Photomorphogenesis
I. Introduction A. Photomorphogenesis: control of plant morphological development by light. B. Photoreceptors: 1. Phytochrome: a chromoprotein that absorbs red and far-red light as well as blue light. There are two major forms of phytochrome; type 1 from etiolated seedlings and type 2 from green plants. 2. Cryptochrome: an unidentified group of favonoid pigments that absorb strongly in the blue and long-wave ultraviolet wavelengths. Named from its importance in cryptogams (non- flowering plants). 3. UV-B photoreceptor: compounds that absorb ultraviolet light between 280 and 320 nm. 4. Protochlorophyllide a: the immediate precursor of chlorophyll a that absorbs red and blue light in order to make the change to chlorophyll. C. The most important factor controlling light responses in photomorphogenesis is the competence to respond or sensitivity of the receptor cells. Besides the need for an amplification system like Ca2+ and calmodulin, there are two stages that are important to the process of photomorphogenesis: 1. Pattern Specification: developing cells and tissues become competent to react to light 2. Pattern Realization: the competent cells and tissues respond to light. II. Phytochrome A. A brief history: 1. Early work on the effect of flowering was done by W.W. Garner and H.A. Allard in the 1920's. The found that the duration of light and dark periods controlled flowering in plants. One of the major research species was cocklebur with required nights longer than a critical minimum to flower (i.e. short day plants). It was found that different wavelengths of light had different abilities to induce flowering. Red light was the most effective in inducing flowering. 2. Most of the research that first described phytochrome was done between 1945 and 1960 at the U.S.D.A. in Beltsville, Maryland by Harry Borthwick and Sterling Hendricks. Borthwick and Hendricks worked with seed germination of Grand Rapids lettuce seeds. They completed an action spectrum for promotion of germination. There was a peak of seed germination in the red wavelengths that could be reversed by treatment with far-red light (wavelengths between 700-800 nm). They found that what ever light treatment was given last determined whether the seeds germinated. This finding laid the ground work for the discovery and isolation of phytochrome. B. Phytochrome and its properties: 1. There are two forms of phytochrome. The Pr form which absorbs red light is blue in color. When Pr absorbs red light it is converted to the Pfr form which is olive-green in color. The Pfr form absorbs far-red light and is subsequently converted into the Pr form. The Pr form is considered the active form of phytochrome. 2. Absorption spectra for phytochrome: a. Angiosperms: maxima in red wavelengths is 666 nm (Pr absorbing form) maxima in far-red wavelength is 730 nm (Pfr absorbing form) b. Found in angiosperms, gymnosperms, ferns, mosses, liverworts, and green, red, and brown algae. The protein moieties are different but the chromophore is the same in all species. Phytochrome is synthesized in the Pr form. Phytochrome is found in the cytosol and nucleus but does not seem to be associated with any particular organelle. 3. Phytochrome is a chromoprotein. The protein portion is a homodimer consisting of two identical polypeptides of 120 kDa. The chromophore is an open-chain tetrapyrrole connected to the protein moiety through the sulfur of a cysteine. When phytochrome absorbs red light there is a cis-trans isomerization of the chromophore which causes changes in the protein moiety. The changes in the protein are responsible for the physiological changes. 4. When the Pr form absorbs red light about 85% of it is converted to Pfr. Pfr is also converted back to Pr because it can absorb a small amount of the red light. 5. There are two types of phytochrome (each can exists in the Pr or Pfr form): a. Type 1: found in etiolated seedlings b. Type 2: found in green plants. Pr absorption maxima is 654 nm for red light and 724 nm for far-red light. Several (at least five) different protein moieties have been found. c. Seedlings grown in the dark have much more type 1 phytochrome than type 2 phytochrome. This allows the seedlings to respond to very low levels of red light. Upon absorption of red light the majority of type 1 phytochrome is lost. There are three controlling factors that govern this lose of type 1 phytochrome: (1) mRNA for type 1 phytochrome is no longer produced, (2) mRNA for type 1 phytochrome is highly unstable and is therefore quickly degraded, (3) the type 1 phytochrome itself is quickly degraded. Phytochrome self regulates the gene for type 1 phytochrome production. This gene is active in the dark, but is inactive in the light. 6. Evidence that support phytochrome as the pigment responsible for photomorphogenesis are: (1) a correlation between the absorption spectrum of phytochrome and the action spectra for plant responses, (2) plant responses to red light can be immediately reversed by exposure to far-red light, (3) the irradiance level for the plant responses is quite low. 7. f (Psi)=Pfr/Pr + Pfr: the ratio of Pfr to the total amount of phytochrome of both forms. This value is used to describe the amount of phytochrome in a plant tissue. In full sunlight the ratio of red to far-red photons is 1.1- 1.2. Pr absorbs red light more efficiently than Pfr absorbs far-red light, which means that Pr will be converted to Pfr quicker than Pfr can convert back to Pr. Therefor, in sun light there is more Pfr than Pr and the f (Psi) value is about 0.6. 8. If type 1 phytochrome found in etiolated plants receives a brief red-light treatment, some of the Pfr formed will gradually disappear over time. This disappearance of Pfr is due to: (1) destruction or breakdown of Pfr by attachment to ubiquitin (a 76 amino acid protein) which targets the Pfr for degradation by proteases, or (2) dark reversion which takes several hours. Dark reversion occurs in gymnosperms and dicots, but not monocots. 9. Type 2 phytochrome does not undergo destruction or dark reversion because it is more stable. III. Cryptochrome: In 1864 Julius vonSachs discovered that blue light caused phototropism. Later it was found that near ultraviolet (UV) light called UV-A radiation between 320 and 400 nm was also involved in many plant developmental processes. The pigment responsible for the absorption of light at these wavelengths is called cryptochrome. Cryptochrome is a flavoprotein that is associated with a cytochrome protein in the plasma membrane. Its action spectrum maximum is found at 450 nm. IV. Photomorphogenesis and the effect of light dosage. A. High Irradiance Reactions (HIR): 1. Plant photomorphogenic responses that require high light levels and have action spectra different from that observed with phytochrome. Most phytochrome responses show saturation of red light at 200 J m-2. HIR needs about 100X more red light energy in their responses. 2. HIR have three kinds of action spectra: a. A single peak in the blue/UV-A spectral region b. Two spectral peaks in the blue/UV-A and red regions c. Three spectral peaks in the blue/UV-A, red, and far-red regions. 3. When etiolated seedlings are exposed to light they turn green (contain less type 1 phytochrome) and lose their sensitivity to far-red light for HIR. HIR also do not show red/far-red reversibility. 4. Etiolated angiosperm seedlings must activate cryptochrome in order to become competent to respond to phytochrome. It appears that cryptochrome activation is need before Pfr can be expressed. Many cases have been recorded where both cryptochrome and phytochrome cooperate in photomorphogenesis. B. Very Low Fluence Responses (VLFR): these plant responses involve activation by very low levels of red light. But the red light responses are not reversed by far-red light. C. Low-fluence Responses (LFR): these are responses that are typical of phytochrome. The red light response can be reversed by far-red light. Also, the amount of light needed is the same as those typically found with phytochrome action. V. The effect of light in seed germination A. Examples of light-dependent germination: 1. Seeds that respond to light are usually not from domesticated stock. This would seem practical, single most agricultural seed stocks have been developed so that they are not dormant. The seed tends to be high is fat and small in size. This would mean that a buried seed may not have enough energy to germinate and push through the soil to the surface. Therefor, the response to light ensures that the seed is on the soil surface. Far-red light inhibits germination while red light stimulates germination. Far-red light would decrease the amount of Pfr phytochrome in the seed tissues.. 2. Photodormancy: seeds that need light to germinate. Dormancy: seeds or buds that fail to grow when exposed to adequate moisture, temperature, and air for growth. B. Interactions between light and temperature in seed photodormancy: 1. Temperature does not effect the interconversions between Pr and Pfr. But, temperature does effect the processes that are controlled by Pfr. Example: Grand Rapids Lettuce (Lactuca sativa). Light needed for seed germination. If the seed are treated with 35oC after light treatment they remain dormant. Cool temperatures (10-15 oC) precludes a light treatment. 2. High temperatures decrease the Pfr level by increasing the rate of reversion to Pr. Since Pfr is the active form of phytochrome, reduction in its levels would inhibit a positive response. 3. Seeds need to be partially or fully imbibed (water uptake) before they will break dormancy. Phytochrome in the Pr form is stable, so the seed needs only the proper moisture, temperature, and air in order to respond to light and germinate. 4. Seed germination that requires a light treatment will also be controlled by the amount of Pfr the seed has acquired from the maternal parent. Since chlorophyll absorbs red light and prevents Pfr formation, seed embryos that ripen covered by maternal tissues containing high amounts of chlorophyll tend to require a light treatment for germination. Seed embryo that ripen covered by maternal tissues with little chlorophyll do not require a light treatment. 5. The length of night and day during ripening affects photodormancy. Long days (short nights) favor photodormant seeds while short days (long nights) favor nondormant seeds. C. Ecological aspects of photodormant seeds: 1. Photodormant Seed: a. Assures that the seed is not covered by soil. The seed will be able to photosynthesize soon after germination. b. Assures that seed with germinate over several years as the soil is disturbed. Prolongs longevity of the species. 2. Seed germination inhibited by light: a. Seed germination is inhibited until the seed is buried in the soil. b. Assures that the seed is protected by soil and that adequate moisture from the soil is available. 3. Phytochrome also provides the seed with clues as to the amount of canopy cover the seed will face. a. Leaves in a canopy transmit more far-red light than red light. Far-red light usually inhibits seed germination in light-requiring seed. The far-red light converts Pfr to Pr. This would indicate to a seed that the canopy cover is dense. If germination occurred, there may not be enough light penetration for photosynthesis to occur in the new seedling. b. Plant species that require shade conditions for growth are not affected by the amount of Pfr in their tissue (or the amount of far-red light transmitted through a plant canopy). D. Red and far-red light are both absorbed by the hypocotyl- radicle region of the seed. Phytochrome in the Pfr form increases the growth potential of the radicle by decreasing the water potential of the radicle cells so that they readily absorb water from the soil and germinate. Germination is a contest between the growth potential of the radicle and the mechanical restrictiveness of the surrounding seed cell layers. This mechanical restrictiveness can be either slight or substantial. In response, the radicle may need little or a great deal of force, caused by the growing tissues to break dormancy. The amount of Pfr may determine how much the radicle grows. E. Hormones, Phytochrome, and Photodormancy: 1. Gibberellins: substitute for light or other environmental requirements like temperature. Gibberellins induce the weakening of the endosperm near the tip of the radicle. This would allow radicle protrusion. 2. Cytokinins: can also substitute for a light treatment 3. Auxins: do not promote germination of photodormant or nondormant seed. Can be inhibitory at high temperatures. 4. Ethylene: role is unclear; cannot break dormancy but does effect other aspects of seed dormancy. 5. Abscisic Acid: retards germination 6. Pfr may break dormancy by causing synthesis of gibberellin and cytokinins while inhibiting abscisic acid. VI. Seedling establishment and vegetative growth of plants in response to light. A. Grass seedling (monocot) development in relation to light: 1. Light effects leaf growth and coleoptile elongation. 2. Phytochrome controls the unrolling of grass leaves. This unrolling is possibly caused by gibberellin or cytokinin whose levels are controlled by phytochrome (Pfr). B. Dicot seedling development in relation to light: 1. Dicots form a hook near the stem apex after seed germination. The seedling pushes through the soil pulling the meristem after it. 2. Hook formation is an ethylene response. Red light promotes hook opening. Hook opening occurs because ethylene synthesis in the hook is inhibited. 3. Light also increases leaf-blade expansion, petiole elongation, chlorophyll formation, and chloroplast development. C. Promotion of leaf growth by light in dicots is through HIR (High Irradiance Reaction). The blue light causes cell expansion by epidermal cell wall acidification. This loosens the cell walls so that the leaf expands quickly under turgor pressure. Pfr triggers chlorophyll formation and chloroplast development. Pfr causes aminolevulinic acid (ALA), the precursor of the pyrrole rings in chlorophyll, formation from glutamic acid. Without blue and red light, the metabolic pathway in formation of chlorophyll stops at protochlorophyllide a (the immediate precursor of chlorophyll a). Blue and red light are needed to add the phytol tail (from isoprenoid pathway) to protochlorophyllide a to make chlorophyll a. Chlorophyll a is then metabolized into chlorophyll b. VII. Affects of photomorphogenesis on vegetative growth in plants: A. Stems do not grow as quickly during the day as they do at night. Cryptochrome (blue light response) and phytochrome (red response) are both required for stem elongation. 1. Plants growing under a leaf canopy receive more far-red light than red light. This would cause the conversion of Pfr to Pr. Thus the stems would elongate, carrying the leaves (hopefully) toward the light. 2. Plants growing under a leaf canopy have reduced branching. this allows more energy to be used in stem elongation to carry the leaves to the top of the canopy. 3. Crop or greenhouse plants planted in outer rows are shorter and more highly branched that those planted in inner rows. This phenomenon is used in reforestation work were proper spacing of trees can yield straight, knot free timber. 4. Shade tolerant plants usually do not respond to far-red light stem elongation. B. Far-red light reflection from one plant to another can also effect plant growth. As competing plants grow, the reflected far-red light can cause adjacent plants to elongate in a race to keep ahead of their neighbors. C. Tillering (branching at the base of grass stems) is promoted by red light. Again, closely spaced plants that receive more far-red light show less tillering. This allows the individual plants to receive more light. VIII. Photoperiods: plants respond to the time of day that light is received. Phytochrome is the main plant pigment involved in photoperiodic effects such as bud dormancy and production of flowers and seeds. Long days promoted stem elongation and short days lead to plant changes associated with autumn (bud dormancy, frost-hardiness). IX. Light effects on anthocyanin and flavonoid synthesis and chloroplast arrangement. A. Anthocyanin and flavonoid synthesis is promoted by light. These substances are formed in specialized cells in the organ in which they are produced (fruits, leaves, stems). B. Both phytochrome and cryptochrome are the photoreceptors. UV- B receptor may also be important in flavonoid synthesis. C. Phototaxis: the movement of an organism or organelle in response to light. 1. Under high light levels chloroplasts are lined up along the radial walls of the cell. This allows the chloroplasts to shade one another thereby reducing photooxidation. Under low light the chloroplasts are distributed along the nearest and farthest walls from the light source. This maximized light absorption. 2. In angiosperms and mosses blue light, an hence cryptochrome, is responsible for the phototaxic response of chloroplasts. Phytochrome is not involved in this movement. 3. The chloroplast movement is affected by cytoplasmic streaming which is controlled by the orientation of microfilaments and microtubules of the cytoskeleton. Blue light is absorbed by some component in the cells which affects the cytoskeleton orientation. X. Source of photomorphogenesis - how photoreceptors work: A. There are two kinds of effects. The first is a fast membrane- permeability effect, the second is a slower effect on gene expression. Phytochrome and cryptochrome act on the receptor-transduction system. B. Pfr acts by changing membrane permeability. There is no evidence that phytochrome is part of any plant membrane. 1. An example is the Tanada effect where root caps that are treated with red-light develop a positive charge, causing the root tips to stick to glass. H+ are transported from the cytosol to cell walls by an ATPase in the plasma membrane. Far-red light decreases this positive charge and results in release of the root tips from the glass. 2. Nyctinastic movements of legumes leaves occurs through changes in membrane permeability to potassium ions. The electropotential across the plasma membrane is altered by Pfr which allows leakage of potassium ions out of the pulvini. 3. Ca2+ transport across the membranes is also affected by Pfr. C. Phytochrome controls gene activation and deactivation. The phytochrome effect depends on the cells involved and their developmental state. 1. Stability of mRNA is one point of the gene control. 2. Pfr stimulates the Ca-calmodulin-dependent enzyme NAD+ kinase. Thus enzyme activation may be another way that phytochrome controls gene expression. 3. Phytochrome may also act by a second-messenger in transcription.