Abstract
Longan (Dimocarpus longan Lour.) is a subtropical fruit tree of significant economic importance. Flowering is a key event in longan and other fruit trees. In this study, GIGANTEA (GI) and FLAVIN-BINDING, KELCH REPEAT, F-BOX1 (FKF1) homologs were cloned from longan and named DlGI and DlFKF1, respectively. Translated sequences of DlGI and DlFKF1 revealed a high homology to GI and FKF1 sequences from other plants. DlGI and DlFKF1 transcript levels varied seasonally in the shoots and leaves during floral bud differentiation of longan. Expression levels of DlGI and DlFKF1 in the shoot tips increased and reached a peak in November which is the time of physiological differentiation of floral buds in longan. Ectopic overexpression of DlGI and DlFKF1 in Arabidopsis resulted in early-flowering phenotypes and adventitious root formation under LD conditions. The expression levels of YUCCA 9 and PIN-FORMED 2 were found to be elevated in DlGI-overexpressing and DlFKF1-overexpressing Arabidopsis plants under LD conditions. These results suggest that both DlGI and DlFKF1 are flowering promoters and they might be involved in the regulation of physiological differentiation of floral buds, inducing floral initiation by affecting endogenous auxin synthesis and transport in longan. Our results will provide more insight into flowering regulation in longan and woody plants.
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References
Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013
Baudry A, Ito S, Song YH, Strait AA, Kiba T, Lu S, Henriques R, Pruneda-Paz JL, Chua NH, Tobin EM (2010) F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression. Plant Cell 22:606–622
Bendix C, Mendoza JM, Stanley DN, Meeley R, Harmon FG (2013) The circadian clock-associated gene gigantea1 affects maize developmental transitions. Plant Cell Environ 36:1379–1390
Bi CL, Liu X, Zhang XY (2006) The function of F-box protein in plant growth and development. Hereditas 28:1337–1342
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44
Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Van OH, Van MM, Inzé D (1995) superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405–1419
Brock MT, Tiffin P, Weinig C (2007) Sequence diversity and haplotype associations with phenotypic responses to crowding: GIGANTEA affects fruit set in Arabidopsis thaliana. Mol Ecol 16:3050–3062
Cheng P, He Q, Yang Y, Wang L, Liu Y (2003) Functional conservation of light, oxygen, or voltage domains in light sensing. Proc Natl Acad Sci U S A 100:5938–5943
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Corbesier L, Coupland G (2006) The quest for florigen: a review of recent progress. J Exp Bot 57:3395–3403
Dalchau N, Kay SA (2011) The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc Natl Acad Sci U S A 108:5104–5109
Dunford RP, Griffiths S, Christodoulou V, Laurie DA (2005) Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA. Theor Appl Genet 110:925–931
Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86
Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18:4679–4688
Garner WW, Allard HA (1920) Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res 11:553–606
Habets MEJ, Offringa R (2014) PIN-driven polar auxin transport in plant developmental plasticity: a key target for environmental and endogenous signals. New Phytol 203:362–377
Heller WP, Ying Z, Davenport TL, Keith LM, Matsumoto TK (2014) Identification of members of the Dimocarpus longan Flowering Locus T gene family with divergent functions in flowering. Trop Plant Biol 7:19–29
Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci U S A 97:9789–9794
Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89
Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11:550–558
Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–306
Jia T, Wei D, Meng S, Allan AC, Zeng L (2014) Identification of regulatory genes implicated in continuous flowering of Longan (Dimocarpus longan L.) PLoS ONE 9:e114568–e114568
Jr CJ, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9:2131–2142
Jung JH, Seo YH, Seo PJ, Reyes JL, Ju Y, Chua NH, Park CM (2007) The GIGANTEA-regulated MicroRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19:2736–2748
Li F, Zhang X, Hu R, Wu F, Ma J, Meng Y, Fu YF (2013) Identification and molecular characterization of FKF1 and GI homologous genes in Soybean. PLoS ONE 8:e79036–e79036
Matsumoto TK (2006) Genes uniquely expressed in vegetative and potassium chlorate induced floral buds of Dimocarpus longan. Plant Sci 170:500–510
Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17:2255–2270
Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101:331–340
Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285:1579–1582
Penfield S, Hall A (2009) A role for multiple circadian clock genes in the response to signals that break seed dormancy in Arabidopsis. Plant Cell 21:1722–1732
Peng J, Xie LJ, Xu BQ, Dang JZ, Li YH, Lu ZH, Zhang SA, Yu ZY, Bai XQ, Cai ZF (2010) Study on biological characters of ‘Sijihua’ longan. Acta Hortic 863:249–258
Qiu JD, Wu DY, Zhang HL (2001) A study on flower differentiation of ‘Shixia’ longan (Dimocarpus longana Lour. cv. Shixia). J South China Agric Univ 22:27–30
Sawa M, Kay SA (2011) GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc Natl Acad Sci U S A 108:11698–11703
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265
Schultz TF, Kiyosue T, Yanovsky M, Wada M, Kay SA (2001) A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13:2659–2670
Somers DE, Schultz TF, Milnamow M, Kay SA (2000) ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101:319–329
Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336:1045–1049
Sorin C, Negroni L, Balliau T, Corti H, Jacquemot MP, Davanture M, Sandberg G, Zivy M, Bellini C (2006) Proteomic analysis of different mutant genotypes of Arabidopsis led to the identification of 11 proteins correlating with adventitious root development. Plant Physiol 140:349–364
Su M (1997) Effects of endogenous hormones in bearing basal shoots of “Shuizhang” longan on floral bud differentiation. Chinese J Trop Crops 18:66–71
Sukumar P, Maloney GS, Muday GK (2013) Localized induction of the ATP-binding cassette B19 auxin transporter enhances adventitious root formation in Arabidopsis. Plant Physiol 162:1392–1405
Tamaki S (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Thomas B, Vince-Prue D (1997) Photoperiodism in plants, second edition. Academic Press, San Diego
Tseng TS, Salomé PA, McClung CR, Olszewski NE (2004) SPINDLY and GIGANTEA interact and act in Arabidopsis thaliana pathways involved in light responses, flowering, and rhythms in cotyledon movements. Plant Cell 16:1550–1563
Winterhagen P, Tiyayon P, Samach A, Hegele M, Wünsche JN (2013) Isolation and characterization of FLOWERING LOCUS T subforms and APETALA1 of the subtropical fruit tree Dimocarpus longan. Plant Physiol Biochem 71:184–190
Xiang YZ, Mao SL, Jia RL, Guan CM, Xian SZ (2005) The wheat TaGI1, involved in photoperiodic flowering, encodesan Arabidopsis GI ortholog. Plant Mol Biol 58:53–64
Xu JF, Zu N, Wen C, Zeng LH (2011) Cloning and sequence analysis of LEAFY gene promoter from longan (Dimocarpus longan L.) J Fruit Sci 4:689–693
Yunde Z., Auxin Biosynthesis. (2014). The Arabidopsis Book, First published on June 13, 2014: e0173. doi: 10.1199/tab.0173
Zeng LH, Guan L, Wu SH (2010) LLFY, a longan LEAFY ortholog, is associated with differentiation and maintenance of inflorescence bud. Acta Hortic 863:123–128
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Conceived and designed the experiments: LZ, FH. Performed the experiments: FH, ZF. Analyzed the data: FH. Contributed reagents/materials/analysis tools: FH, ZF. Wrote the paper: LZ, FH, MMB.
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Huang, F., Fu, Z., Zeng, L. et al. Isolation and characterization of GI and FKF1 homologous genes in the subtropical fruit tree Dimocarpus longan . Mol Breeding 37, 90 (2017). https://doi.org/10.1007/s11032-017-0691-z
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DOI: https://doi.org/10.1007/s11032-017-0691-z