Journal of Experimental Botany, Vol. 57, No. 13, pp. 3387–3393, 2006 Major Themes in Flowering Research Special Issue doi:10.1093/jxb/erl071 Advance Access publication 15 September, 2006

Light signals and flowering

Brian Thomas* Warwick HRI, University of Warwick, Wellesbourne CV35 9EF, UK

Received 14 March 2006; Accepted 31 May 2006

Abstract considered both with regard to light acting directly through photomorphogenetic mechanisms, or alterations in photo- Physiological studies over a long period have shown synthetic assimilation or as part of the more complex that light acts to regulate flowering through the three regulatory mechanisms of photoperiodism. Much of the main variables of quality, quantity, and duration. body of literature on physiological studies will be assumed Intensive molecular genetic and genomic studies with although it is worth noting that many of the revelations the model Arabidopsis have given considerable from recent molecular genetic studies were presaged by insight into the mechanisms involved, particularly careful whole plant studies. Thus, concepts of photoper- with regard to quality and photoperiod. For photo- iodic control of flowering, based on physiological studies, periodism light, acting through and envisaged an external coincidence circadian model with , the main photomorphogenetic photo- multiple photoreceptors acting in the leaf to generate receptors, acts to entrain and interact with a circadian a complex mobile flowering signal (Thomas and Vince- rhythm of CONSTANS (CO) expression leading to Prue, 1997). The explosion of knowledge and resources in transcription of the mobile floral integrator, FLOW- has resulted in much of the fine detail ERING LOCUS T (FT). The action of phytochromes beneath the model being teased out to confirm and extend and cryptochromes in photoperiodism is augmented this basic concept. For light to affect a particular biological by ZEITLUPE (ZTL) and FLAVIN-BINDING, KELCH RE- process it must be detected through the excitation of a light- PEAT, F-BOX (FKF1) acting as accessory photore- absorbing pigment (or photoreceptor) which then passes on ceptors on entrainment and interaction, respectively. the light as energy or as a signal through highly refined Light quality acts independently of the circadian regulatory pathways or networks. A consideration of light system through Phytochromes B, D, and E to regulate signalling is therefore inseparable from a consideration of FT. Light quantity effects, on the other hand, are still the roles of photoreceptors in the process of flowering. incompletely understood but are likely to be linked either directly or indirectly to patterns of assimilate partitioning and resource utilization within the plant. Light and photoperiodism Key words: Arabidopsis, , flowering, light, photo- receptors, photoperiodism . Daylength is a major regulator of flowering time and allows sexual reproduction to take place at an appropriate time or times of the year and helps ensure that flowering is co- ordinated to enable cross-pollination where this forms part Introduction of the plant’s adaptive strategy. Studies on Arabidopsis As with almost all aspects of plant development, the have enabled the framework of understanding, based on flowering behaviour of higher is modified by physiological studies over more than half a century, to be environmental signals. Light is foremost among these supported by detailed information on the cellular and environmental signals and can modify flowering in several molecular genetic processes that give rise to the occurrence different ways. This is not particularly surprising as plants of photoperiodism. It is worth remembering that Arabi- need to adapt to precise ecological niches defined both dopsis is typical of a particular photoperiodic class, namely spatially and temporally in terms of a favourable environ- a facultative cruciferous, light-dominant, long-day plant mental envelope. In this review the action of light is (LDP). This is only one of a range of patterns of response

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ª The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental ]. All rights reserved. For Permissions, please e-mail: [email protected] 3388 Thomas that plants show to daylength (Thomas and Vince-Prue, shown to contribute input to the clock (Somers et al., 1997). Resolving the relationship of the Arabidopsis model 1998b; Devlin and Kay, 2000). A suite of photoreceptors to species with contrasting physiological responses, for acting singly or together enables the clock to be entrained example, short-day plants (SDP) is an area that is currently by light at a range of wavelengths and irradiances. PHYB, being addressed by a range of research groups. As these PHYD, and PHYE are primarily responsible for mediating other species almost always lack the exquisite combination red light at high irradiances while CRY1 and CRY2 of genetic properties and resources that make Arabidopsis mediate high irradiance blue light. Perception of low such a powerful model, resolving their photoperiodic irradiance red and blue light is mediated by PHYA. Devlin mechanisms is a considerable challenge, but will almost and Kay (2000) also provided evidence that cryptochrome certainly add levels of subtlety and complexity to our may act downstream of PHYA on the input to the clock. understanding. Light affects components of the circadian oscillator at several levels. First, light promotes transcription of the LATE ELONGATED HYPOCOTYL (LHY), and CIRCA- Light and clock entrainment DIAN CLOCK-ASSOCIATED 1 (CCA1) genes in the As a starting point for examining the role of light, daylength early part of the day (Martinez-Garcia et al., 2000; Kim measurement will be taken to result from an external et al., 2003). Light also acts through through the effect of coincidence model based on a (Carre, ZEITLUPE (ZTL) to modulate the accumulation of the 2001; Yanovsky and Kay, 2002). In this model, light has TIMING OF CAB1 (TOC1) protein (Somers et al., 2000; two roles. Firstly, it acts to entrain the circadian clock and, Mas et al., 2003). ZTL containins a LOV domain which is secondly, it interacts with an output from the clock at cri- highly similar to the flavin chromophore binding site in tical phases to allow or prevent flowering. Reconciliation PHOTOTROPINS, which act as blue light photoreceptors of earlier physiological and more recent genetic models has for phototropism and other orientation responses. ZTL is been achieved through the findings that the clock acts to also an F-box protein that acts to target specific molecules, establish a rhythm of the CONSTANS (CO) gene expres- for example, TOC1 for degradation via the 26S proteasome. sion, at least partially mediated by the flowering time gene GIGANTEA (GI) (Mizoguchi et al., 2005). CO levels are Light and the clock output high towards the end of a long-day (LD) and the interac- tion with light results in the transcriptional activation of The multiple effects of light on the timing mechanism that FLOWERING LOCUS T (FT) (Kardailsky et al., 1999; act to set the phase of the photoperiodic response rhythm Samach et al., 2000; Yanovsky and Kay, 2002). The and the separate effects of light acting downstream of the regulation of FT takes place in leaves from which FT clock to mediate floral response can be distinguished. As mRNA travels to the apex to interact with FD and initiate with light input to the clock, phytochromes, cryptochromes, floral development (Huang et al., 2005; Abe et al., 2005; and potentially novel photoreceptors all appear to have Wigge et al., 2005). a role. All five phytochromes contain identical tetrapyrrole Much of the basic information on the circadian clock chromophores (Lagarias and Rapoport, 1980; Kendrick and underlying daylength measurement derives from transgenic Weller, 2004). Mutants or transgenic plants in which plants using reporters of circadian regulated photosynthetic chromophore biosynthesis is impaired, will be incapaci- genes fused to a luciferase reporter. It is assumed that tated with regard to all of the functional phytochromes. essentially the same clock elements will form the basis of Such plants show altered daylength responses, flowering the photoperiodic clock. In general, this is supported by earlier than wild types in both LDP and SDP ( Montgomery the fact that under the right conditions mutations that et al., 2001; Izawa et al., 2002; Sawers et al., 2002) alter expression of components of the circadian clock alter although, as different phytochromes may have opposing flowering time (Somers et al., 1998a; Doyle et al., 2002; actions, it is difficult to draw any real significance from this. Matsushika et al., 2002; Sato et al., 2002; Yamamoto et al., PHYA typically acts to detect light rich in far-red in de- 2003). For example, the EARLY FLOWERING 3 mutation etiolating seedlings (Whitelam et al., 1993; Weller et al., ELF3 exhibits light-dependent arrhythmia of the clock and 2001). Low irradiance treatments with far-red rich in- the gene product is thought to modulate the action of photo- candescent lamps are routinely given as photoperiod receptors on the input to the clock. Entrainment of the extension treatments in daylength experiments and found circadian clock to cycles of light and darkness involves to be highly effective, implying a potential role for PHYA the action of multiple photoreceptors. There are five mem- in daylength sensing. Supporting evidence for a role for bers of the phytochrome gene family in Arabidopsis and PHYA in promoting flowering in LDP came from the equivalent gene families in other species (Izawa et al., action spectrum for flowering in which shows a far- 2002; Kendrick and Weller, 2004). In Arabidopsis, at least red peak similar to the far-red high irradiance response in four of the five PHYTOCHROMES (PHYA, B, D, and E) dark-grown seedlings and which is mediated by PHYA and both CRYPTROCHROMES (CRY1,2) have been (Carr-Smith et al., 1989, 1994). This has been confirmed Light signals and flowering 3389 and extended by more recent genetic studies. PHYA is flavin mononucleotide and is photoactive. In addition, required for normal perception of long days in Arabidopsis FKF1’s action to regulate CO requires light and it may, and in the LDP, (Johnson et al., 1994; Neff and Chory, therefore, act as an auxiliary blue light photoreceptor 1998; Weller et al., 2001). PHYA acts principally through (Imaizumi et al., 2003). It has been recently shown that the photoperiod pathway as it has no effect on flowering FKF1 controls daily CO expression in part by degrading time under short days. Arabidopsis mutants deficient in CDF1, a repressor of CO transcription, to boost CO PHYB flower earlier than the wild type in both SD and LD, production at the critical point in the photoperiod for long but retain sensitivity to daylength (Reed et al., 1994). day sensing (Imaizumi et al., 2005). PHYB, along with PHYD and PHYE mediates early flowering in Arabidopsis in response to low red to far-red ratios (Franklin et al., 2003; Halliday et al., 2003). This Light and short-day plants response plays a role in shade avoidance and is distinct The bulk of published information on photoperiodic mech- from the role of PHYB in photoperiodism (see section on anisms is derived from Arabidopsis, a facultative LDP. Light Quality and Flowering below). By contrast, PHYB is There is accumulating evidence that elements of the LD- essential for daylength perception in since the sensing model also form part of the mechanism in SDP (Liu BMDR-1 mutant of Barley, which contains a defective et al., 2001; Searle and Coupland, 2004). Genetic analysis PHYB is insensitive to photoperiod (Hanumappa et al., has identified that in species that act as SDPs, common 1999) and similarly the PHYB mutant of pea is aphoto- components to those found in Arabidopsis are involved periodic (Weller et al., 2001). in the photoperiodic response. In , a SDP, Hd1, an Cryptochromes are flavoproteins that act as blue light orthologue of CO, and Hd3a, an orthologue of FT, are photoreceptors. The participation of cryptochromes in the required for flowering in response to short-days (Yano control of flowering in Arabidopsis is consistent with et al., 2000; Hayama et al., 2003). The relationship physiological studies that have shown that blue light has between the CO and FT orthologues is, however, reversed a promotive effect on flowering for LDP of the Cruciferae from that found in Arabidopsis. In rice Hd1 is under although this is not necessarily true for other families circadian regulation and Hd1 mRNA accumulates towards (Thomas and Vince-Prue, 1997; Runkle and Heins, 2001). the end of the day in LD. Coincidental exposure to light at Two members of the cryptochrome gene family (CRY1 and this time acts to suppress transcription of Hd3a (Hayama CRY2) are present in Arabidopsis (Lin and Shalitin, 2003). and Coupland, 2004) and consequently inhibits flower- CRY2 is thought to be the major blue photoreceptor for ing in LD. Orthologues of CO have been isolated from the flowering in Arabidopsis (Guo et al., 1998), although cry1 SDP Pharbitis nil and show diurnal regulation of ex- cry2 double mutants flowered earlier in blue light than the pression (Liu et al., 2001), consistent with a general mech- single mutants, indicating that both cryptochromes play anism for daylength regulation. a role to promote flowering (Mockler et al., 1999). CRY1 A consequence of these opposite actions of CO and and CRY 2 act along with PHYA to stabilize CO protein orthologues in different species is that mutants lacking CO synthesized towards the end of a LD treatment (Valverde default to late flowering in LDP and early flowering in SDP. et al., 2004), which provides a mechanism for an external Mutants of FT on the other hand would be expected always coincidence model of day length regulation. There is to be late flowering, irrespective of response type. If it is evidence that allelic diversity in cryptochromes contribute further assumed that FT is the mobile florigenic signal, to the natural variation in the response of Arabidopsis to this reversible relationship between CO and FT provides an daylength. A QTL for flowering time was accounted for by explanation for the observations from experiments an allele of CRY2 (El-Assal et al., 2001) indicating that the that the flowering stimulus is interchangeable between blue light photoreceptor has a significant role in daylength response types as well as between species and in some sensing under natural conditions. The early flowering cases, genera (Thomas and Vince-Prue, 1997). phenotype resulted from a single amino acid substitution that reduces the light-induced turnover of the CRY2 protein under short photoperiods. There is as yet no physiological Light quality and flowering evidence for a specific role for blue light, and by inference, cryptochromes, in SDP, but this remains to be confirmed in Plants grown under canopy shade conditions or in the genetic and comparative genomic studies. proximity of other plants show a range of responses to the A further novel photoreceptor may play an additional change in red (R) to far-red (FR) ratio of the ambient light. role in the Arabidopsis photoperiodic mechanism. A This response, known as the shade-avoidance or near FLAVIN-BINDING, KELCH REPEAT, F-BOX (FKF1) neighbour detection response is characterized by increased (Nelson et al., 2000) protein is required to generate peak the internode extension, reduced leaf area and acceleration of of CO transcription observed towards the end of a long day. flowering (Halliday et al., 1994). Many of the characteristics The mRNA is under circadian control and the protein binds of the shade avoidance response can be mimicked by a 3390 Thomas short end-of-day FR treatment, implicating light-stable Light quantity responses phytochrome as the photoregulator. PHYB is a major player While increased light levels are usually accepted as having in this response, but there is redundancy with PHYD and a positive effect on flowering, the plant response to light PHYE such that double or triple mutants show increasingly quantity for flowering is very variable. In a study of 41 extreme phenotypes (Halliday et al., 1994; Aukerman herbaceous species, 10 were found to have a facultative et al., 1997; Devlin et al., 1998, 1999). Mutants in PHYB in irradiance response while 28 were unaffected (Mattson and Arabidopsis flower earlier than WT in both LD and SD but Erwin, 2005). Interestingly, three species in this study had retain a differential response to daylength indicating a light- a negative response to increasing irradiance. In general, dependent non-photoperiodic regulatory pathway. Both light quantity responses are assumed to be linked to light-dependent pathways, photoperiodic and light quality, photosynthesis and the availability of assimilates, the act through the regulation of FT. Regulation of FT by PHYB photoreceptors in this case being chlorophylls and other occurs through the nuclear protein, PHYTOCHROME photosynthetic pigments. This idea is supported by ex- AND FLOWERING TIME 1 (PFT1) (Cerdan and Chory, periments in which a strong irradiance dependence on 2003). Another characteristic of this pathway is that the flowering in Brassica campestris could be eliminated early flowering phenotype in the absence of PHYB is tem- by supplying sucrose (Friend, 1984). Bagnall and King perature sensitive (Halliday et al., 2003). As other aspects (2001) found that flowering was delayed under low of the shade-avoidance response do not show the same irradiance in PHYA mutants, but not at higher irradiances, response to temperature, sensitivity lies in a flowering- and suggested that part of PHYA action was mediated specific branch of the PHYB signalling pathway. indirectly through photosynthesis although it is not clear PHYB acts through FT, implying that the light quality how such a mechanism might operate. pathway is leaf-based. This is supported by experiments Light quantity seems to be particularly important during with enhancer trap lines that showed suppression of FT early development, particularly with herbaceous species expression by PHYB expressed in mesophyll cells that show a clear juvenile phase (Perilleux and Bernier, (Endo et al., 2005). In pea, however, the inhibitory ef- 2002). It is proposed that the inability to flower during this fect of PHYB on flowering was found not to be graft- juvenile period is because of a foliar inability to produce transmissible, in contrast to the photoperiodic effect of floral signals and/or of the competence of the apex to PHYA (Weller et al., 1997). One difference between pea respond (Zeevaart, 1985; McDaniel, 1996; McDaniel et al., and Arabidopsis appears to be that, in pea, a transmissible 1996). The length of the juvenile phase in photoperiod- inhibitor is linked to the effect of PHYA whereas in sensitive plants can be revealed by reciprocal transfers Arabidopsis, control by events in the leaf is mediated between permissive and non-permissive daylengths. Such entirely through FT, a floral promoter. experiments with Petunia showed that the length of the

Fig. 1. Multiple actions of light affect flowering. The diagram indicates the main targets of light and the photoreceptors involved. Photoperiodic control involves the entrainment of the and interaction with the output, primarily through CO to regulate FT. Light acts directly through phytochromes in the leaf via FT. In addition, light acts indirectly through chlorophyll (Chla/b) via photosynthesis and the availability of assimilates which are translocated to the apex with FT. (Modified from Thomas B, Carre´ I, Jackson SD. 2006. Photoperiodism and flowering. In: Jordan BR, ed. The molecular biology and biotechnology of flowering, 2nd edn. CAB International, 3–25, and reproduced by kind permission of CAB International.) Light signals and flowering 3391 juvenile phase is prolonged at lower irradiances (Adams, Bernier G, Perilleux C. 2005. A physiological overview of the 1999). genetics of flowering time control. Plant Biotechnology Journal What is not clear is the precise molecular mechanisms by 3, 3–16. Carr-Smith HD, Johnson CB, Thomas B. 1989. Action spectrum which irradiance, if acting through photosynthetic assimi- for the effect of day-extensions on flowering and apex elongation lation, can modify the length of the juvenile phase. It may in green, light-grown wheat (Triticum aestivum L.). Planta 179, well be that assimilates themselves act as part of a complex 428–432. flowering signal (Perilleux and Bernier, 2002; Bernier and Carr-Smith HD, Johnson CB, Plumpton C, Butcher GW, Perilleux, 2005) or it may be that the delivery of the mobile Thomas B. 1994. The kinetics of Type-1 phytochrome in green, light-grown wheat (Triticum aestivum L.). Planta 194, flowering signals such as FT is dependent upon a sufficient 136–142. mass flow of assimilates. One factor inhibiting a resolution Carre IA. 2001. Day-length perception and the photoperiodic of this issue is that the juvenile phase is very short in regulation of flowering in Arabidopsis. Journal of Biological Arabidopsis and experimental separation of source–sink Rhythms 16, 415–423. relationships in very young seedlings is difficult to achieve Cerdan PD, Chory J. 2003. Regulation of flowering time by light in a manner that is comparable to the extended juvenile quality. Nature 423, 881–885. Devlin PF, Kay SA. 2000. Cryptochromes are required for phase of many herbaceous species. phytochrome signaling to the circadian clock but not for rhythmicity. The Plant Cell 12, 2499–2509. Devlin PF, Patel SR, Whitelam GC. 1998. Phytochrome E Conclusions influences internode elongation and flowering time in Arabidopsis. The Plant Cell 10, 1479–1487. Physiological studies over a long period have shown that Devlin PF, Robson PRH, Patel SR, Goosey L, Sharrock RA, light acts to regulate flowering through the three main Whitelam GC. 1999. Phytochrome D acts in the shade-avoidance variables of quality, quantity, and duration (Fig. 1). syndrome in Arabidopsis by controlling elongation growth and Intensive molecular genetic and genomic studies with the flowering time. Plant 119, 909–915. model plant Arabidopsis have given considerable insight Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma- Bognar L, Nagy F, Millar AJ, Amasino RM. 2002. The ELF4 into the mechanisms involved, particularly with regard gene controls circadian rhythms and flowering time in Arabidopsis to quality and duration. The Arabidopsis model is now thaliana. Nature 419, 74–77. being extended to other plants, including crops and dif- El-Assal SED, Alonso-Blanco C, Peeters AJM, Raz V, ferent response types and a range of variations can be Koornneef M. 2001. A QTL for flowering time in Arabidopsis expected to emerge as more studies are undertaken. Light reveals a novel allele of CRY2. Nature Genetics 29, 435–440. quantity effects, on the other hand, are still incompletely Endo M, Nakamura S, Araki T, Mochizuki N, Nagatani A. 2005. Phytochrome B in the mesophyll delays flowering by suppressing understood but are likely to be linked either directly or FLOWERING LOCUS T expression in Arabidopsis vascular indirectly to patterns of assimilate partitioning and resource bundles. The Plant Cell 17, 1941–1952. utilization within the plant. Franklin KA, Praekelt U, Stoddart WM, Billingham OE, Halliday KJ, Whitelam GC. 2003. Phytochromes B, D, and E act redundantly to control multiple physiological responses in Acknowledgements Arabidopsis. 131, 1340–1346. Friend DJC. 1984. The interaction of photosynthesis and photo- The author would like to acknowledge support from the Department periodism in induction. In: Vince-Prue D, Thomas B, Cockshull for Environment, Food and Rural Affairs (Defra) in preparing this E, eds. Light and the flowering process. London: Academic review. Press. Guo HW, Yang WY, Mockler TC, Lin CT. 1998. Regulations of flowering time by Arabidopsis photoreceptors. Science 279, References 1360–1363. Halliday KJ, Koornneef M, Whitelam GC. 1994. Phytochrome B Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, and at least one other phytochrome mediate the accelerated Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T. 2005. flowering response of Arabidopsis thaliana L to low red/far-red FD, a bZIP protein mediating signals from the floral pathway ratio. Plant Physiology 104, 1311–1315. integrator FT at the shoot apex. Science 309, 1052–1056. Halliday KJ, Salter MG, Thingnaes E, Whitelam GC. 2003. Adams SR. 1999. The effects of temperature and light integral on the Phytochrome control of flowering is temperature sensitive and phases of photoperiod sensitivity in Petunia3hybrida. Annals of correlates with expression of the floral integrator FT. The Plant Botany 83, 263–269. Journal 33, 875–885. Aukerman MJ, Hirschfeld M, Wester L, Weaver M, Clack T, Hanumappa M, Pratt LH, Cordonnier-Pratt MM, Deitzer GF. Amasino RM, Sharrock RA. 1997. A deletion in the PHYD gene 1999. A photoperiod-insensitive barley line contains a light-labile of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome B. Plant Physiology 119, 1033–1039. phytochrome D in red/far-red light sensing. The Plant Cell 9, Hayama R, Coupland G. 2004. The molecular basis of diversity in 1317–1326. the photoperiodic flowering responses of Arabidopsis and rice. Bagnall DJ, King RW. 2001. Phytochrome, photosynthesis and Plant Physiology 135, 677–684. flowering of Arabidopsis thaliana: photophysiological studies Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K. 2003. using mutants and transgenic lines. Australian Journal of Plant Adaptation of photoperiodic control pathways produces short-day Physiology 28, 401–408. flowering in rice. Nature 422, 719–722. 3392 Thomas Huang T, Bohlenius H, Eriksson S, Parcy F, Nilsson O. 2005. The induced phytochrome chromophore deficiency in transgenic mRNA of the Arabidopsis gene FT moves from leaf to shoot apex tobacco. Plant Physiology 125, 266–277. and induces flowering. Science 309, 1694–1696. Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B. 2000. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA. 2003. FKF1, a clock-controlled gene that regulates the transition to FKF1 is essential for photoperiodic-specific light signalling in flowering in Arabidopsis. Cell 101, 331–340. Arabidopsis. Nature 426, 302–306. Neff MM, Chory J. 1998. Genetic interactions between phyto- Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA. 2005. chrome A, phytochrome B, and cryptochrome 1 during FKF1F-BOX protein mediates cyclic degradation of a repressor of Arabidopsis development. Plant Physiology 118, 27–36. CONSTANS in Arabidopsis. Science 309, 293–297. Perilleux C, Bernier G. 2002. The control of flowering: do genetical Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, and physiological approaches converge. In: O’Neill SD, Roberts Shimamoto K. 2002. Phytochrome mediates the external light JA, eds. Plant reproduction, Annual Plant Reviews, Vol. 6. signal to repress FT orthologs in photoperiodic flowering of rice. Sheffield: Academic Press, 1–32. Genes and Development 16, 2006–2020. Reed JW, Nagatani A, Elich TD, Fagan M, Chory J. 1994. Johnson E, Bradley M, Harberd NP, Whitelam GC. 1994. Phytochrome A and phytochrome B have overlapping but distinct Photoresponses of light-grown phya mutants of Arabidopsis: functions in Arabidopsis development. Plant Physiology 104, phytochrome A is required for the perception of daylength 1139–1149. extensions. Plant Physiology 105, 141–149. Runkle ES, Heins RD. 2001. Specific functions of red, far red, and Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, blue light in flowering and stem extension of long-day plants. Nguyen JT, Chory J, Harrison MJ, Weigel D. 1999. Activation Journal of the American Society for Horticultural Science 126, tagging of the floral inducer FT. Science 286, 1962–1965. 275–282. Kendrick RE, Weller JL. 2004. Phytochromes and other Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, photoreceptors. In: Thomas B, Murphy DJ, Murray BG, eds. Yanofsky MF, Coupland G. 2000. Distinct roles of CONSTANS Encyclopedia of applied plant sciences. Oxford: Elsevier, target genes in reproductive development of Arabidopsis. Science 1063–1069. 288, 1613–1616. Kim JY, Song HR, Taylor BL, Carre IA. 2003. Light-regulated Sato E, Nakamichi N, Yamashino T, Mizuno T. 2002. Aberrant translation mediates gated induction of the Arabidopsis clock expression of the Arabidopsis circadian-regulated APRR5 gene protein LHY. EMBO Journal 22, 935–944. belonging to the APRR1/TOC1 quintet results in early flower- Lagarias JC, Rapoport H. 1980. Chromopeptides from phyto- ing and hypersensitiveness to light in early . chrome. The structure and linkage of the Pr form of the Plant and Cell Physiology 43, 1374–1385. phytochrome chromophore. Journal of the Americal Chemistry Sawers RJH, Linley PJ, Farmer PR, Hanley NP, Costich DE, Society 102, 4821–4828. Terry MJ, Brutnell TP. 2002. elongated mesocotyl1, a phyto- Lin CT, Shalitin D. 2003. Cryptochrome structure and signal chrome-deficient mutant of . Plant Physiology 130, transduction. Annual Review of Plant Biology 54, 469–496. 155–163. Liu JY, Yu JP, McIntosh L, Kende H, Zeevaart JAD. 2001. Searle I, Coupland G. 2004. Induction of flowering by seasonal Isolation of a CONSTANS ortholog from Pharbitis nil and its role changes in photoperiod. EMBO Journal 23, 1217–1222. in flowering. Plant Physiology 125, 1821–1830. Somers DE, Webb AAR, Pearson M, Kay SA. 1998a. The McDaniel CN. 1996. Developmental physiology of floral initiation short-period mutant, toc1-1, alters circadian clock regulation of in Nicotiana tabacum L. Journal of Experimental Botany 47, multiple outputs throughout development in Arabidopsis thaliana. 465–475. Development 125, 485–494. McDaniel CN, Hartnett LK, Sangrey KA. 1996. Regulation of Somers DE, Devlin PF, Kay SA. 1998b. Phytochromes and node number in day-neutral Nicotiana tabacum: a factor in plant cryptochromes in the entrainment of the Arabidopsis circadian size. The Plant Journal 9, 55–61. clock. Science 282, 1488–1490. Martinez-Garcia JF, Huq E, Quail PH. 2000. Direct targeting of Somers DE, Schultz TF, Milnamow M, Kay SA. 2000. ZEITLUPE light signals to a promoter element-bound transcription factor. encodes a novel clock-associated PAS protein from Arabidopsis. Science 288, 859–863. Cell 101, 319–329. Mas P, Kim WY, Somers DE, Kay SA. 2003. Targeted degradation Thomas B, Vince-Prue D. 1997. Photoperiodism in plants. London: of TOC1 by ZTL modulates circadian function in Arabidopsis Academic Press. thaliana. Nature 426, 567–570. Thomas B, Carre´ I, Jackson SD. 2006. Photoperiodism and Matsushika A, Imamura A, Yamashino T, Mizuno T. 2002. flowering. In: Jordan BR, ed. The molecular biology and bio- Aberrant expression of the light-inducible and circadian-regulated technology of flowering, 2nd edn. CAB International, 3–25. APRR9 gene belonging to the circadian-associated APRR1/TOC1 Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, quintet results in the phenotype of early flowering in Arabidopsis Coupland G. 2004. Photoreceptor regulation of CONSTANS thaliana. Plant and Cell Physiology 43, 833–843. protein in photoperiodic flowering. Science 303, 1003–1006. Mattson NS, Erwin JE. 2005. The impact of photoperiod and Weller JL, Murfet IC, Reid JB. 1997. Pea mutants with reduced irradiance on flowering of several herbaceous ornamentals. sensitivity to far-red light define an important role for phytochrome Scientia Horticulturae 104, 275–292. A in day-length detection. Plant Physiology 115, 1291–1291. Mizoguchi T, Wright L, Fujiwara S, et al. 2005. Distinct roles of Weller JL, Beauchamp N, Kerckhoffs LHJ, Platten JD, Reid JB. GIGANTEA in promoting flowering and regulating circadian 2001. Interaction of phytochromes A and B in the control of de- rhythms in Arabidopsis. The Plant Cell 17, 2255–2270. etiolation and flowering in pea. The Plant Journal 26, 283–294. Mockler TC, Guo HW, Yang HY, Duong H, Lin CT. 1999. Whitelam GC, Johnson E, Peng JR, Carol P, Anderson ML, Antagonistic actions of Arabidopsis cryptochromes and phyto- Cowl JS, Harberd NP. 1993. Phytochrome A null mutants of chrome B in the regulation of floral induction. Development 126, Arabidopsis display a wild-type phenotype in white-light. The 2073–2082. Plant Cell 5, 757–768. Montgomery BL, Franklin KA, Terry MJ, Thomas B, Jackson Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann SD, Crepeau MW, Lagarias JC. 2001. Biliverdin reductase- JU, Weigel D. 2005. Integration of spatial and temporal Light signals and flowering 3393 information during floral induction in Arabidopsis. Science 309, Yano M, Katayose Y, Ashikari M, et al. 2000. Hd1, a major 1056–1059. photoperiod sensitivity quantitative trait locus in rice, is closely Yamamoto Y, Sato E, Shimizu T, Nakamich N, Sato S, Kato T, related to the Arabidopsis flowering time gene CONSTANS. Tabata S, Nagatani A, Yamashino T, Mizuno T. 2003. The Plant Cell 12, 2473–2483. Comparative genetic studies on the APRR5 and APRR7 genes Yanovsky MJ, Kay SA. 2002. Molecular basis of seasonal time belonging to the APRR1/TOC1 quintet implicated in circadian measurement in Arabidopsis. Nature 419, 308–312. rhythm, control of flowering time, and early photomorphogenesis. Zeevaart JAD. 1985. Bryophyllum. In: Halevy AH, ed. Handbook Plant and Cell Physiology 44, 1119–1130. of flowering. Boca Raton: CRC Press Inc, 89–100.