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.