Abstract
Flowering is the change from the vegetative state to the reproductive state. Flowering initiation is regulated by endogenous genetic components and by numerous environmental factors. These stimuli determine the different molecular mechanisms that are required to give way to flowering and vary according to the dose of the stimulus and the crop used. Jatropha curcas is a perennial shrub that produces oil from its seeds of adequate quality to be transformed into biofuels. However, this plant still presents limitations for its establishment as a commercial crop since it produces low seeds, which can be attributed to its low production of female flowers. This plant also presents multiple and asynchronous flowering periods as a consequence of the accession and of the climatic conditions, which implies that the fruits do not ripen synchronously, and therefore the harvests are constant, manual, and expensive. Knowing the mechanisms that regulate the flowering of J. curcas is important to improve its seed production. Therefore, current revision covers the analysis of genes involved in flowering to gain information on the pathways involved in floral transition and in the differentiation of the sexual organs of J. curcas.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated during the study are included in this published article.
References
Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365. https://doi.org/10.1242/dev.01206
Adriano-Anaya ML, Pérez-Castillo E, Salvador-Figueroa M, Ruiz-González S, Vázquez-Ovando A, Grajales-Conesa J, Ovando-Medina I (2016) Sex expression and floral diversity in Jatropha curcas: a population study in its center of origin. PeerJ 4:e2071. https://doi.org/10.7717/peerj.2071
Ahsan MU, Hayward A, Irihimovitch V, Fletcher SJ, Tanurdzic M, Pocock A, Beveridge CA, Mitter N (2019) Juvenility and vegetative phase transition in tropical/subtropical tree crops. Front Plant Sci 10:729. https://doi.org/10.3389/fpls.2019.00729
Alam NCN, Abdullah TL, Nur APA, Abdullah NA (2011) Flowering and fruit set under Malaysian climate of Jatropha curcas L. J Agric Biol Sci 6:142–147. https://doi.org/10.3844/ajabssp.2011.142.147
Alonso- Peral MM, Li J, Li Y, Allen RS, Schnippenkoetter W, Ohms S, White RG, Millar AA (2010) The MicroRNA159-regulated GAMYB-like genes inhibit growth and promote programmed Cell Death in Arabidopsis. Plant Physiol 154:757–771. https://doi.org/10.1104/pp.110.160630
Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 1:627–639. https://doi.org/10.1038/nrg3291
Andrés F, Porri A, Torti S, Mateos J, Romera-Branchat M, Garcia-Martinez JL et al (2014) SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition. Proc Natl Acad Sci USA 111:E2760–E2769. https://doi.org/10.1073/pnas.1409567111
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15(11):2730–2741. https://doi.org/10.1105/tpc.016238
Ausin I, Alonso-Blanco C, Martínez-Zapater JM (2005) Environmental regulation of flowering. Int J Dev Biol 49(5–6):689–705. https://doi.org/10.1387/ijdb.052022ia
Azizi P, Rafii MY, Maziah M, Abdullah SNA, Hanafi MM, Latif MA, Rashid AA, Sahebi M (2015) Understanding the shoot apical meristem regulation: A study of the phytohormones, auxin and cytokinin, in rice. Mech Dev 135:1–15. https://doi.org/10.1016/j.mod.2014.11.001
Barazesh S, McSteen P (2008) Hormonal control of grass inflorescence development. Trends Plant Sci 13(12):656–662. https://doi.org/10.1016/j.tplants.2008.09.007
Bartrina I, Otto E, Strnad M, Werner T, Schmulling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23(1):69–80. https://doi.org/10.1105/tpc.110.079079
Bennett S, Alvarez J, Bossinger G (1995) Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J 8(4):505–2098. https://doi.org/10.1046/j.1365-313X.1995.8040505.x
Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10(5):791–800. https://doi.org/10.1105/tpc.10.5.791
Blümel M, Dally N, Jung C (2015) Flowering time regulation in crops-what did we learn from Arabidopsis? Curr Opin Biotechno 32:121–129. https://doi.org/10.1016/j.copbio.2014.11.023
Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Robert A (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408(6815):967–971. https://doi.org/10.1038/35050091
Chen X (2004) MicroRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666):2022–2025. https://doi.org/10.1126/science.1088060
Chen MS, Pan BZ, Wang GJ, Ni J, Niu L, Xu ZF (2014) Analysis of the transcriptional responses in inflorescence buds of Jatropha curcas exposed to cytokinin treatment. BMC Plant Biol 14:318. https://doi.org/10.1186/s12870-014-0318-z
Chen MS, Pan BZ, Fu Q, Tao YB, Martínez-Herrera J, Niu L, Ni J, Dong Y, Zhao ML, Xu ZF (2017) Comparative transcriptome analysis between gynoecious and monoecious plants identifies regulatory networks controlling sex determination in Jatropha curcas. Front Plant Sci 17(7):1953. https://doi.org/10.3389/fpls.2016.01953
Chen Y, Wu P, Zhao Q, Tang Y, Chen Y, Li M, Jiang H, Wu G (2018) Overexpression of a phosphate starvation response AP2/ERF gene from physic nut in Arabidopsis alters root morphological traits and phosphate starvation-induced anthocyanin accumulation. Front Plant Sci 9:1186. https://doi.org/10.3389/fpls.2018.01186
Chen MS, Zhao ML, Wang GJ, He HY, Bai X, Pan BZ, Fu QT, Tao YB, Tang MY, Martínez-Herrera J, Xu ZF (2019) Transcriptome analysis of two inflorescence branching mutants reveals cytokinin is an important regulator in controlling inflorescence architecture in the woody plant Jatropha curcas. BMC Plant Biol 19(1):1–16. https://doi.org/10.1186/s12870-019-2069-3
Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D et al (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064. https://doi.org/10.1242/dev.00992
Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18(2):412–421. https://doi.org/10.1105/tpc.105.038943
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353(6339):31–37. https://doi.org/10.1038/353031a0
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. https://doi.org/10.1126/science.1141752
D’Aloia M, Bonhomme D, Bouche F, Tamseddak K, Ormenese S, Torti S, Coupland G, Perilleux C (2011) Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 65(6):972–979. https://doi.org/10.1111/j.1365-313X.2011.04482.x
Davière JM, Achard P (2013) Gibberellin Signaling in Plants Development 140(6):1147–1151. https://doi.org/10.1242/dev.087650
De Lucas M et al (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451(7177):480–484. https://doi.org/10.1038/nature06520
Djami AT, Sanan N, Ntushelo K, Dubery IA (2017) Functional roles of microRNAs in agronomically important plants-potential as targets for crop improvement and protection. Front Plant Sci 8:378. https://doi.org/10.3389/fpls.2017.00378
Dong B, Deng Y, Wang H, Gao R, Stephen GUK, Chen S, Jiang J, Chen F (2017) Gibberellic acid signaling is required to induce flowering of chrysanthemums grown under both short and long days. Int J Mol Sci 18(6):1259. https://doi.org/10.3390/ijms18061259
Evans MM, Poehtig RS (1995) Gibberellins promote vegetative phase change and reproductive maturity in maize. Plant Physiol 108(2):475–487. https://doi.org/10.1104/pp.108.2.475
Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of auxin response factor3 by TAS3ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16(9):939–944. https://doi.org/10.1016/j.cub.2006.03.065
Fang Y, Spector DL (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr Biol 17(9):818–823. https://doi.org/10.1016/j.cub.2007.04.005
Freytes SN, Canelo M, Cerdán PD (2021) Regulation of flowering time: when and where? Curr Opin Plant Biol 63:102049. https://doi.org/10.1016/j.pbi.2021.102049
Fujiwara S, Oda A, Yoshida R, Niinuma K, Miyata K, Tomozoe Y et al (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell 20(11):2960–2971. https://doi.org/10.1105/tpc.108.061531
Galli V, Guzman F, Oliveira LFV, Moraise GL, Korbes AP, Silva DA, Pinheiro MMANM, Margis R (2014) Identifying microRNAs and transcript targets in Jatropha seeds. PLoS ONE 9(2):e83727. https://doi.org/10.1371/journal.pone.0083727
Galvão VC, Horrer D, Küttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development 139(21):4072–4082. https://doi.org/10.1242/dev.080879
Gangwar M, Shankar J (2020) Molecular mechanisms of the floral biology of Jatropha curcas: opportunities and challenges as an energy crop. Front Plant Sci 11:609. https://doi.org/10.3389/fpls.2020.00609
Gangwar M, Sood H, Chauhan RS (2016) Genomics and relative expression analysis identifies key genes associated with high female to male flower ratio in Jatropha curcas L. Mol Biol Rep 43(4):305–322. https://doi.org/10.1007/s11033-016-3953-7
Gao CC, Ni J, Chen MS, Xu ZF (2015) Characterization of genes involved in gibberellin metabolism and signaling pathway in the biofuel plant Jatropha curcas. Plant Diversity 37(2):157–167. https://doi.org/10.7677/ynzwyj201514076
Ghosh A, Chikara J, Chaudhary DR, Prakash AR, Boricha G, Zala A (2010) Paclobutrazol arrests vegetative growth and unveils unexpressed yield potential of Jatropha curcas. J Plant Growth Regul 29:307–315. https://doi.org/10.1007/s00344-010-9137-0
Goslin K, Zheng B, Serrano-Mislata A, Rae L, Ryan PT, Kwaśniewska K, Thomson B, Ó’Maoiléidigh DS, Madueño F, Wellmer F, Graciet E (2017) Transcription factor interplay between LEAFY and APETALA1/CAULIFLOWER during floral initiation. Plant Physiol 174(2):1097–1109. https://doi.org/10.1104/pp.17.00098
Goto K, Kyozuka J, Bowman JL (2001) Turning floral organs into leaves, leaves into floral organs. Curr Opin Gen Dev 11(4):449–456. https://doi.org/10.1016/s0959-437x(00)00216-1
Gras DE, Vidal EA, Undurraga SF, Riveras E, Moreno S, Dominguez-Figueroa J, Alabadi D, Blázquez MA, Medina J, Gutiérrez RA (2018) SMZ/SNZ and gibberellin signaling are required for nitrate-elicited delay of flowering time in Arabidopsis thaliana. J Exp Bot 69(3):619–631. https://doi.org/10.1093/jxb/erx423
Gupta S, Malviya N, Kushwaha H, Nasim J, Bisht NC, Singh V, Yadav D (2015) Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta 241(3):549–562. https://doi.org/10.1007/s00425-014-2239-3
Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385. https://doi.org/10.1023/A:1015207114117
Hartmann U, Höhmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21(4):351–360. https://doi.org/10.1046/j.1365-313x.2000.00682.x
Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530. https://doi.org/10.1016/S1360-1385(00)01790-8
Honma T, Goto K (2001) Complexes of MADS - box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529. https://doi.org/10.1038/35054083
Hu YX, Tao YB, Xu ZF (2017) Overexpression of Jatropha gibberellin 2-oxidase 6 (JCGA2OX6) induces dwarfism and smaller leaves, flowers and fruits in Arabidopsis and Jatropha. Front Plant Sci 8:2103. https://doi.org/10.3389/fpls.2017.02103
Hui W, Yang Y, Wu G, Peng C, Chen X, Zayed MZ (2017) Transcriptome profile analysis reveals the regulation mechanism of floral sex differentiation in Jatropha curcas L. Sci Rep 7(1):16421. https://doi.org/10.1038/s41598-017-16545-5
Hui WK, Wang Y, Chen XY, Zayed MZ, Wu GJ (2018) Analysis of transcriptional responses of the inflorescence meristems in Jatropha curcas following gibberellin treatment. Int J Mol Sci 19:432. https://doi.org/10.3390/ijms19020432
Hui WK, Liu MQ, Wu GJ, Wang JY, Zhong Y, Li HY, Tang HL, Zeng W, Ma LX, Zhang Y, **ang L, Chen XY, Gong W (2021) Ectopic expression of an AGAMOUS homologue gene in Jatropha curcas causes early flowering and heterostylous phenotypes. Gene 766:145141. https://doi.org/10.1016/j.gene.2020.145141
Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138(19):4117–4129. https://doi.org/10.1242/dev.063511
Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309(5732):293–297. https://doi.org/10.1126/science.1110586
Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17(12):1050–1054. https://doi.org/10.1016/j.cub.2007.05.008
Jang S, Torti S, Coupland G (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J 60(4):614–625. https://doi.org/10.1111/j.1365-313X.2009.03986.x
** D, Wang Y, Zhao Y, Chen M (2013) MicroRNAs and their cross-talks in plant development. J Genet Genomics 40(4):161–170. https://doi.org/10.1016/j.jgg.2013.02.003
Joshi G, Shukla A, Shukla A (2011) Synergistic response of auxin and ethylene on physiology of Jatropha curcas L. Braz J Plant Physiol 23:66–77. https://doi.org/10.1590/s1677-04202011000100009
Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007) The Gigantea-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19(9):2736–2748. https://doi.org/10.1105/tpc.107.054528
Jung JH, Ju Y, Seo PJ, Lee JH, Park CM (2012) The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. Plant J 69(4):577–588. https://doi.org/10.1111/j.1365-313X.2011.04813.x
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
Kant S, Rothstein S (2009) Auxin-responsive SAUR39 gene modulates auxin level in rice. Plant Signal Behav 4(12):1174–1175. https://doi.org/10.4161/psb.4.12.10043
Kant S, Bi YM, Zhu T, Rothstein SJ (2009) SAUR39, a small auxin-up RNA gene, acts as a negative regulator of auxin synthesis and transport in rice. Plant Physiol 151:691–701. https://doi.org/10.1104/pp.109.143875
Karlgren A, Gyllenstrand N, Clapham D, Lagercrantz U (2013) FLOWERING LOCUS T/TERMINAL FLOWER1-like genes affect growth rhythm and bud set in Norway spruce. Plant Physiol 163:792–803. https://doi.org/10.1104/pp.113.224139
Kim DH, Sung S (2013) Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis. Plant Cell 25(2):454–469. https://doi.org/10.1105/tpc.112.104760
Kim W, Ahn HJ, Chiou TJ, Ahn JH (2011) The role of the miR399-PHO2 module in the regulation of flowering time in response to different ambient temperatures in Arabidopsis thaliana. Mol Cells 32(1):83–88. https://doi.org/10.1007/s10059-011-1043-1
Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH (2012) The microrNA156-SQUAMOSA promoter binding protein-like3 module regulates ambient temperature-responsive flowering via flowering locus in Arabidopsis. Plant Physiol 159(1):461–478. https://doi.org/10.1104/pp.111.192369
Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev 11(9):597–610. https://doi.org/10.1038/nrg2843
Kruszka K, Pieczynski M, Windels D, Bielewicz D, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F (2012) Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169(16):1664–1672. https://doi.org/10.1016/j.jplph.2012.03.009
Kumar A, Sharma S (2008) An evaluation of multipurpose oil seed crop for industrial uses (Jatropha curcas L): are view. Ind Crops Prod 28:1–10. https://doi.org/10.1016/j.indcrop.2008.01.001
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
Kyozuka J (2007) Control of shoot and root meristem function by cytokinin. Curr Opin Plant Biol 10(5):442–446. https://doi.org/10.1016/j.pbi.2007.08.010
Lau S, Jürgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20(7):1738–1746. https://doi.org/10.1105/tpc.108.060418
Lee J, Oh M, Park H, Lee I (2008a) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates LEAFY. Plant J 55(5):832–843. https://doi.org/10.1111/j.1365-313X.2008.03552.x
Lee S, Choi SC, An G (2008b) Rice SVP-group MADS-box proteins, OsMADS22 and OsMADS55, are negative regulators of brassinosteroid responses. Plant J 54(1):93–105. https://doi.org/10.1111/j.1365-313X.2008.03406.x
Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38(9):3081–3093. https://doi.org/10.1093/nar/gkp1240
Li C, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55(4):543–554. https://doi.org/10.1111/j.1365-313X.2008.03526.x
Li C, Zhang B (2016) MicroRNAs in control of plant development. J Cell Physiol 231(2):303–313. https://doi.org/10.1002/jcp.25125
Li X, Bian H, Song D, Ma S, Han N, Wang J, Zhu M (2013) Flowering time control in ornamental gloxinia (Sinningia speciosa) by manipulation of miR159 expression. Ann Bot 111(5):791–799. https://doi.org/10.1093/aob/mct034
Li C, Luo L, Fu Q, Niu L, Xu ZF (2014) Isolation and functional characterization of JcFT, a flowering LOCUST (FT) homologous gene from the biofuel plant Jatropha curcas. BMCP Plant Biol 14:125. https://doi.org/10.1186/1471-222914-125
Li C, Luo L, Fu Q, Niu L, Xu ZF (2015) Identification and characterization of the FT/TFL1 gene family in the biofuel plant Jatropha curcas. Plant Mol Biol Rep 33(2):326–333. https://doi.org/10.1007/s11105-014-0747-8
Li C, Fu Q, Niu L, Luo L, Chen J, Xu ZF (2017) Three TFL1 homologues regulate floral initiation in the biofuel plant Jatropha curcas. Sci Rep 7:43090. https://doi.org/10.1038/srep43090
Li J, Gao X, Sang S, Liu C (2019) Genome-wide identification, phylogeny, and expression analysis of the SBP-box gene family in Euphorbiaceae. BMC Genomics 20:1–15. https://doi.org/10.1186/s12864-019-6319-4
Li M, Yu G, Cao C, Liu P (2021) Metabolism, signaling, and transport of jasmonates. Plant Commun 2(5):1–14. https://doi.org/10.1016/j.xplc.2021.100231
Li C, Xu M, Cai X, Han Z, Si J, Chen D (2022) Jasmonate signaling pathway modulates plant defense, growth, and their trade-offs. Int J Mol Sci 23(7):3945. https://doi.org/10.3390/ijms23073945
Liu H, Yu X, Li K, Klejnot J, Yang H et al (2008a) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322(5907):1535–1539. https://doi.org/10.1126/science.1163927
Liu LJ, Zhang YC, Li QH, Sang Y, Mao J, Lian HL, Wang L, Yang HQ (2008b) COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20(2):292–306. https://doi.org/10.1105/tpc.107.057281
Liu T, Li Y, Ren J, Qian Y, Yang X, Duan W, Hou X (2013a) Nitrate or NaCl regulates floral induction in Arabidopsis thaliana. Biologia 68:215–222. https://doi.org/10.2478/s11756-013-0004-x
Liu Z, Wu Y, Yang F, Zhang Y, Chen S, **e Q, Tian X, Zhou JM (2013b) BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc Natl Acad Sci USA 110(15):6205–6210. https://doi.org/10.1073/pnas.1215543110
Luo Y, Guo Z, Li L (2013) Evolutionary conservation of microRNA regulatory programs in plant flower development. Dev Biol 380(2):133–144. https://doi.org/10.1016/j.ydbio.2013.05.009
MacMillan J (2001) Occurrence of gibberellins in vascular plants, fungi, and bacteria. J Plant Growth Regul 20(4):387–442. https://doi.org/10.1007/s003440010038
Makwana V, Shukla P, Robin P (2010) GA application induces alteration in sex ratio and cell death in Jatropha curcas. Plant Growth Regul 61(2):121–125. https://doi.org/10.1007/s10725-010-9457-x
McClure BA, Guilfoyle TJ (1987) Characterization of a class of small auxin-inducible soybean polyade- nylated RNAs. Plant Mol Biol 9:611–623. https://doi.org/10.1007/BF00020537. PMID: 24277197
Michaels SD, Amasino RM (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13(4):935–941. https://doi.org/10.1105/tpc.13.4.935
Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137(1):149–156. https://doi.org/10.1104/pp.104.052811
Mockler T, Yang H, Yu X, Parikh D, Cheng Y, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci USA 100(4):2140–2145. https://doi.org/10.1073/pnas.0437826100
Nakamura M, Mozgova I, Hennig L (2017) Lost memories of winter: breaking the FLC silence. Mol Plant 10(12):1477–1479. https://doi.org/10.1016/j.molp.2017.11.009
Okada K, Ueda J, Komaki MK, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3(7):677–684. https://doi.org/10.1105/tpc.3.7.677
Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94(13):7076–7081. https://doi.org/10.1073/pnas.94.13.7076
Osnato M, Castillejo C, Matías-Hernández L, Pelaz S (2012) TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nat Commun 3:808. https://doi.org/10.1038/ncomms1810
Pan BZ, Chen MS, Ni J, Xu ZF (2014) Transcriptome of the inflorescence meristems of the biofuel plant Jatropha curcas treated with cytokinin. BMC Genomics 15(1):974. https://doi.org/10.1186/1471-216415-974
Pi XJ, Pan BZ, Xu ZF (2013) Induction of bisexual flowers by gibberellin in monoecious biofuel plant Jatropha curcas (Euphorbiaceae). Plant Divers Resour 35:26–32. https://doi.org/10.7677/ynzwyj201312063
Porri A, Torti S, Romera-Branchat M, Coupland G (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development 139(12):2198–2209. https://doi.org/10.1242/dev.077164
Radhamani J, Sivaraj N (2012) Chapter 24. Conservation strategies and management of Jatropha germplasm. In: Carels N, Sujatha M, Bahadur B (eds) Jatropha, challenges for a new energy crop (Vol. 1). Springer, NewYork, pp 479–500. https://doi.org/10.1007/978-1-4614-4806-8
Raza A, Charagh S, Zahid Z et al (2021) Jasmonic acid: a key frontier in conferring abiotic stress tolerance in plants. Plant Cell Rep 40:1513–1541. https://doi.org/10.1007/s00299-020-02614-z
Rijpkema AS, Vandenbussche M, Koes R, Heijmans K, Gerats T (2010) Variations on a theme: changes in the floral ABCs in angiosperms. Semin Cell Dev Biol 21(1):100–107. https://doi.org/10.1016/j.semcdb.2009.11.002
Rubio SI, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16(5):258–264. https://doi.org/10.1016/j.tplants.2011.03.001
Sánchez A, Ovando I, Adriano L, Vázquez A, Salvador M (2018) Dynamics of miR156 and miR172 involved in the flowering of Jatropha curcas L. Acta Bot Brasil 32(1):99–106. https://doi.org/10.1590/0102-33062017abb0179
Sato S et al (2011) Sequence analysis of the genome of an oil-bearing tree. Jatropha Curcas l DNA Research 18(1):65–76. https://doi.org/10.1093/dnares/dsq030
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318(5848):261–265. https://doi.org/10.1126/science.1146994
Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohman JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130(24):6001–6012. https://doi.org/10.1242/dev.00842
Seesangboon A, Gruneck L, Pokawattana T, Eungwanichayapant PD, Tovaranonte J, Popluechai S (2018) Transcriptome analysis of Jatropha curcas L flower buds responded to the paclobutrazol treatment. Plant Physiol Biochem 127:276–286. https://doi.org/10.1016/j.plaphy.2018.03.035
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
Siriwardana NS, Lamb RS (2012) The poetry of reproduction: the role of LE FY in Arabidopsis thaliana flower formation. Int J Dev Biol 56:207–221. https://doi.org/10.1387/ijdb.113450ns
Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, **e D (2011) The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23(3):1000–1013. https://doi.org/10.1105/tpc.111.083089
Song YH, Lee I, Lee SY, Imaizumi T, Hong JC (2012) CONSTANS and ASYMMETRIC LEAVES 1 complex is involved in the induction of FLOWERING LOCUS T in photoperiodic flowering in Arabidopsis. Plant J 69(2):332–342. https://doi.org/10.1111/j.1365-313X.2011.04793.x
Song J, Chen MS, Li JL, Niu LJ, Xu ZF (2013a) Effects of soil-applied paclobutrazol on the vegetative and reproductive growth of biofuel plant Jatropha curcas. Plant Divers Resour 35(2):173–179. https://doi.org/10.7677/ynzwyj201312086
Song YH, Ito S, Imaizumi T (2013b) Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci 18(10):575–583. https://doi.org/10.1016/j.tplants.2013.05.003
Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464. https://doi.org/10.1146/annurev-arplant-043014-115555
Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D et al (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promotes cell expansion. Plant J 70:978–990. https://doi.org/10.1111/j.1365-313X.2012.04946.x
Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, **e DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191. https://doi.org/10.1016/j.cell.2008.01.047
Susila H, Nasim Z, Ahn JH (2018) Ambient temperature-responsive mechanisms coordinate regulation of flowering time. Int J Mol Sci 19(10):3196. https://doi.org/10.3390/ijms19103196
Tang M, Tao YB, Fu Q, Song Y, Niu L, Xu ZF (2016a) An ortholog of LEAFY in Jatropha curcas regulates flowering time and floral organ development. Sci Rep 6:37306. https://doi.org/10.1038/srep37306
Tang M, Tao YB, Xu ZF (2016b) Ectopic expression of Jatropha curcas APETALA1 (JcAP1) caused early flowering in Arabidopsis, but not in Jatropha. Peer J 4:e1969. https://doi.org/10.7717/peerj.1969
Tang M, Bai X, Niu LJ, Chai X, Chen MS, Xu ZF (2018) Mir172 Regulates Both Vegetative and Reproductive Development in the Perennial Woody Plant Jatropha curcas. Plant Cell Physiol 59(12):2549–2563. https://doi.org/10.1093/pcp/pcy175
Taoka I, Ohki H, Tsuji C, Kojima K, Shimamoto K (2013) Structure and function of florigen and the receptor complex Trends. Plant Sci 18:287–294. https://doi.org/10.1016/j.tplants.2013.02.002
Telfer A, Bollman KM, Poethig RS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124:645–654
Terzi LC, Simpson GG (2008) Regulation of flowering time by RNA processing. Curr Top Microbiol Immunol 326:201–218. https://doi.org/10.1007/978-3-540-76776-3_11
Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4(1):75–85. https://doi.org/10.1016/s1369-5266(00)00139-4
Theissen G, Saedler H (2001) Plant biology: floral quartets. Nature 409(6819):469–471. https://doi.org/10.1038/35054172
Tiwari SB et al (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187(1):57–66. https://doi.org/10.1111/j.1469-8137.2010.03251.x
Tong H, **ao Y, Liu D, Gao S, Liu L, Yin Y, ** Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26(11):4376–4393. https://doi.org/10.1105/tpc.114.132092
Tsuji H, Nakamura H, Taoka KI, 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
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9(11):1963–1971. https://doi.org/10.1105/tpc.9.11.1963
Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303(5660):1003–1006. https://doi.org/10.1126/science.1091761
Waheed S, Zeng L (2020) The critical role of miRNAs in regulation of flowering time and flower development. Genes 11(3):1–24. https://doi.org/10.3390/genes11030319
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 W, Bai M, Wang Z (2014) The brassinosteroid signaling network a paradigm of signal integration. Curr Opin Plant Biol 21:147–153. https://doi.org/10.1016/j.pbi.2014.07.012
Wang P, Li J, Gao X, Zhang D, Li A, Liu C (2018) Genome-wide screening and characterization of the Dof gene family in physic nut (Jatropha curcas L.). International J Mol Sci 19(6):1598. DOI: https://doi.org/10.3390/ijms19061598
Werner T, Schmulling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12(5):527–538. https://doi.org/10.1016/j.pbi.2009.07.002
Whittaker C, Dean C (2017) The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu Rev Cell Dev Biol 6(33):555–575. https://doi.org/10.1146/annurev-cellbio-100616-060546
Wigge PA (2011) FT, a mobile development signal in plants. Curr Biol 21(9):R374–R378. https://doi.org/10.1016/j.cub.2011.03.038
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547. https://doi.org/10.1242/dev.02521
Wu G, Park MY, Conway SR, Wang J, Weigel D, Scott R (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750–759. https://doi.org/10.1016/j.cell.2009.06.031
Wu J, Liu Y, Tang L, Zhang F, Chen F (2011) A study on structural features in early flower development of Jatropha curcas L. and the classification of its inflorescences. Afr J Agric Res 6(2):275–284. https://doi.org/10.5897/AJAR09.727
**e K, Wu C, **ong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142(1):280–293. https://doi.org/10.1104/pp.106.084475
Xu W, Mulpuri S, Liu A (2012) Genetic diversity in the Jatropha genus and its potential application. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 7(059):1–15. https://doi.org/10.1079/PAVSNNR20127059
Xu G, Luo R, Yao Y (2013) Paclobutrazol improved the reproductive growth and the quality of seed oil of Jatropha curcas. J Plant Growth Regul 32:875–883. https://doi.org/10.1007/s00344-013-9353-5
Xu MY, Zhang L, Li WW, Hu XL, Wang MB, Fan YL, Zhang CY, Wang L (2014) Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J Exp Bot 65(1):89–101. https://doi.org/10.1093/jxb/ert353
Xu G et al (2016a) Transcriptome analysis of flower sex differentiation in Jatropha curcas L. using RNA sequencing. PLos One 11:e0145613. https://doi.org/10.1371/journal.pone.0145613
Xu M, Hu T, Zhao J, Park MY, Earley KW, Wu G, Yang L, Poethig RS (2016b) Developmental functions of miR156-regulated SQUAMOSA promoter binding protein-like (SPL) Genes in Arabidopsis thaliana. PLoS Genet 12(8):e1006263. https://doi.org/10.1371/journal.pgen.1006263
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. https://doi.org/10.1146/annurev.arplant.59.032607.092804
Yamaguchi A, Abe M (2012) Regulation of reproductive development by non-coding RNA in arabidopsis: to flower or not to flower. J Plant Res 125(6):693–704. https://doi.org/10.1007/s10265-012-0513-7
Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17(2):268–278. https://doi.org/10.1016/j.devcel.2009.06.007
Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22(2):508–522. https://doi.org/10.1105/tpc.109.068874
Yanagisawa S (2002) The Dof family of plant transcription factors. Trends Plant Sci 7(12):555–560. https://doi.org/10.1016/s1360-1385(02)02362-2
Yang J, Yang MF, Wang D, Chen F, Shen SH (2010) JcDof1, a Dof transcription factor gene, is associated with the light-mediated circadian clock in Jatropha curcas. Physiol Plant 139(3):324–334. https://doi.org/10.1111/j.1399-3054.2010.01363.x
Yang J, Yang MF, Wen PZ, Fan C, Shen SH (2011) A putative flowering time related Dof transcription factor gene, JcDof3, is controlled by the circadian clock in Jatropha curcas. Plant Sci 181:667–674. https://doi.org/10.1016/j.plantsci.2011.05.003
Yang M, Lu H, Xue F, Ma L (2019) Identifying high confidence microRNAs in the develo** seeds of Jatropha curcas. Sci Rep 9(1):1–11. https://doi.org/10.1038/s41598-019-41189-y)
Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor apetala2. Plant Cell 22(7):2156–2170. https://doi.org/10.1105/tpc.110.075606
Ye J, Geng Y, Zhang B, Mao H, Qu J, Chua NH (2014) The jatropha FT ortholog is a systemic signal regulating growth and flowering time. Biotechnol Biofuels 7:91. https://doi.org/10.1186/1754-6834-7-91
Yu S et al (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24:3320–3332. https://doi.org/10.1105/tpc.112.101014
Yu N, Yang JC, Yin GT, Li RS, Zou WT (2020) Genome-wide characterization of the SPL gene family involved in the age development of Jatropha curcas. BMC Genomics 21(1):1–14. https://doi.org/10.1186/s12864-020-06776-8
Zhai Q, Zhang X, Wu F, Feng H, Deng L, Xu L et al (2015) Transcriptional mechanism of jasmonate receptor COI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27(10):2814–2828. https://doi.org/10.1105/tpc.15.00619
Zhang N, Wen J, Zimmer EA (2015a) Expression patterns of AP1, FUL, FT and LEAFY orthologs in vitaceae support the homology of tendrils and inflorescences throughout the grape family. J Syst Evol 53:469–476. https://doi.org/10.1111/jse.12138
Zhang TQ, Wang JW, Zhou CM (2015b) The role of miR156 in developmental transitions in Nicotiana tabacum. Sci China Life Sci 58(3):253–260. https://doi.org/10.1007/s11427-015-4808-5
Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291(5502):306–309. https://doi.org/10.1126/science.291.5502.306
Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, ** Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29. https://doi.org/10.1186/1471-2199-10-29
Zhao ML, Chen MS, Ni J, Xu CJ, Yang Q, Xu ZF (2020) Comparative transcriptome analysis of gynoecious and monoecious inflorescences reveals regulators involved in male flower development in the woody perennial plant Jatropha curcas. Plant Reprod 33:191–204. https://doi.org/10.1007/s00497-020-00396-8
Zhao ML, Zhou ZF, Chen MS, Xu CJ, Xu ZF (2022) An ortholog of the MADS - box gene SEPALLATA3 regulates stamen development in the woody plant Jatropha curcas. Planta 255(6):1–15. https://doi.org/10.1007/s00425-022-03886-3
Zhou CM, Wang JW (2013) Regulation of flowering time by microRNAs. J Genet Genomics 40(5):211–215. https://doi.org/10.1016/j.jgg.2012.12.003
Zhu QH, Helliwell AC (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62(2):487–495. https://doi.org/10.1093/jxb/erq295
Zhu Y et al (2020) Terminal flower 1-FD complex target genes and competition with FLOWERING LOCUS T. Nat Commun 11(1):5118. https://doi.org/10.1038/s41467-020-18782-1
Zou Z, Zhang X (2019) Genome-wide identification and comparative evolutionary analysis of the Dof transcription factor family in physic nut and castor bean. PeerJ 7:e6354. https://doi.org/10.7717/peerj.6354
Author information
Authors and Affiliations
Contributions
All authors contributed to the idea conception and design for the article. The literature search and data analysis were performed by Adriana Sánchez-Gutiérrez and Miguel Salvador-Figueroa. The first draft of the manuscript was written by Adriana Sánchez-Gutiérrez. Miguel Salvador-Figueroa and José Alberto Narvaez-Zapata critically reviewed the work. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical Approval
Not applicable.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sánchez-Gutiérrez, A., Narváez-Zapata, J.A. & Salvador-Figueroa, M. Genes Involved in the Transition and Floral Sexual Differentiation of Jatropha curcas L. Plant Mol Biol Rep 42, 201–217 (2024). https://doi.org/10.1007/s11105-023-01423-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-023-01423-4