Phototropic Response Research Articles

ARCHITECTURE OF A COOL-TEMPERATE RAIN FOREST CANOPY

There have been few descriptions of tree crown asymmetry and its development. Here I present the most comprehensive geometric description to date of crown asymmetry within a forest canopy and use allometric, trigonometric, and growth analyses to tentatively identify the dominant cause. A 25.6 × 25.6 m quadrat within a pure stand of Atherosperma moschatum Labillardière (Monimiaceae) in Tasmania was mapped with respect to the locations of tree trunks and crowns. Trunk girths and tree heights were also measured. Trunk girths were again measured ten years later. Standing biomass, growth rates, and structural properties of the trees were estimated from models. Crowns were more evenly spaced than trunks and showed a significant alignment by angle, both characteristics consistent with a tendency toward the optimal packing of the canopy. The displacement of crown locations from trunk locations was correlated both with the nearness of neighbors and with the east-facing aspect. For the quadrat as a whole, there was a projected tilt to the trees of 0.73 m 76.3° east of north. The displacement of crown locations from trunk locations was largely achieved early in tree development, consistent with a phototropic response to acute photosynthetically active radiation (PAR) limitation to growth in the understory, evident in the lower relative (projected canopy-area-specific) growth rates of the smaller trees, and with the propensity of A. moschatum to reproduce by vegetative sprouting. There was little evidence of size-dependent variation in the mechanical stresses within the trunks, but more detailed analysis of wood structure is needed. The overall height safety factor (a measure of buckling resistance) for the trees in the quadrat was 4.2, the highest reported factor to date for any tree species. Tasmania is an island in the “roaring forties,” and the high value of the safety factor is a likely response to strong and persistent winds. The estimates of the maximum growth rates of individual trees were 14.9 and 8.7 kg/yr for each of two models. The estimates of the growth rate for the whole stand were 12.1 and 7 m3·ha−1·yr−1 (8.5 and 4.9 metric tons per hectare per year, respectively).

Auxins and tropisms.

Differential growth of plants in response to the changes in the light and gravity vectors requires a complex signal transduction cascade. Although many of the details of the mechanisms by which these differential growth responses are induced are as yet unknown, auxin has been implicated in both gravitropism and phototropism. Specifically, the redistribution of auxin across gravity or light-stimulated tissues has been detected and shown to be required for this process. The approaches by which auxin has been implicated in tropisms include isolation of mutants altered in auxin transport or response with altered gravitropic or phototropic response, identification of auxin gradients with radiolabeled auxin and auxin-inducible gene reporter systems, and by use of inhibitors of auxin transport that block gravitropism and phototropism. Proteins that transport auxin have been identified and the mechanisms which determine auxin transport polarity have been explored. In addition, recent evidence that reversible protein phosphorylation controls this process is summarized. Finally, the data in support of several hypotheses for mechanisms by which auxin transport could be differentially regulated during gravitropism are examined. Although many details of the mechanisms by which plants respond to gravity and light are not yet clear, numerous recent studies demonstrate the role of auxin in these processes.

Phototropism: a family business

Blue light regulates several developmental processes in plants, including de-etiolation, tropisms and entrainment of the circadian clock. Phototropic responses involve the familiar bending of seedling hypocotyls toward blue light, but also the relocation movements of chloroplasts within the plant cell to optimize light capture. These relocation responses, which are reminiscent of the phototactic behavior of unicellular organisms, are sophisticated in Arabidopsis. Under low levels of blue light, the chloroplasts migrate toward the brightest spots within the cell (accumulation response), whereas under high-intensity illumination, the chloroplasts ‘hide’ themselves near the side cell walls, thereby avoiding exposure to potentially harmful light levels (avoidance response). Winslow Briggs and co-workers had demonstrated that hypocotyl bending responses toward low irradiances of blue light are mediated by a photoreceptor that they called nph1 (for non-phototropic hypocotyl), or phototropin. This receptor is a plasma-membrane-associated protein that contains a kinase domain located within its C-terminus. The N-terminal region contains two LOV motifs that bind the chromophore, flavin mononucleotide (FMN). Until now, the photosensors involved in other phototropic responses, such as hypocotyl phototropism in response to high irradiances and chloroplast relocation remained unknown.Two recent papers shed new light into the regulation of tropisms by blue wavelengths. The take-home message? nph1 is not alone – it is a member of a family of flavin-based photoreceptors. Takatoshui Kagawa et al.1xArabidopsis npl1: a phototropin homolog controlling the chloroplast high-light avoidance response. Kagawa, T. et al. Science. 2001; 291: 2138–2141CrossRef | PubMed | Scopus (398)See all References1 devised an ingenious method to isolate mutants deficient in the chloroplast high-light-avoidance response. They covered leaves of mutagenized Arabidopsis plants using black plates with open slits, and exposed them to strong light. In leaves of wild-type plants, the area under the slits became pale-green; by contrast, in a few mutants, the exposed area remained green, indicating an impaired chloroplast-avoidance response. The mutation sites of these mutants, initially termed cav1 mutants (for chloroplast avoidance), were located within the recently described NPL1 gene (NPH1 Like), which encodes a protein similar in sequence to phototropin. In a related study, Tatsuya Sakai et al.2xArabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Sakai, T. et al. Proc. Natl. Acad. Sci. U. S. A. 2001; 98: 6969–6974CrossRef | PubMed | Scopus (424)See all References2 showed that npl1, like nph1, noncovalently binds FMN within the LOV domains and functions as a light receptor kinase. Sakai et al. expanded the analysis of npl1 function using nph1 npl1 double mutants. These mutants showed impaired hypocotyl phototropism under both low- and high-intensity blue light, and lacked chloroplast relocation responses to low- and high-intensity blue light.The phototropin family of photoreceptors appears to be ubiquitous throughout the plant kingdom 3xThe phototropin family of photoreceptors. Briggs, W.R. et al. Plant Cell. 2001; 13: 933–997See all References3, and it is intriguing that the members of this family seem to have specialized in the control of movement. Movement of organelles within the cell probably requires interactions between phototropin signaling elements and the cytoskeleton. By contrast, tropic movements at the whole-organ level are based on coordinated responses of a population of cells. It will be interesting to learn which mechanisms allow the members of the phototropin family to control the tropism business in environments that appear to be so radically different in terms of scale and complexity. As a first step to facilitate communication, phototropin connoisseurs have recently agreed to use a common terminology, and the photoreceptors nph1 and nph2 have been redesignated as phot1 and phot2, respectively 3xThe phototropin family of photoreceptors. Briggs, W.R. et al. Plant Cell. 2001; 13: 933–997See all References3.

Phototropism in Arabidopsis roots is mediated by two sensory systems.

Phototropism has been well-characterized in stems and stem-like organs, but there have been relatively few studies of root phototropism. Our experiments suggest that there are two photosensory systems that elicit phototropic responses in roots of Arabidopsis thaliana: a previously identified blue-light photoreceptor system mediated by phototropin (=NPH1 protein) and a novel red-light-based mechanism. The phototropic responses in roots are much weaker than the graviresponse, which competes with and often masks the phototropic response. It was through the use of mutant plants with a weakened graviresponse that we were able to identify the activity of the red-light-dependent phototropic system. In addition, the red-light-based photoresponse in roots is even weaker compared to the blue-light response. Our results also suggest that phytochrome may be involved in mediating positive phototropism in roots.

Light-driven movements of the primary leaves of bean (Phaseolus vulgaris L.):A kinetic analysis

The skotonastic and phototropic responses of primary leaves of bean (Phaseolusvulgaris L.) were studied, using one primary leaf as an untreated control for its treated twin. A sudden, drastic step-down in photon fluence rate, FFR, resulted in the typical skotonastic down folding. The magnitude and kinetics of this responsewere independent of the preceding FFR as well as of the initial laminar elevation (attransition). The skotonastic response was eventually followed by increase in laminarelevation, as part of a progressive adaptation to the new (very low) FFR. The pulvinus exhibited positive and reversible phototropic curvature in response to adaxial and lateral exposure to high FFR. Adaxial exposure at different stages of its adaptation to low FFR resulted in very similar positive phototropic responses (rate and magnitude). At saturation, abaxial exposure of the pulvinus to equivalent FFR resulted in full reversal, to the same level as exposure of both sectors to low FFR, coinciding with the level of the...

The hypocotyl chloroplast plays a role in phototropic bending of Arabidopsis seedlings: developmental and genetic evidence

Chloroplasts of guard cells and coleoptiles have been implicated in the sensory transduction of blue light. The present study was aimed at establishing whether the chloroplast of the hypocotyl from Arabidopsis, another blue light-responding organ, has similar characteristics to that of sensory-transducing guard cell and coleoptile chloroplasts. Results showed that the phototropic curvature and arch length induced by blue light in Arabidopsis seedlings matched the distribution of mature chloroplasts in the bending hypocotyl. The bending arch consistently included the region of the hypocotyl containing mature chloroplasts, and never extended beyond that region. Manipulation of the extent of greening of dark-grown hypocotyls by varying red light pretreatments elicited blue light-stimulated curvatures and arch lengths that depended on the duration of the red light pretreatment and on the distribution of mature chloroplasts in the hypocotyl. Albino psd2 mutants of Arabidopsis, which lack mature chloroplasts, are devoid of phototropic sensitivity under conditions in which wild-type seedlings show large curvatures. The star mutant of Arabidopsis has a delayed greening and a delayed phototropic response as compared with wild type. Measurements of photosynthetic oxygen evolution and carbon fixation, dark respiration, and light-dependent zeaxanthin formation in the hypocotyl showed features similar to those of guard cells and coleoptiles, and distinctly different from those of mesophyll tissue. These results indicate that the hypocotyl chloroplast has characteristics similar to those associated with guard cell and coleoptile chloroplasts, and that phototropic bending of Arabidopsis hypocotyls appears to require mature chloroplasts.

Microinjection of heme oxygenase genes rescues phytochrome-chromophore-deficient mutants of the moss Ceratodon purpureus.

In protonemal tip cells of the moss Ceratodon purpureus (Hedw.) Brid., phototropism and chlorophyll accumulation are regulated by the photoreceptor phytochrome. The mutant ptr116 lacks both responses as a result of a defect in the biosynthesis of phytochromobilin, the chromophore of phytochrome, at the point of biliverdin formation. The rescue of the phototropic response and of chlorophyll synthesis were tested by injecting different substances into tip cells of ptr116. Microinjection was first optimised with the use of fluorescent dyes and an expression plasmid containing a green fluorescent protein (GFP) gene. Injected phycocyanobilin, which substitutes for phytochromobilin, rescued both the phototropic response and light-induced chlorophyll accumulation in ptr116. The same results were obtained when expression plasmids with heme oxygenase genes of rat (HO-1) and Arabidopsis thaliana (L.) Heynh. (HY1) were injected. Heme oxygenase catalyses the conversion of heme into biliverdin. Whereas HY1 has a plastid target sequence and is presumably transferred to plastids, HO-1 is proposed to be cytosolic. The data show that ptr116 lacks heme oxygenase enzyme activity and indicate that heme oxygenases of various origin are active in Ceratodon bilin synthesis. In addition, it can be inferred from the data that the intracellular localisation of the expressed heme oxygenase is not important since the plastid enzyme can be replaced by a cytosolic one.

Repetition of the Classical Boysen-Jensen and Nielsen's Experiment on Phototropism of Oat Coleoptiles

The classical experiment of phototropic response as reported by Boysen-Jensen and Nielsen (1926), which supports the Cholodny-Went theory, was repeated in detail. In the original experiment, etiolated oat (Avena sativa L. cv. Victory) coleoptiles with mica inserted into their tip only showed a positive response when the mica was placed parallel toward the light source and not if it was inserted perpendicularly. On the contrary, we found a positive response irrespective of whether the mica was inserted parallel or perpendicularly to the light source. Damage owing to rude splitting severely reduced the response upon perpendicular insertion. These results invalidate the Boysen-Jensen and Nielsen's experiment as a support of the Cholodny-Went theory and lend support to the Bruinsma-Hasegawa theory ascribing phototropism to the local light-induced accumulation of growth inhibitors against a background of even auxin distribution, the diffusion of auxin being unaffected.

RPT2: A Signal Transducer of the Phototropic Response in Arabidopsis

The blue light receptor NPH1 (for nonphototropic hypocotyl) has been considered to be the only UV-A/blue light receptor that induces a phototropic response by the hypocotyl and root of Arabidopsis. By analysis of root phototropism (rpt) mutants, we show, however, the involvement of another blue light receptor as well as the existence of two separate signaling pathways working downstream of these receptors in the phototropic response. A newly isolated gene, RPT2, controls one of these pathways. The RPT2 gene is light inducible; encodes a novel protein with putative phosphorylation sites, a nuclear localization signal, a BTB/POZ domain, and a coiled-coil domain; and belongs to a large gene family that includes the recently isolated NPH3 gene. From genetic, physiological, and biochemical evidence, we propose a genetic model of the signaling pathways that induce the phototropic response in Arabidopsis.

RPT2: A Signal Transducer of the Phototropic Response in Arabidopsis

RPT2: A Signal Transducer of the Phototropic Response in Arabidopsis

RPT2: A signal transducer of the phototropic response in Arabidopsis: Sakai T, Wada T, Ishiguro S, Okada K: Plant Cell 2000, 12:225–236

RPT2: A signal transducer of the phototropic response in Arabidopsis: Sakai T, Wada T, Ishiguro S, Okada K: Plant Cell 2000, 12:225–236

RPT2: A signal transducer of the phototropic response in Arabidopsis: Sakai T, Wada T, Ishiguro S, Okada, K: Plant Cell 2000, 12:225–236

RPT2: A signal transducer of the phototropic response in Arabidopsis: Sakai T, Wada T, Ishiguro S, Okada, K: Plant Cell 2000, 12:225–236

RPTs: A signal transducer of the phototropic response in Arabidopsis: Sakai T, Wada T, Ishiguro S, Okada K: Plant Cell 2000, 12:225–236

RPTs: A signal transducer of the phototropic response in Arabidopsis: Sakai T, Wada T, Ishiguro S, Okada K: Plant Cell 2000, 12:225–236

Phototropism: a "simple" physiological response modulated by multiple interacting photosensory-response pathways.

Phototropism is the process by which plants reorient growth of various organs, most notably stems, in response to lateral differences in light quantity and/or quality. The ubiquitous nature of the phototropic response in the plant kingdom implies that it provides some adaptive evolutionary advantage. Upon visual inspection it is tempting to surmise that phototropic curvatures result from a relatively simple growth response to a directional stimulus. However, detailed photophysiological, and more recently genetic and molecular, studies have demonstrated that phototropism is in fact regulated by complex interactions among several photosensory systems. At least two receptors, phototropin and a presently unidentified receptor, appear to mediate the primary photoreception of directional blue light cues in dark-grown plants. PhyB may also function as a primary receptor to detect lateral increases in far-red light in neighbor-avoidance responses of light-grown plants. Phytochromes (phyA and phyB at a minimum) also appear to function as secondary receptors to regulate adaptation processes that ultimately modulate the magnitude of curvature induced by primary photoperception. As a result of the interactions of these multiple photosensory systems plants are able to maximize the adaptive advantage of the phototropic response in ever changing light environments.

Plant biology: Head into the Blue Light

The phototropism response of plants directs growth toward light sources. Motchoulski and Liscum have now identified and characterized one of the early molecular components, NPH3, that Arabidopsis uses to respond to blue light. The NPH3 protein interacts with the NPH1 photoreceptor and may function as a scaffold that brings together the various molecular components responsible for the initial phototropic response to blue light. Motchoulski, A., and Liscum, E. (1999) Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science 286 : 961-964. [Abstract] [Full Text]

Role of a white collar-1-white collar-2 complex in blue-light signal transduction

Mutations in either white collar-1 (wc-1) or white collar-2 (wc-2) lead to a loss of most blue-light-induced phenomena in Neurospora crassa. Sequence analysis and in vitro experiments show that WC-1 and WC-2 are transcription factors regulating the expression of light-induced genes. The WC proteins form homo- and heterodimers in vitro; this interaction could represent a fundamental step in the control of their activity. We demonstrate in vivo that the WC proteins are assembled in a white collar complex (WCC) and that WC-1 undergoes a change in mobility due to light-induced phosphorylation events. The phosphorylation level increases progressively upon light exposure, producing a hyperphosphorylated form that is degraded and apparently replaced in the complex by a newly synthesized WC-1. WC-2 is unmodified and also does not change quantitatively in the time frame examined. Light-dependent phosphorylation of WC-1 also occurs in a wc-2 mutant, suggesting that a functional WC-2 is dispensable for this light-specific event. These results suggest that light-induced phosphorylation and degradation of WC-1 could play a role in the transient expression of blue-light-regulated genes. Our findings suggest a mechanism by which WC-1 and WC-2 mediate light responses in Neurospora.

Phytochrome-controlled phototropism of protonemata of the moss ceratodon purpureus: physiology of the wild type and class 2 ptr-mutants

Phototropism and polarotropism in protonemata of the moss Ceratodon purpureus are controlled by the photoreceptor phytochrome. One class of phototropism mutants is characterised by growing randomly when kept for a prolonged time (5 d or longer) in unilateral red light. It was found that a subclass of these mutants grows faster than the wild type, the rate of cell division and the length of the cells being increased. This difference is found for light-grown and dark-grown filaments. It is therefore suggested that the mutant phenotype neither results from a defect in phytochrome photoconversion nor from a defect in phytochrome-gradient formation. Instead, it is possible that a factor which is involved in both signal transduction of phototropism and regulation of cell size and cell division is deregulated. If dark-grown mutant filaments are phototropically stimulated for 24 h, they show a weak phototropic response. Phototropism and polarotropism fluence-rate effect curves for mutants were flattened and shifted to higher fluence rates compared with those for the wild type. With wild-type filaments, a previously unreported response was observed. At a low fluence rate, half of the filaments grew positively phototropically, while the other half grew negatively phototropically. It seems that under these conditions, a phytochrome gradient with two maxima for the far-red-absorbing form of phytochrome (Pfr) within the cross-section of the cell is displayed by the response of the filaments. At higher fluence rates, all filaments of the wild type grew towards the light. These data and results from microbeam irradiation experiments and from phototropism studies with filaments growing within agar, indicate that light refraction plays an important role in the formation of the Pfr gradient in phototropism of Ceratodon.

LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): Binding sites for the chromophore flavin mononucleotide

Phototropism, the bending response of plant organs to or away from a directional light source, is one of the best studied blue light responses in plants. Although phototropism has been studied for more than a century, recent advances have improved our understanding of the underlying signaling mechanisms involved. The NPH1 gene of Arabidopsis thaliana encodes a blue light-dependent autophosphorylating protein kinase with the properties of a photoreceptor for phototropism. NPH1 apoprotein noncovalently binds FMN to form the holoprotein nph1. The N-terminal region of the protein contains two LOV (light, oxygen, or voltage) domains that share homology with sensor proteins from a diverse group of organisms. These include the bacterial proteins NIFL and AER, both of which bind FAD, and the phy3 photoreceptor from Adiantium capillus-veneris. The LOV domain has therefore been proposed to reflect a flavin-binding site, regulating nph1 kinase activity in response to blue light-induced redox changes. Herein we demonstrate that the LOV domains of two nph1 proteins and phy3 bind stoichiometric amounts of FMN when expressed in Escherichia coli. The spectral properties of the chromopeptides are similar to the action spectrum for phototropism, implying that the LOV domain binds FMN to function as a light sensor. Thus, our findings support the earlier model that nph1 is a dual-chromophoric flavoprotein photoreceptor regulating phototropic responses in higher plants. We therefore propose the name phototropin to designate the nph1 holoprotein.

Arabidopsis contains at least four independent blue-light-activated signal transduction pathways.

We have investigated the stomatal and phototropic responses to blue light of a number of single and double mutants at various loci that encode proteins involved in blue-light responses in Arabidopsis. The stomatal responses of light-grown mutant plants (cry1, cry2, nph1, nph3, nph4, cry1cry2, and nph1cry1) did not differ significantly from those of their wild-type counterparts. Second positive phototropic responses of etiolated mutant seedlings, cry1, cry2, cry1cry2, and npq1-2, were also similar to those of their wild-type counterparts. Although npq1 and single and double cry1cry2 mutants showed somewhat reduced amplitude for first positive phototropism, threshold, peak, and saturation fluence values for first positive phototropic responses of etiolated seedlings did not differ from those of wild-type seedlings. Similar to the cry1cry2 double mutants and to npq1-2, a phyAphyB mutant showed reduced curvature but no change in the position or shape of the fluence-response curve. By contrast, the phototropism mutant nph1-5 failed to show phototropic curvature under any of the irradiation conditions used in the present study. We conclude that the chromoproteins cry1, cry2, nph1, and the blue-light photoreceptor for the stomatal response are genetically separable. Moreover, these photoreceptors appear to activate separate signal transduction pathways.

Tree Growth Regulator Effect on Phototropism - Its Implication for Utility Forestry

Pruning procedures such as V-trimming or side-trimming used by electric utilities in tree maintenance programs result in asymmetrical light exposure within tree canopies, producing the potential for phototropic growth response. The tree growth regulators (TGRs) paclobutrazol and flurprimidol are used to reduce the rate of shoot regrowth following pruning. The mode of action involves complexing of the growth retardant with cytochrome P -dependent enzymes in the metabolic pathway for gibberellins, plant hormones responsible for shoot elongation. Because cytochrome P450 also is a part of the blue light receptor system that controls phototropism, it was hypothesized that shoot growth, as well as phototropic curvature, would be reduced by paclobutrazol and flurprimidol. Effects of soil-applied (0, 0.5, 1, and 5 ppm) paclobutrazol and flurprimidol on shoot growth and phototropism of greenhouse-grown seedlings were found to vary among species. Neither shoot growth nor phototropic curvature in American sycamore (Platanus occidentalis L.) was reduced by treatment with the TGRs. In contrast, shoot growth of silver maple (Acer saccharinum L.) was reduced by all concentrations of both paclobutrazol and flurprimidol, whereas phototropic curvature was reduced only by flurprimidol. Phototropic curvature of etiolated zinnia {Zinnia elegans 'Scarlet'Jacq.) was reduced by both growth regulators.