PerspectivePlant Science

The Right Time and Place for Making Flowers

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Science  12 Aug 2005:
Vol. 309, Issue 5737, pp. 1024-1025
DOI: 10.1126/science.1117203

Reproductive success in plants depends on the synchronization of flowering [HN1] within a given species. Many plants have developed a highly complex signaling network that monitors environmental conditions, such as day length, temperature, or nutrient availability, and determines the appropriate timing for flowering (1, 2). This is the case for the model plant Arabidopsis thaliana [HN2] and the pea that both flower in spring when day length and ambient temperature increase, or certain rice varieties and soybean that flower early in the fall when days get shorter. The initiation of flowering requires an additional developmental program to specify the floral identity of the new structures that continuously arise at the shoot apex (3). For instance, during the long vegetative phase in Arabidopsis, every primordium [HN3], the groups of cells poised to differentiate, forms a leaf. However, once the decision to flower has been made, all newly emerging primordia follow a developmental program that culminates in the formation of flowers rather than leaves. Thus, constructing a flower requires both temporal and spatial information that restricts the initiation of flowering to specific locations. But how this information is integrated has not been clear. Three studies now reveal the molecular mechanism by which this integration is achieved. In this issue, Abe et al. [HN4] on page 1052 (4) and Wigge et al. [HN5] on page 1056 (5) report that interaction between Flowering Locus T (FT) [HN6], a protein encoded by a gene that is expressed in leaves, and FD, a bZIP transcription factor [HN7] that is present only in the shoot apex, triggers the expression of floral identity genes in the new primordia. The third paper by Huang et al. [HN8] in this week's Science Express (6) reports how the two factors meet—FT transcript travels from leaf to shoot via the plant vascular tissue.

It has been known for at least 50 years that flowering is triggered at the shoot apex through a mobile signal, or “florigen,” [HN9] that is generated in leaves in response to conditions that promote the production of flowers. In a classic experiment, the leaves of florally induced Perilla crispa [HN10] plants promoted flowering when grafted onto control plants (7). In Arabidopsis, perception of day length in the leaves operates through a transcription factor encoded by CONSTANS (CO) [HN11], a gene whose expression oscillates in a circadian manner, peaking at around dusk (see the figure). During the short days of winter, CO accumulates in leaves after sunset. But prolonged days in the spring allow the protein to accumulate in the presence of light, the stimulus that activates CO (8). Overexpression of CO causes early flowering, and among the target genes directly activated by CO, two seem to be most relevant for floral induction: FT and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1. Interestingly, CO acts in the phloem, the vascular tissue of plants, to activate FT expression in leaves in a cell-autonomous manner. This is based on the observation that CO activates FT expression and promotes flowering only when expressed under the control of phloem-specific promoters in the leaf, but not apex-specific promoters in the shoot (9, 10). These results suggest that the activity of CO is central for the generation of the mobile signal that originates in the leaf but has to be perceived in the apex to establish flowering. The up-regulation of FT expression by CO is required because loss of FT function prevents early flowering caused by overexpression of CO, whereas increasing FT expression causes premature flowering (11, 12). Thus, an important question has been how FT produced in the leaves would activate the transcription of floral identity genes, such as APETALA1 (AP1) [HN12], at the shoot apex.

Integration of signals to generate a flower.

Appropriate day length allows the accumulation of the transcription factor CO that controls expression of FT in the leaf. (Inset) FT transcript moves through the phloem to the shoot apex where the FT protein is produced and interacts with the transcription factor FD. The complex then activates key genes such as AP1 to start flower development. LEAFY (LFY) is a transcription factor required for AP1 expression in wild-type plants. LFY expression is up-regulated by FT in the shoot apex.

To solve the spatial paradox of FT action, Abe et al. and Wigge et al. analyzed a gene encoding a new bZIP transcription factor, FD, that is expressed preferentially at the shoot apex in the region where new primordia are being generated (4, 5). Multiple lines of evidence in these studies suggest a model by which FD provides the spatial framework for timely activation of flowering by FT. First, FD is required by FT to promote flowering because mutations in the FD gene delayed both up-regulation of AP1 expression and the early flowering phenotype caused by FT overexpression. Second, although FD is not as efficient as FT in promoting early flowering when either one is overexpressed, there was synergistic interaction between them in plants that overexpress both factors. And third, FT and FD proteins interact physically, as shown in yeast by two-hybrid assays and as seen in plants by fluorescence microscopy.

How relevant is the interaction between FT and FD for the regulation of flowering? FT has no known DNA binding domain. However, constitutive expression of a fusion protein containing FT and the glucocorticoid receptor accelerated flowering in the presence of dexamethasone [HN13], a synthetic steroid that activates the glucocorticoid receptor and allows translocation of the fusion protein into the nucleus (4). Furthermore, a key experiment strongly suggests that FD and FT act together to activate downstream targets: Ectopic expression of FD caused up-regulation of AP1 expression in leaves only when they were subjected to treatments that increase FT expression, such as transfer of plants from short- to long-day conditions (5).

The finding that FT and FD act together to activate reproductive development in plants fills a gap in our understanding of how temporal information and spatial constraints are integrated, but several questions remain. For instance, it is intriguing how AP1 expression is established precisely in floral primordia, given that FD is more widely expressed in the shoot apex. As proposed by Abe et al., other proteins must restrict AP1 expression to the correct location, and in this context, it is worth mentioning that TERMINAL FLOWER 1 [HN14], a protein with strong sequence similarity to FT, is a well-known regulator of AP1 expression that prevents AP1 from invading the central part of the shoot apex (13).

The model presented by Abe et al. and Wigge et al. implies that FT itself might be an important component of the elusive mobile signal that induces flowering, because FT is expressed in a plant tissue different from the cells in which its direct interaction with FD is needed. The study by Huang et al. (6) answers this question, showing that the transcript of FT moves from the leaf to the shoot apex. By locally inducing FT expression in a single Arabidposis leaf, the authors demonstrate that a pulse of FT expression in the leaf results in transport of the FT transcript to the shoot apex, and is sufficient to trigger flowering. Indeed, long-distance movement of RNAs through the phloem has been well documented in plants (14), but it remains to be determined if specific proteins are invloved in the transport of FT transcripts through the phloem. In a more complicated scenario, FT presence in the apex might also be the result of the activity of a different FT-induced signal moving through the phloem or from cell to cell. Movement of transcription factors through plasmodesmata, junctions that allow direct communication between the cytoplasm of adjacent plant cells, has also been described (15). It remains to be determined if specific proteins are involved in the transport of FT transcripts through the phloem. Although the composition of the florigenic signal is very likely complex (16), it seems that our understanding of this phenomenon is coming full circle.

HyperNotes Related Resources on the World Wide Web

General Hypernotes

Dictionaries and Glossaries

The BioTech Life Science Dictionary is provided by the Ellington Lab, University of Texas.

A biology dictionary is provided by Biology Online.

A glossary is provided by the Virtual Plant Web site.

A Glossary of Botanical Terms is provided by GardenWeb.

A botany glossary with illustrations is provided by F. Muth, Biology Department, Pacific Union College, Angwin, CA.

Web Collections, References, and Resource Lists

Academic Info provides links to Internet resources on botany and plant biology.

The Google Directory offers links to Internet resources in plant molecular biology and plant physiology.

Biology Web Site References for Teachers and Students includes a section of Internet resources on plant anatomy and physiology.

The Plant Link Library is provided by the Department of Plant Sciences, Wageningen University, Netherlands.

The American Society of Plant Biologists provides a collection of Internet resource links.

Lehle Seeds provides links to Internet resources on Arabidopsis.

The Arabidopsis Information Resource (TAIR) is a comprehensive resource for the scientific community working with Arabidopsis thaliana.

Online Texts and Lecture Notes

J. Kimball maintains Kimball's Biology Pages, an online biology textbook and glossary.

Online Resources in General Plant Biology are presentations for a course made available by the Department of Horticulture and Crop Science, Ohio State University.

Plant Physiology Online is the companion Web site for the third edition of Plant Physiology by L. Taiz and E. Zeiger.

Botany online is an Internet hypertextbook by P. von Sengbusch, Faculty of Biology, University of Hamburg, who also maintains the Internet Library, a resource for teaching botany and related topics.

A tutorial on angiosperm anatomy is provided by the Internet Biology Education Project, University of the Western Cape, Bellville, South Africa.

A Plant Physiology Information Site is provided by R. Konig, Biology Department, Eastern Connecticut State University, Willimantic, CT.

F. Muth, Biology Department, Pacific Union College, Angwin, CA, provides lecture notes for a botany course.

J. Haseloff, Department of Plant Sciences, University of Cambridge, offers lecture notes, readings, and other resources for plant science courses.

The Department of Botany, University of Toronto, makes available lecture notes by N. Dengler for a course on plant development.

S. G. Saupe, Biology Department, College of St. Benedict-St. John's University, Collegeville, MN, provides lecture notes for a plant physiology course.

P. Becraft, Department of Agronomy, Iowa State University, makes available lecture notes for a course on plant growth and development.

B. Fristensky, Department of Plant Science, University of Manitoba, Canada, provides lecture notes for a course on plant molecular genetics.

P. E. McClean, Department of Plant Sciences, North Dakota State University, offers lecture notes for a course on plant molecular genetics.

General Reports and Articles

The 12 April 2002 issue of Science had a Review by G. G. Simpson and C. Dean titled “Arabidopsis, the Rosetta Stone of flowering time?” (2).

The 15 December 2000 issue of Science had a special section on Arabidopsis.

S. A. Kay, Department of Cell Biology, Scripps Research Institute, makes available in PDF format an April 2003 review article by M. J. Yanovsky and S. A. Kay titled “Living by the calendar: How plants know when to flower” (1) and other publications.

The June 2003 issue of Plant Physiology had an article by M. E. Eriksson and A. J. Millar titled “The circadian clock. A plant's best friend in a spinning world.”

The October 1993 issue of the Plant Cell was a special review issue on plant reproduction with a section on flower development that included an article (PDF format) by G. Bernier et al. titled “Physiological signals that induce flowering” (16). The June 2004 issue had a supplement on plant reproduction with a section on flower development.

The 2 June 2000 issue of Science had a Perspective by P. F. Devlin and S. A. Kay titled “Flower arranging in Arabidopsis” about a Research Article by A. Somach et al. titled “Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis” and a 30 April 2000 Nature article by M. A. Blázquez and D. Weigel titled “Integration of floral inductive signals in Arabidopsis.”

Numbered Hypernotes

1. Flowering. Kimball's Biology Pages includes a presentation on flowering. P. von Sengbusch's Botany online includes a section on the features of flowering plants. D. T. Webb, Department of Botany, University of Hawaii, Manoa, provides an overview of flowers for a plant anatomy course. Plant Physiology Online offers a presentation on the control of flowering. P. E. McClean offers a presentation on genes controlling flower development for a course on plant molecular genetics. S. G. Saupe provides lecture notes on flowering for a plant physiology course. B. Fristensky provides lecture notes on flowering for a course on plant molecular genetics. The June 2004 supplement of the Plant Cell had an article by T. Jack titled “Molecular and genetic mechanisms of floral control” and an article by P. K. Boss, R. M. Bastow, J. S. Mylne, and C. Dean titled “Multiple pathways in the decision to flower: Enabling, promoting, and resetting.” The December 2001 issue of EMBO Reports had a meeting report by M. Bl·zquez, M. Koornneef, and J. Putterill titled “Flowering on time: Genes that regulate the floral transition.” The Flowering WWWeb summarizes information on labs from all over the world that work on flowering time.

2. Model plant Arabidopsis thaliana. Kimball's Biology Pages provide an introduction to Arabidopsis thaliana. Wikipedia has articles on Arabidopsis and Arabidopsis thaliana. TAIR provides an introduction to Arabidopsis thaliana. The Arabidopsis Book of the American Society of Plant Biologists is made available on the Web by BioOne. The Yanofsky Lab, Division of Biological Sciences, University of California, San Diego, offers a presentation about flower development in Arabidopsis. The Wiegal World Web site offers a picture gallery of Arabidopsis plants.

3. Primordium is defined in G. Muth's glossary; a diagram of a leaf primordium is provided. The glossary of the Plant Anatomy Web site provided by A. Roberts, Department of Biological Sciences, University of Rhode Island, includes definitions of types of primordia.

4. Mitsutoma Abe, Sumiko Yamamoto, Yasufumi Daimon, Ayako Yamaguchi, Yoko Ikeda, Harutaka Ichinoki, Michitaka Notaguchi, and Takashi Araki are in the Laboratory of Plant Developmental Genetics, Kyoto University, Japan. Yasushi Kobayashi is in the Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany. Koji Goto is at the Research Institute for Biological Sciences, Okayama, Japan, and at the Japan Science and Technology Agency.

5. Philip A. Wigge and Katja E. Jaeger are in the Department of Cell and Developmental Biology, John Innes Centre, Norwich, UK. Min Chul Kim, Wolfgang Busch, Jan U. Lohmann, and Detlef Weigel are at the Max Planck Institute for Developmental Biology, Tübingen, Germany.

6. Flowering Locus T (FT). TAIR has an entry for Flowering Locus T (FT). Swiss-Prot has an entry for Flowering Locus T. The 3 December 1999 issue of Science had a Report by Y. Kobayashi, H. Kaya, K. Goto, M. Iwabuchi, and T. Araki titled “A pair of related genes with antagonistic roles in mediating flowering signals” (11) and a Report by I. Kardailsky et al. titled “Activation tagging of the floral inducer FT” (12).

7. bZIP transcription factor. An entry for bZIP transcription factor is included in InterPro. PROSITE offers information on the bZIP superfamily. The Database of Arabidopsis Transcription Factors provides an introduction to the bZIP family. TAIR has an entry for the bZIP transcription factor gene family.

8. Tao Huang, Henrick Böhlenius, Sven Eriksson, and Ove Nilsson are at the Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå. François Parcy is at the Laboratoire de Physiologie Cellulaire Végétale, UMR CEA CNRS 5168, Grenoble, France.

9. Florigen. Botany online has a section on florigen. Plant Physiology Online makes available an essay by S. Hoffmann-Benning and J. A. D. Zeevaart titled “Searching for florigen” and an essay by B. G. Ayre and R. Turgeon titled “Florigen and a genetic approach to long-distance signaling through the phloem.”

10. Perilla. An entry for Perilla frutescens (L.) Britt. var. crispa is included in the USDA Plants Database. A fact sheet on Perilla is provided by the Center for New Crops and Plant Products, Purdue University; a 1993 proceedings paper by D. M. Brenner titled “Perilla: Botany, uses and genetic resources” is also available. PubMed Central makes available a April 1973 Plant Physiology article by R. W. King and J. A. D. Zeevaart titled “Floral stimulus movement in Perilla and flower inhibition caused by noninduced leaves.” The June 1976 issue of the Annual Review of Plant Physiology had a review by J. A. D. Zeevaart titled “Physiology of flower formation” (7) that described the classic experiment.

11. CONSTANS gene in Arabidopsis. TAIR has an entry for CONSTANS (CO). Swiss-Prot has an entry for the Arabidopsis protein CONSTANS. The 13 February 2004 issue of Science had a Report by F. Valverde, A. Mouradov, W. Soppe, D. Ravenscroft, A. Samach, and G. Coupland titled “Photoreceptor regulation of CONSTANS protein in photoperiodic flowering” (8) and a related Perspective by J. Klejnot and C. Lin titled “A CONSTANS experience brought to light.” The Max Planck Society issued a 12 February 2004 press release about this research titled “Molecular mechanisms that trigger flowering in spring.” G. Coupland, Max Planck Institute for Plant Breeding Research, offers a research presentation on CO and the control of flowering time. The 1 August 2004 issue of Development had an article by H. An et al. titled “CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis” (9). The August 2004 issue of Plant Physiology had an article by B. G. Ayre and R. Turgeon titled “Graft transmission of a floral stimulant derived from CONSTANS” (10). The Cornell Chronicle makes available an 21 October 2004 article by S. N. Davidson about this research titled “Biologists close in on ‘florigen,’ the signal that causes plants to flower.”

12. APETALA1. TAIR has an entry for APETALA 1 (AP1). The Yanofsky Lab offers a presentation about APETALA1. The 23 July 1999 issue of Science had a Report by D. Wagner, R. W. M. Sablowski, and E. M. Meyerowitz titled “Transcriptional activation of APETALA1 by LEAFY.” The June 1999 issue of the Plant Cell had an article by S. J. Liljegren et al. titled “Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate.”

13. Information about dexamethasone is provided by RxList. Wikipedia has an entry on dexamethasone.

14. TERMINAL FLOWER 1. TAIR has an entry for TERMINAL FLOWER 1. Swiss-Prot has an entry for TERMINAL FLOWER 1 protein. The 15 March 1999 issue of Development had an article by O. J. Ratcliffe, D. J. Bradley, and E. S. Coen titled “Separation of shoot and floral identity in Arabidopsis” (13).

15. Miguel A. Blázquez is at the Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia, Spain.


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