Abstract
The star fruit is a perennial woody fruit tree, which can blossom and bear fruit many times a year. The time and quantity of flowering are the key indicators of its economic value. However, the flowering molecular mechanism of star fruit is still unknown. This study provides a genome-wide analysis of the key flowering genes of star fruit. Based on a previous morphological study of flower bud differentiation, the reproductive buds, vegetative buds and mature leaves of star fruit were sampled for transcriptome analysis. The results showed that the expression of GI, COL4, COL5, FT, FCA, FVE, PIF4, LFY, SVP-like, AP1 and FUL was correlated with floral induction and transition. The expression of TFL1, SVP-like genes (Yangtao2015203 and Yangtao2021074) was correlated with the inhibition of floral transition. Thus, we proposed a putative network of flower blooming in star fruit. This study provides useful information for investigating the genetic mechanism of flowering in star fruit and other perennial woody fruit trees.
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Data Availability
The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi.nlm. nih.gov/bioproject/PRJNA855616.
References
Argout X, Martin G, Droc G, Fouet O, Labadie K, Rivals E, Aury JM, Lanaud C (2017) The cacao Criollo genome v2.0: an improved version of the genome for genetic and functional genomic studies. BMC Genomics 18(1):730. https://doi.org/10.1186/s12864-017-4120-9
Bangerth KF (2009) Floral induction in mature, perennial angiosperm fruit trees: similarities and discrepancies with annual/biennial plants and the involvement of plant hormones. Sci Hortic 122(2):153–163. https://doi.org/10.1016/j.scienta.2009.06.014
Bao S, Hua C, Shen L, Yu H (2020) New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol 62(1):118–131. https://doi.org/10.1111/jipb.12892
Blázquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33(2):168–171. https://doi.org/10.1038/ng1085
Blümel M, Dally N, Jung C (2015) Flowering time regulation in crops—what did we learn from Arabidopsis? Curr Opin Biotechnol 32:121–129. https://doi.org/10.1016/j.copbio
Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape “green revolution” mutation. Nature 416(6883):847–850. https://doi.org/10.1038/416847a
Bouché F, Lobet G, Tocquin P, Périlleux C (2016) FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res 44(D1):D1167–D1171. https://doi.org/10.1093/nar/gkv1054
Carmona MJ, Calonje M, Martínez-Zapater JM (2007) The FT/TFL1 gene family in grapevine. Plant Mol Biol 63(5):637–650. https://doi.org/10.1007/s11103-006-9113-z
Carmona MJ, Cubas P, Martínez-Zapater JM (2002) VFL, the grapevine FLORICAULA/LEAFY ortholog, is expressed in meristematic regions independently of their fate. Plant Physiol 130(1):68–77. https://doi.org/10.1104/pp.002428
Choi K, Kim J, Hwang HJ, Kim S, Park C, Kim SY, Lee I (2011) The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23(1):289–303. https://doi.org/10.1105/tpc.110.075911
Falavigna VDS, Guitton B, Costes E, Andrés F (2019) I Want to (Bud) Break Free: The Potential Role of DAM and SVP-Like Genes in Regulating Dormancy Cycle in Temperate Fruit Trees. Front Plant Sci 9:1990. https://doi.org/10.3389/fpls.2018.01990
Fan CM, Wang X, Wang YW, Hu RB, Zhang XM, Chen JX, Fu YF (2013) Genome-wide expression analysis of soybean MADS genes showing potential function in the seed development. PLoS ONE 8(4):e62288. https://doi.org/10.1371/journal.pone
Ferreira JA (2007) The Benjamini-Hochberg method in the case of discrete test statistics. Int J Biostat 3(1):Article 11. https://doi.org/10.2202/1557-4679.1065
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39(Web Server issue):W29-W37. https://doi.org/10.1093/nar/gkr367
Freiman A, Golobovitch S, Yablovitz Z, Belausov E, Dahan Y, Peer R, Avraham L, Freiman Z, Evenor D, Reuveni M, Sobolev V, Edelman M, Shahak Y, Samach A, Flaishman MA (2015) Expression of flowering locus T2 transgene from Pyrus communis L. delays dormancy and leaf senescence in Malus×domestica Borkh, and causes early flowering in tobacco. Plant Sci 241:164–176. https://doi.org/10.1016/j.plantsci.2015.09.012
Fukushima K, Fang X, Alvarez-Ponce D, Cai H, Carretero-Paulet L, Chen C, Chang TH, Farr KM, Fujita T, Hiwatashi Y, Hoshi Y, Imai T, Kasahara M, Librado P, Mao L, Mori H, Nishiyama T, Nozawa M, Pálfalvi G, Pollard ST, Rozas J, Sánchez-Gracia A, Sankoff D, Shibata TF, Shigenobu S, Sumikawa N, Uzawa T, Xie M, Zheng C, Pollock DD, Albert VA, Li S, Hasebe M (2017) Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nat Ecol Evol 1(3):59. https://doi.org/10.1038/s41559-016-0059
Goldberg-Moeller R, Shalom L, Shlizerman L, Samuels S, Zur N, Ophir R, Blumwald E, Sadka A (2013) Effects of gibberellin treatment during flowering induction period on global gene expression and the transcription of flowering-control genes in Citrus buds. Plant Sci 198:46–57. https://doi.org/10.1016/j.plantsci.2012.09.012
Golicz AA, Steinfort U, Arya H, Singh MB, Bhalla PL (2020) Analysis of the quinoa genome reveals conservation and divergence of the flowering pathways. Funct Integr Genomics 20(2):245–258. https://doi.org/10.1007/s10142-019-00711-1
Goralogia GS, Howe GT, Brunner AM, Helliwell E, Nagle MF, Ma C, Lu H, Goddard AL, Magnuson AC, Klocko AL, Strauss SH (2021) Overexpression of SHORT VEGETATIVE PHASE-LIKE (SVL) in Populus delays onset and reduces abundance of flowering in field-grown trees. Hortic Res 8(1):167. https://doi.org/10.1038/s41438-021-00600-4
Grimplet J, Martínez-Zapater JM, Carmona MJ (2016) Structural and functional annotation of the MADS-box transcription factor family in grapevine. BMC Genomics 17:80. https://doi.org/10.1186/s12864-016-2398-7
Gu X, Le C, Wang Y, Li Z, Jiang D, Wang Y, He Y (2013) Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat Commun 4:1947. https://doi.org/10.1038/ncomms2947
Han X, Yu H, Yuan R, Yang Y, An F, Qin G (2019) Arabidopsis Transcription Factor TCP5 Controls Plant Thermomorphogenesis by Positively Regulating PIF4 Activity. iScience 15:611–622. https://doi.org/10.1016/j.isci.2019.04.005
Hassidim M, Harir Y, Yakir E, Kron I, Green RM (2009) Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis. Planta 230(3):481–491. https://doi.org/10.1007/s00425-009-0958-7
Helliwell CA, Wood CC, Robertson M, James Peacock W, Dennis ES (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J 46(2):183–192. https://doi.org/10.1111/j.1365-313X.2006.02686.x
Hu G, Kurgan L (2019) Sequence Similarity Searching. Curr Protoc Protein Sci 95(1):e71. https://doi.org/10.1002/cpps.71
Igasaki T, Watanabe Y, Nishiguchi M, Kotoda N (2008) The FLOWERING LOCUS T/TERMINAL FLOWER 1 family in Lombardy poplar. Plant Cell Physiol 49(3):291–300. https://doi.org/10.1093/pcp/pcn010
Jin S, Ahn JH (2021) Regulation of flowering time by ambient temperature: repressing the repressors and activating the activators. New Phytol 230(3):938–942. https://doi.org/10.1111/nph.17217
Jung JH, Lee HJ, Ryu JY, Park CM (2016) SPL3/4/5 Integrate Developmental Aging and Photoperiodic Signals into the FT-FD Module in Arabidopsis Flowering. Mol Plant 9(12):1647–1659. https://doi.org/10.1016/j.molp.2016.10.014
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360. https://doi.org/10.1038/nmeth.3317
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484(7393):242–245. https://doi.org/10.1038/nature10928
Lagercrantz U, Axelsson T (2000) Rapid evolution of the family of CONSTANS LIKE genes in plants. Mol Biol Evol 17(10):1499–1507. https://doi.org/10.1093/oxfordjournals.molbev.a026249
Lakmal K, Yasawardene P, Jayarajah U, Seneviratne SL (2021) Nutritional and medicinal properties of Star fruit (Averrhoa carambola): A review. Food Sci Nutr 9(3):1810–1823. https://doi.org/10.1002/fsn3.2135
Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61(9):2247–2254. https://doi.org/10.1093/jxb/erq098
Lee JH, Ryu HS, Chung KS, Posé D, Kim S, Schmid M, Ahn JH (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342(6158):628–632. https://doi.org/10.1126/science.1241097
Lent R (1966) The origin of the cauliflorous inflorescence of Theobroma cacao. Turrialba (IICA) v, 16: 352–358
Li D, Liu C, Shen L, Wu Y, Chen H, Robertson M, Helliwell CA, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15(1):110–120. https://doi.org/10.1016/j.devcel.2008.05.002
Li XF, Jia LY, Xu J, Deng XJ, Wang Y, Zhang W, Zhang XP, Fang Q, Zhang DM, Sun Y, Xu L (2013) FT-like NFT1 gene may play a role in flower transition induced by heat accumulation in Narcissus tazetta var. chinensis. Plant Cell Physiol 54(2):270–281. https://doi.org/10.1093/pcp/pcs181
Li XF, Wu WT, Zhang XP, Qiu Y, Zhang W, Li R, Xu J, Sun Y, Wang Y, Xu L (2015) Narcissus tazetta SVP-like gene NSVP1 affects flower development in Arabidopsis. J Plant Physiol 173:89–96. https://doi.org/10.1016/j.jplph.2014.08.017
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7):923–930. https://doi.org/10.1093/bioinformatics/btt656
Liu C, Teo ZW, Bi Y, Song S, Xi W, Yang X, Yin Z, Yu H (2013) A conserved genetic pathway determines inflorescence architecture in Arabidopsis and rice. Dev Cell 24(6):612–622. https://doi.org/10.1016/j.devcel.2013.02.013
Liu X, Sun Z, Dong W, Wang Z, Zhang L (2018) Expansion and Functional Divergence of the SHORT VEGETATIVE PHASE (SVP) Genes in Eudicots. Genome Biol Evol 10(11):3026–3037. https://doi.org/10.1093/gbe/evy235
Lü J, Suo H, Yi R, Ma Q, Nian H (2015) Glyma11g13220, a homolog of the vernalization pathway gene VERNALIZATION 1 from soybean [Glycine max (L.) Merr.], promotes flowering in Arabidopsis thaliana. BMC Plant Biol 15:232. https://doi.org/10.1186/s12870-015-0602-6
Madueño F, Ruiz Garcia L, Wilkinson M, Haughn G, Salinas J, Martinez Zapater J (1996) Different roles of flowering time genes in the activation of floral initiation genes in Arabidopsis. Int J Dev Biol Suppl 1:125S-126S
Meng X, Li Y, Yuan Y, Zhang Y, Li H, Zhao J, Liu M (2020) The regulatory pathways of distinct flowering characteristics in Chinese jujube. Hortic Res 7:123. https://doi.org/10.1038/s41438-020-00344-7
Mohd Suhaimi NI, Mat Ropi AA, Shaharuddin S (2021) Safety and quality preservation of starfruit (Averrhoa carambola) at ambient shelf life using synergistic pectin-maltodextrin-sodium chloride edible coating. Heliyon 7(2):e06279. https://doi.org/10.1016/j.heliyon.2021.e06279
Moyroud E, Kusters E, Monniaux M, Koes R, Parcy F (2010) LEAFY blossoms. Trends Plant Sci 15(6):346–352. https://doi.org/10.1016/j.tplants.2010.03.007
Muñoz-Fambuena N, Mesejo C, González-Mas MC, Iglesias DJ, Millo EP, Agustí M (2012) Gibberellic acid reduces flowering intensity in sweet orange [Citrus sinensis (L.) Osbeck] by Repressing CiFT Gene Expression. J Plant Growth Regul 31:529–536. https://doi.org/10.1007/s00344-012-9263-y
Nunez-Elisea R, Crane JH (2000) Selective pruning and crop removal increase early-season fruit production of carambola (Averrhoa carambola L.). Sci Hortic 86(2): 115–126. https://doi.org/10.1016/S0304-4238(00)00141-2
Oliveira GP, Angelotti-Mendonça J, Tanaka F, Silva S, Filho JS (2019) Origin and development of reproductive buds in jabuticaba cv. Sabará (Plinia jaboticaba Vell). Sci Hortic 249:432–438. https://doi.org/10.1016/j.scienta.2019.02.020
Owens S, Ewers F (2011) The development of cauliflory in redbud, Cercis canadensis (Fabaceae). Can J Bot 69(9):1956–1963. https://doi.org/10.1139/b91-245
Peña L, Martín-Trillo M, Juárez J, Pina JA, Navarro L, Martínez-Zapater JM (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat Biotechnol 19(3):263–267. https://doi.org/10.1038/85719
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
Reinecke DM, Wickramarathna AD, Ozga JA, Kurepin LV, Jin AL, Good AG, Pharis RP (2013) Gibberellin 3-oxidase gene expression patterns influence gibberellin biosynthesis, growth, and development in pea. Plant Physiol 163(2):929–945. https://doi.org/10.1104/pp.113.225987
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288(5471):1613–1616. https://doi.org/10.1126/science.288.5471.1613
Shim JS, Kubota A, Imaizumi T (2017) Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration. Plant Physiol 173(1):5–15. https://doi.org/10.1104/pp.16.01327
Song YH (2016) The Effect of Fluctuations in Photoperiod and Ambient Temperature on the Timing of Flowering: Time to Move on Natural Environmental Conditions. Mol Cells 39(10):715–721. https://doi.org/10.14348/molcells.2016.0237
Southerton SG, Strauss SH, Olive MR, Harcourt RL, Decroocq V, Zhu X, Llewellyn DJ, Peacock WJ, Dennis ES (1998) Eucalyptus has a functional equivalent of the Arabidopsis floral meristem identity gene LEAFY. Plant Mol Biol 37(6):897–910. https://doi.org/10.1023/a:1006056014079
Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68(12):2013–2037. https://doi.org/10.1007/s00018-011-0673-y
Wada M, Cao QF, Kotoda N, Soejima J, Masuda T (2002) Apple has two orthologues of FLORICAULA/LEAFY involved in flowering. Plant Mol Biol 49(6):567–577. https://doi.org/10.1023/a:1015544207121
Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339(6120):704–707. https://doi.org/10.1126/science.1230406
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749. https://doi.org/10.1016/j.cell.2009.06.014
Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138. https://doi.org/10.1093/bioinformatics/btp612
Wang YH, Xie L, Yang B, Cao YR, Li YH (2019) Flowering genes in oilseed rape: identification, characterization, evolutionary and expression analysis. Acta Agron Sin 45(8):1137–1145. https://doi.org/10.3724/SP.J.1006.2019.84159
Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends Genet 26(12):519–527. https://doi.org/10.1016/j.tig.2010.09.001
Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER1 Gene Family: Functional Evolution and Molecular Mechanisms. Mol Plant 8(7):983–997. https://doi.org/10.1016/j.molp.2015.01.007
Wu S, Sun W, Xu Z, Zhai J, Li X, Li C, Zhang D, Wu X, Shen L, Chen J, Ren H, Dai X, Dai Z, Zhao Y, Chen L, Cao M, Xie X, Liu X, Peng D, Dong J, Hsiao YY, Chen SL, Tsai WC, Lan S, Liu ZJ (2020) The genome sequence of star fruit (Averrhoa carambola). Hortic Res 7(1):95. https://doi.org/10.1038/s41438-020-0307-3
Wu, PP, Zhou BY (2007) Differentiation of flower buds and changes in carbohydrate content of Averrhoa carambola. Acta Horticulturae Sinica, 34(5): 1151–1156. https://doi.org/10.16420/j.issn.0513-353x.2007.05.018 (in chinese)
Yu Q, Moore PH, Albert HH, Roader AH, Ming R (2005) Cloning and characterization of a FLORICAULA/LEAFY ortholog, PFL, in polygamous papaya. Cell Res 15(8):576–584. https://doi.org/10.1038/sj.cr.7290327
Zhang S, Gottschalk C, van Nocker S (2019) Genetic mechanisms in the repression of flowering by gibberellins in apple (Malus x domestica Borkh.). BMC Genomics 20(1):747. https://doi.org/10.1186/s12864-019-6090-6
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We thank Professor Baoming Feng (Plant Immunity Center, Fujian Agriculture and Forestry University) for manuscript revising.
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This work was financially supported by Basic Scientific Research for Special Projects of Guangxi Academy of Agricultural Sciences, China (Grant No. 2021YT046), Disciplinary Professional Construction Project of College of Art & College of Landscape Architecture, Fujian Agriculture and Forestry University (Grant No. YSYL-kjtd-1) and 2019 Fujian Agriculture and Forestry University "Rural Revitalization Service Team" Support Program Project (Grant No. 11899170124).
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SW, JZ, ZL and XL conceived and designed the experiments; SQ wrote the article with contributions of all the authors; CW, LY, DP and SA revised the article; HR collected samples and provided technical support. All authors read and approved the final manuscript.
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Qin, S., Li, XP., Wu, CM. et al. Genome-wide Transcriptome Analysis Reveals the Gene Regulatory Network in Star Fruit Flower Blooming. Tropical Plant Biol. 16, 1–11 (2023). https://doi.org/10.1007/s12042-022-09322-w
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DOI: https://doi.org/10.1007/s12042-022-09322-w