on earth, colonization of the land brought with it unique problems. Photosynthetic organisms by design are adapted for optimal performance in the light environment. Studies of recessive mutants that de-etiolate in darkness demonstrated that the de-etiolation arises as a result of suppression of a series of repressors. Once activated, the photoreceptors relieve this suppression resulting in the plant adopting its default strategy. While mutants deficient in individual photoreceptors survive in the laboratory, due to genetic redundancy between them, it is predicted that they would be severely disadvantaged in the natural environment. Such a seedling would have to expend more energy before perceiving the light environment, decreasing survival prospects. It is ironic that the R/FR reversible phyA, the most abundant phytochrome in a dark-grown seedling and the first detected spectrophotometrically, probably plays little role in detection of the R : FR photon ratio. It can be considered as an antenna phytochrome, hence, the relatively high concentration present.
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Shade Avoidance and Near Neighbor Detection Even after it is established in the light and becomes fully photosynthetic, a seedling remains in competition for the available photosynthetically active radiation. Under highly competitive conditions where the degree of shading by other larger plants is high, seedlings are able to modulate their growth to resume a light seeking strategy (Figure 1). This is referred to as the shade avoidance syndrome, and is in effect a partial re-etiolation (Table 3). As described above in ‘‘Germination,’’ the fact that FR is transmitted through leaves, whereas R is absorbed, makes the R : FR photon ratio a good indicator of the degree of shading. Under laboratory conditions, the addition of FR to the background white light results in dramatic effects on growth and development, despite the fact that it cannot be used for photosynthesis. Harry Smith and his colleagues at Leicester University, UK have shown that in many species the growth rate is related to the R : FR ratio in a negative way; in other words, the lower the ratio the greater the growth rate. Changes in the R : FR ratio have been shown to modulate growth rate with a lag of only 15 min, indicating that the plant continuously monitors its surroundings. Sensitivity to R : FR is sufficiently high that, in some cases, plants can even sense the quality of reflected light, and thus can detect the presence of adjacent plants even before direct shading occurs. This may explain the observation that photoreceptors are present in the surface layers of young growing tissues, since in the interior of green stems, the R : FR photon ratio decreases as a result of absorption of R by chlorophyll. The B-type phytochrome family members play a dominant role in the way plants respond to changes in R : FR photon ratio as a result of direct shade of other
Table 3 The shade avoidance syndrome Parameter
Response
Extension growth
Accelerated rapid internode extension with reduced specific stem weight Retarded, resulting in thinner leaves with a smaller leaf area that exhibit early senescence; plastid development and chlorophyll retarded; reduction of anthocyanin levels in immature leaves Strengthened, branching inhibited Accelerated Markedly changed storage deposition; leaf and root sinks reduced at the expense of stems
Leaf development
Apical dominance Flowering Assimilate distribution
plants or reflectance from neighbors. Plants continue to use phytochrome as a detector of vegetational shade throughout their period of vegetative growth. Part of the shade avoidance syndrome is an increased apical dominance and acceleration of flowering. This acceleration of reproduction and seed production is a clear survival strategy for a plant that finds itself in deep shade.
Photoperiodism Another parameter of the light environment that changes is the daily duration of light and darkness, dependent on the time of year. This can be used as a reliable signal or indicator of seasonal change, such as the onset of winter. This phenomenon of photoperiodism was first characterized in detail in plants by Whiteman W Garner and Harry Allard, but later shown in insects, birds, and mammals. Both plants and animals have evolved pigment systems that can provide information about the duration of light and darkness, enabling them to anticipate the seasons. In animals, examples of photoperiodism are the onset of bird migration and initiation of sexual behavior. In plants, the most widely studied photoperiodic response is associated with reproduction: flowering and the development of dormancy mechanisms, such as the production of winter buds in deciduous trees and the formation of bulbs and corms. Daylength is the most constant parameter of the environment that can predict the time of year. Temperature can show considerable fluctuations, and therefore it is perhaps not surprising that living organisms have locked on to the parameter of photoperiod and are not fooled by conditions such as a few warm days in early spring. An example of man’s interference with photoperiodism in plants can be seen in autumn in situations where deciduous trees grow close to street lights. On branches adjacent to the light, the leaves remain green and leaf fall is delayed as a result of the artificially long days typical of summer. Although an oversimplification, the flowering responses of plants can for convenience be split into three groups: short-day plants (e.g., Chrysanthemum ssp., Japanese morning glory (Pharbitis nil)) that flower as days grow shorter in autumn (Figure 1); long-day plants (e.g., many grasses and cereals) that flower as days grow longer in late spring and summer; and day-length-indifferent plants (e.g., roses (Rosa spp.) and tomato (Lycopersicon esculentum)) that given a suitable temperature will flower at any time of the year. Such photoperiodic responses demonstrate that plants have the capacity for time measurement.
REGULATORS OF GROWTH / Photomorphogenesis
Research has shown that the plants effectively measure the length of darkness in each daily sequence. In Japanese morning glory, a short-day plant, flowering is readily induced under a daily cycle of 10 h light and 14 h darkness, whereas plants remain entirely vegetative when the daily light period is extended to 16 h. In fact, it is not necessary for this extension to be made with continuous light, and a short light break of a few minutes given at approximately the middle of the 14-h night period is equally effective in preventing flowering. In many long-day plants, a light break in the night under short days has the same effect as long days. If the effectiveness of different wavelengths of light is investigated it is found that R is most effective and that FR can negate its effect. Experiments have shown that phytochromes present in the leaves perceive the light signal, and this results in the release of a chemical signal that is transported to the apical meristem of the plants where it changes the fate of the cells produced. Photoperiodism has been used to human advantage. Since the daylength is detected by phytochrome, only low levels of energy are required to artificially extend the day. Light breaks are also effective in switching development at the expense of little energy. Daylength can be shortened by simply covering plants with a black plastic sheet to shorten naturally long days. Using these simple procedures it is possible for horticulturists to manipulate the growth of plants such as Chrysanthemum, a flower traditionally typical of autumn, to flower at any predetermined date throughout the year.
Phototropism The phenomenon of phototropism, or bending of plants toward the light, was first described a long time before the discovery of phytochrome. Charles Darwin wrote a very clear account of it in his book ‘‘The Power of Plant Movement,’’ published in 1880. Action spectra subsequently showed that the photoreceptor absorbs in the BL and UV-A region of the spectrum, but the favored candidates for the photoreceptors, flavins and carotenoids, both lacked some of the predicted absorption bands in the action spectrum, which meant that the photoreceptor remained elusive for many years. Eventually, a genetic approach enabled the photoreceptor to be identified. The isolation of aphototropic mutants (i.e., mutants lacking the capacity to exhibit phototropism) in Arabidopsis showed that phototropism can be genetically separated from phytochrome and cryptochrome action. However, excitation of both cryptochrome and phytochrome can modify
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the phototropic response to BL. Recently, Winslow R. Briggs and colleagues at the Carnegie Institute of Washington at Stanford, USA cloned the gene impaired in one group of aphototropic mutants, and showed that the gene product, which they named phototropin, had clear characteristics of a BL photoreceptor. The phototropin protein is related to sensory proteins in other organisms from bacteria to mammals, which respond to light, oxygen, or voltage. Phototropin has two flavin chromophores.
Light Signal Transduction Light responses are very diverse, and occur over a wide range of time scales. Any explanation of light signaling must take into account this diversity. Considering the rapidity of some phytochrome responses, Stirling B. Hendricks and Harry A. Borthwick suggested in 1967 that the primary mechanism of phytochrome action might involve changes in membrane permeability. However, as phytochrome shows little affinity for membranes, it is not clear how it can influence membrane related processes. In addition, phytochrome present in the cytosol in the dark clearly influences gene transcription, which occurs in the nucleus upon irradiation. Both phytochromes and cryptochromes are now known to move to the nucleus upon exposure to activating light, suggesting the possibility of a relatively direct link between photoreceptors and the modification of gene expression. The phytochrome molecule itself has kinase activity, which is different in its two forms. Researchers are currently looking for molecules that may act as molecular partners or substrates for phytochrome. Both nuclear and cytosolic phytochrome interacting proteins have now been identified, suggesting multiple sites of phytochrome action. Transcription factors, as well as other key proteins are involved in phytochrome signal transduction. Other studies have implicated signaling pathways similar to those observed in animals and microorganisms. Activation of a guanine triphosphate (GTP) binding protein, modification of phosphatidylinositol metabolism, involvement of cyclic guanine monophosphate (GMP), changes in cytoplasmic calcium concentration, activation of calmodulin, and induction of kinase activity have all been implicated in phytochrome signal transduction. There is even evidence for different transduction chains being induced by phytochrome within a single cell. Studies of signal transduction in cryptochrome responses have implicated the following elements:
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GTP binding proteins, membrane depolarizations, redox chains, and electron transport, as well as calcium/calmodulin cascades. Ultimately, these processes could mediate changes in plant hormone metabolism (by modification of synthesis, degradation, their effectiveness, or the availability of their receptors), resulting in changes in growth and development. In the case of phototropin, the photoreceptor is a serine/threonine kinase, which upon excitation with BL autophosphorylates itself. How the modified photoreceptor sets in motion the chain of events leading to differential growth is still not understood, although calcium metabolism again appears to play a role. A great deal of research over the years has implicated a central role for the plant hormone auxin in growth curvatures of plant organs. In the case of the oat (Avena sativa) coleoptile, excitation of the photoreceptor in the tip, close to the point of auxin synthesis, results in asymmetric distribution of auxin as it moves downward to the elongating zone. This results in cell wall plasticity being maintained for a longer period on the shaded side resulting in differential growth and curvature toward the light.
Biotechnological Modification of Photomorphogenesis Knowledge of photomorphogenic processes, such as the photoperiodic control of flowering, has already led to efficient crop production strategies in photoperiodic species. A continued increase in fundamental knowledge of photomorphogenesis should enable us to modify the architecture and response of plants to our advantage. Most crops are grown in dense stands, and this leads to shade avoidance responses at the expense of crop yield. At face value, the suppression of shade avoidance offers a good prospect to increase yield in monocultures or increase the diversity of crops that can be grown in the shade of other plants. In contrast, an elongated, shade avoiding morphology is actually desirable in some fiber crops, and is usually achieved by highdensity sowing and a relatively inefficient use of seed. Constitutively shade avoiding plants could then be grown at lower densities.
List of Technical Nomenclature Absorption spectrum
A graph indicating the relative absorption of different wavelengths of light by a substance.
Action spectrum A graph indicating the relative responsiveness of different wavelengths of light in eliciting a standard response. Chromophore
The constituent of a proteinaceous photoreceptor that gives it the capacity to absorb visible light.
Cryptochromes
A family of blue/UV-A photoreceptors.
Far-red light
Light in the waveband 700–800 nm.
Photomorphogenesis
Responses of plants that occur as a result of processing information about their light environment.
Photoperiod
The length of the daily light period, which varies with the time of year.
Photoreceptor
A chromoprotein that absorbs light and is used in energy transfer or information processing.
Phototropin
The blue/UV-A photoreceptor involved in phototropism.
Phytochromes
A family of photochromic photoreceptors that absorb red and far-red light.
Seedling establishment (deetiolation)
The transition of an etiolated darkgrown seedling into a green autotrophic plant.
Skotomorphogenesis (etiolation)
The strategy of dark growth that leads to etiolation.
See also: Regulators of Growth: Auxins; Circadian Rhythms; Photoperiodism; Phytochromes and other Photoreceptors.
Further Reading Ballere´ CL (1999) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends in Plant Science 4: 97–102. Kendrick RE and Kronenberg GHM (eds) (1994) Photomorphogenesis in Plants, 2nd edn. Dordrecht: Kluwer Academic Publishers. Neff MM, Fankhauser C, and Chory J (2000) Light: an indicator of time and place. Genes & Development 14: 257–271. Sage LC (1992) Pigment of the Imagination. A History of Phytochrome Research. San Diego: Academic Press. Smith H (1998) Engineering a phytochrome gene. In: Cockshull KE, Gray D, Seymore GB, and Thomas B (eds) Genetic and Environmental Control of Horticultural Crops, pp. 175–190. Oxford: CABI Publishing. Smith H (2000) Phytochromes and light signal perception by plants – an emerging synthesis. Nature 407: 585–591. Thomas B and Vince-Prue D (1997) Photoperiodism in Plants. London: Academic Press.
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level of Pfr present after far-red light is insufficient to lead to a response. If an increasing period of darkness is introduced between a red pulse and a far-red pulse there is an escape from reversibility. Such experiments provide information about the kinetics of phytochrome action. Analysis of mutants reveals that B-type phytochromes play an important role in this response mode of phytochrome action.
Cryptochrome
A blue/UV-A-absorbing photomorphogenic photoreceptor.
Etiolation
The strategy of dark growth.
Photochromic
A compound that exists in two forms that are interconvertible by light.
Photomorphogenesis
The responses of plants to the light environment about them.
Very Low Fluence Response (VLFR)
Photoreceptor
A protein with an attached chromophore that absorbs light.
Phototropin
The blue/UV-A-absorbing photoreceptor involved in phototropism.
Phytochrome
A red/far-red-absorbing photomorphogenic photoreceptor.
Skotomorphogenesis
The strategy of dark growth or etiolation.
Action spectra for these responses coincide with the absorption spectrum of the Pr form of phytochrome. They are incredibly sensitive and can be saturated by very low fluences of red light. It has been calculated that only one in a million molecules of Pr have to be excited. This means that these responses can be elicited by the green light often used as safelight for photomorphogenic studies and even by the low level of conversion of Pr to Pfr occurring in response to far-red light. Therefore, these responses can only be studied by growing plants in absolute darkness and they are obviously not reversible by far-red light. Examples of processes showing this kind of response are the stimulation of seed germination and regulation of gene expression. Analysis of mutants has revealed that phyA is active in this mode of phytochrome action. High Irradiance Responses (HIR)
In contrast, other responses require continuous irradiation for maximal effect and show an increase in response to irradiance. Such responses cannot be explained on the basis of the absence or presence of Pfr, but reflect the cycling between the two forms. This implies that phytochrome can act as a photon counter. Both phytochromes and cryptochromes can act as irradiance sensors. In the case of de-etiolation, far-red light has been shown to be very effective in de-etiolation and is consequently called the far-redHIR. Physiological analysis predicted that this was a labile phytochrome and type-specific mutants showed that it is the phyA pool that is involved in this response. Red-HIR responses have also been demonstrated. Under continuous irradiation with red light, the phyA pool is rapidly depleted and the phyB-type phytochrome family members act as irradiance sensors. By definition, where the cryptochromes are involved in photon counting it can be described as a blue-HIR response.
List of Technical Nomenclature Apoprotein
The protein part of a chromoprotein.
Chromophore
The part of a photoreceptor that gives it the capacity to absorb light.
See also: Regulators of Growth: Circadian Rhythms; Photomorphogenesis.
Further Reading Kendrick RE and Kronenberg GHM (eds) (1994) Photomorphogenesis in Plants, 2nd edn, p. 828. Dordrecht: Kluwer Academic Publishers. Lin C (2000) Photoreceptors and regulation of flowering time. Plant Physiology 123: 39–50. Neff MM, Fankhauser C, and Chory J (2000) Light: an indicator of time and place. Genes and Development 14: 257–271. Sage LC (1992) Pigment of the Imagination. A History of Phytochrome Research. San Diego: Academic Press. Smith H (2000) Phytochromes and light signal perception by plants – an emerging synthesis. Nature 407: 585–591.
Photomorphogenesis R E Kendrick, Wageningen University, Wageningen, The Netherlands J L Weller, University of Tasmania, Hobart, Australia Copyright 2003, Elsevier Ltd. All Rights Reserved.
Introduction Life on earth depends on the energy emitted as a result of nuclear fusion in the sun. This solar energy, which takes the form of electromagnetic radiation (Table 1), is initially fixed in the biosphere by the process of photosynthesis in plants and microorganisms. Photosynthesis is the main source of energy
1070 REGULATORS OF GROWTH / Photomorphogenesis Table 1 The visible spectrum and its flanking regions Region
Wavelength (nm)
UV UV-C UV-B UV-A
o280 280–320 320–400
Visible Blue Green Yellow Orange Red
400–480 480–550 550–590 590–650 650–700
Near infra-red Far-red
700–800
for the green plant, and the efficient use of the available photosynthetic radiation is the key strategy for plant survival. It is therefore not surprising that plants have evolved photosynthetic pigments that together can harvest light over the broad band of available radiation. The main photosynthetic pigments, the chlorophylls, are present at high concentration and absorb across a range of wavelengths from 400 to 700 nm. Within this range, their main absorption peaks are in the blue (BL) and red (R) regions of the spectrum. The less effective absorption by chlorophylls in the green region of the spectrum results in a preferential reflection and transmission of green light, which gives leaves their typical green color. Since light is the energy source for plants, they essentially compete with each other for access to it. Most green plants are sedentary and, unlike most animals, are unable to move in search of a more energy rich environment. Instead, plants can modify the way they grow, so that they can use the available energy in a more efficient way. Any modification of development that increases the plant’s ability to compete for light will provide a clear advantage, which can be acted upon by natural selection. A number of different developmental strategies have evolved, and any individual plant species may exhibit different strategies in different situations. For example, the plant may increase the efficiency of its light capture by modifying its photosynthetic structures. This may include modification of the chloroplasts, and of the shape, size, and thickness of leaves (i.e., they show shade tolerance). Other species compete directly for access to light by outgrowing their neighbors (i.e., they show shade avoidance). Arrangement of leaves may also be modified to minimize self-shading. Yet other species avoid competition by shifting their period of vegetative growth to a time of year when fewer other species are
Table 2 List of responses throughout the life cycle of a plant, which are collectively grouped under the title plant photomorphogenesis Regulation of seed germination Seedling establishment (de-etiolation) Responses to UV-B Phototropism Sun-tracking of flowers and leaves Shade avoidance and near neighbor detection Entrainment of the circadian clock Photoperiodic processes such as induction of flowering and dormancy mechanisms
present. In addition, plants often exhibit a growth bending toward the light (phototropism). These growth changes in response to light, which provide a clear selective advantage, can be clearly demonstrated by time-lapse photography. Another important developmental response to light is seen predominantly in seed plants. With the development of the seed habit it became necessary for seeds to germinate in a moist environment, often below the soil surface. This has resulted in the development of a seedling growth strategy in darkness or under very low light levels in which normal development of leaves is repressed and stem elongation is stimulated. Upon emergence into light, elongation dramatically slows down, and leaves begin to develop before the limited food reserves in the seed are exhausted. Collectively, modifications of plant development in response to light such as these are known as ‘‘photomorphogenesis’’ (from the Greek words ‘‘photo’’ meaning light and ‘‘morphogenesis’’ meaning development of form). Table 2 lists a number of processes that are encompassed by this term. In the related phenomenon of ‘‘photoperiodism,’’ processes such as flowering, bud outgrowth, and storage organ formation are regulated by daylength, rather than by just the quantity and quality of light. Finally, in addition to these developmental responses to light, some plants also show daily movements in response to light. Examples are the phenomena of sun tracking and sleep movements of leaves and flowers.
Photoreceptors in Photomorphogenesis Developmental responses to light do not depend on the highly abundant light harvesting pigments of photosynthesis, but on distinct photoreceptors, which provide information to the plant about the light conditions under which it is growing. However, given the importance of photosynthesis for plant growth, we could expect that wavelengths of light most appropriate to serve as developmental signals would also be those that are best for photosynthesis.
REGULATORS OF GROWTH / Photomorphogenesis
It is now known that there are several different families of photomorphogenic photoreceptors, which do predominantly absorb light in the R and BL regions of the spectrum. These include the phytochromes, which absorb principally in the R and far-red (FR) light regions, and several other photoreceptors that absorb in the BL/UV region, including the cryptochromes (see Regulators of Growth: Phytochromes and other Photoreceptors). These photoreceptors also vary in their sensitivity to other variables in the light environment, such as irradiance and duration. Thus, it seems that selective pressures have favored the development of a relatively sophisticated light sensing system, which allows the plant to respond in different ways to different competitive situations throughout its life cycle.
Action Spectra Unlike in animals, plant photoreceptors are not organized into specialized structures, but are distributed throughout the plant. Also, unlike the light harvesting pigments, photomorphogenic photoreceptors are generally present at very low levels, which means that they are not obvious to the naked eye. Their existence was first inferred from physiological experiments that determined the relative effectiveness of different wavelengths of light in the induction of a given photomorphogenic response. This relationship is known as an ‘‘action spectrum.’’ The light absorbing properties of many biological pigments derive from the interaction between the protein and an attached chemical group called a chromophore. Different chromophore groups have characteristic light absorbing properties, which determine their colors. Comparison of the action spectrum for a photomorphogenic response with absorption spectra of known pigments can therefore provide useful information about the general nature of the photoreceptor or photoreceptors regulating the response in question. In some cases, predictions made on the basis of action spectra have been remarkably accurate, as in the case of the discovery of phytochrome. However, the level of resolution in the measurement of action spectra is usually fairly low, relative to that of absorption spectroscopy. Action spectra are therefore of limited value in distinguishing the action of photoreceptors, which have only minor differences in their absorption spectra.
Germination A dormant seed is essentially in a state of suspended animation and must make the critical (all or none)
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decision of whether or not to germinate. This is particularly critical for small seeds with limited food reserves. It is clear that for small seeds buried in soil, it is a selective advantage to remain dormant until brought close to the soil surface (Figure 1). Otherwise, the germinating seedling risks expending all the energy reserve of the seed before reaching the full light conditions under which photosynthesis can begin. Light is known to regulate seed germination in several different ways, depending on the species. In some species, dormant seeds can be induced to germinate by incredibly small amounts of light. In these cases, the response does not depend on the wavelength of the light. It has been shown that very sensitive responses such as this are regulated by phytochrome A (phyA), a member of the phytochrome photoreceptor family (see Regulators of Growth: Phytochromes and other Photoreceptors). Such extreme sensitivity to light may represent a very early warning to buried seeds that they are near the soil surface. In other cases, the induction of germination requires higher amounts of light, and shows wavelength dependence more characteristic of phytochrome action. A typical example is provided by dormant lettuce (Lactuca sativa) seeds, which germinate if exposed to a few minutes of R after imbibition, but do not germinate if maintained in darkness. An irradiation with FR given immediately after the R negates the effect of the R. This R/FR reversibility of germination can be repeated many times, and the germination response is only dependent on the final irradiation. Observations such as this have led to the idea that phytochrome operates as a molecular switch, and is activated when it is converted from the R-absorbing form (Pr) to the FR-absorbing form (Pfr). In this response, as in others discussed below, phytochrome clearly detects the presence or absence of R. The significance of being able to monitor R is obvious when it is considered that photosynthetic pigments have an absorption maximum in the R. High levels of R are therefore a good indicator of an environment productive for photosynthesis, and linking germination to R is therefore a sensible strategy. But what is the significance of FR to the plant? The answer to this question appears to lie in the changing spectral quality of light in the natural environment. Under a dense vegetation canopy, the light is depleted in the R region of the spectrum, but is still relatively rich in longer FR wavelengths. A low R : FR photon ratio is thus a specific indicator of vegetational shade. Phytochrome, specifically phytochrome B, gives a
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FR> R R > FR
Germination
De-etiolation
Blue
FR>R
R> FR
Shade avoidance
Phototropism
Short days
Long days
Short - day plant
Long - day plant
Flowering Figure 1 Examples of photomorphogenic processes exhibited by plants throughout their life cycle.
seed the ability to monitor this ratio, and allows it to make an ‘‘informed decision’’ about whether or not to germinate (Figure 1). Phytochrome has also been implicated in other responses in which seed germination is actively inhibited by light. It is possible that these different modes of light responsiveness for germination may coexist in many species. Their relative prominence may also explain differences in the specific light requirements for germination among species.
Skotomorphogenesis (Etiolation) and Seedling Establishment (De-etiolation) Because the germinating seed has only a limited supply of energy, it is important that the emerging seedling reaches the light and becomes a selfsufficient photosynthetic green plant as quickly as possible. Seedlings germinating under the soil initially direct their energy into rapid, negatively geotropic elongation growth, and do not waste
REGULATORS OF GROWTH / Photomorphogenesis
energy in producing leaves. This strategy of growth has been called skotomorphogenesis or etiolation, and is generally seen wherever seedlings are germinated in darkness (Figure 1). The bean sprouts (Phaseolus aureus) eaten in Chinese restaurants provide a typical example of an etiolated seedling. These seedlings have an elongated hypocotyl and poorly developed primary leaves, which are devoid of chlorophyll. In addition, the shoot apex is protected by the formation of a characteristic hook structure. Once exposed to light, the whole developmental strategy of the plant rapidly changes. Stem elongation ceases, the apical hook opens, and the primary leaves expand to become photosynthetic. Protective pigments such as anthocyanin may also be produced. This process of seedling establishment in the light environment is called de-etiolation. Underlying the visible changes in the seedling are profound changes in the expression of many genes, e.g., the formation of the photosynthetically competent plastids. The genes that encode ribulose bisphosphate carboxylase/oxygenase, the key enzyme involved in the fixation of carbon dioxide in photosynthesis and the most abundant protein on earth, are inactive in etiolated seedlings, but rapidly become active after exposure to light. This is a tightly coordinated process involving the integrated action of both plastid and nuclear genomes. Inhibition of elongation growth results from a modification of cell wall properties, such as deposition of the cellulose microfibrils in the secondary cell wall. These processes could be mediated by changes in plant hormone metabolism and action. De-etiolation of the aerial parts of the plant is accompanied by enhanced growth and branching of roots below the soil surface. Both inhibition of elongation growth and expansion of leaves can result from photoconversion of Pr to Pfr by R, in the classical low fluence response mode of phytochrome action. However, other wavelengths are also clearly effective, particularly in the BL and FR regions of the spectrum. Unlike the response to R, which can be induced by a single pulse of light, responses to BL and FR generally require continuous exposure at high irradiance, and have therefore been termed high irradiance responses. Mutants deficient in specific phytochromes have shown that the FR high irradiance response is regulated by phyA, whereas R/FR-reversible responses are predominantly regulated by phyB. The basis for the differences in wavelength and irradiance requirements of these two phytochromes has yet to be satisfactorily explained.
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Phytochrome also absorbs BL and is also partially responsible for de-etiolation responses to this waveband. However, the existence of other, specific BL-absorbing photoreceptors for de-etiolation was postulated for a long time. Progress in identifying photoreceptors responsible for BL-mediated phenomena has been hampered by the fact that action spectra for BL-induced responses have several peaks of action in the BL/UV-A region of the spectrum. Flavins and carotenoids were long considered as two candidate pigments, but neither shows the full absorption profile predicted by action spectra. It is now known that the primary photoreceptors for BL-mediated photomorphogenic responses, the cryptochromes, each carry two chromophores: a pterin and a flavin. The stage of seedling establishment is a critical step in the life cycle of every plant, hence the very strong selection pressure for the use of multiple photoreceptors and cross-talk between them to signal this transition. It is obvious that at low light levels below the soil surface no individual photoreceptor will be saturated, and having a higher photoreceptor concentration would confer selective advantage. This would clearly favor the duplication of the phytochrome gene family in seed plants. This gives the seedling an early warning of proximity to the soil surface. Analysis of mutants for most photoreceptors involved in de-etiolation has shown that heterozygotes exhibit a partial loss of response particularly under low irradiances. This is termed haplo-insufficiency, and implies that light responses are limited by the photoreceptor abundance. During the evolution of seed plants on earth, colonization of the land brought with it unique problems. Photosynthetic organisms by design are adapted for optimal performance in the light environment. Studies of recessive mutants that de-etiolate in darkness demonstrated that the de-etiolation arises as a result of suppression of a series of repressors. Once activated, the photoreceptors relieve this suppression resulting in the plant adopting its default strategy. While mutants deficient in individual photoreceptors survive in the laboratory, due to genetic redundancy between them, it is predicted that they would be severely disadvantaged in the natural environment. Such a seedling would have to expend more energy before perceiving the light environment, decreasing survival prospects. It is ironic that the R/FR reversible phyA, the most abundant phytochrome in a dark-grown seedling and the first detected spectrophotometrically, probably plays little role in detection of the R : FR photon ratio. It can be considered as an antenna phytochrome, hence, the relatively high concentration present.
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Shade Avoidance and Near Neighbor Detection Even after it is established in the light and becomes fully photosynthetic, a seedling remains in competition for the available photosynthetically active radiation. Under highly competitive conditions where the degree of shading by other larger plants is high, seedlings are able to modulate their growth to resume a light seeking strategy (Figure 1). This is referred to as the shade avoidance syndrome, and is in effect a partial re-etiolation (Table 3). As described above in ‘‘Germination,’’ the fact that FR is transmitted through leaves, whereas R is absorbed, makes the R : FR photon ratio a good indicator of the degree of shading. Under laboratory conditions, the addition of FR to the background white light results in dramatic effects on growth and development, despite the fact that it cannot be used for photosynthesis. Harry Smith and his colleagues at Leicester University, UK have shown that in many species the growth rate is related to the R : FR ratio in a negative way; in other words, the lower the ratio the greater the growth rate. Changes in the R : FR ratio have been shown to modulate growth rate with a lag of only 15 min, indicating that the plant continuously monitors its surroundings. Sensitivity to R : FR is sufficiently high that, in some cases, plants can even sense the quality of reflected light, and thus can detect the presence of adjacent plants even before direct shading occurs. This may explain the observation that photoreceptors are present in the surface layers of young growing tissues, since in the interior of green stems, the R : FR photon ratio decreases as a result of absorption of R by chlorophyll. The B-type phytochrome family members play a dominant role in the way plants respond to changes in R : FR photon ratio as a result of direct shade of other
Table 3 The shade avoidance syndrome Parameter
Response
Extension growth
Accelerated rapid internode extension with reduced specific stem weight Retarded, resulting in thinner leaves with a smaller leaf area that exhibit early senescence; plastid development and chlorophyll retarded; reduction of anthocyanin levels in immature leaves Strengthened, branching inhibited Accelerated Markedly changed storage deposition; leaf and root sinks reduced at the expense of stems
Leaf development
Apical dominance Flowering Assimilate distribution
plants or reflectance from neighbors. Plants continue to use phytochrome as a detector of vegetational shade throughout their period of vegetative growth. Part of the shade avoidance syndrome is an increased apical dominance and acceleration of flowering. This acceleration of reproduction and seed production is a clear survival strategy for a plant that finds itself in deep shade.
Photoperiodism Another parameter of the light environment that changes is the daily duration of light and darkness, dependent on the time of year. This can be used as a reliable signal or indicator of seasonal change, such as the onset of winter. This phenomenon of photoperiodism was first characterized in detail in plants by Whiteman W Garner and Harry Allard, but later shown in insects, birds, and mammals. Both plants and animals have evolved pigment systems that can provide information about the duration of light and darkness, enabling them to anticipate the seasons. In animals, examples of photoperiodism are the onset of bird migration and initiation of sexual behavior. In plants, the most widely studied photoperiodic response is associated with reproduction: flowering and the development of dormancy mechanisms, such as the production of winter buds in deciduous trees and the formation of bulbs and corms. Daylength is the most constant parameter of the environment that can predict the time of year. Temperature can show considerable fluctuations, and therefore it is perhaps not surprising that living organisms have locked on to the parameter of photoperiod and are not fooled by conditions such as a few warm days in early spring. An example of man’s interference with photoperiodism in plants can be seen in autumn in situations where deciduous trees grow close to street lights. On branches adjacent to the light, the leaves remain green and leaf fall is delayed as a result of the artificially long days typical of summer. Although an oversimplification, the flowering responses of plants can for convenience be split into three groups: short-day plants (e.g., Chrysanthemum ssp., Japanese morning glory (Pharbitis nil)) that flower as days grow shorter in autumn (Figure 1); long-day plants (e.g., many grasses and cereals) that flower as days grow longer in late spring and summer; and day-length-indifferent plants (e.g., roses (Rosa spp.) and tomato (Lycopersicon esculentum)) that given a suitable temperature will flower at any time of the year. Such photoperiodic responses demonstrate that plants have the capacity for time measurement.
REGULATORS OF GROWTH / Photomorphogenesis
Research has shown that the plants effectively measure the length of darkness in each daily sequence. In Japanese morning glory, a short-day plant, flowering is readily induced under a daily cycle of 10 h light and 14 h darkness, whereas plants remain entirely vegetative when the daily light period is extended to 16 h. In fact, it is not necessary for this extension to be made with continuous light, and a short light break of a few minutes given at approximately the middle of the 14-h night period is equally effective in preventing flowering. In many long-day plants, a light break in the night under short days has the same effect as long days. If the effectiveness of different wavelengths of light is investigated it is found that R is most effective and that FR can negate its effect. Experiments have shown that phytochromes present in the leaves perceive the light signal, and this results in the release of a chemical signal that is transported to the apical meristem of the plants where it changes the fate of the cells produced. Photoperiodism has been used to human advantage. Since the daylength is detected by phytochrome, only low levels of energy are required to artificially extend the day. Light breaks are also effective in switching development at the expense of little energy. Daylength can be shortened by simply covering plants with a black plastic sheet to shorten naturally long days. Using these simple procedures it is possible for horticulturists to manipulate the growth of plants such as Chrysanthemum, a flower traditionally typical of autumn, to flower at any predetermined date throughout the year.
Phototropism The phenomenon of phototropism, or bending of plants toward the light, was first described a long time before the discovery of phytochrome. Charles Darwin wrote a very clear account of it in his book ‘‘The Power of Plant Movement,’’ published in 1880. Action spectra subsequently showed that the photoreceptor absorbs in the BL and UV-A region of the spectrum, but the favored candidates for the photoreceptors, flavins and carotenoids, both lacked some of the predicted absorption bands in the action spectrum, which meant that the photoreceptor remained elusive for many years. Eventually, a genetic approach enabled the photoreceptor to be identified. The isolation of aphototropic mutants (i.e., mutants lacking the capacity to exhibit phototropism) in Arabidopsis showed that phototropism can be genetically separated from phytochrome and cryptochrome action. However, excitation of both cryptochrome and phytochrome can modify
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the phototropic response to BL. Recently, Winslow R. Briggs and colleagues at the Carnegie Institute of Washington at Stanford, USA cloned the gene impaired in one group of aphototropic mutants, and showed that the gene product, which they named phototropin, had clear characteristics of a BL photoreceptor. The phototropin protein is related to sensory proteins in other organisms from bacteria to mammals, which respond to light, oxygen, or voltage. Phototropin has two flavin chromophores.
Light Signal Transduction Light responses are very diverse, and occur over a wide range of time scales. Any explanation of light signaling must take into account this diversity. Considering the rapidity of some phytochrome responses, Stirling B. Hendricks and Harry A. Borthwick suggested in 1967 that the primary mechanism of phytochrome action might involve changes in membrane permeability. However, as phytochrome shows little affinity for membranes, it is not clear how it can influence membrane related processes. In addition, phytochrome present in the cytosol in the dark clearly influences gene transcription, which occurs in the nucleus upon irradiation. Both phytochromes and cryptochromes are now known to move to the nucleus upon exposure to activating light, suggesting the possibility of a relatively direct link between photoreceptors and the modification of gene expression. The phytochrome molecule itself has kinase activity, which is different in its two forms. Researchers are currently looking for molecules that may act as molecular partners or substrates for phytochrome. Both nuclear and cytosolic phytochrome interacting proteins have now been identified, suggesting multiple sites of phytochrome action. Transcription factors, as well as other key proteins are involved in phytochrome signal transduction. Other studies have implicated signaling pathways similar to those observed in animals and microorganisms. Activation of a guanine triphosphate (GTP) binding protein, modification of phosphatidylinositol metabolism, involvement of cyclic guanine monophosphate (GMP), changes in cytoplasmic calcium concentration, activation of calmodulin, and induction of kinase activity have all been implicated in phytochrome signal transduction. There is even evidence for different transduction chains being induced by phytochrome within a single cell. Studies of signal transduction in cryptochrome responses have implicated the following elements:
1076 REGULATORS OF GROWTH / Photomorphogenesis
GTP binding proteins, membrane depolarizations, redox chains, and electron transport, as well as calcium/calmodulin cascades. Ultimately, these processes could mediate changes in plant hormone metabolism (by modification of synthesis, degradation, their effectiveness, or the availability of their receptors), resulting in changes in growth and development. In the case of phototropin, the photoreceptor is a serine/threonine kinase, which upon excitation with BL autophosphorylates itself. How the modified photoreceptor sets in motion the chain of events leading to differential growth is still not understood, although calcium metabolism again appears to play a role. A great deal of research over the years has implicated a central role for the plant hormone auxin in growth curvatures of plant organs. In the case of the oat (Avena sativa) coleoptile, excitation of the photoreceptor in the tip, close to the point of auxin synthesis, results in asymmetric distribution of auxin as it moves downward to the elongating zone. This results in cell wall plasticity being maintained for a longer period on the shaded side resulting in differential growth and curvature toward the light.
Biotechnological Modification of Photomorphogenesis Knowledge of photomorphogenic processes, such as the photoperiodic control of flowering, has already led to efficient crop production strategies in photoperiodic species. A continued increase in fundamental knowledge of photomorphogenesis should enable us to modify the architecture and response of plants to our advantage. Most crops are grown in dense stands, and this leads to shade avoidance responses at the expense of crop yield. At face value, the suppression of shade avoidance offers a good prospect to increase yield in monocultures or increase the diversity of crops that can be grown in the shade of other plants. In contrast, an elongated, shade avoiding morphology is actually desirable in some fiber crops, and is usually achieved by highdensity sowing and a relatively inefficient use of seed. Constitutively shade avoiding plants could then be grown at lower densities.
List of Technical Nomenclature Absorption spectrum
A graph indicating the relative absorption of different wavelengths of light by a substance.
Action spectrum A graph indicating the relative responsiveness of different wavelengths of light in eliciting a standard response. Chromophore
The constituent of a proteinaceous photoreceptor that gives it the capacity to absorb visible light.
Cryptochromes
A family of blue/UV-A photoreceptors.
Far-red light
Light in the waveband 700–800 nm.
Photomorphogenesis
Responses of plants that occur as a result of processing information about their light environment.
Photoperiod
The length of the daily light period, which varies with the time of year.
Photoreceptor
A chromoprotein that absorbs light and is used in energy transfer or information processing.
Phototropin
The blue/UV-A photoreceptor involved in phototropism.
Phytochromes
A family of photochromic photoreceptors that absorb red and far-red light.
Seedling establishment (deetiolation)
The transition of an etiolated darkgrown seedling into a green autotrophic plant.
Skotomorphogenesis (etiolation)
The strategy of dark growth that leads to etiolation.
See also: Regulators of Growth: Auxins; Circadian Rhythms; Photoperiodism; Phytochromes and other Photoreceptors.
Further Reading Ballere´ CL (1999) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends in Plant Science 4: 97–102. Kendrick RE and Kronenberg GHM (eds) (1994) Photomorphogenesis in Plants, 2nd edn. Dordrecht: Kluwer Academic Publishers. Neff MM, Fankhauser C, and Chory J (2000) Light: an indicator of time and place. Genes & Development 14: 257–271. Sage LC (1992) Pigment of the Imagination. A History of Phytochrome Research. San Diego: Academic Press. Smith H (1998) Engineering a phytochrome gene. In: Cockshull KE, Gray D, Seymore GB, and Thomas B (eds) Genetic and Environmental Control of Horticultural Crops, pp. 175–190. Oxford: CABI Publishing. Smith H (2000) Phytochromes and light signal perception by plants – an emerging synthesis. Nature 407: 585–591. Thomas B and Vince-Prue D (1997) Photoperiodism in Plants. London: Academic Press.