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Advances in plant GDSL lipases: from sequences to functional mechanisms

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Abstract

GDSL lipases form multigene families in Arabidopsis, rice and some other sequenced plant species. Unlike classical GxSxG motif-containing lipases, this new sub-family of lipolytic enzymes possesses a GDSL sequence motif (GDSxxDxG), and members are active in the hydrolysis and synthesis of a variety of lipids. Research on plant GDSL lipases started later than studies of microbial and animal GDSL lipases; therefore, our knowledge regarding plant GDSL lipases, from sequences to functional mechanisms, is limited. Recently, some GDSL lipase genes have been cloned and identified in different plant species. In this paper, we present a comprehensive review of the advances in research on plant GDSL lipases, which include their structures, distributions, biochemical activities, expression patterns and biological functions. Plant GDSL lipases have very flexible enzyme active sites, which can lead to extensive substrate binding and result in multifunctional properties. They play important roles in many physiological and biochemical processes, such as plant growth and development, organ morphogenesis, adversity stress and lipid metabolism. In addition, their potential applications in agriculture and industry are discussed.

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References

  • Agee AE, Surpin M, Sohn EJ, Girke T, Rosado A, Kram BW, Carter C, Wentzell AM, Kliebenstein DJ, Jin HC, Park OK, Jin H, Hicks GR, Raikhel NV (2010) MODIFIED VACUOLE PHENOTYPE1 is an Arabidopsis myrosinase-associated protein involved in endomembrane protein trafficking. Plant Physiol 152:120–132

    Article  CAS  Google Scholar 

  • Cao Y, Han Y, Meng D, Abdullah M, Yu J, Li D, Jin Q, Lin Y, Cai Y (2018) Expansion and evolutionary patterns of GDSL-type esterases/lipases in Rosaceae genomes. Funct Integr Genomics 18:673–684

    Article  CAS  Google Scholar 

  • Cheeseman JD, Tocilj A, Park S, Schrag JD, Kazlauskas RJ (2004) Structure of an aryl esterase from Pseudomonas fluorescens. Acta Crystallogr D Biol Crystallogr 60:1237–1243

    Article  Google Scholar 

  • Chen M, Du X, Zhu Y, Wang Z, Hua S, Li Z, Guo W, Zhang G, Peng J, Jiang L (2012) Seed fatty acid reducer acts downstream of gibberellin signalling pathway to lower seed fatty acid storage in Arabidopsis. Plant Cell Environ 35:2155–2169

    Article  CAS  Google Scholar 

  • Chepyshko H, Lai CP, Huang LM, Liu JH, Shaw JF (2012) Multifunctionality and diversity of GDSL esterase/lipase gene family in rice (Oryza sativa L. japonica) genome: new insights from bioinformatics analysis. BMC Genomics 13:309

    Article  CAS  Google Scholar 

  • Clauss K, Baumert A, Nimtz M, Milkowski C, Strack D (2008) Role of a GDSL lipase-like protein as sinapine esterase in Brassicaceae. Plant J 53:802–813

    Article  CAS  Google Scholar 

  • Clauss K, von Roepenack-Lahaye E, Böttcher C, Roth MR, Welti R, Erban A, Kopka J, Scheel D, Milkowski C, Strack D (2011) Overexpression of sinapine esterase BnSCE3 in oilseed rape seeds triggers global changes in seed metabolism. Plant Physiol 155:1127–1145

    Article  CAS  Google Scholar 

  • Correia MA, Prates JA, Brás J, Fontes CM, Newman JA, Lewis RJ, Gilbert HJ, Flint JE (2008) Crystal structure of a cellulosomal family 3 carbohydrate esterase from Clostridium thermocellum provides insights into the mechanism of substrate recognition. J Mol Biol 379:64–72

    Article  CAS  Google Scholar 

  • Cummins I, Edwards R (2004) Purification and cloning of an esterase from the weed black-grass (Alopecurus myosuroides), which bioactivates aryloxyphenoxypropionate herbicides. Plant J 39:894–904

    Article  CAS  Google Scholar 

  • Ding LN, Guo XJ, Li M, Fu ZL, Yan SZ, Zhu KM, Wang Z, Tan XL (2019) Improving seed germination and oil contents by regulating the GDSL transcriptional level in Brassica napus. Plant Cell Rep 38:243–253

    Article  CAS  Google Scholar 

  • Dong X, Yi H, Han CT, Nou IS, Hur Y (2016) GDSL esterase/lipase genes in Brassica rapa L.: genome-wide identification and expression analysis. Mol Genet Genomics 291:531–542

    Article  CAS  Google Scholar 

  • Gao M, Yin X, Yang W, Lam SM, Tong X, Liu J, Wang X, Li Q, Shui G, He Z (2017) GDSL lipases modulate immunity through lipid homeostasis in rice. PLoS Pathog 13:e1006724

    Article  Google Scholar 

  • Girard AL, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J, Runavot JL, Quemener B, Petit J, Germain V, Rothan C, Marion D, Bakan B (2012) Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24:3119–3134

    Article  CAS  Google Scholar 

  • He W, Li L, Zhao J, Xu H, Rui J, Cui D, Li H, Zhang H, Liu X (2019) Candida sp. 99–125 lipase-catalyzed synthesis of ergosterol linolenate and its characterization. Food Chem 280:286–293

    Article  CAS  Google Scholar 

  • Hong JK, Choi HW, Hwang IS, Kim DS, Kim NH, Choi DS, Kim YJ, Hwang BK (2008) Function of a novel GDSL-type pepper lipase gene, CaGLIP1, in disease susceptibility and abiotic stress tolerance. Planta 227:539–558

    Article  CAS  Google Scholar 

  • Jiang YY, Chen RJ, Dong JL, Xu ZJ, Gao XL (2012) Analysis of GDSL lipase (GLIP) family genes in rice (Oryza sativa). Plant Omics J 5:351–358

    CAS  Google Scholar 

  • Kandzia R, Grimm R, Eckerskorn C, Lindemann P, Luckner M (1998) Purification and characterization of lanatoside 15′-O-acetylesterase from Digitalis lanata Ehrh. Planta 204:383–389

    Article  CAS  Google Scholar 

  • Kikuta Y, Ueda H, Takahashi M, Mitsumori T, Yamada G, Sakamori K, Takeda K, Furutani S, Nakayama K, Katsuda Y, Hatanaka A, Matsuda K (2012) Identification and characterization of a GDSL lipase-like protein that catalyzes the ester-forming reaction for pyrethrin biosynthesis in Tanacetum cinerariifolium-a new target for plant protection. Plant J 71:183–193

    Article  CAS  Google Scholar 

  • Kikuta Y, Yamada G, Mitsumori T, Takeuchi T, Nakayama K, Katsuda Y, Hatanaka A, Matsuda K (2013) Requirement of catalytic-triad and related amino acids for the acyltransferase activity of Tanacetum cinerariifolium GDSL lipase/esterase TcGLIP for ester-bond formation in pyrethrin biosynthesis. Biosci Biotechnol Biochem 77:1822–1825

    Article  CAS  Google Scholar 

  • Kim KJ, Lim JH, Kim MJ, Kim T, Chung HM, Paek KH (2008) GDSL-lipase1 (CaGL1) contributes to wound stress resistance by modulation of CaPR-4 expression in hot pepper. Biochem Biophys Res Commun 374:693–698

    Article  CAS  Google Scholar 

  • Kim HG, Kwon SJ, Jang YJ, Nam MH, Chung JH, Na YC, Guo H, Park OK (2013) GDSL LIPASE1 modulates plant immunity through feedback regulation of ethylene signaling. Plant Physiol 163:1776–1791

    Article  CAS  Google Scholar 

  • Kim HG, Kwon SJ, Jang YJ, Chung JH, Nam MH, Park OK (2014) GDSL lipase 1 regulates ethylene signaling and ethylene-associated systemic immunity in Arabidopsis. FEBS Lett 588:1652–1658

    Article  CAS  Google Scholar 

  • Kondou Y, Nakazawa M, Kawashima M, Ichikawa T, Yoshizumi T, Suzuki K, Ishikawa A, Koshi T, Matsui R, Muto S, Matsui M (2008) RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol 147:1924–1935

    Article  CAS  Google Scholar 

  • Kram BW, Bainbridge EA, Perera MA, Carter C (2008) Identification, cloning and characterization of a GDSL lipase secreted into the nectar of lee. Plant Mol Biol 68:173–183

    Article  CAS  Google Scholar 

  • Kwon SJ, Jin HC, Lee S, Nam MH, Chung JH, Kwon SI, Ryu CM, Park OK (2009) GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant J 58:235–245

    Article  CAS  Google Scholar 

  • Lai CP, Huang LM, Chen LO (2017) Genome-wide analysis of GDSL-type esterases/lipases in Arabidopsis. Plant Mol Biol 95:181–197

    Article  CAS  Google Scholar 

  • Lee KA, Cho TJ (2003) Characterization of a salicylic acid- and pathogen-induced lipase-like gene in Chinese cabbage. J Biochem Mol Biol 36:433–441

    CAS  PubMed  Google Scholar 

  • Lee DS, Kim BK, Kwon SJ, Jin HC, Park OK (2009) Arabidopsis GDSL lipase 2 plays a role in pathogen defense via negative regulation of auxin signaling. Biochem Biophys Res Commun 379:1038–1042

    Article  CAS  Google Scholar 

  • Li ZL, Hua SJ, Jiang LX (2014) Advances in studying plant GDSL-type lipase genes. J Agr Biotechnol 22:916–924

    CAS  Google Scholar 

  • Ling H (2008) Sequence analysis of GDSL lipase gene family in Arabidopsis thaliana. Pak J Biol Sci 11:763–767

    Article  Google Scholar 

  • Ling H, Zhao J, Zuo K, Qiu C, Yao H, Qin J, Sun X, Tang K (2006) Isolation and expression analysis of a GDSL-like lipase gene from Brassica napus L. J Biochem Mol Biol 39:297–303

    CAS  PubMed  Google Scholar 

  • Lo YC, Lin SC, Shaw JF, Liaw YC (2003) Crystal structure of Escherichia coli thioesterase I/protease I/lysophospholipase L1: consensus sequence blocks constitute the catalytic center of SGNH-hydrolases through a conserved hydrogen bond network. J Mol Biol 330:539–551

    Article  CAS  Google Scholar 

  • Ma R, Yuan H, An J, Hao X, Li H (2018) A Gossypium hirsutum GDSL lipase/hydrolase gene (GhGLIP) appears to be involved in promoting seed growth in Arabidopsis. PLoS One 13:e0195556

    Article  Google Scholar 

  • Mangos TJ, Jones KC, Foglia TA (1999) Lipase-catalyzed synthesis of structured low-calorie triacylglycerols. J Am Oil Chem Soc 76:1127–1132

    Article  CAS  Google Scholar 

  • Miyazawa T, Onishi K, Murashima T, Yamada T, Tsai SW (2005) Resolution of non-protein amino acids via Carica papaya lipase-catalyzed enantioselective transesterification. Cheminform 16:2569–2573

    CAS  Google Scholar 

  • Muralidharan M, Buss K, Larrimore KE, Segerson NA, Kannan L, Mor TS (2013) The Arabidopsis thaliana ortholog of a purported maize cholinesterase gene encodes a GDSL-lipase. Plant Mol Biol 81:565–576

    Article  CAS  Google Scholar 

  • Naranjo MA, Forment J, RoldÁN M, Serrano R, Vicente O (2006) Overexpression of Arabidopsis thaliana LTL1, a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in yeast and transgenic plants. Plant Cell Environ 29:1890–1900

    Article  CAS  Google Scholar 

  • Ng IS, Tsai SW (2005) Partially purified Carica papaya lipase: a versatile biocatalyst for the hydrolytic resolution of (R, S)-2-arylpropionic thioesters in water-saturated organic solvents. Biotechnol Bioeng 91:106–113

    Article  CAS  Google Scholar 

  • Oh IS, Park AR, Bae MS, Kwon SJ, Kim YS, Lee JE, Kang NY, Lee S, Cheong H, Park OK (2005) Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17:2832–2847

    Article  CAS  Google Scholar 

  • Park JJ, Jin P, Yoon J, Yang JI, Jeong HJ, Ranathunge K, Schreiber L, Franke R, Lee IJ, An G (2010) Mutation in Wilted Dwarf and Lethal 1 (WDL1) causes abnormal cuticle formation and rapid water loss in rice. Plant Mol Biol 74:91–103

    Article  CAS  Google Scholar 

  • Philippe G, Gaillard C, Petit J, Geneix N, Dalgalarrondo M, Bres C, Mauxion JP, Franke R, Rothan C, Schreiber L, Marion D, Bakan B (2016) Ester cross-link profiling of the cutin polymer of wild-type and cutin synthase tomato mutants highlights different mechanisms of polymerization. Plant Physiol 170:807–820

    Article  CAS  Google Scholar 

  • Pinyaphong P, Phutrakul S (2009) Synthesis of cocoa butter equivalent from palm oil by Carica papaya lipase-catalyzed interesterification. Chiang Mai J Sci 36:359–368

    CAS  Google Scholar 

  • Pringle D, Dickstein R (2004) Purification of ENOD8 proteins from Medicago sativa root nodules and their characterization as esterases. Plant Physiol Biochem 42:73–79

    Article  CAS  Google Scholar 

  • Reina JJ, Guerrero C, Heredia A (2007) Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. leaf epidermis. J Exp Bot 58:2717–2731

    Article  CAS  Google Scholar 

  • Riemann M, Gutjahr C, Korte A, Riemann M, Danger B, Muramatsu T, Bayer U, Waller F, Furuya M, Nick P (2007) GER1, a GDSL motif-encoding gene from rice is a novel early light- and jasmonate-induced gene. Plant Biol (Stuttg) 9:32–40

    Article  CAS  Google Scholar 

  • Rombolá-Caldentey B, Rueda-Romero P, Iglesias-Fernández R, Carbonero P, Oñate-Sánchez L (2014) Arabidopsis DELLA and two HD-ZIP transcription factors regulate GA signaling in the epidermis through the L1 box cis-element. Plant Cell 26:2905–2919

    Article  Google Scholar 

  • Ruppert M, Woll J, Giritch A, Genady E, Ma X, Stöckigt J (2005) Functional expression of an ajmaline pathway-specific esterase from Rauvolfia in a novel plant-virus expression system. Planta 222:888–898

    Article  CAS  Google Scholar 

  • Sagane Y, Nakagawa T, Yamamoto K, Michikawa S, Oguri S, Momonoki YS (2005) Molecular characterization of maize acetylcholinesterase: a novel enzyme family in the plant kingdom. Plant Physiol 138:1359–1371

    Article  CAS  Google Scholar 

  • Takahashi K, Shimada T, Kondo M, Tamai A, Mori M, Nishimura M, Hara-Nishimura I (2010) Ectopic expression of an esterase, which is a candidate for the unidentified plant cutinase, causes cuticular defects in Arabidopsis thaliana. Plant Cell Physiol 51:123–131

    Article  CAS  Google Scholar 

  • Tecelão C, Rivera I, Sandoval G, Ferreira-Dia S (2012) Carica papaya latex: a low-cost biocatalyst for human milk fat substitutes production. Eur J Lipid Sci Technol 114:266–276

    Article  Google Scholar 

  • Updegraff EP, Zhao F, Preuss D (2009) The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen. Sex Plant Reprod 22:197–204

    Article  CAS  Google Scholar 

  • Upton C, Buckley JT (1995) A new family of lipolytic enzymes? Trends Biochem Sci 20:178–179

    Article  CAS  Google Scholar 

  • Volokita M, Rosilio-Brami T, Rivkin N, Zik M (2011) Combining comparative sequence and genomic data to ascertain phylogenetic relationships and explore the evolution of the large GDSL-lipase family in land plants. Mol Biol Evol 28:551–565

    Article  CAS  Google Scholar 

  • Yamamoto K, Oguri S, Momonoki YS (2008) Characterization of trimeric acetylcholinesterase from a legume plant, Macroptilium atropurpureum Urb. Planta 227:809–822

    Article  CAS  Google Scholar 

  • Yamamoto K, Oguri S, Chiba S, Momonoki YS (2009) Molecular cloning of acetylcholinesterase gene from Salicornia europaea L. Plant Signal Behav 4:361–366

    Article  CAS  Google Scholar 

  • Youens-Clark K, Buckler E, Casstevens T, Chen C, Declerck G, Derwent P, Dharmawardhana P, Jaiswal P, Kersey P, Karthikeyan AS, Lu J, McCouch SR, Ren L, Spooner W, Stein JC, Thomason J, Wei S, Ware D (2011) Gramene database in 2010: updates and extensions. Nucleic Acids Res 39(Database issue):D1085–D1094

    Article  CAS  Google Scholar 

  • Zhang H, Zhou J, Zheng X, Zhang Z, Wang Z, Tan X (2016a) Characterization of a desiccation stress induced lipase gene from Brassica napus L. J Agric Sci Tech 18:1129–1141

    Google Scholar 

  • Zhang Z, Ober JA, Kliebenstein DJ (2016b) The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis. Plant Cell 18:1524–1536

    Article  Google Scholar 

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Acknowledgements

We acknowledge financial support by Grant Nos. 2016YFD0101904 and 2016YFD0100305 from the National Key R&D Program of China, and 31471527 and 31271760 from the National Natural Science Foundation of China.

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Authors and Affiliations

  1. Institute of Life Sciences, Jiangsu University, Zhenjiang, China

    Li-Na Ding, Ming Li, Wei-Jie Wang, Jun Cao, Zheng Wang, Ke-Ming Zhu, Yan-Hua Yang, Yu-Long Li & Xiao-Li Tan

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  1. Li-Na Ding
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  2. Ming Li
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Correspondence to Xiao-Li Tan.

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Communicated by M. Prasad.

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Ding, LN., Li, M., Wang, WJ. et al. Advances in plant GDSL lipases: from sequences to functional mechanisms. Acta Physiol Plant 41, 151 (2019). https://doi.org/10.1007/s11738-019-2944-4

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