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Plant Signal Behav. 2011 Apr; 6(4): 471–476.
Published online 2011 Apr 1. doi:  10.4161/psb.6.4.14496
PMCID: PMC3142372

Shedding light on flower development

Phytochrome B regulates gynoecium formation in association with the transcription factor SPATULA


Accurate development of the gynoecium, the female reproductive organ, is necessary to achieve efficient fertilization. In Arabidopsis, the correct patterning of the apical-basal axis of the gynoecium requires the establishment of a morphogenic gradient of auxin. This allows the production of specialized tissues, whose roles consist of attracting pollen, allowing pollen tube growth and protecting the ovules within the ovaries. Mutations in the bHLH transcription factor SPATULA (SPT) are known to impair the development of the apical tissues of the gynoecium. Here, we show that the spt phenotype is rescued by the removal of phytochrome B, and discuss how light signaling may control flower development.

Key words: flower development, gynoecium, SPATULA, phytochrome, auxin


In Arabidopsis, the gynoecium, the female reproductive organ, is a highly specialized organ resulting from the congenital fusion of two carpels, forming a hollow cylinder. A fully developed gynoecium consists of a short basal gynophore on which sits the large ovary, within which the ovules develop. The ovary is divided into two compartments by a septum, and is extended apically by a short style and a stigma. The stigmatic tissue is designed to trap the pollen and during fertilization, the pollen tubes germinate on the stigma and grow through the transmitting tract that develops within the style and the septum, before swerving laterally to eventually reach the mature ovules.1

Several regulatory mechanisms are involved in the formation of the gynoecium and its apical-basal specification. The current dogma implies the formation of a morphogenic gradient of auxin, where an auxin maximum on the apical side of the gynoecium is needed to promote the formation of the style and stigma. Progressively diminishing levels of auxin towards the basal side of the gynoecium specify the ovaries area and eventually the gynophore at the basal side, where auxin concentration reaches a minimum.2,3 A large number of transcription factors have been described to take part in gynoecium patterning via the mediation of auxin-related processes, including ETTIN (ETT), STYLISH (STY), SPATULA (SPT), HECATE (HEC) and SEUSS (SEU) (reviewed in refs. 1, 3 and 4).

Mutations in the SPATULA (SPT) gene impair the development of the apical tissues of the gynoecium, as the carpels fail to fuse properly, disrupting the formation of the transmitting tract, the style and the stigma.57 This results in a reduced frequency of fertilization and low seed production.8 Several lines of evidence have linked SPT and the establishment of the morphogenic auxin gradient throughout the basal-apical axis of the gynoecium: indeed, spt apical phenotype can be rescued by the application of N-1-naphthylphthalamic acid (NPA), a polar auxin transport inhibitor, suggesting that SPT activity may result in disrupting auxin transport. Furthermore, the auxin-response factor ETTIN (ETT) is crucial for both the setup and the interpretation of the auxin gradient, and has been shown to mainly act by restricting SPT expression.2 In addition to its role in gynoecium patterning, SPT has also been shown to be involved in defining the fate of the apical meristem during the very early stages of flower development.6

SPT is a basic helix-loop-helix transcription factor, belonging to the Phytochrome Interacting Factors/PIF-Like (PIF/PIL) family, where almost all members have been shown to regulate different aspects of light development.7,9 Phytochromes are red/ far-red light photoreceptors which, upon red light activation, change into an active conformation and rapidly migrate into the nucleus, where they bind members of the PIF family, leading to the de-repression of PIFs-controlled transcription. While PIF1, PIF3, PIF4, PIF5, PIF6 and PIF7 bind to the phytochromes directly,1014 PIL factors lack the ability to bind phytochromes directly.11 They however can form heterodimers with true PIFs, and modulate their function.15,16 SPT belongs to this later PIL category.11

SPT has been shown, together with PIF1, to control seed germination in response to both cold and light treatment.17,18 One mechanism through which SPT and PIF1 act is by regulating gibberellic acid (GA) biosynthetic genes in the developing seed.14,1719 GA is a phytohormone triggering cell expansion, and is required for seed germination, as well as growth at many stages throughout the plant life. Of particular interest, GA is necessary for the development of the fruit post-fertilization. In this instance, it was recently shown that auxin promotes GA metabolism in fertilized ovules, and that constitutive GA signaling is sufficient to trigger parthenocarpy, independently of the fertilization event.20

SPT is also involved in seedling development: while spt mutants present large cotyledons, an overexpression of SPT leads to the development of a long hypocotyl and very small cotyledons when grown in red light, resembling a phytochrome B (phyB)-null mutant.17 Additionally, SPT also controls leaf size in a similar manner, especially under colder conditions.21,22

The possibility of a role for SPT in phytochrome signaling, as well as its dramatic action in gynoecium development, led us to investigate whether phyB could influence SPT-dependent gynoecium development.


In spt monogenic mutants, the gynoecium develops abnormally, with unfused carpels at the upper-most side and reduced stigmatic papillae. However, when polar auxin transport is inhibited by NPA treatment, the spt gynoecium presents a morphology similar to an untreated wt gynoecium2,6 (Fig. 1). We have previously shown that SPT regulates GA biosynthesis in the seed,17 and it has been demonstrated that, post-fertilization, an auxin signal is able to trigger GA production in the developing fruit.20 We therefore set out to determine whether the spt gynoecium phenotype could be affected or rescued by GA treatment. Figure 1 shows that GA treatment of a wt gynoecium does not affect its formation (Fig. 1C), but is unable to rescue spt-11 gynoecium development (Fig. 1G). However, GA treatment does not prevent spt-11 phenotypic rescue by NPA treatment (Fig. 1H). This suggests that, when controlling gynoecium development, SPT is not targeting GA biosynthesis.

Figure 1
Effect of hormone treatment on gynoecium development. Light microscopy images of the apical extremity of Col (A–D) and spt-11 (E–H) gynoecia dissected from stage 12 flowers. The early buds were treated as indicated and the flowers were ...

Since SPT belongs to the same clade as the light regulated PIF proteins, we next decided to test whether SPT function during gynoecium formation was phytochrome-dependent. Null phyB mutant fruits develop normally, both pre- and post-fertilization (Fig. 2A–C), the final silique's size being only slightly longer in a phyB-1 mutant (Ler ecotype), but not in a phyB-9 mutant (Col ecotype) (Fig. 2B). Both the Ler spt-2 and the Col null allele spt-11 present the previously described gynoecium development defect6,21 (Fig. 2A). However, in a phyB null background, this phenotype is fully rescued (Fig. 2A). Additionally, the phyB mutation rescues the spt short silique phenotype (Fig. 2B) as well as spt larger seed size (Fig. 2C). This clearly demonstrates that, for gynoecium and fruit development, the function of SPT is phyB-dependent.

Figure 2
phyB mutation complements the spt gynoecium, silique and seed phenotypes. (A) Light microscopy images of the apical extremity of Ler, spt-2, phyB-1, spt-2phyB-1, Col, spt-11, phyB-9 and spt-11phyB-9 gynoecia dissected from stage 11 flowers. Bar = 100 ...

SPT function has been shown to be involved at different stages of the gynoecium development: indeed, on one hand, SPT promotes carpel development early during flower formation,6 and on the other hand SPT is required for normal tract formation and apical fusion during gynoecium development.57 We therefore set out to observe the phyB-dependence of the spt gynoecium phenotype through a number of developmental stages (Fig. 3). While both Col gynoecium and phyB-9 gynoecium apices are fused throughout development, spt-11 gynoecium presents a lack of carpel fusion at the apical pole as early as we could observe (stage 8). Interestingly, the spt-11 phyB-9 double mutant is very similar to a spt-11 mutant at these early developmental stages. Fusion of the carpels and rescue of the spt phenotype only occurred by stage 11 of gynoecium development. This suggests that the phyB mutation is only able to rescue SPT function at a later developmental stage, when the basal-apical axis of the gynoecium is being defined.

Figure 3
phyB mutation does not complement the spt early phenotype. Time series of gynoecium development: Col, spt-11, phyB-9 and spt-11phyB-9 flowers from stage 8 to 16 were dissected and their gynoecium was observed by light microscopy. Bar = 100 µm. ...


Phytochrome's paramount role in controlling numerous aspects of the plant life, from germination and early development to plant architecture and flowering, have been studied at length in the past years.2325 However, this is the first report of a role for phyB in flower development.

A large body of evidence has shown that, under the regulation of the transcription factor STYLISH (STY), auxin forms a morphogenetic gradient within the gynoecium, which is believed to be interpreted by ETT, SPT and HECATE (HEC), leading to the formation of a series of different structures along the apical-basal axis of the gynoecium, in an auxin concentration-dependent manner.2,2629 Meanwhile, numerous recent studies have investigated the relationship between phyB and phytohormones, with a large focus on auxin pathways. Indeed, phytochrome signaling has been shown to influence auxin pathways at different levels: auxin production, auxin distribution and sensitivity to auxin signals (reviewed in ref. 30).

Phytochromes have recently been shown to directly control auxin production. Active phyB reduces auxin production via the concurrent activation of (SUPERROOT 2) SUR2, a suppressor of auxin biosynthesis and the inhibition of TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1), an enhancer of auxin biosynthesis.3033 Conversely, it has been shown that reduced levels of phyB, triggered by shade conditions, set off the opposite response, with an elevation of IAA production.30,33 Strikingly, mutations in TAA1, together with its homolog TRYPTOPHAN AMINOTRANSFERASE RELATED 2 (TAR2) lead to the production of a gynoecium presenting an apicalized phenotype, with reduced or nonexistent valve area and an over-abundance of stigmatic tissue,34 showing that the integrity of the TAA1-dependent branch of auxin biosynthesis is essential for a correct patterning of the gynoecium. Interestingly, the expression pattern of both TAA1 and TAR2 in the gynoecium coincides with SPT expression, suggesting a causal link between SPT and auxin production, with SPT either directly responding to or being involved in auxin production.35 Here, we show that in a phyB-null mutant, the spt gynoecium phenotype is rescued. This suggest that, in a spt mutant, where the auxin gradient fails to either be set-up or interpreted, reducing phyB levels could result in a modification of auxin production, participating to local changes in auxin concentration throughout the gynoecium, and resulting in a rescue of the spt phenotype.

Additionally, polar auxin transport and light signaling have been functionally linked in numerous studies, mainly looking at seedling development, shoot-root communication and the control of branching. Indeed, phytochrome mutants have reduced sensitivity to NPA-induced hypocotyl growth inhibition, suggesting that polar auxin transport requires functional phytochrome action.36 Similarly, phytochrome mutants show reduced shoot-root auxin transport,37 as well as reduced auxin-dependent branching.25 At the molecular level, phytochromes were shown to influence both the expression and the localization of a handful of auxin transporter involved in polar auxin transport.3740 This means that the absence of phyB in a spt background could impair auxin transport through the gynoecium in a NPA-mimicking way, resulting in the establishment of the auxin gradient needed for the correct specification of the gynoecium apex, and a rescue of the spt phenotype.

Eventually, both light and auxin pathways share common targets and are highly integrated, especially during the shade avoidance response, where neighboring vegetation produce a far-red light rich environment, which depletes the active phyB pool (reviewed in refs. 30 and 41). There, phyB depletion leads to the accumulation of PIF family members, resulting in the induction of the expression of a number of transcription factors. These include the SPT homologs LONG HYPOCOTYL IN FAR-RED (HFR1), PIL1 and PIL2,4244 as well as the more distant relatives PHYTOCHROME RAPIDLY REGULATED1 (PAR1) and PAR2.45,46 Interestingly, both HFR1 and PAR1/2 have been shown to suppress the transcription of a number of auxin signaling targets including members of the SAUR and the Aux/IAA family, suggesting that shade conditions lead to a de-repression of auxin signaling.43,45,46 Moreover, PIF4 was also shown to regulate auxin-mediated signaling pathways in response to high temperature.47 Additionally, members of the PIF/PIL family are known to regulate each other's expression44 and have highly redundant functions.12,48 Taken together, these results offer the possibility that SPT could regulate auxin signaling by targeting shade-induced genes like HFR1 and PIL1. In this case, SPT function could therefore be supplemented in a phyB-null mutant by the action of members of the PIF family like PIF4 and PIF5 that are stabilized.

In this context, it is also interesting to notice that SPT is able to heterodimerize with a wide range of bHLH transcription factors, showing interaction in yeast-2-hybrid experiments with HEC1/2/3,28 as well as with PIF1 and PIF4 (Bou-Torrent and Martinez-Garcia, personal communication). This therefore offers the possibility that in the gynoecium, SPT and PIF4 could dimerize, leading to an increase in PIF4 stability, and an induction of shade related genes.

Alternatively, as the spt phenotype could result from a decrease in auxin sensitivity,2 the de-repression of auxin signaling when phyB levels are depleted could increase the general sensitivity for auxin, rescuing the gynoecium development in a spt mutant.

In conclusion, we show here that the spt phenotype is rescued equally by NPA addition and by a phyB mutation: this is correlative evidence that phyB could be acting on auxin production, distribution or sensitivity within the gynoecium to promote the establishment of the basal-apical axis of the developing flower. This work demonstrates a role for phyB in the control of flower development, and shows a cooperative function for the PIF3-homologue SPT and phyB in this developmental process. Future work, however, will be necessary to identify the exact point(s) of interaction between phyB and SPT signaling leading to the establishment of the auxin gradient within the gynoecium.

Materials and Methods

Lines and growth conditions.

Both Landsberg erecta (Ler) and Columbia-0 (Col) accessions of Arabidopsis thaliana were used. The spt-2 and phyB-1 mutants (Ler alleles) as well as the spt-11 and phyB-9 mutants (Col alleles) were described previously in references 6, 21 and 49. spt-2 phyB-1 and spt-11 phyB-9 were obtained by cross-pollination of their respective parents and were selected via PCR and sequencing methods.

Plants were grown in a (2:1) soil-sand mixture under long days conditions (16:8) at 22°C under 100 µmol.m−2.s−1 of white light.

Hormone treatments.

All siliques, flowers and large buds were removed, and the inflorescences were dipped 2 days in a row in the indicated solution of hormone (NPA or GA3) or water (mock) prepared in 0.01% silwet L-77 (Lehle seeds, VIS-02). Flowers were then observed 7 days later.

Light microscopy and size measurements.

Unstained plant material was dissected and viewed with a Leica MZ 16 F microscope. Silique length (n = 20) and seed area (n = 200) were measured using the ImageJ software (http://rsbweb.nih.gov/ij/). Gynoecium development stages were defined as published in references 1 and 50.


This work was supported by the UK Biotechnology and Biological Sciences Research Council (B.B.S.R.C.) grants BBE0003631 to K.J.H. and BBE0005411 to I.A.G.


bHLHbasic helix-loop-helix
PIFphytochrome interacting factor
NPAN-1-naphthylphthalamic acid
GAgibberellic acid


1. Roeder AHK, Yanofsky MF. The Arabidopsis Book: The American Society of Plant Biologists. 2008. Fruit Development in Arabidopsis; pp. 1–50.
2. Nemhauser JL, Feldman LJ, Zambryski PC. Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development. 2000;127:3877–3888. [PubMed]
3. Staldal V, Sundberg E. The role of auxin in style development and apical-basal patterning of the Arabidopsis thaliana gynoecium. Plant Signal Behav. 2009;4:83–85. [PMC free article] [PubMed]
4. Østergaard L. Don't ‘leaf’ now. The making of a fruit. Curr Opin Plant Biol. 2009;12:36–41. [PubMed]
5. Alvarez J, Smyth DR. Genetic pathways controlling carpel development in Arabidopsis thaliana. J Plant Res. 1998;111:295–298.
6. Alvarez J, Smyth DR. CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development. 1999;126:2377–2386. [PubMed]
7. Heisler MG, Atkinson A, Bylstra YH, Walsh R, Smyth DR. SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development. 2001;128:1089–1098. [PubMed]
8. Groszmann M, Paicu T, Smyth DR. Functional domains of SPATULA, a bHLH transcription factor involved in carpel and fruit development in Arabidopsis. Plant J. 2008;55:40–52. [PubMed]
9. Toledo-Ortiz G, Huq E, Quail PH. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell. 2003;15:1749–1770. [PMC free article] [PubMed]
10. Al-Sady B, Ni W, Kircher S, Schafer E, Quail PH. Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell. 2006;23:439–446. [PubMed]
11. Khanna R, Huq E, Kikis EA, Al-Sady B, Lanzatella C, Quail PH. A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell. 2004;16:3033–3044. [PMC free article] [PubMed]
12. Leivar P, Monte E, Al-Sady B, Carle C, Storer A, Alonso JM, et al. The Arabidopsis phytochromeinteracting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell. 2008;20:337–352. [PMC free article] [PubMed]
13. Shen Y, Khanna R, Carle CM, Quail PH. Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol. 2007;145:1043–1051. [PMC free article] [PubMed]
14. Oh E, Yamaguchi S, Kamiya Y, Bae G, Chung WI, Choi G. Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J. 2006;47:124–139. [PubMed]
15. Hornitschek P, Lorrain S, Zoete V, Michielin O, Fankhauser C. Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 2009;28:3893–3902. [PMC free article] [PubMed]
16. Lorrain S, Trevisan M, Pradervand S, Fankhauser C. Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 2009;60:449–461. [PubMed]
17. Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ, Graham IA. Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol. 2005;15:1998–2006. [PubMed]
18. Oh E, Kim J, Park E, Kim JI, Kang C, Choi G. PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell. 2004;16:3045–3058. [PMC free article] [PubMed]
19. Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, Paik I, et al. PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell. 2007;19:1192–1208. [PMC free article] [PubMed]
20. Dorcey E, Urbez C, Blazquez MA, Carbonell J, Perez-Amador MA. Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J. 2009;58:318–332. [PubMed]
21. Ichihashi Y, Horiguchi G, Gleissberg S, Tsukaya H. The bHLH transcription factor SPATULA controls final leaf size in Arabidopsis thaliana. Plant Cell Physiol. 2010;51:252–261. [PubMed]
22. Sidaway-Lee K, Josse EM, Brown A, Gan Y, Halliday KJ, Graham IA, et al. SPATULA links daytime temperature and plant growth rate. Curr Biol. 2010;20:1493–1497. [PubMed]
23. Franklin KA, Quail PH. Phytochrome functions in Arabidopsis development. J Exp Bot. 2010;61:11–24. [PMC free article] [PubMed]
24. Josse EM, Foreman J, Halliday KJ. Paths through the phytochrome network. Plant Cell Environ. 2008;31:667–678. [PubMed]
25. Finlayson SA, Krishnareddy SR, Kebrom TH, Casal JJ. Phytochrome regulation of branching in Arabidopsis. Plant Physiol. 2010;152:1914–1927. [PMC free article] [PubMed]
26. Sohlberg JJ, Myrenas M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, et al. STY1 regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium. Plant J. 2006;47:112–123. [PubMed]
27. Balanza V, Navarrete M, Trigueros M, Ferrandiz C. Patterning the female side of Arabidopsis: The importance of hormones. J Exp Bot. 2006;57:3457–3469. [PubMed]
28. Gremski K, Ditta G, Yanofsky MF. The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development. 2007;134:3593–3601. [PubMed]
29. Stewart JL, Nemhauser JL. Do trees grow on money? Auxin as the currency of the cellular economy. Cold Spring Harb Perspect Biol. 2010;2:1420. [PMC free article] [PubMed]
30. Halliday KJ, Martinez-Garcia JF, Josse EM. Integration of light and auxin signaling. Cold Spring Harb Perspect Biol. 2009;1:1586. [PMC free article] [PubMed]
31. Hoecker U, Toledo-Ortiz G, Bender J, Quail PH. The photomorphogenesis-related mutant red1 is defective in CYP83B1, a red light-induced gene encoding a cytochrome P450 required for normal auxin homeostasis. Planta. 2004;219:195–200. [PubMed]
32. Wagner D, Hoecker U, Quail PH. RED1 is necessary for phytochrome B-mediated red light-specific signal transduction in Arabidopsis. Plant Cell. 1997;9:731–743. [PMC free article] [PubMed]
33. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell. 2008;133:164–176. [PMC free article] [PubMed]
34. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, et al. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 2008;133:177–191. [PubMed]
35. Groszmann M, Bylstra Y, Lampugnani ER, Smyth DR. Regulation of tissue-specific expression of SPATULA, a bHLH gene involved in carpel development, seedling germination and lateral organ growth in Arabidopsis. J Exp Bot. 2010;61:1495–1508. [PMC free article] [PubMed]
36. Jensen PJ, Hangarter RP, Estelle M. Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol. 1998;116:455–462. [PMC free article] [PubMed]
37. Salisbury FJ, Hall A, Grierson CS, Halliday KJ. Phytochrome coordinates Arabidopsis shoot and root development. Plant J. 2007;50:429–438. [PubMed]
38. Devlin PF, Yanovsky MJ, Kay SA. A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol. 2003;133:1617–1629. [PMC free article] [PubMed]
39. Laxmi A, Pan J, Morsy M, Chen R. Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS One. 2008;3:1510. [PMC free article] [PubMed]
40. Wu G, Cameron JN, Ljung K, Spalding EP. A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome 1 and phytochrome B. Plant J. 2010;62:179–191. [PubMed]
41. Franklin KA. Shade avoidance. New Phytol. 2008;179:930–944. [PubMed]
42. Salter MG, Franklin KA, Whitelam GC. Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature. 2003;426:680–683. [PubMed]
43. Sessa G, Carabelli M, Sassi M, Ciolfi A, Possenti M, Mittempergher F, et al. A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev. 2005;19:2811–2815. [PMC free article] [PubMed]
44. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 2008;53:312–323. [PubMed]
45. Roig-Villanova I, Bou J, Sorin C, Devlin PF, Martinez-Garcia JF. Identification of primary target genes of phytochrome signaling. Early transcriptional control during shade avoidance responses in Arabidopsis. Plant Physiol. 2006;141:85–96. [PMC free article] [PubMed]
46. Roig-Villanova I, Bou-Torrent J, Galstyan A, Carretero-Paulet L, Portoles S, Rodriguez-Concepcion M, et al. Interaction of shade avoidance and auxin responses: A role for two novel atypical bHLH proteins. EMBO J. 2007;26:4756–4767. [PMC free article] [PubMed]
47. Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol. 2009;19:408–413. [PubMed]
48. Leivar P, Monte E, Oka Y, Liu T, Carle C, Castillon A, et al. Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol. 2008;18:1815–1823. [PMC free article] [PubMed]
49. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell. 1993;5:147–157. [PMC free article] [PubMed]
50. Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell. 1990;2:755–767. [PMC free article] [PubMed]

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