Abstract
Flowering determines the yield of saffron, whereas synchronized sprouting determines plant fitness; thus, their regulation is of utmost importance. In saffron, corm sprouting is marked with the emergence of flowers and leaves simultaneously. PEBP genes have a conserved role in regulating flowering and vegetative growth in plants, but their role in saffron is confined due to the non-availability of genomic resources. In the present study, we isolated their homologues in saffron and examined their alleged role in promoting flowering. Here we report that at least 6 FTs (FLOWERING LOCUS T), 2 TFL1s (TERMINAL FLOWER 1), and 2 MFTs (MOTHER OF FT AND TFL1) genes are present in saffron. The sequence analysis suggests they possess a conserved structural genetic organization with other plant species gene members. Interestingly, two FT genes (CsatFT4 and CsatFT6) showed the presence of characteristic amino acids of TFL-like genes but were aligned in FT genes clade. Phylogenetic analysis divided them into FT-like, TFL1-like, and MFT-like clades. The expression of identified genes varied among different tissues. The spatial and temporal expressions during sprouting suggest that they might have different functions. Tissue and organ-specific expression profiling suggest that CsatFT3 might act locally in apical buds to promote flowering, while CsatFT1 and 2 are involved in promoting vegetative growth. Antagonistically, CsatTFL1-1 and CsatTFL1-2 might regulate vegetative growth and flowering, respectively. Additionally, comparative expression profiling between flowering competent (big) vs non-competent (small) corms affirm the specific role of CsatFT3 as a plausible flowering regulator.
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References
Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, Yoo SY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. Embo J 25(3):605–614. https://doi.org/10.1038/sj.emboj.7600950
Bagri J, Yadav A, Anwar K, Dkhar J, Singla-Pareek SL, Pareek A (2017) Metabolic shift in sugars and amino acids regulates sprouting in saffron corm. Sci Rep. https://doi.org/10.1038/s41598-017-10528-2
Banfield M, Brady R (2000) The structure of Antirrhinum centroradialis protein (CEN) suggests a role as a kinase regulator. J Mol Biol 297(5):1159–1170
Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312(5776):1040–1043. https://doi.org/10.1126/science.1126038
Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275(5296):80–83
Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61(5):579–590
Chaurasia AK, Patil HB, Krishna B, Subramaniam V, Sane PV, Sane AP (2017) Flowering time in banana (Musa spp.) a day neutral plant, is controlled by at least three flowering locus T homologues. Sci Rep 7(1):1–14
Chen Y, Xu X, Chen X, Chen Y, Zhang Z, Xuhan X, Lin Y, Lai Z (2018) Seed-specific gene MOTHER of FT and TFL1 (MFT) involved in embryogenesis, hormones and stress responses in Dimocarpus longan Lour. Int J Mol Sci 19(8):2403
Conti L, Bradley D (2007) Terminal flower1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19(3):767–778. https://doi.org/10.1105/tpc.106.049767
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316(5827):1030–1033
Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR (2008) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol 146(1):250–264
Gaston A, Potier A, Alonso M, Sabbadini S, Delmas F, Tenreira T, Cochetel N, Labadie M, Prévost P, Folta KM, Mezzetti B, Hernould M, Rothan C, Denoyes B (2021) The FveFT2 florigen/FveTFL1 antiflorigen balance is critical for the control of seasonal flowering in strawberry while FveFT3 modulates axillary meristem fate and yield. New Phytol 232(1):372–387. https://doi.org/10.1111/nph.17557
Gohari AR, Saeidnia S, Mahmoodabadi MK (2013) An overview on saffron, phytochemicals, and medicinal properties. Pharmacogn Rev 7(13):61
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652. https://doi.org/10.1038/nbt.1883
Haghighi R, Sayed Tabatabaei BE, Maibody S, Talebi M, Molina RV, Nebauer SG, Renau-Morata B (2020) A flowering inhibitor of the temperature-dependent pathway in Crocus sativus L. Mol Biol Rep 47(3):2171–2179. https://doi.org/10.1007/s11033-020-05316-7
Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci USA 102(21):7748–7753
Hedman H, Kallman T, Lagercrantz U (2009) Early evolution of the MFT-like gene family in plants. Plant Mol Biol 70(4):359–369. https://doi.org/10.1007/s11103-009-9478-x
Hiraoka K, Yamaguchi A, Abe M, Araki T (2013) The florigen genes FT and TSF modulate lateral shoot outgrowth in Arabidopsis thaliana. Plant Cell Physiol 54(3):352–368. https://doi.org/10.1093/pcp/pcs168
Howes M-JR, Perry E (2011) The role of phytochemicals in the treatment and prevention of dementia. Drugs Aging 28(6):439–468
Hsu C-Y, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18(8):1846–1861
Hsu C-Y, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, Wickett N, Gunter LE, Tuskan GA, Brunner AM, Page GP, Barakat A, Carlson JE, dePamphilis CW, Luthe DS, Yuceer C (2011) <em>Flowering locus T</em> duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci 108(26):10756–10761. https://doi.org/10.1073/pnas.1104713108
Hu J, Liu YP, Tang XH, Rao HJ, Ren CX, Chen J, Wu QH, Jiang Y, Geng FC, Pei J (2020) Transcriptome profiling of the flowering transition in saffron (Crocus sativus L.). Sci Rep 10:9680. https://doi.org/10.1038/s41598-020-66675-6
Huang Y, Niu BF, Gao Y, Fu LM, Li WZ (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26(5):680–682. https://doi.org/10.1093/bioinformatics/btq003
Jensen CS, Salchert K, Nielsen KK (2001) A TERMINAL FLOWER1-like gene from perennial ryegrass involved in floral transition and axillary meristem identity. Plant Physiol 125(3):1517–1528
Jin S, Nasim Z, Susila H, Ahn JH (2021) Evolution and functional diversification of FLOWERING LOCUS T/TERMINAL FLOWER 1 family genes in plants. Semin Cell Dev Biol 109:20–30. https://doi.org/10.1016/j.semcdb.2020.05.007
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer <i>FT</i>. Science 286(5446):1962–1965. https://doi.org/10.1126/science.286.5446.1962
Karlgren A, Gyllenstrand N, Källman T, Sundström JF, Moore D, Lascoux M, Lagercrantz U (2011) Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol 156(4):1967–1977. https://doi.org/10.1104/pp.111.176206
Khosa J, Bellinazzo F, Kamenetsky Goldstein R, Macknight R, Immink RG (2021) PHOSPHATIDYLETHANOLAMINE-BINDING PROTEINS: the conductors of dual reproduction in plants with vegetative storage organs. J Exp Bot 72(8):2845–2856
Kinoshita T, Ono N, Hayashi Y, Morimoto S, Nakamura S, Soda M, Kato Y, Ohnishi M, Nakano T, Inoue S-i (2011) FLOWERING LOCUS T regulates stomatal opening. Curr Biol 21(14):1232–1238
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286(5446):1960–1962
Kothari D, Thakur R, Kumar R (2021) Saffron (Crocus sativus L.): gold of the spices—a comprehensive review. Hortic, Environ, Biotechnol 62(5):661–677
Kurokawa K, Kobayashi J, Nemoto K, Nozawa A, Sawasaki T, Nakatsuka T, Yamagishi M (2020) Expression of LhFT1, the flowering inducer of Asiatic hybrid lily, in the bulb scales. Front Plant Sci. https://doi.org/10.3389/fpls.2020.570915
Lazakis CM, Coneva V, Colasanti J (2011) ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. J Exp Bot 62(14):4833–4842
Le Nard M, De Hertogh A (1993) Bulb growth and development and flowering. Elsevier, Amsterdam
Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21(4):397–402. https://doi.org/10.1101/gad.1518407
Lee R, Baldwin S, Kenel F, McCallum J, Macknight R (2013) FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat Commun 4(1):1–9
Leeggangers HA, Nijveen H, Bigas JN, Hilhorst HW, Immink RG (2017) Molecular regulation of temperature-dependent floral induction in Tulipa gesneriana. Plant Physiol 173(3):1904–1919
Leeggangers HA, Rosilio-Brami T, Bigas-Nadal J, Rubin N, van Dijk AD, de Caceres N, Gonzalez FF, Saadon-Shitrit S, Nijveen H, Hilhorst HW, Immink RG (2018) Tulipa gesneriana and Lilium longiflorum PEBP genes and their putative roles in flowering time control. Plant Cell Physiol 59(1):90–106
Li Q, Fan C, Zhang X, Wang X, Wu F, Hu R, Fu Y (2014) Identification of a soybean MOTHER OF FT AND TFL1 homolog involved in regulation of seed germination. PLoS ONE 9(6):e99642. https://doi.org/10.1371/journal.pone.0099642
Lifschitz E, Ayre BG, Eshed Y (2014) Florigen and anti-florigen–a systemic mechanism for coordinating growth and termination in flowering plants. Front Plant Sci 5:465
Maurya JP, Miskolczi PC, Mishra S, Singh RK, Bhalerao RP (2020) A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen. Proc Natl Acad Sci USA 117(21):11523–11530. https://doi.org/10.1073/pnas.2004705117
Mimida N, Kotoda N, Ueda T, Igarashi M, Hatsuyama Y, Iwanami H, Moriya S, Abe K (2009) Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus× domestica Borkh). Plant Cell Physiol 50(2):394–412
Miskolczi P, Singh RK, Tylewicz S, Azeez A, Maurya JP, Tarkowska D, Novak O, Jonsson K, Bhalerao RP (2019) Long-range mobile signals mediate seasonal control of shoot growth. Proc Natl Acad Sci USA 116(22):10852–10857. https://doi.org/10.1073/pnas.1902199116
Mohamed R, Wang CT, Ma C, Shevchenko O, Dye SJ, Puzey JR, Etherington E, Sheng X, Meilan R, Strauss SH (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in populus. Plant J 62(4):674–688
Molina R, Valero M, Navarro Y, Guardiola JL, Garcia-Luis A (2005a) Temperature effects on flower formation in saffron (Crocus sativus L.). Sci Hortic 103(3):361–379. https://doi.org/10.1016/j.scienta.2004.06.005
Molina RV, Valero M, Navarro Y, Garcia-Luis A, Guardiola JL (2005b) Low temperature storage of corms extends the flowering season of saffron (Crocus sativus L.). J Hortic Sci Biotechnol 80(3):319–326. https://doi.org/10.1080/14620316.2005b.11511937
Moraes TS, Dornelas MC, Martinelli AP (2019) FT/TFL1: calibrating plant architecture. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00097
Navarro C, Abelenda JA, Cruz-Oro E, Cuellar CA, Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478(7367):119-U132. https://doi.org/10.1038/nature10431
Negbi M, Dagan B, Dror A, Basker D (1989) Growth, flowering, vegetative reproduction, and dormancy in the saffron crocus (Crocus sativus L.). Isr J Plant Sci 38(23):95–113. https://doi.org/10.1080/0021213X.1989.10677116
Noy-Porat T, Cohen D, Mathew D, Eshel A, Kamenetsky R, Flaishman MA (2013) Turned on by heat: differential expression of FT and LFY-like genes in Narcissus tazetta during floral transition. J Exp Bot 64(11):3273–3284. https://doi.org/10.1093/jxb/ert165
Patil HB, Chaurasia AK, Azeez A, Krishna B, Subramaniam VR, Sane AP, Sane PV (2018) Characterization of two TERMINAL FLOWER1 homologs PgTFL1 and PgCENa from pomegranate (Punica granatum L.). Tree Physiol 38(5):772–784. https://doi.org/10.1093/treephys/tpx154
Pin PA, Nilsson O (2012) The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ 35(10):1742–1755. https://doi.org/10.1111/j.1365-3040.2012.02558.x
Plantenga FD, Bergonzi S, Abelenda JA, Bachem CW, Visser RG, Heuvelink E, Marcelis LF (2019) The tuberization signal StSP6A represses flower bud development in potato. J Exp Bot 70(3):937–948
Renau-Morata B, Nebauer SG, García-Carpintero V, Cañizares J, Minguet EG, de los Mozos M, Molina RV (2021) Flower induction and development in saffron: timing and hormone signalling pathways. Ind Crops Prod 164:113370
Singh RK, Svystun T, AlDahmash B, Jonsson AM, Bhalerao RP (2017) Photoperiod- and temperature-mediated control of phenology in trees—a molecular perspective. New Phytol 213(2):511–524. https://doi.org/10.1111/nph.14346
Singh RK, Maurya JP, Azeez A, Miskolczi P, Tylewicz S, Stojkovic K, Delhomme N, Busov V, Bhalerao RP (2018) A genetic network mediating the control of bud break in hybrid aspen. Nat Commun. https://doi.org/10.1038/s41467-018-06696-y
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316(5827):1033–1036. https://doi.org/10.1126/science.1141753
Taoka K-i, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri YA, Tamaki S (2011a) 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476(7360):332–335
Taoka K, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri YA, Tamaki S, Ogaki Y, Shimada C, Nakagawa A, Kojima C, Shimamoto K (2011b) 14–3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476(7360):332–335. https://doi.org/10.1038/nature10272
Taoka K, Ohki I, Tsuji H, Kojima C, Shimamoto K (2013) Structure and function of florigen and the receptor complex. Trends Plant Sci 18(5):287–294. https://doi.org/10.1016/j.tplants.2013.02.002
Tribhuvan KU, Das A, Srivastava H, Kumar K, Durgesh K, Mithra SV, Jain PK, Gaikwad K (2020) Identification and characterization of PEBP family genes reveal CcFT8 a probable candidate for photoperiod insensitivity in C. Cajan. 3 Biotech 10(5):194. https://doi.org/10.1007/s13205-020-02180-x
Tsaftaris A, Pasentsis K, Kalivas A, Michailidou S, Madesis P, Argiriou A (2012) Isolation of a CENTRORADIALIS/TERMINAL FLOWER1 homolog in saffron (Crocus sativus L.): characterization and expression analysis. Mol Biol Rep 39(8):7899–7910
Tsaftaris A, Pasentsis K, Argiriou A (2013) Cloning and characterization of FLOWERING LOCUS T-like genes from the perennial geophyte saffron crocus (Crocus sativus). Plant Mol Biol Rep 31(6):1558–1568
Tsuji H, Nakamura H, Taoka K, Shimamoto K (2013) Functional diversification of FD transcription factors in rice, components of florigen activation complexes. Plant Cell Physiol 54(3):385–397. https://doi.org/10.1093/pcp/pct005
Wang M, Tan Y, Cai C, Zhang B (2019) Identification and expression analysis of phosphatidy ethanolamine-binding protein (PEBP) gene family in cotton. Genomics 111(6):1373–1380. https://doi.org/10.1016/j.ygeno.2018.09.009
Wang Z, Li X, Xu JX, Yang Z, Zhang YC (2021) Effects of ambient temperature on flower initiation and flowering in saffron (Crocus sativus L.). Sci Hortic. https://doi.org/10.1016/j.scienta.2020.109859
Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Mol Plant 8(7):983–997
Xi W, Liu C, Hou X, Yu H (2010) Mother of FT and TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 22(6):1733–1748
Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) Twin sister of FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46(8):1175–1189. https://doi.org/10.1093/pcp/pci151
Yang Z, Chen L, Kohnen MV, Xiong B, Zhen X, Liao J, Oka Y, Zhu Q, Gu L, Lin C, Liu B (2019) Identification and characterization of the PEBP family genes in moso bamboo (Phyllostachys heterocycla). Sci Rep 9(1):14998. https://doi.org/10.1038/s41598-019-51278-7
Yoo SY, Kardailsky I, Lee JS, Weigel D, Ahn JH (2004) Acceleration of flowering by overexpression of MFT (Mother of FT and TFL1). Mol Cells 17(1):95–101
Zhang X, Wang C, Pang C, Wei H, Wang H, Song M, Fan S, Yu S (2016) Characterization and functional analysis of PEBP family genes in upland cotton (Gossypium hirsutum L.). Plos One 11(8):e0161080. https://doi.org/10.1371/journal.pone.0161080
Zhang M, Li P, Yan X, Wang J, Cheng T, Zhang Q (2021) Genome-wide characterization of PEBP family genes in nine Rosaceae tree species and their expression analysis in P. mume. BMC Ecol Evol 21(1):32. https://doi.org/10.1186/s12862-021-01762-4
Zhu Y, Klasfeld S, Jeong CW, Jin R, Goto K, Yamaguchi N, Wagner D (2020) TERMINAL FLOWER 1-FD complex target genes and competition with FLOWERING LOCUS T. Nat Commun 11(1):1–12
Acknowledgements
We acknowledge the financial support by SERB-Startup Research Grant (SRG/2021/000562/LS) to Rajesh Kumar Singh. Junior Research Fellowship provided to Diksha Kalia (by UGC) and Joel Jose-Santhi (CSIR), India, is gratefully acknowledged. The manuscript represents the CSIR- IHBT communication number 4949.
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RKS conceptualized the idea. DK and JJS performed the experiments and data analysis. RK did the bioinformatics for sequence identification from online submitted data. All authors contributed to writing and reviewing the manuscript.
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Kalia, D., Jose-Santhi, J., Kumar, R. et al. Analysis of PEBP Genes in Saffron Identifies a Flowering Locus T Homologue Involved in Flowering Regulation. J Plant Growth Regul 42, 2486–2505 (2023). https://doi.org/10.1007/s00344-022-10721-2
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DOI: https://doi.org/10.1007/s00344-022-10721-2