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The influences of phytohormones on triacylglycerol accumulation in an oleaginous marine diatom Phaeodactylum tricornutum

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Abstract

Environmental stresses such as nitrate deprivation and high light are effective at increasing lipid content in microalgae, but they can also slow down and even stop growth. In this study, the phytohormones methyl jasmonate, salicylic acid, gibberellin, abscisic acid, and ethephon were introduced to cultures of the oleaginous marine diatom Phaeodactylum tricornutum in an attempt to increase growth and lipid production. Single-factor experiments showed that the influences of some of the phytohormones were closely related to their concentrations. Methyl jasmonate, abscisic acid, and salicylic acid promoted P. tricornutum growth and lipid accumulation at certain concentrations. The differing effects of the three phytohormones on P. tricornutum may be related to the respective phytohormone’s responsive cis-regulatory elements in the upstream regions of the triacylglycerol (TAG) synthesis genes. Methyl jasmonate, abscisic acid, and salicylic acid were further studied in response surface experiments, through which a 141% increase in TAG production was attained for 10-L cultures of P. tricornutum grown under optimal conditions. This study suggests that some phytohormones can promote P. tricornutum lipid accumulation without hindering growth. It also provides another strategy for improving the production of microalgae for use as biodiesel.

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References

  • Bajguz A, Piotrowska-Niczyporuk A (2014) Interactive effect of brassinosteroids and cytokinins on growth, chlorophyll, monosaccharide and protein content in the green alga Chlorella vulgaris (Trebouxiophyceae). Plant Physiol Biochem 80:176–183

    Article  CAS  PubMed  Google Scholar 

  • Barka F, Angstenberger M, Ahrendt T, Lorenzen W, Bode HB, Büchel C (2016) Identification of a triacylglycerol lipase in the diatom Phaeodactylum tricornutum. Biochim Biophys Acta 1861:239–248

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, de Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kröger N, Kroth PG, la Roche J, Lindquist E, Lommer M, Martin–Jézéquel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Secq MPO–L, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, van de Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Zhao P, Wang XQ, Pang GC (2009) Effect on biomass and the content of active components of Spirulina sp. by three phytohormones. Mar Sci 33:11–16 (In Chinese)

    CAS  Google Scholar 

  • Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prásil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17

    Google Scholar 

  • Cui YL, Zheng GT, Li XQ, Lin HZ, Jiang P, Qin S (2013) Cloning and characterization of a novel diacylglycerol acyltransferase from the diatom Phaeodactylum tricornutum. J Appl Phycol 25:1509–1512

    Article  CAS  Google Scholar 

  • Cui YL, Zhao JL, Wang YC, Qin S, Lu YD (2018) Characterization and engineering of a dual-function diacylglycerol acyltransferase in theoleaginous marine diatom Phaeodactylum tricornutum. Biotechnol Biofuels 11:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge F, Huang W, Chen Z, Zhang C, Xiong Q, Bowler C (2014) Methylcrotonyl-coA carboxylase regulates triacylglycerol accumulation in the model diatom Phaeodactylum tricornutum. Plant Cell 26:1681–1697

  • Gong YM, Zhang J, Guo X, Wan X, Liang Z, Hu CJ, Jiang M (2013) Identification and characterization of PtDGAT2B, an acyltransferase of the DGAT2 acyl-coenzyme A: diacylglycerol acyltransferase family in the diatom Phaeodactylum tricornutum. FEBS Lett 587:481–487

    Article  CAS  PubMed  Google Scholar 

  • Guihéneuf F, Leu S, Zarka A, Khozin-Goldberg I, Khalilov I, Boussiba S (2011) Cloning and molecular characterization of a novel acyl-CoA: diacylglycerol acyltransferase 1-like gene (PtDGAT1) from the diatom Phaeodactylum tricornutum. FEBS J 278:3651–3666

    Article  CAS  PubMed  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Hara M, Furukawa J, Sato A (2012) Abiotic stress and role of salicylic acid in plants. In: Ahamd P (ed) Abiotic stress response in plants. Spinger, New York, pp 235–251

    Chapter  Google Scholar 

  • Hunt RW, Chinnasamy S, Bhatnagar A, Das KC (2010) Effect of biochemical stimulants on biomass productivity and metabolite content of the microalga, Chlorella sorokiniana. Appl Biochem Biotechnol 162:2400–2414

    Article  CAS  PubMed  Google Scholar 

  • Jiang XJ, Lin HT, Lin MS, Chen YH, Wang H, Lin YX, Shi J, Lin YF (2018) A novel chitosan formulation treatment induces disease resistance of harvested litchi fruit to Peronophythora litchii in association with ROS metabolism. Food Chem 266:299–308

    Article  CAS  PubMed  Google Scholar 

  • Kansedo J, Keatteong L (2013) Process optimization and kinetic study for biodiesel production from non-edible sea mango (Cerbera odollam) oil using response surface methodology. Chem Eng J 214:157–164

    Article  CAS  Google Scholar 

  • Kim S-H, Lim SR, Hong S-J, Cho B-K, Lee H, Lee C-G, Choi H-K (2016) Effect of ethephon as an ethylene-releasing compound on the metabolic profile of Chlorella vulgaris. J Agric Food Chem 64:4807–4816

    Article  CAS  PubMed  Google Scholar 

  • Kousar R, Qureshi R, Jalal-Ud-Din MM, Shabbir G (2018) Salicylic acid mediated heat stress tolerance in selected bread wheat genotypes of Pakistan. Pak J Bot 50:2141–2146

    CAS  Google Scholar 

  • Le Henry M, Charton M, Alignan M, Maury P, Luniov A, Pelletier I, Pontalier P-Y, Binder BM, Vaca-Garcia C, Chervin C (2017) Ethylene stimulates growth and affects fatty acid content of Synechocystis sp. PCC 6803. Algal Res 26:234–239

    Article  Google Scholar 

  • Levitan O, Dinamarca J, Zelzion E, Lun DS, Guerra LT, Kim MK, Kim J, Van Mooy BA, Bhattacharya D, Falkowski PG (2015) Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress. Proc Nat Acad Sci 112:412–417

    Article  CAS  PubMed  Google Scholar 

  • Lin B, Ahmed F, Du H, Li Z, Yan Y, Huang Y, Cui M, Yin Y, Li B, Wang M, Meng C, Gao Z (2018) Plant growth regulators promote lipid and carotenoid accumulation in Chlorella vulgaris. J Appl Phycol 30:1549–1561

    Article  CAS  Google Scholar 

  • Liu JY, Song Y, Qiu W (2017a) Oleaginous microalgae Nannochloropsis as a new model for biofuel production: review & analysis. Renew Sust Energ Rev 72:154–162

    Article  CAS  Google Scholar 

  • Liu F, Wang C, Wang ZY, Liu TT, Li YQ (2017b) Effect of induction with phytohormones analogs on biomass and lipid accumulation in Chlorella vulgaris cells. Chin J Biol 30:390–394 (In Chinese)

    Google Scholar 

  • Lu YD, Jiang P, Liu SF, Gan QH, Cui HL, Qin S (2010) Methyl jasmonate- or gibberellins A3-induced astaxanthin accumulation is associated with up-regulation of transcription of b-carotene ketolase genes (bkts) in microalga Haematococcus pluvialis. Bioresour Technol 101:6468–6474

    Article  CAS  PubMed  Google Scholar 

  • Mohan SV, Rohit MV, Chiranjeevi P, Chandra R, Navaneeth B (2015) Heterotrophic microalgae cultivation to synergize biodiesel production with waste remediation: progress and perspectives. Bioresour Technol 184:169–178

    Article  CAS  Google Scholar 

  • Muhammad S, Zora S, Ahmad SK (2013) Time of methyl jasmonate application influences the development of ‘Cripps Pink’ apple fruit color. J Sci Food Agr 93:611–618

    Article  CAS  Google Scholar 

  • Niu YF, Zhang M, Li D, Yang W, Liu J, Bai W, Li HY (2013) Improvement of neutral lipid and polyunsaturated fatty acid biosynthesis by overexpressing a type 2 diacylglycerol acyltransferase in marine diatom Phaeodactylum tricornutum. Mar Drugs 11:4558–4569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozturk B, Bektas E, Aglar E, Karakaya O, Gun S (2018) Cracking and quality attributes of jujube fruits as affected by covering and pre-harvest Parka and GA(3) treatments. Sci Hortic 240:65–71

    Article  CAS  Google Scholar 

  • Parsaeimehr A, Mancera-Andrade EI, Robledo-Padilla F, Iqbal HMN, Parra-Saldivar R (2017) A chemical approach to manipulate the algal growth, lipid content and high-value alpha-linolenic acid for biodiesel production. Algal Res 26:312–322

    Article  Google Scholar 

  • Peng X, Liu S, Zhang W, Zhao Y, Chen L, Wang H (2014) Triacylglycerol accumulation of Phaeodactylum tricornutum with different supply of inorganic carbon. J Appl Phycol 26:131–139

    Article  CAS  Google Scholar 

  • Thongkum M, McAtee PM, Schaffer RJ, Allan AC, Ketsa S (2018) Characterization and differential expression of ethylene receptor genes during fruit development and dehiscence of durian (Durio zibethinus). Sci Hortic 240:623–630

    Article  CAS  Google Scholar 

  • Vankova R (2012) Abscisic acid signaling in plants. In: Ahamd P (ed) Abiotic stress response in plants. Springer, New York, pp 235–251

    Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  CAS  PubMed  Google Scholar 

  • Xu F, Chen X, Yang Z, Jin P, Wang K, Shang H, Wang X, Zheng Y (2013) Maintaining quality and bioactive compounds of broccoli by combined treatment with 1-methylcyclopropene and 6-benzylaminopurine. J Sci Food Agric 93:1156–1161

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Fan X, Li X, Liu G, Zhang Z, Zhu Y, Fu Z, Qian H (2017) Effect of salicylic acid on fatty acid accumulation in Phaeodactylum tricornutum during stationary growth phase. J Appl Phycol 29:2801–2810

    Article  CAS  Google Scholar 

  • Yang ZK, Niu YF, Ma YH, Xue J, Zhang MH, Yang WD, Liu JS, Lu SH, Guan LF, Li HY (2013) Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol Biofuels 6:67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang ZK, Ma YH, Zheng JW, Yang WD, Liu JS, Li HY (2014) Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum. J Appl Phycol 26:73–82

    Article  CAS  PubMed  Google Scholar 

  • Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (2012) Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell 24:3708–3724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu SJ, Shen XF, Ge HQ (2016) Role of sufficient phosphorus in biodiesel production from diatom Phaeodactylum tricornutum. Appl Microbiol Biotechnol 100:6927–6934

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to acknowledge with apologies many excellent studies that could not be cited due to space limitations. We are grateful to the anonymous reviewers for their valuable improvement to this manuscript. We thank Natalie Kim, PhD, from Liwen Bianji, Edanz Editing, China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Funding

This research was supported by the National Key Research and Development Program of China (2016YFB0601001), the Science and Technology Service Network Initiative of the Chinese Academy of Sciences (KFJ-STS-ZDTP-023), the Project of Innovation & Development of Marine Economy (HHCL201803), the seed project of Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences(YIC755031013).

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Correspondence to Yulin Cui or Song Qin.

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Chu, J., Li, Y., Cui, Y. et al. The influences of phytohormones on triacylglycerol accumulation in an oleaginous marine diatom Phaeodactylum tricornutum. J Appl Phycol 31, 1009–1019 (2019). https://doi.org/10.1007/s10811-018-1623-y

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  • DOI: https://doi.org/10.1007/s10811-018-1623-y

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