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Flowers Into Shoots: Photo and Hormonal Control of a Meristem Identity Switch in Arabidopsis (Gibberellins͞phytochrome͞floral Reversion)

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Flowers Into Shoots: Photo and Hormonal Control of a Meristem Identity Switch in Arabidopsis (Gibberellins͞phytochrome͞floral Reversion) Proc. Natl. Acad. Sci. USA Vol. 93, pp. 13831–13836, November 1996 Developmental Biology Flowers into shoots: Photo and hormonal control of a meristem identity switch in Arabidopsis (gibberellinsyphytochromeyfloral reversion) JACK K. OKAMURO*, BART G. W. DEN BOER†,CYNTHIA LOTYS-PRASS,WAYNE SZETO, AND K. DIANE JOFUKU Department of Biology, University of California, Santa Cruz, CA 95064 Communicated by Bernard O. Phinney, University of California, Los Angeles, CA, September 10, 1996 (received for review February 1, 1996) ABSTRACT Little is known about the signals that govern MOUS (AG) (3, 15, 17, 21–23). The LFY gene encodes a novel the network of meristem and organ identity genes that control polypeptide that is reported to have DNA binding activity in flower development. In Arabidopsis, we can induce a hetero- vitro (20). AG encodes a protein that belongs to the evolu- chronic switch from flower to shoot development, a process tionarily conserved MADS domain family of eukaryotic tran- known as floral meristem reversion, by manipulating photo- scription factors (24, 25). However, little is known about how period in the floral homeotic mutant agamous and in plants these proteins govern meristem identity at the cellular and heterozygous for the meristem identity gene leafy. The trans- molecular levels. Previous studies suggest that the mainte- formation from flower to shoot meristem is suppressed by hy1, nance of flower meristem identity in lfy and in ag mutants is a mutation blocking phytochrome activity, by spindly, a mu- controlled by photoperiod and by one class of plant growth tation that activates basal gibberellin signal transduction in regulators, the gibberellins (12, 15, 21). Under short day (SD) a hormone independent manner, or by the exogenous appli- photoperiod heterozygous lfy-6 and homozygous ag-1 flowers cation of gibberellins. We propose that LFY and AG play an display a heterochronic transformation from flower to inflo- important role in the maintenance of flower meristem identity rescence shoot meristem—a novel developmental switch and that floral meristem reversion in heterozygous lfy and in called floral meristem reversion (21). We have used the floral ag flowers is regulated by a phytochrome and gibberellin meristem reversion process to begin exploring the photo and signal transduction cascade. hormonal control of flower meristem identity in Arabidopsis. Plant growth and morphogenesis is controlled by meristems, organized tissues containing pluripotent stem cells whose MATERIALS AND METHODS identities and activities are regulated by intrinsic and environ- Plant Material. Landsberg-erecta (L-er) was used as wild- mental signals. In Arabidopsis, the shoot apical meristem type flower control. ag-1 (L-er) and hy1-1 (L-er) were provided undergoes two phases, vegetative and inflorescence; both by Maarten Koornneef (Wageningen Agricultural University, phases are characterized by reiterative and indeterminate Wageningen, The Netherlands). lfy-6 (L-er) was provided by patterns of growth and organogenesis (1). The vegetative Detlef Weigel (Salk Institute, La Jolla, CA). The lfy-6 allele is meristem produces a compact rosette consisting of a short stem a well-characterized null mutant (14, 16). spy-2 and spy-3 (Col) and a variable number of leaves. By contrast, the inflorescence (26) were provided by Neil Olszewski (University of Minne- meristem produces an elongated stem punctuated by narrow sota, Minneapolis). cauline leaves, lateral secondary shoots, and flowers that are Plant Growth Conditions. Plants were grown under a mix- derived from the flanks of the inflorescence meristem. Al- ture of cool white fluorescent (Sylvania CWyVHO) and though closely related spatially and by cell lineage to the incandescent lights (Phillips) in a Conviron E15 chamber inflorescence meristem, the floral meristem proceeds along a (Controlled Environments, Asheville, NC) in a 1:1:1 mixture determinate developmental pathway producing four compact containing vermiculiteyperliteypeat moss. Long day (LD) whorls of organs (four sepals, four petals, six stamens, and two growth conditions consist of 16 h light, 150–180 mmolzm22zs21, carpels). At the completion of organogenesis, the floral mer- and 8 h darkness. SD conditions were 9 h light, 150–180 istem is thought to be depleted or its activity is suppressed (2, mmolzm22zs21, and 15 h darkness. SD double incident light 3). The transition from vegetative to inflorescence shoot [SD(D)] conditions consist of 9 h light, 300 mmolzm22zs21. meristem is controlled by environmental signals including Plants were watered with a 1y4 strength Peter’s solution photoperiod and temperature (4–6), by intrinsic growth reg- (Grace-Sierra, Milpitas, CA). For night-break experiments, ulators such as the gibberellins (6–8), and by a system of red light was produced by using Sylvania cool white fluorescent flowering time genes (9). The inflorescence meristem in turn lamps wrapped in a Lee HT026 filter (Lee Colortran, Burbank, produces an indeterminate number of floral meristems. Ge- CA). The transmission of light at wavelengths less than 580 nm netic and molecular studies have shown that the establishment was less than 0.5%. For gibberellin spray experiments, exog- of floral meristem identity is governed by a network of genes enous application of gibberellin A (GA ) (Sigma) and gib- including APETALA1 (AP1), APETALA2 (AP2), CAULI- 3 3 berellin A (GA ) was performed as described by Wilson FLOWER (CAL), CLAVATA1 (CLV1), CLAVATA3 (CLV3), 417 417 et al. (8). GA was kindly provided by Phil Grau (Abbott and LEAFY (LFY) (3, 10–18), and several models have been 417 proposed to explain how these genes function together (17, 19, Laboratories). Analysis of Floral Reversion. 20). By comparison, much less is known about the signals and Plants segregating for lfy-6 and genes required for the maintenance of flower meristem iden- ag-1 were grown under SD(D) light conditions as described tity. previously and were scored for the presence of ectopic shoots Recently several genes have been implicated in the main- tenance of flower meristem identity including LFY and AGA- Abbreviations: GA3, gibberellin A3;GA417, gibberellin A417; LD, long day; SD, short day; [SD(D)], SD double incident light. *To whom reprint requests should be addressed. The publication costs of this article were defrayed in part by page charge †Present address: Institut de Ge´ne´tique et de Biologie Mole´culaireet payment. This article must therefore be hereby marked ‘‘advertisement’’ in Cellulaire, BP 163, Centre Universitaire de Strasbourg Illkirsch accordance with 18 U.S.C. §1734 solely to indicate this fact. Cedex, France. 13831 Downloaded by guest on September 29, 2021 13832 Developmental Biology: Okamuro et al. Proc. Natl. Acad. Sci. USA 93 (1996) or swollen carpels by position from basipetal to acropetal on Color balance and brightness were adjusted using PHOTOSHOP the primary inflorescence. For lfy-6, 31 of 60 plants displayed 3.0.1 (Adobe Systems, Mountain View, CA). Printed images a strong floral reversion phenotype. All 31 plants were con- were generated using a Codonics NP1600 printer (Codonics, firmed heterozygous by F1 analysis. Thirteen plants were Middleburg Heights, OH). confirmed as homozygous wild type for LFY. The remaining 17 plants were homozygous lfy-6 and did not produce flowers RESULTS or seed. For ag-1, 16 plants were homozygous ag-1, and all produced flowers displaying floral meristem reversion. To Transforming Flowers into Shoots. Homozygous lfy mutants generate lfy-6 spy mutants, homozygous lfy-6 was crossed with are characterized by a partial and conditional block in the spy-2 and spy-3. F2 seedlings homozygous for spy were selected establishment of the flower meristem (12, 15, 16). Under LD by germination on 1.2 3 1024 M paclobutrazol (26), washed photoperiod, early-arising basipetal flowers are indeterminate extensively with H2O, transplanted to soil, and grown under and shoot-like, whereas the later-arising acropetal flowers are SD(D) conditions. determinate. As shown in Fig. 1A, a homozygous acropetal Structural Analysis Using Light Microscopy. Flowers were lfy-6 flower is distinguished by the production of sepals and fixed overnight in FAA (3.7% formaldehydey5% acetic acidy carpels and by the absence of petals and stamens when grown 50% ethanol), dehydrated in a graded ethanol series, infil- under LDs. By contrast, lfy-6 flower development is strongly trated, and embedded in plastic resin. Serial 2 mm longitudinal repressed under SD conditions. Determinate floral buds are sections were stained with toluidine blue-basic fuchsin. Images replaced by indeterminate shoots that continuously produce were obtained by using bright-field optics. leaf-like organs (Fig. 1B). In Situ Hybridization Analysis. In situ hybridizations were We previously suggested that SD photoperiod dramatically performed by using a digoxygenin-labeled AG RNA probe alters flower development in heterozygous lfy-6 plants (21). (24) as described (27) with the exception that the acetylation SDs can induce heterozygous lfy-6 flowers to undergo a step was omitted. Hybridization was detected using a modified heterochronic transformation from flower to shoot develop- Genius (Boehringer Mannheim) procedure (G. N. Drews, ment. Fig. 1C shows that initially the heterozygous lfy-6 floral personal communication). Images were photographed using meristem produces the normal complement of floral organs— dark-field optics. four sepals, four petals, six stamens, and two carpels.
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