JXB Advance Access originally published online on December 12, 2003
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Journal of Experimental Botany, Vol. 55, No. 395, pp. 271-276, January 1, 2004
© 2004 Oxford University Press
Light Signalling and Clock |
Light signals, phytochromes and cross-talk with other environmental cues
Received 29 April 2003; Accepted 8 October 2003
Department of Biology, University of Leicester, Leicester LE1 7RH, UK
* To whom correspondence should be addressed. Fax: +44 (0)116 252 2791. E-mail: gcw1{at}le.ac.uk
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Abstract |
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 Top Abstract IntroductionPhotoreceptor interactionsInteraction of light and...Interaction of light and...ConclusionsReferences |
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Plants have evolved highly complex sensory mechanisms to monitor their surroundings and adapt their growth and development to the prevailing environmental conditions. The integration of information from multiple environmental cues enables the co-ordination of development with favourable seasonal conditions and, ultimately, determines plant form. Light signals, perceived via the phytochrome, cryptochrome and phototropin photoreceptor families, are especially important environmental signals. Redundancy of function among phytochromes and their interaction with blue light photoreceptors enhance sensitivity to light signals, facilitating the accurate detection of, and response to, environmental fluctuations. In this review, current understanding of Arabidopsis phytochrome functions will be summarized, in particular, the interactions among the phytochromes and the integration of light signals with directional and temperature sensing mechanisms.
Key words: Arabidopsis, environmental cues, light signals, photoreceptors, temperature sensing mechanisms.
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Introduction |
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TopAbstractIntroductionPhotoreceptor interactionsInteraction of light and...Interaction of light and...ConclusionsReferences |
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As sessile organisms that cannot choose their surroundings, plants need to modify their growth and development to suit their ambient environment. Such developmental plasticity involves the integration of multiple environmental signals, enabling plants to synchronize their growth with seasonal changes and compete effectively with neighbours for essential resources. Light signals are amongst the most important environmental cues regulating plant development. In addition to light quantity, plants monitor the quality, periodicity and direction of light and use the information to modulate multiple physiological responses, from seed germination and seedling establishment through to mature plant architecture and the onset of reproductive development. In higher plants there are three principal families of signal-transducing photoreceptors; the red/far-red (R/FR) light-absorbing phytochromes and the UV-A/blue light-absorbing cryptochromes and phototropins (reviewed in Quail, 2002). The phytochromes are reversibly photochromic biliproteins that absorb maximally in the red (R) and far-red (FR) regions of the spectrum. In Arabidopsis thaliana, five discrete apophytochrome-encoding genes, PHYA–PHYE, have been isolated and sequenced. These can be clustered by protein similarity into three subfamilies: A/C, B/D and E (Clack et al., 1994; Mathews and Sharrock, 1997).
Phytochrome is synthesized in its inactive R-absorbing (Pr) form and activity is acquired upon phototransformation to the FR-absorbing (Pfr) isomer (Kendrick and Kronenberg, 1994). The photoconversion of phytochrome from its Pr to Pfr form has been demonstrated, at least for phyA and phyB, to trigger translocation of a proportion of the photoreceptor from the cytoplasm to the nucleus (Sakamoto and Nagatani, 1996; Kircher et al., 1999; Yamaguchi et al., 1999). In the nucleus, for phyB at least, Pfr can interact with PIF3, a transcriptional regulator to control expression of a number of target genes (Ni et al., 1999; Martinez-Garcia et al., 2000).
Elucidation of the roles of individual phytochromes in mediating plant growth is often confounded by their redundant and overlapping mechanisms of action. The isolation of mutants deficient in individual phytochromes and the subsequent creation of multiple mutant combinations have, therefore, been essential in the determination of individual phytochrome functions and the dissection of functional interactions between family members. In addition to providing insights into individual phytochrome functions, the use of multiple mutant combinations has also enabled progress in the understanding of how light signals integrate with other environmental cues. The focus here is on the use of Arabidopsis mutants, deficient in multiple phytochromes, in order to elucidate the complex overlapping roles of individual family members during photomorphogenesis. The role of these mutants in dissecting cross-talk between light-, gravity- and temperature-sensing mechanisms is also discussed.
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Photoreceptor interactions |
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TopAbstractIntroductionPhotoreceptor interactionsInteraction of light and...Interaction of light and...ConclusionsReferences |
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Seedling establishment
The light environment in which a seedling develops can influence not only the timing of seed germination but the ensuing developmental strategy of a plant. Induction of Arabidopsis seed germination by R involves both phyA and phyB (Shinomura et al., 1994, 1996). Germination responses displaying R/FR reversibility are characteristic of the low fluence response (LFR) mode of phytochrome action and enables buried seeds to detect proximity to the soil surface and exposed seeds to identify canopy gaps. The retention of R/FR reversible germination responses in phyAphyB double mutants implicated the participation of another phytochrome in this response, a role subsequently assigned to phyE (Hennig et al., 2002).
Many seeds that have been imbibed in darkness acquire extreme sensitivity to light that is typical of the phyA-mediated very low fluence response (VLFR) mode of phytochrome action. It is estimated that these sensitized seeds would be induced to germinate following exposure to only a few milliseconds of daylight, thus enabling the opportunistic exploitation of very brief soil disturbances (Smith, 1982). Inhibition of germination following prolonged exposure to FR, most likely represents the phyA-mediated high irradiance response (FR-HIR) mode of phytochrome action and may be ecologically relevant as a means of delaying the germination of seeds situated under chlorophyllous vegetation or leaf litter (Smith and Whitelam, 1990).
Following the induction of germination, light signals act to constrain hypocotyl extension while initiating the expansion of cotyledons and the concomitant synthesis of chlorophyll. Despite showing no obvious mutant phenotype following growth under white light or R, mutants deficient in phyA have revealed a unique role for this photoreceptor in mediating the inhibition of hypocotyl elongation growth under FR and FR-enriched light environments (Nagatani et al., 1993; Parks and Quail, 1993; Whitelam et al., 1993). By contrast, phyB-deficiency confers no aberrant phenotype under FR, but leads to a marked loss of seedling sensitivity to R for a wide range of de-etiolation responses (Koornneef et al., 1980; Somers et al., 1991; Reed et al., 1993). Seedlings deficient in both phyA and phyB display a greater insensitivity to R than monogenic phyB seedlings (Reed et al., 1994). Thus, although phyB plays the major role in inhibition of hypocotyl elongation in red light, phyA can also contribute to this response. An additional minor role is performed by phyD (Aukerman et al., 1997) whereas the contribution of phyE to seedling de-etiolation appears negligible (Devlin et al., 1998).
The recent identification of mutants at the PHYC locus has revealed a role for this phytochrome in the R-mediated inhibition of hypocotyl elongation (Franklin et al., 2003a; Monte et al., 2003). The combined loss of phyA and phyC in the Ws ecotype (phyC-1) resulted in a significant increase in hypocotyl length, an effect greater than that observed in phyC-1 plants. Since loss of phyA alone has no effect on sensitivity to R, the possibility exists that phyA and phyC act redundantly to regulate the R-control of hypocotyl growth (Franklin et al., 2003a). The role of phyC in this response was most pronounced at low fluence rates and not observable in the phyB mutant background, suggesting a possible role for phyC in modulating phyB function (Franklin et al., 2003a). No role for phyC was identified in the inhibition of hypocotyl elongation in FR (Franklin et al., 2003a; Monte et al., 2003).
The isolation and characterization of mutants deficient in cryptochromes 1 and 2 (cry1 and cry2) have defined roles for these photoreceptors throughout seedling development (Lin et al., 1996, 1998). Despite uncertainty over the exact nature of co-action, it is accepted that B-mediated de-etiolation involves the interaction of both phytochrome and cryptochrome signalling (Yanovsky et al., 1995; Ahmad and Cashmore, 1997; Casal and Mazzella, 1998). A physical interaction between CRY1 and PHYA proteins has been demonstrated (Ahmad et al., 1998; Ahmad, 1999) in addition to a functional interaction between cry2 and phyB (Más et al., 2000). Mutant combinations deficient in phyC displayed elongated hypocotyls in B, an effect most evident at low fluence rates (Franklin et al., 2003a). Under these conditions, it has been shown that the cry2 function predominates in the regulation of hypocotyl elongation (Lin et al., 1998). The hyposensitivity of phyC mutants to low fluence rate of B may therefore indicate a possible functional interaction between phyC and cry2. There is also evidence of functional redundancy between phytochromes and cryptochromes. For example, the inhibition of hypocotyl growth by a R pulse in phyB seedlings that have been pretreated with white light, requires the presence of either phyD or cry1 (Hennig et al., 1999).
Mature plant development
In Arabidopsis and many other plant species, deficiency of phyB has a marked effect on the architecture of the mature light-grown plant. Phytochrome B-deficient plants display an elongated growth habit, retarded leaf development, increased apical dominance, and early flowering (Robson et al., 1993; Halliday et al., 1994; Devlin et al., 1996). This pleiotropic phenotype resembles the shade avoidance syndrome shown by wild-type plants following the perception of low R:FR ratio and suggests a predominant role for phyB in suppressing this response under natural conditions (Whitelam and Devlin, 1997). The ability to respond to the perceived threat of shading, and therefore to execute architectural changes before canopy closure, provides a crucial competitive strategy to plants growing in dense stands (Ballaré et al., 1990).
The retention of shade avoidance responses in phyB null mutants indicated the involvement of additional phytochromes (Whitelam and Smith, 1991; Robson et al., 1993; Halliday et al., 1994). Multiple mutant analyses have since revealed that the perception of low R:FR in Arabidopsis is mediated solely by phyB, D and E, acting in a functionally redundant manner (Devlin et al., 1996, 1998, 1999; Franklin et al., 2003b). These represent the most recently evolved members of the phytochrome family and form a distinct subgroup (Mathews and Sharrock, 1997). It is therefore possible that competition for light may have provided the selective pressure for their evolution (Devlin et al., 1998).
Adult Arabidopsis plants structure their leaves in a compact rosette phenotype. The elongated internodes observed in phyAphyBphyE-triple mutant plants was the basis on which the phyE mutation was isolated and led to the proposal that maintenance of the rosette phenotype is regulated, redundantly, by phyA, B and E (Devlin et al., 1998). The elongated appearance of phyAphyBphyDphyE-quadruple mutants grown under white light, a phenotype not displayed in phyBphyDphyE-triple mutants has supported such a proposal (Franklin et al., 2003b). Physiological comparison of these genotypes also revealed a significant role for phyA in the modulation of rosette leaf expansion and petiole elongation in high R:FR (Franklin et al., 2003b). Analysis of mutants deficient in phyC revealed this phytochrome to play a similar role to phyA in regulating rosette leaf elongation in high R:FR (Franklin et al., 2003b; Monte et al., 2003).
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Interaction of light and directional sensing systems |
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TopAbstractIntroductionPhotoreceptor interactionsInteraction of light and...Interaction of light and...ConclusionsReferences |
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Gravity provides plants with a continuous and unidirectional signal, enabling emerging seedlings to orientate themselves within the soil. Correct spatial orientation ensures that primary roots grow downwards to find water and essential minerals (positive gravitropism) while primary shoots grow upwards towards light at the soil surface (negative gravitropism). Multiple plant organs are also subject to reorientation and can change their growth angle in response to gravitational signals (Hangarter, 1997). The angle from the vertical at which an organ shows no gravity-induced differential growth is termed the gravitational set-point angle (GSA) (Digby and Firn, 1995). Gravitropism responses are, however, not independent from other environmental stimuli and are often modulated by light signals perceived through phytochromes.
Exposure of dark-grown maize roots to R can alter the GSA from perpendicular to the gravity vector to a positively gravitropic orientation (Lu et al., 1996). The gravitropism of stems is also modulated by light. In etiolated Arabidopsis seedlings, R and FR, acting through either phyA or phyB, lead to agravitropism of the hypocotyl (Liscum and Hangarter, 1993; Poppe et al., 1996; Robson and Smith, 1996). It is possible that this phenomenon is of ecological significance, effectively leading to ‘enhancement’ of phototropic curvature via elimination of gravitropic compensation which can occur when phototropically-stimulated plant organs bend in relation to the gravitational vector. In the lazy-2 mutant of tomato, R was shown to reverse the GSA of hypocotyls, resulting in positive gravitropism (Gaiser and Lomax, 1993). In addition to effects on primary roots and shoots, light can also regulate gravitropism in apical hooks and secondary stems (Myers et al., 1994).
The phytochromes are also known to interact more directly with phototropism. For example, R, acting predominantly through phyA is known to lead to enhancement of subsequent phototropic curvature (Parks et al., 1996; Janoudi et al., 1997a). This appears to be a discrete response, not related to phytochrome-mediated agravitropism, mediated by both phyA and phyB. It has also been established that manifestation of first positive phototropic curvature is abolished in Arabidopsis seedlings which are doubly null for phyA and phyB, indicating a specific requirement for phytochrome action for the display of this archetypal blue light response (Janoudi et al., 1997b).
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Interaction of light and temperature sensing |
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TopAbstractIntroductionPhotoreceptor interactionsInteraction of light and...Interaction of light and...ConclusionsReferences |
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Alterations in the ambient growth temperature can dramatically affect plant physiology. In many species, exposure to a period of cold treatment provides seasonal information, enabling plants to germinate (stratification) or initiate reproduction (vernalization) under more favourable conditions. The ability to anticipate and, consequently, prevent the adverse effects of a particular seasonal environment is selectively advantageous to plants through reducing competition for resources and increasing the chances of outbreeding and genetic recombination. Such information is often integrated with other environmental stimuli, such as daylength. Extended periods of cold temperature and reduced daylength provide plants with a reliable indication of seasonal progression and are amongst the most important environmental factors governing the timing of floral transition (Samach and Coupland, 2000; Simpson and Dean, 2002). Sensitivity to the timing of light and darkness, termed photoperiodism, involves the integration of temporal information, provided by the circadian oscillator, with light/dark discrimination provided by specific photoreceptors. In the long-day plant (LDP) Arabidopsis, flowering is accelerated under photoperiods exceeding a critical daylength. Here, the presence of light is perceived through the action of either cry2 or phyA (Yanovsky and Kay, 2002).
Genetic and physiological analyses have grouped mutations that delay flowering into independent promotory pathways. These include the long-day pathway, the autonomous pathway and the gibberellic acid (GA)-dependent pathway (Koornneef et al., 1998). The vernalization response acts separately, but similarly, to the autonomous pathway to repress transcript levels of the floral repressor FLC (Michaels and Amasino, 1999). The stable repression of FLC levels requires a nuclear localized protein, VRN2, although this is not required for the initial reduction in transcript levels (Gendall et al., 2001). The requirement of vernalization is conferred by dominant alleles of the FRI gene, the product of which promotes FLC accumulation (Johanson et al., 2000). Downstream targets of FLC include the floral integrators FT and SOC1/AGL20 (Lee et al., 2000; Rouse et al., 2002).
In addition to photoperiod and vernalization, ambient growth temperature can have profound effects on flowering (Blázquez et al., 2003; Halliday et al., 2003). Growth of Arabidopsis plants at reduced temperatures has revealed a novel thermosensory pathway controlling floral initiation (Blázquez et al., 2003). Delayed flowering was observed in wild-type plants grown at 16 °C, a response absent in the autonomous pathway mutants, fca-1 and fve-1 (Blázquez et al., 2003). The authors propose a dual role for these proteins in flowering control: a temperature-dependent mechanism, where they act jointly and a temperature-independent mechanism where they act redundantly. Both FCA and FVE are believed to down-regulate the floral repressor FLC (Sheldon et al., 2000; Michaels and Amasino, 2001). The modest increases in FLC levels observed at lower temperatures suggest that the temperature-dependent control of flowering time by FCA and FVE operates through an FLC-independent pathway (Blázquez et al., 2003). This information is believed to be integrated with other environmental signals, such as daylength, through the floral promoter FT (Kardailsky et al., 1999; Kobayashi et al., 1999).
Observations revealing temperature-dependency in the flowering responses of photoreceptor mutants have provided insight into the interaction between light and temperature signalling (Blázquez et al., 2003; Halliday et al., 2003). Mutants deficient in the B-photoreceptor cry2 (fha) displayed an exaggerated flowering response to change in ambient temperature, with a significant delay at 16 °C. The combined deficiency of cry2 and phyA revealed synergism between these photoreceptors, with the double mutant flowering as late at 23 °C as the fha/cry2 mutant at 16 °C (Blázquez et al., 2003). Growth at 16 °C also abolished the early flowering phenotypes of phyB and phyAphyBphyD-triple mutants, despite plants retaining elongation responses characteristic of the shade avoidance syndrome (Halliday et al., 2003). The early flowering response of plants at 23 °C was shown to correlate with elevated levels of the floral promoter FT and provides evidence of discrete pathways controlling the flowering and elongation components of low R:FR perception (Halliday et al., 2003). Repression of flowering in the phyAphyBphyD-triple mutant at 16 °C was relieved by the additional loss of phyE, suggesting a novel and important role for this phytochrome in repressing floral induction at lower temperatures.
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Conclusions |
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TopAbstractIntroductionPhotoreceptor interactionsInteraction of light and...Interaction of light and...ConclusionsReferences |
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Light signals are amongst the most important environmental factors that regulate the growth and development of plants. The phenotypic plasticity awarded by effective monitoring of the ambient light environment confers considerable advantage to plants growing in natural communities. The capacity to respond to the perceived threat of shading promotes survival by enabling plants to overtop competing vegetation and precociously initiate reproduction. The integration of gravitropic and phototropic signalling are of adaptive significance in orientating plant organs within their environment. Such adaptations enhance photosynthetic efficiency by enabling plants to grow towards sunlight and position their lateral organs for optimum light capture and gas exchange. Synchronization of flowering time to environmental cues, such as photoperiod and temperature, enhance survival through promoting seed set during optimal seasonal conditions and increasing the chance of out-breeding and genetic recombination.
The multiplicity of responses available to plants in response to environmental light signals results from functional divergence within the phytochrome family of photoreceptors. Redundancy between family members and co-actions with blue light-sensing mechanisms increase sensitivity to environmental fluctuations and permit an array of developmental responses. Phylogenetic studies in Arabidopsis have revealed common evolutionary ancestry between phytochromes B, D and E. These form a distinct subgroup that act redundantly to control responses to perceived vegetational shade in addition to their own, individual, functions. Phytochrome A shares a common ancestry with phyC and performs regulatory roles in plant architecture, flowering and FR sensing. Until recently, the absence of a phyC mutant has precluded functional analysis of this phytochrome. Mutant analyses have since revealed phyC to be a weak R sensor with no role in FR sensing (Franklin et al., 2003a; Monte et al., 2003). Preliminary evidence suggests that phyC acts as a modulator of phyB in R and performs a role in B-sensing, possibly through interaction with cry2 (Franklin et al., 2003a). The future creation and characterization of mutants, deficient in multiple phytochrome combinations, should provide further insight into the integration of light signalling with other environmental stimuli and ultimately broaden understanding of adaptive plasticity in natural light environments.
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References |
|---|
|
TopAbstractIntroductionPhotoreceptor interactionsInteraction of light and...Interaction of light and...ConclusionsReferences |
|---|
Ahmad M. 1999. Seeing the world in red and blue: insight into plant vision and photoreceptors. Current Opinion in Plant Biology 2, 230–235.[CrossRef][Web of Science][Medline]
Ahmad M, Cashmore AR. 1997. The blue light receptor cryptochrome 1 shows functional dependence on phytochrome A or phytochrome B in Arabidopsis thaliana. The Plant Journal 11, 421–427.[CrossRef][Web of Science][Medline]
Ahmad M, Jarillo J, Smirnova O, and Cashmore AR. 1998. The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro. Molecular Cell 1, 939–948.[CrossRef][Web of Science][Medline]
Aukerman MJ, Hirschfeld M, Wester L, Weaver M, Clack T, Amasino RM, Sharrock RA. 1997. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. The Plant Cell 9, 1317–1326.[Abstract]
Ballaré CL, Scopel AL, Sánchez RA. 1990. Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247, 329–332.
Blázquez MA, Ahn JH, Weigel D. 2003. A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nature Genetics 33, 168–171.[CrossRef][Web of Science][Medline]
Casal JJ, Mazzella MA. 1998. Conditional synergism between cryptochrome 1 and phytochrome B is shown by analysis of phyA, phyB, hy4 simple, double and triple mutants in Arabidopsis. Plant Physiology 118, 19–25.
Clack T, Mathews S, Sharrock RA. 1994. The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Molecular Biology 25, 413–427.[CrossRef][Web of Science][Medline]
Devlin PF, Halliday KJ, Harberd NP, Whitelam GC. 1996. The rosette habit of Arabidopsis thaliana is dependent upon phytochrome action: novel phytochromes control internode elongation and flowering time. The Plant Journal 10, 1127–1134.[CrossRef][Web of Science][Medline]
Devlin PF, Patel SR, Whitelam GC. 1998. Phytochrome E influences internode elongation and flowering time in Arabidopsis. The Plant Cell 10, 1479–1487.
Devlin PF, Robson PRH, Patel SR, Goosey L, Sharrock RA, Whitelam GC. 1999. Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation and flowering time. Plant Physiology 119, 909–915.
Digby J, Firn R. 1995. The gravitropic set-point angle (GSA): the identification of an important developmentally controlled variable governing plant architecture. Plant, Cell and Environment 18, 1434–1440.[CrossRef][Medline]
Franklin KA, Davis SJ, Stoddart WM, Vierstra RD and Whitelam GC. 2003a. Mutant analyses define multiple roles for phytochrome C in Arabidopsis thaliana photomorphogenesis. The Plant Cell 15, 1981–1989.
Franklin KA, Praekelt U, Stoddart WM, Billingham OE, Halliday KJ, Whitelam GC. 2003b. Phytochromes B, D and E act redundantly to control multiple physiological responses in Arabidopsis. Plant Physiology 131, 1340–1346.
Gaiser JC, Lomax TL. 1993. The altered gravitropic response of the lazy-2 mutant of tomato is phytochrome regulated. Plant Physiology 102, 339–344.[Abstract]
Gendall AR, Levy YY, Wilson A, Dean C. 2001. The VERNALIZATION 2 gene mediates the epigenic regulation of vernalization in Arabidopsis. Cell 107, 525–535.[CrossRef][Web of Science][Medline]
Halliday KJ, Koorneef M, Whitelam GC. 1994. Phytochrome B and at least one other phytochrome mediate the accelerated flowering response of Arabidopsis thaliana L. to low red/far-red ratio. Plant Physiology 104, 1311–1315.[Abstract]
Halliday KJ, Salter MG, Thingnaes MG, Whitelam GC. 2003. The phyB-controlled flowering pathway is temperature sensitive and is mediated by the floral integrator FT. The Plant Journal 33, 875–885.[CrossRef][Web of Science][Medline]
Hangarter RP. 1997. Gravity, light and plant form. Plant, Cell and Environment 20, 796–800.[CrossRef][Medline]
Hennig L, Funk M, Whitelam GC, Schäfer E. 1999. Functional interaction of cryptochrome 1 and phytochrome D. The Plant Journal 20, 289–294.[Web of Science][Medline]
Hennig L, Stoddart WM, Dieterle M, Whitelam GC, Schäfer E. 2002. Phytochrome E controls light-induced germination of Arabidopsis. Plant Physiology 128, 194–200.
Janoudi AK, Gordon WR, Wagner D, Quail P, Poff KL. 1997a. Multiple phytochromes are involved in red-light induced enhancement of first positive phototropism in Arabidopsis thaliana. Plant Physiology 113, 975–979.[Abstract]
Janoudi AK, Konjevic R, Whitelam GC, Gordon W, Poff KL. 1997b. Both phytochrome A and phytochrome B are required for the normal expression of phototropism in Arabidopsis thaliana seedlings. Physiologia Plantarum 101, 278–282.[CrossRef]
Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347.
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D. 1999. Activation tagging of the floral inducer FT. Science 286, 1962–1965.
Kendrick RE, Kronenberg GHM. 1994. Photomorphogenesis in plants, 2nd edn. Dordrecht, The Netherlands: Kluwer Academic Publishers.
Kircher S, Kozma-Bognor L, Adam E, Harter K, Schäfer E, Nagy F. 1999. Light quality-dependent nuclear import of the plant photoreceptors A and B. The Plant Cell 11, 1445–1456.
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T. 1999. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960–1962.
Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Peeters AJM. 1998. Genetic interactions among late flowering mutants of Arabidopsis. Genetics 148, 885–892.
Koornneef M, Rolff E, Spruitt CJP. 1980. Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana L. Heynh. Zeitschrift für Pflanzenphysiologie 100, 147–160.[Web of Science]
Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I. 2000. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes and Development 14, 2366–2376.
Lin C, Ahmad M, Cashmore AR. 1996. Arabidopsis cryptochrome 1 is a soluble protein mediating blue light-dependent regulation of plant growth and development. The Plant Journal 10, 893–902.[CrossRef][Web of Science][Medline]
Lin C, Yang H, Guo H, Mocker T, Chen J, Cashmore AR. 1998. Enhancement of blue light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proceedings of the National Academy of Sciences, USA 95, 7686–7699.
Liscum E, Hangarter RP. 1993. Genetic evidence that the Pr form of phytochrome B plays a role in Arabidopsis thaliana gravitropism. Plant Physiology 103, 15–19.[Abstract]
Lu YT, Hidaka H, Feldman LJ. 1996. Characterization of a calcium/calmodulin-dependent protein kinase homolog from maize roots showing light-regulated gravitropism. Planta 199, 18–24.[Web of Science][Medline]
Martinez-Garcia JF, Huq E, Quail PH. 2000. Direct targeting of light signals to a promoter element–bound transcription factor. Science 288, 859–863.
Más P, Devlin P, Panda S, Kay SA. 2000. Functional interaction of phytochrome B and crytochrome 2. Nature 408, 207–211.[CrossRef][Medline]
Mathews S, Sharrock RA. 1997. Phytochrome gene diversity. Plant, Cell and Environment 20, 666–671.[CrossRef]
Michaels SD, Amasino RM. 2001. Loss of FLOWERING LOCUS C activity eliminates the late-flowering time phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. The Plant Cell 13, 935–941.
Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. The Plant Cell 11, 949–956.
Monte E, Alonso JM, Ecker JR, Zhang Y, Li X, Young J, Austin-Phillips S, Quail PH. 2003. Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signalling pathways. The Plant Cell 15, 1962–1980.
Myers AB, Firn RD, Digby J. 1994. Gravitropic sign reversal: a fundamental feature of the gravitropic perception or response mechanisms in some plant organs. Journal of Experimental Botany 45, 77–83.
Nagatani A, Reed JW, Chory J. 1993. Isolation and initial characterisation of Arabidopsis mutants that are deficient in functional phytochrome A. Plant Physiology 102, 269–277.[Abstract]
Ni M, Tepperman JM, Quail PH. 1999. Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400, 781–784.[CrossRef][Medline]
Parks BM, Quail PH, Hangarter RP. 1996. Phytochrome A regulates red light induction of phototropic enhancement in Arabidopsis. Plant Physiology 110, 155–162.[Abstract]
Parks BM, Quail PH. 1993. hy8, a new class of Arabidopsis long hypocotyl mutants deficient in functional phytochrome A. The Plant Cell 3, 39–48.
Poppe C, Hangarter RP, Sharrock RA, Nagy F, Schäfer E. 1996. The light-induced reduction of the gravitropic growth-orientation of seedlings of Arabidopsis thaliana (L.) Heynh. is a photomorphogenic response mediated synergistically by the far-red absorbing forms of phytochromes A and B. Planta 119, 511–514.
Quail PH. 2002. Photosensory perception and signalling in plant cells: new paradigms? Current Opinions in Plant Biology 14, 180–188.
Reed JW, Nagatani A, Elich T, Fagan M, Chory J. 1994. Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiology 104, 1139–1149.[Abstract]
Reed JW, Nagpal P, Poole DS, Furuya M, Chory J. 1993. Mutations in the gene for red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. The Plant Cell 5, 147–157.[Abstract]
Robson PRH, Smith H. 1996. Genetic and transgenic evidence that phytochromes A and B act to modulate the gravitropic orientation of Arabidopsis thaliana hypocotyls. Plant Physiology 110, 211–216.[Abstract]
Robson PRH, Whitelam GC, Smith H. 1993. Selected components of the shade-avoidance syndrome are displayed in a normal manner in mutants of Arabidopsis thaliana and Brassica rapa deficient in phytochrome B. Plant Physiology 102, 1179–1184.[Abstract]
Rouse DT, Sheldon CC, Bagnall DJ, Peacock WJ, Dennis ES. 2002. FLC, a repressor of flowering, is regulated by genes in different inductive pathways. The Plant Journal 29, 183–191.[CrossRef][Web of Science][Medline]
Sakamoto K, Nagatani A. 1996. Nuclear localisation activity of phytochrome B. The Plant Journal 10, 859–868.[CrossRef][Web of Science][Medline]
Samach A, Coupland G. 2000. Time measurement and the control of flowering in plants. Bioessays 22, 38–47.[CrossRef][Web of Science][Medline]
Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES. 2000. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proceedings of the National Academy of Sciences, USA 97, 3753–3758.
Shinomura T, Nagatani A, Chory J, Furuya M. 1994. The induction of seed germination in Arabidopsis thaliana is regulated principally by phytochrome B and secondarily by phytochrome A. Plant Physiology 104, 363–371.[Abstract]
Shinomura T, Nagatani A, Manzawa H, KubotaM, Watanabe M, Furuya M. 1996. Action spectra for phytochrome A and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 93, 8129–8133.
Simpson GG, Dean C. 2002. Arabidopsis, the Rosetta stone of flowering time? Science 296, 285–289.
Smith H. 1982. Light quality, photoperception and plant strategy. Annual Review of Plant Physiology 33, 481–518.[Web of Science]
Smith H, Whitelam GC. 1990. Phytochrome, a family of photoreceptors with multiple physiological roles. Plant, Cell and Environment 13, 695–707.[CrossRef]
Somers DE, Sharrock RA, Tepperman JM, Quail PH. 1991. The hy3 long hypocotyl mutant of Arabidopsis is deficient in phytochrome B. The Plant Cell 3, 1263–1274.
Whitelam GC, Devlin PF. 1997. Roles for different phytochromes in Arabidopsis photomorphogenesis. Plant, Cell and Environment 20, 752–758.[CrossRef]
Whitelam GC, Johnson E, Peng J, Carol P, Anderson MC, Cowl JS, Harberd NP. 1993. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. The Plant Cell 5, 757–768.
Whitelam GC, Smith H. 1991. Retention of phytochrome-mediated shade avoidance responses in phytochrome-deficient mutants of Arabidopsis, cucumber and tomato. Journal of Plant Physiology 139, 119–125.
Yamaguchi R, Nakamura M, Mochizuki N, Kay S, Nagatani A. 1999. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus of transgenic Arabidopsis. Journal of Cell Biology 145, 437–445.
Yanovsky MJ, Casal JJ, Whitelam GC. 1995. Phytochrome A, phytochrome B and HY4 are involved in hypocotyl growth responses to natural radiation in Arabidopsis: weak de-etiolation of the phyA mutant under dense canopies. Plant, Cell and Environment 18, 788–794.[CrossRef]
Yanovsky MJ, Kay SA. 2002. Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308–312.[CrossRef][Medline]
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