Abstract
Photoperiod regulates different morphophysiological processes in plants, directly impacting photosynthetic performance and, consequently, primary and secondary metabolism. To date, there are no studies reporting the influence of photoperiod on the biosynthesis of phytoecdysteroids, such as 20-hydroxyecdisone (20-E). Here, we evaluated the effects of photoperiod on the development and metabolism of in vitro grown Pfaffia glomerata, an important medicinal species and producer of 20-E. Two P. glomerata accessions (Ac22 and Ac43) were cultivated for 40 days under different photoperiods: 4, 8, 16, and 24 h. Then, growth, physiological performance, 20-E content and gene expression related to the synthesis of this compound were evaluated. Longer photoperiods resulted in higher photosynthetic rates, growth, and biomass accumulation in both accessions. P. glomerata showed great plasticity to the different photoperiods tested and no sign of photoinhibition (Fv/Fm). Primary metabolism was modulated by photoperiod, with marked differences in the production of soluble sugars, starch, and amino acids. Anthocyanin production was also affected by the photoperiod. However, the accessions showed contrasting responses, in which longer photoperiods led to the highest anthocyanin contents in Ac22 and the lowest in Ac43, reflecting different adaptive strategies the light conditions. As a result of better photosynthetic performance and higher carbon availability, P. glomerata accumulated more 20-E during longer photoperiods. In this way, growing P. glomerata plants for longer photoperiods may represent a strategy for obtaining plants with larger biomass and higher 20-E yields.
Key Message
Photoperiod regulates the primary and secondary metabolism of P. glomerata plants grown in vitro, and longer photoperiods increase growth, photosynthetic performance, and accumulation of the phytoecdysteroid 20-hydroxyecdysone (20-E).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams WW (2018) An integrative approach to photoinhibition and photoprotection of photosynthesis. Environ Exp Bot 154:1–3. https://doi.org/10.1016/J.ENVEXPBOT.2018.05.006
Adams SR, Langton FA (2005) Photoperiod and plant growth: a review. J Hortic Sci Biotechnol 80:2–10. https://doi.org/10.1080/14620316.2005.11511882
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759
Batista DS, Dias LLC, Rêgo M, Saldanha CW, Otoni WC (2017) Flask sealing on in vitro seed germination and morphogenesis of two types of ornamental pepper explants. Cienc Rural 47:e20150245. https://doi.org/10.1590/0103-8478cr20150245
Batista DS, Koehler AD, Romanel E, Souza VC, Silva TD, Almeida MC, Maciel TEF, Ferreira PRB, Felipe SHS, Saldanha CW, Maldaner J, Dias LLC, Festucci-Buselli RA, Otoni WC (2018) De novo assembly and transcriptome of Pfaffia glomerata uncovers the role of photoautotrophy and the P450 family genes in 20-hydroxyecdysone production. Protoplasma 256:601–614. https://doi.org/10.1007/s00709-018-1322-1
Batista DS, Moreira VS, Felipe SHS, Fortini EA, Silva TD, Chagas K, Louback E, Romanel E, Costa MGC, Otoni WC (2019) Reference gene selection for qRT-PCR in Brazilian-ginseng [Pfaffia glomerata (Spreng.) Pedersen] as affected by various abiotic factors. Plant Cell Tissue Organ Cult 138:97–107. https://doi.org/10.1007/s11240-019-01606-6
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bukhov NG (2004) Dynamic light regulation of photosynthesis (a review). Russ J Plant Physiol 51:742–753. https://doi.org/10.1023/B:RUPP.0000047822.66925.bf
Cagnola JI, Cerdan PD, Pacin M, Andrade A, Rodriguez MV, Zurbriggen MD, Legris M, Buchovsky S, Carrillo N, Chory J, Blazquez MA, Alabadi D, Casal JJ (2018) Long-day photoperiod enhances jasmonic acid-related plant defense. Plant Physiol 178:163–173. https://doi.org/10.1104/pp.18.00443
Caleffi ER, Krausová G, Hyršlová I, Paredes LLR, Santos MM, Sassaki GL, Gonçalves RAC, Oliveira AJB (2015) Isolation and prebiotic activity of inulin-type fructan extracted from Pfaffia glomerata (Spreng) Pedersen roots. Int J Biol Macromol 80:392–399. https://doi.org/10.1016/j.ijbiomac.2015.06.053
Castro KM, Batista DS, Fortini EA, Silva TD, Felipe SHS, Fernandes AM, Sousa RMJ, Nascimento LSQ, Campos VR, Grazul RM, Viccini LF, Otoni WC (2019) Photoperiod modulates growth, morphoanatomy, and linalool content in Lippia alba L. (Verbenaceae) cultured in vitro. Plant Cell Tissue Organ Cult 139:139–153. https://doi.org/10.1007/s11240-019-01672-w
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Method Enzymol 2:764–775. https://doi.org/10.1016/S0076-6879(55)02300-8
Chaubey MK (2018) Role of phytoecdysteroids in insect pest management: A review. J Agron 17:1–10
Corrêa JPO, Vital CE, Pinheiro MVM, Batista DS, Azevedo JFL, Saldanha CW, Cruz ACF, DaMatta FM, Otoni WC (2015) In vitro photoautotrophic potential and ex vitro photosynthetic competence of Pfaffia glomerata (Spreng.) Pedersen accessions. Plant Cell Tissue Organ Cult 121:289–300. https://doi.org/10.1007/s11240-014-0700-4
Cross JM, von Korff M, Altmann T, Bartzetko L, Sulpice R, Gibon Y, Palacios N, Stitt M (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol 142:1574–1588. https://doi.org/10.1104/pp.106.086629
Cruz CD (2016) Genes Software – extended and integrated with the R. Matlab and Selegen Acta Sci-Agron 38:547. https://doi.org/10.4025/actasciagron.v38i3.32629
Cui L, Zou Z, Zhang J, Zhao Y, Yan F (2016) 24-Epibrassinoslide enhances plant tolerance to stress from low temperatures and poor light intensities in tomato (Lycopersicon esculentum Mill.). Funct Integr Genomic 16:29–35. https://doi.org/10.1007/s10142-015-0464-x
de Wit M, Galvão VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67:513–537. https://doi.org/10.1146/annurev-arplant-043015-112252
Dias FCR, Martins ALP, de Melo FCSA, Cupertino MC, Gomes MLM, Oliveira JM, Damasceno EM, Silva J, Otoni WC, Matta SLP (2019) Hydroalcoholic extract of Pfaffia glomerata alters the organization of the seminiferous tubules by modulating the oxidative state and the microstructural reorganization of the mice testes. J Ethnopharmacol 233:179–189. https://doi.org/10.1016/j.jep.2018.12.047
Dietz KJ (2015) Efficient high light acclimation involves rapid processes at multiple mechanistic levels. J Exp Bot 66:2401–2414. https://doi.org/10.1093/jxb/eru505
Dinan L, Lafont R (2006) Effects and applications of arthropod steroid hormones (ecdysteroids) in mammals. J Endocrinol 191:1–8. https://doi.org/10.1677/joe.1.06900
Dinan L, Harmatha J, Volodin V, Lafont R (2009) Phytoecdysteroids: diversity, biosynthesis and distribution. Ecdysone: structures and functions. Springer, Netherlands, Dordrecht, pp 3–45
Dodd AN (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633. https://doi.org/10.1126/science.1115581
Fankhauser C, Chory J (2002) Light control of plant development. Annu Rev Cell Dev Biol 13:203–229. https://doi.org/10.1146/annurev.cellbio.13.1.203
Felipe SHS, Batista DS, Chagas K, Correia LNF, Silva TD, Fortini EA, Silva PO, Otoni WC (2019a) Accessions of Brazilian ginseng (Pfaffia glomerata) with contrasting anthocyanin content behave differently in growth, antioxidative defense, and 20-hydroxyecdysone levels under UV-B radiation. Protoplasma 256:1557–1571. https://doi.org/10.1007/s00709-019-01400-3
Felipe SHS, Batista DS, Vital CE, Chagas K, Silva PO, Silva TD, Fortini EA, Correia LNF, Ávila RT, Maldaner J, Festucci-Buselli RA, DaMatta FM, Otoni WC (2019b) Salinity-induced modifications on growth, physiology and 20-hydroxyecdysone levels in Brazilian-ginseng [Pfaffia glomerata (Spreng.) Pedersen]. Plant Physiol Biochem 140:43–54. https://doi.org/10.1016/j.plaphy.2019.05.002
Feng L, Raza MA, Li Z, Chen Y, Khalid MHB, Du J, Liu W, Wu X, Song C, Yu L, Zhang Z, Yuan S, Yang W, Yang F (2019) The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of Soybean. Front Plant Sci 9:1952. https://doi.org/10.3389/fpls.2018.01952
Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001) Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212:250–263. https://doi.org/10.1007/s004250000386
Festucci-Buselli RA, Contim LAS, Barbosa LCA, Stuart J, Otoni WC (2008) Biosynthesis and potential functions of the ecdysteroid 20-hydroxyecdysone—a review. Botany 86:978–987. https://doi.org/10.1139/b08-049
Freitas CS, Baggio CH, Da Silva-Santos JE, Rieck CADM, Santos CC, Júnior LC, Ming DAG, Cortez MCA (2004) Involvement of nitric oxide in the gastroprotective effects of an aqueous extract of Pfaffia glomerata (Spreng) Pedersen, Amaranthaceae, in rats. Life Sci 74:1167–1179. https://doi.org/10.1016/j.lfs.2003.08.003
Galvão VC, Fankhauser C (2015) Sensing the light environment in plants: photoreceptors and early signaling steps. Curr Opin Neurobiol 34:46–53. https://doi.org/10.1016/J.CONB.2015.01.013
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/PP.59.2.309
Gibala M, Kicia M, Sakamoto W, Gola EM, Kubrakiewicz J, Smakowska E, Janska H (2009) The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod. Plant J 59:685–699. https://doi.org/10.1111/j.1365-313X.2009.03907.x
Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32:859–874. https://doi.org/10.1111/j.1365-3040.2009.01965.x
Gomes MP, Cristina T, Lanza L, Marques M, Martins GA, Mercia M, Carvalho L, Soares AM (2013) Cd-tolerance markers of Pfaffia glomerata (Spreng.) Pedersen plants: anatomical and physiological features. Braz J Plant Physiol 24:293–304. https://doi.org/10.1590/S1677-04202012000400008
Gould KS, Jay-Allemand C, Logan BA, Baissac Y, Bidel LPR (2018) When are foliar anthocyanins useful to plants? Re-evaluation of the photoprotection hypothesis using Arabidopsis thaliana mutants that differ in anthocyanin accumulation. Environ Exp Bot 154:11–22. https://doi.org/10.1016/J.ENVEXPBOT.2018.02.006
Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16:598–610. https://doi.org/10.1038/nrg3976
Gu Z, Chen H, Yang R, Ran M (2018) Identification of DFR as a promoter of anthocyanin accumulation in poinsettia (Euphorbia pulcherrima Willd. ex Klotzsch) bracts under short-day conditions. Sci Hortic 236:158–165. https://doi.org/10.1016/J.SCIENTA.2018.03.032
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. https://doi.org/10.1104/PP.84.2.450
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Henriques R, Papdi C, Ahmad Z, Bögre L (2018) Circadian regulation of plant growth. Annu Plant Rev 1:1–29
Hildebrandt TM, Nunes Nesi A, Araújo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579
Huang J, Reichelt M, Chowdhury S, Hammerbacher A, Hartmann H (2017) Increasing carbon availability stimulates growth and secondary metabolites via modulation of phytohormones in winter wheat. J Exp Bot 68:1251–1263. https://doi.org/10.1093/jxb/erx008
Iarema L, da Cruz ACF, Saldanha CW, Dias LCC, Vieira RF, Oliveira EJ, Otoni WC (2012) Photoautotrophic propagation of Brazilian ginseng [Pfaffia glomerata (Spreng.) Pedersen]. Plant Cell Tissue Organ Cult 110:227–238. https://doi.org/10.1007/s11240-012-0145-6
Jackson SD (2009) Plant responses to photoperiod. New Phytol 181:517–531. https://doi.org/10.1111/j.1469-8137.2008.02681.x
Kamada T, Picoli E, Vieira R, Barbosa L, Cruz AC, Otoni WC (2009) Variation of morphological and physiological characters in natural populations of Pfaffia glomerata (Spreng.) Pedersen and their correlation with β-ecdysone production. Rev Bras Plantas Med 11:247–256. https://doi.org/10.1590/S1516-05722009000300004
Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66. https://doi.org/10.1016/S0070-2153(10)91002-8
Kannangara CG, Hansson M (1998) Arrest of chlorophyll accumulation prior to anthocyanin formation in Euphorbia pulcherrima. Plant Physiol Biochem 36:843–848. https://doi.org/10.1016/S0981-9428(99)80001-1
Karnovsky M (1965) A formaldehyde glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138
Khan T, Abbasi BH, Khan MA (2018) The interplay between light, plant growth regulators and elicitors on growth and secondary metabolism in cell cultures of Fagonia indica. J Photochem Photobiol B 185:153–160. https://doi.org/10.1016/j.jphotobiol.2018.06.002
Lei XY, Xia J, Wang JW, Zheng LP (2018) Comparative transcriptome analysis identifies genes putatively involved in 20-hydroxyecdysone biosynthesis in Cyanotis arachnoidea. Int J Mol Sci 19:1885. https://doi.org/10.3390/ijms19071885
Li J, Wang C, Han X, Qi W, Chen Y, Wang T, Zheng Y, Zhao X (2016) Transcriptome analysis to identify the putative biosynthesis and transport genes associated with the medicinal components of Achyranthes bidentata Bl. Front Plant Sci 7:1860. https://doi.org/10.3389/fpls.2016.01860
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry–based metabolite profiling in plants. Nat Protoc 1:387–396. https://doi.org/10.1038/nprot.2006.59
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using Real-Time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/METH.2001.1262
Malnoë A (2018) Photoinhibition or photoprotection of photosynthesis? Update on the (newly termed) sustained quenching component qH. Environ Exp Bot 154:123–133. https://doi.org/10.1016/J.ENVEXPBOT.2018.05.005
Martín G, Rovira A, Veciana N, Soy J, Toledo-Ortiz G, Gommers CGM, Boix M, Henriques R, Minguet EG, Alabadí D, Halliday KJ, Leivar P, Monte E (2018) Circadian waves of transcriptional repression shape PIF-regulated photoperiod-responsive growth in Arabidopsis. Curr Biol 28:311–318. https://doi.org/10.1016/J.CUB.2017.12.02
Martins SCV, Araújo WL, Tohge T, Fernie AR, DaMatta FM (2014) In High-light-acclimated coffee plants the metabolic machinery is adjusted to avoid oxidative stress rather than to benefit from extra light enhancement in photosynthetic yield. PLoS ONE 9:e94862. https://doi.org/10.1371/journal.pone.0094862
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659
Mendes FR (2011) Tonic, fortifier and aphrodisiac: adaptogens in the Brazilian folk medicine. Rev Bras Farmacogn 21:754–763. https://doi.org/10.1590/S0102-695X2011005000097
Mengin V, Pyl ET, Moraes TA, Sulpice R, Krohn N, Encke B, Stitt M (2017) Photosynthate partitioning to starch in Arabidopsis thaliana is insensitive to light intensity but sensitive to photoperiod due to a restriction on growth in the light in short photoperiods. Plant Cell Environ 40:2608–2627. https://doi.org/10.1111/pce.13000
Merzlyak MN, Chivkunova OB (2000) Light-stress-induced pigment changes and evidence for anthocyanin photoprotection in apples. J Photochem Photobiol B 55:155–163. https://doi.org/10.1016/S1011-1344(00)00042-7
Michelet L, Krieger-Liszkay A (2012) Reactive oxygen intermediates produced by photosynthetic electron transport are enhanced in short-day grown plants. BBA Bioenergetics 1817:1306–1313. https://doi.org/10.1016/J.BBABIO.2011.11.014
Morales M, Munné-Bosch S (2019) Malondialdehyde: facts and artifacts. Plant Physiol 180:1246–1250. https://doi.org/10.1104/pp.19.00405
Munir J, Dorn LA, Donohue K, Schmitt J (2001) The effect of maternal photoperiod on seasonal dormancy in Arabidopsis thaliana (Brassicaceae). Am J Bot 88:1240–1249. https://doi.org/10.2307/3558335
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Neff MM, Chory J (1998) Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol 118:27–35. https://doi.org/10.1104/pp.118.1.27
Neto AG, Costa JMLC, Belati CC, Vinhólis AHC, Possebom LS, Silva Filho AA, Cunha WR, Carvalho JCT, Bastos JK, Silva MLA (2005) Analgesic and anti-inflammatory activity of a crude root extract of Pfaffia glomerata (Spreng.) Pedersen. J Ethnopharmacol 96:87–91. https://doi.org/10.1016/j.jep.2004.08.035
O’Brien TP, McCully ME (1981) The study of plant structure principles and selected methods. Termarcarphi Pty. Ltd., Melbourne
Powles SB, Thorne SW (1981) Effect of high-light treatments in inducing photoinhibition of photosynthesis in intact leaves of low-light grown Phaseolus vulgaris and Lastreopsis microsora. Planta 152:471–477. https://doi.org/10.1007/BF00385365
Saldanha CW, Otoni CG, Notini MM, Kuki KN, Cruz ACF, Neto AR, Dias LLC, Otoni WC (2014) A CO2-enriched atmosphere improves in vitro growth of Brazilian ginseng [Pfaffia glomerata (Spreng.) Pedersen]. In Vitro Cell Dev Biol Plant 49:433–444. https://doi.org/10.1007/s11627-013-9529-5
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089
Serrano-Bueno G, Romero-Campero FJ, Lucas-Reina E, Romero JM, Valverde F (2017) Evolution of photoperiod sensing in plants and algae. Curr Opin Plant Biol 37:10–17. https://doi.org/10.1016/j.pbi.2017.03.007
Silva TD, Batista DS, Fortini EA, Castro KM, Felipe SHS, Fernandes AM, Sousa RMA, Chagas K, Silva JVS, Correia LNF, Farias LM, Leite JPV, Rocha DI, Otoni WC (2020) Blue and red light affects morphogenesis and 20-hydroxyecdisone content of in vitro Pfaffia glomerata accessions. J Photochem Photobiol B 203:111761. https://doi.org/10.1016/j.jphotobiol.2019.111761
Skrebsky EC, Tabaldi LA, Pereira LB, Rauber R, Maldaner J, Cargnelutti D, Gonçalves JF, Castro GY, Shetinger MRC, Nicoloso FT (2009) Effect of cadmium on growth, micronutrient concentration, and δ-aminolevulinic acid dehydratase and acid phosphatase activities in plants of Pfaffia glomerata. Braz J Plant Physiol 20:285–294. https://doi.org/10.1590/s1677-04202008000400004
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149
Tóth N, Szabó A, Kacsala P, Héger J, Zádor E (2008) 20-Hydroxyecdysone increases fiber size in a muscle-specific fashion in rat. Phytomedicine 15:691–698. https://doi.org/10.1016/j.phymed.2008.04.015
Tsukagoshi Y, Ohyama K, Seki H, Akashi T, Muranaka T, Suzuki H, Fujimoto Y (2016) Functional characterization of CYP71D443, a cytochrome P450 catalyzing C-22 hydroxylation in the 20-hydroxyecdysone biosynthesis of Ajuga hairy roots. Phytochemistry 127:23–28. https://doi.org/10.1016/j.phytochem.2016.03.010
Vankoughnett MR, Way DA, Henry HAL (2016) Late winter light exposure increases summer growth in the grass Poa pratensis: Implications for snow removal experiments and winter melt events. Environ Exp Bot 131:32–38. https://doi.org/10.1016/J.ENVEXPBOT.2016.06.014
Wake CMF, Fennell A (2000) Morphological, physiological and dormancy responses of three Vitis genotypes to short photoperiod. Physiol Plant 109:203–210. https://doi.org/10.1034/j.1399-3054.2000.100213.x
Wang S, Liu S, Liu H, Zhou S, Jiang RJ, Bendena WG, Li S (2010) 20-Hydroxyecdysone reduces insect food consumption resulting in fat body lipolysis during molting and pupation. J Mol Cell Biol 2:128–138. https://doi.org/10.1093/jmcb/mjq006
Ware MA, Belgio E, Ruban AV (2015) Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities. Photosynth Res 126:261–274. https://doi.org/10.1007/s11120-015-0102-4
Weber H, Chételat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888. https://doi.org/10.1111/j.1365-313X.2003.02013.x
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Zhang KM, Wang JW, Guo ML, Du WL, Wu RH, Wang X (2016) Short-day signals are crucial for the induction of anthocyanin biosynthesis in Begonia semperflorens under low temperature condition. J Plant Physiol 204:1–7. https://doi.org/10.1016/J.JPLPH.2016.06.021
Zheng S, Hu H, Ren H, Yang Z, Qiu Q, Qi W, Liu X, Chen X, Cui X, Li S, Zhou B, Sun D, Cao X, Du J (2019) The Arabidopsis H3K27me3 demethylase JUMONJI 13 is a temperature and photoperiod dependent flowering repressor. Nat Commun 10:1303. https://doi.org/10.1038/s41467-019-09310-x
Acknowledgements
We thank Prof. Takeshi Kamada (Universidade de Rio Verde, Rio Verde, GO, Brazil), Dr. Roberto F. Vieira and Dr. Rosa Belém Alves Neves (National Center for Genetic Resources and Biotechnology—Embrapa/Cenargen, Brasília, DF, Brazil) for providing the P. glomerata accessions. The Departments of Plant Biology and Biochemistry and Molecular Biology, Universidade Federal de Viçosa, are gratefully acknowledged for providing the facilities for structural, molecular, and biochemical analyses. We would like to thank Editage (www.editage.com) for English language editing.
Funding
This work was supported by the Brazilian agencies Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, Belo Horizonte, MG, Brazil; Grants no. PRONEX-CAG-APQ-01036-09; CRA-APQ-01651-13; CRA-BPD-00046-14 to WCO and CBB-BPD-00020-16 to DSB), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brasília, DF, Brazil; Grant Finance Code 001) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brasília, DF, Brazil: Grants no. MCT/CNPq 480675/2009-0; PQ 459.529/2014-5; and PQ 313901/2018-0 to WCO).
Author information
Authors and Affiliations
Contributions
EAF, DSB, and WCO designed the study; EAF performed most of the experiments; EAF, KMC, TDS, SHSF, LNFC, KC, LMF, and JPVL performed physiological and biochemical analyses; EAF, SHSF, KC, KMC, and TDS evaluated photosynthetic performance; EAF, DSB, and LNFC performed molecular analyses; EAF and DSB analyzed the data; EAF and WCO wrote the article with input from all other authors. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Amita Bhattacharya.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
Micropropagation process of Pfaffia glomerata. (a) P. glomerata (Accession 22), from the germplasm bank of the Plant Tissue Culture Laboratory (UFV), after 30 days of in vitro growth; (b) Nodal explants; (c) Plants at the end of the experiment, after 40 days of in vitro culture
Rights and permissions
About this article
Cite this article
Fortini, E.A., Batista, D.S., de Castro, K.M. et al. Photoperiod modulates growth and pigments and 20-hydroxyecdysone accumulation in Brazilian ginseng [Pfaffia glomerata (Spreng.) Pedersen] grown in vitro. Plant Cell Tiss Organ Cult 142, 595–611 (2020). https://doi.org/10.1007/s11240-020-01886-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-020-01886-3