Abstract
Flowering time is an important agronomic trait, which is of great significance to the plant growth process. Salicylic acid (SA) is a key hormone that regulates plant growth and development. It can be converted into methyl salicylate (MeSA) catalyzed by SA carboxymethyl transferase (SAMT). Previous studies showed that SA was related to the regulation of plant flowering; however, the specific mechanism associated with this process remained to be further elucidated. In this study, the transgenic tobacco overexpressing LcSAMT gene and WT tobacco were cultivated to observe the flowering status of plant. The biomass and growth of tobaccos were recorded at different stages of plant growth. Endogenous MeSA content, phenylalanine ammonia-lyase (PAL) activity, and anthocyanin content were determined in transgenic tobacco plants during flowering stage. It was observed that the flowering time of transgenic tobacco was usually 6–7 days earlier than WT tobacco, and a higher endogenous MeSA content, PAL activity, and anthocyanin content were found in transgenic tobacco plants during flowering stage. Quantitative real-time PCR (qPCR) and transcriptome analysis were also performed in this study. There were 3924 differentially expressed genes (DEGs) identified between WT and transgenic tobacco plants by transcriptome analysis. These DEGs were primarily associated with plant hormone signal transduction pathways, plant pathogen interaction pathways, and mitogen-activated protein kinase (MAPK) pathways. QPCR analysis of 15 DEGs revealed that these genes were markedly upregulated in transgenic tobacco which was in accordance with transcriptome sequencing results. This study indicated that the SAMT gene-mediated SA homeostasis played important roles in the regulation of tobacco flowering.
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Anh Tuan P, Bai S, Saito T, Imai T, Ito A, Moriguchi T (2016) Involvement of EARLY BUD-BREAK, an AP2/ERF transcription factor gene, in bud break in Japanese pear (Pyrus pyrifolia Nakai) lateral flower buds: expression, histone modifications and possible target genes. Plant Cell Physiol 57:1038–1047
Astaneh RK, Bolandnazar S, Nahandi FZ, Oustan S (2018) Effect of selenium application on phenylalanine ammonia-lyase (PAL) activity, phenol leakage and total phenolic content in garlic (Allium sativum L .) under NaCl stress. Info Process Agric 5:339–344
Bayat H, Alirezaie M, Neamati H (2012) Impact of exogenous salicylic acid on growth and ornamental characteristics of calendula (Calendula officinalis L.) under salinity stress. J Physiol Biochem 8:258–267
Chen J, Zhang Q, Wang Q, Feng M, Li Y, Meng Y, Zhang Y, Liu G, Ma Z, Wu H, Gao J, Ma N (2017) RhMKK9, a rose MAP KINASE KINASE gene, is involved in rehydration-triggered ethylene production in rose gynoecia. BMC Plant Biol 17:51
Chen Y, Grimplet J, David K, Castellarin SD, Terol J, Wong DCJ, Luo Z, Schaffer R, Celton JM, Talon M, Gambetta GA, Chervin C (2018) Ethylene receptors and related proteins in climacteric and non-climacteric fruits. Plant Sci 276:63–72
Cleland CF, Ben-Tal Y (1982) Influence of giving salicylic acid for different time periods on flowering and growth in the long-day plant Lemna gibba G3. Plant Physiol 70:287–290
de Lima Silva CC, Shimo HM, de Felício R, Mercaldi GF, Rocco SA, Benedetti CE (2019) Structure-function relationship of a citrus salicylate methylesterase and role of salicylic acid in citrus canker resistance. Sci Rep 9:3901
Edris AE, Chizzola R, Franz C (2007) Isolation and characterization of the volatile aroma compounds from the concrete headspace and the absolute of Jasminum sambac (L.) Ait. (Oleaceae) flowers grown in Egypt. Eur Food Res Technol 226:621–626
Guan C, Wang C, Li Q, Ji J, Wang G, Jin C, Tong Y (2019) LcSABP2, a salicylic acid binding protein 2 gene from Lycium chinense, confers resistance to triclosan stress in Nicotiana tabacum. Ecotoxicol Environ Saf 183:109516
Harmut A (1987) Chlorophylls and carotenoids: pigments of photosynthetic membranes. Methods Enzymol 148:350–383
Hoshino YT, Morimoto S, Hayatsu M, Nagaoka K, Suzuki C, Karasawa T, Takenaka M, Akiyama H (2011) Effect of soil type and fertilizer management on archaeal community in upland field soils. Microbes Environ 26:307–316
Hugot K, Aimé S, Conrod S, Poupet A, Galiana E (1999) Developmental regulated mechanisms affect the ability of a fungal pathogen to infect and colonize tobacco leaves. Plant J 20:163–170
Irisarri P, Zhebentyayeva T, Errea P, Pina A (2016) Differential expression of phenylalanine ammonia lyase (PAL) genes implies distinct roles in development of graft incompatibility symptoms in Prunus. Sci Hortic-Amsterdam 204:16–24
Jaworski K, Pawelek A, Kopcewicz J, Szmidt-Jaworska A (2012) The calcium-dependent protein kinase (PnCDPK1) is involved in Pharbitis nil flowering. J Plant Physiol 169:1578–1585
Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim WY, Van Oosten M, Hyun Y, Somers DE, Lee I, Yun DJ, Bressan RA, Hasegawa PM (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J 53:530–540
Joshi R, Babu KGD, Gulati A (2013) Effect of decaffeination conditions on quality parameters of Kangra orthodox black tea. Food Res Int 53:693–703
Jung C, Müller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14:563–573
Kanani M, Nazarideljou MJ (2017) Methyl jasmonate and α-aminooxi-β-phenyl propionic acid alter phenylalanine ammonia-lyase enzymatic activity to affect the longevity and floral scent of cut tuberose. Hortic Environ Biote 58:136–143
Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40:D109–D114
Khurana A, Khurana JP, Babbar SB (2011) Nitric oxide induces flowering in the duckweed Lemna aequinoctialis Welw. (Syn. L. paucicostata Hegelm.) under noninductive conditions. J Plant Growth Regul 30:378–385
Koo YJ, Kim MA, Kim EH, Song JT, Jung C, Moon JK, Kim JH, Seo HS, Song SI, Kim JK, Lee JS, Cheong JJ, Choi YD (2007) Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol Biol 64:1–15
Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart C, Peeters A (1998) Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148:885–892
Kralemann LEM, Scalone R, Andersson L, Hennig L (2018) North European invasion by common ragweed is associated with early flowering and dominant changes in FT/TFL1 expression. J Exp Bot 69:2647–2658
Kwon SJ, Roy SK, Kim H-R, Moon Y-J, Woo SH, Boo HO, Koo J-W, Kim HH (2018) In vivo acclimatization responses of Platycodon grandiflorum for. duplex to different soil types and environmental factors. J Crop Sci Biotechnol 21:121–127
Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116
Lee S, Park CM (2010) Modulation of reactive oxygen species by salicylic acid in Arabidopsis seed germination under high salinity. Plant Signal Behav 5:1534–1536
Li W, Dai L, Wang G-L (2012) PUB13, a U-box/ARM E3 ligase, regulates plant defense, cell death, and flowering time. Plant Signal Behav 7:898–900
Li YX, Zhang W, Dong HX, Liu ZY, Ma J, Zhang XY (2018) Salicylic acid in Populus tomentosa is a remote signalling molecule induced by Botryosphaeria dothidea infection. Sci Rep 8:14059
Liu J, Li J, Wang H, Fu Z, Liu J, Yu Y (2011) Identification and expression analysis of ERF transcription factor genes in petunia during flower senescence and in response to hormone treatments. J Exp Bot 62:825–840
Long L, Yang WW, Liao P, Guo YW, Kumar A, Gao W (2019) Transcriptome analysis reveals differentially expressed ERF transcription factors associated with salt response in cotton. Plant Sci 281:72–81
Meesilp N, Mesil N (2019) Effect of microbial sanitizers for reducing biofilm formation of Staphylococcus aureus and Pseudomonas aeruginosa on stainless steel by cultivation with UHT milk. Food Sci Biotechnol 28:289–296
Mohsen K (2014) Effect of foliar application with salicylic acid and methyl jasmonate on growth, flowering, yield and fruit quality of tomato. Bull Env Pharmacol Life Sci 3:154–158
Murador DC, Cunha d DT, Rosso d VV (2014) Effects of cooking techniques on vegetable pigments: a meta-analytic approach to carotenoid and anthocyanin levels. Food Res Int 65:177–183
Nakano T, Fujisawa M, Shima Y, Ito Y (2014) The AP2/ERF transcription factor SlERF52 functions in flower pedicel abscission in tomato. J Exp Bot 65:3111–3119
Pacheco AC, Cabral C, Fermino E, Aleman CC (2013) Salicylic acid-induced changes to growth, flowering and flavonoids production in marigold plants. J Med Plant Res 1:95–100
Pearce SL, Clarke DF, East PD, Elfekih S, Gordon K, Jermiin LS, McGaughran A, Oakeshott JG, Papanikolaou A, Perera OP (2017) Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol 15:63
Pott MB, Effmert U, Piechulla B (2003) Transcriptional and post-translational regulation of S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase (SAMT) during Stephanotis floribunda flower development. J Plant Physiol 160:635–643
Rong D, Luo N, Mollet JC, Liu X, Yang Z (2016) Salicylic acid regulates pollen tip growth through an NPR3/NPR4-independent pathway. Molecur Plant 9:1478–1491
Ross JR, Nam KH, D'Auria JC, Pichersky E (1999) S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch Biochem Biophys 367:9–16
Schaller GE (2012) Ethylene and the regulation of plant development. BMC Biol 10:9
Schiessl S, Huettel B, Kuehn D, Reinhardt R, Snowdon RJ (2017) Targeted deep sequencing of flowering regulators in Brassica napus reveals extensive copy number variation. Sci Data 4:170013
Shimakawa A, Shiraya T, Ishizuka Y, Wada KC, Mitsui T, Takeno K (2012) Salicylic acid is involved in the regulation of starvation stress-induced flowering in Lemna paucicostata. J Plant Physiol 169:987–991
Siegrist J, Orober M, Buchenauer H (2000) β-Aminobutyric acid-mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiol Mol Plant Pathol 56:95–106
Song YH, Song NY, Shin SY, Kim HJ, Yun D-J, Lim CO, Lee SY, Kang KY, Hong JC (2008) Isolation of CONSTANS as a TGA4/OBF4 interacting protein. Mol Cells (Springer Science & Business Media BV) 25
Tieman D, Zeigler M, Schmelz E, Taylor MG, Rushing S, Jones JB, Klee HJ (2010) Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J 62:113–123
Toscano S, Ferrante A, Leonardi C, Romano D (2018) PAL activities in asparagus spears during storage after ammonium sulfate treatments. Postharvest Biol Technol 140:34–41
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515
Trusov Y, Botella JR (2006) Silencing of the ACC synthase gene ACACS2 causes delayed flowering in pineapple [Ananas comosus (L.) Merr.]. J Exp Bot 57:3953–3960
Vicente RM, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338
Wada KC, Mizuuchi K, Koshio A, Kaneko K, Mitsui T, Takeno K (2014) Stress enhances the gene expression and enzyme activity of phenylalanine ammonia-lyase and the endogenous content of salicylic acid to induce flowering in pharbitis. J Plant Physiol 171:895–902
Wada KC, Yamada M, Shiraya T, Takeno K (2010) Salicylic acid and the flowering gene FLOWERING LOCUS T homolog are involved in poor-nutrition stress-induced flowering of Pharbitis nil. J Plant Physiol 167:447–452
Wada KC, Yamada M, Takeno K (2013) Stress-induced flowering in pharbitis—a review. Am J Plant Sci 04:74–79
Wai CM, Powell B, Ming R, Min XJ (2016) Analysis of alternative splicing landscape in pineapple (Ananas comosus). Trop Plant Biol 9:150–160
Wang G, Li Q, Wang C, Jin C, Ji J, Guan C (2019) A salicylic acid carboxyl methyltransferase-like gene LcSAMT from Lycium chinense, negatively regulates the drought response in transgenic tobacco. Environ Exp Bot 167:103833
Wang H, Pan J, Li Y, Lou D, Hu Y, Yu D (2016) The DELLA-CONSTANS transcription factor cascade integrates gibberellic acid and photoperiod signaling to regulate flowering. Am Soc Plant Biol 172:479–488
Wang NN, Shih MC, Li N (2005) The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J Exp Bot 56:909–920
Wang R, Albani MC, Vincent C, Bergonzi S, Luan M, Bai Y, Kiefer C, Castillo R, Coupland G (2011) Aa TFL1 confers an age-dependent response to vernalization in perennial Arabis alpina. Plant Cell 23:1307–1321
Wei T, Deng K, Zhang Q, Gao Y, Liu Y, Yang M, Zhang L, Zheng X, Wang C, Liu Z, Chen C, Zhang Y (2017) Modulating AtDREB1C expression improves drought tolerance in Salvia miltiorrhiza. Front Plant Sci 8:52
Yamada M, Takeno K (2014) Stress and salicylic acid induce the expression of PnFT2 in the regulation of the stress-induced flowering of Pharbitis nil. J Plant Physiol 171:205–212
Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107
Zhang L, Cheng J, Sun X, Zhao T, Li M, Wang Q, Li S, Xin H (2018) Overexpression of VaWRKY14 increases drought tolerance in Arabidopsis by modulating the expression of stress-related genes. Plant Cell Rep 37:1159–1172
Zhang Z, Sun C, Yao Y, Mao Z, Sun G, Dai Z (2019) Red anthocyanins contents and the relationships with phenylalanine ammonia lyase (PAL) activity, soluble sugar and chlorophyll contents in carmine radish (Raphanus sativus L.). Hortic Sci 46:17–25
Zhao N, Guan J, Ferrer JL, Engle N, Chern M, Ronald P, Tschaplinski TJ, Chen F (2010) Biosynthesis and emission of insect-induced methyl salicylate and methyl benzoate from rice. Plant Physiol Biochem 48:279–287
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This work was supported by National Natural Science Foundation of China (81901502), Tianjin Science and Technology Research and Development Plan Project (19YFZCSN00280), and Tianjin Rice Industry Technology System Innovation Team Construction (ITTRRS2018007).
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Zhang, Y., Peng, D., Song, Y. et al. Enhancement of methyl salicylate accumulation promotes early flowering in transgenic tobacco plants by overexpressing a carboxymethyl transferase (SAMT) gene from Lycium chinense. Mol Breeding 40, 52 (2020). https://doi.org/10.1007/s11032-020-01131-x
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DOI: https://doi.org/10.1007/s11032-020-01131-x