Key message
Castor patatin-like phospholipase A IIIβ facilitates the exclusion of hydroxy fatty acids from phosphatidylcholine in developing transgenic Arabidopsis seeds.
Abstract
Hydroxy fatty acids (HFAs) are industrial useful, but their major natural source castor contains toxic components. Although expressing a castor OLEATE 12-HYDROXYLASE in Arabidopsis thaliana leads to the synthesis of HFAs in seeds, a high proportion of the HFAs are retained in phosphatidylcholine (PC). Thus, the liberation of HFA from PC seems to be critical for obtaining HFA-enriched seed oils. Plant phospholipase A (PLA) catalyzes the hydrolysis of PC to release fatty acyl chains that can be subsequently channeled into triacylglycerol (TAG) synthesis or other metabolic pathways. To further our knowledge regarding the function of PLAs from HFA-producing plant species, two class III patatin-like PLA cDNAs (pPLAIIIβ or pPLAIIIδ) from castor or Physaria fendleri were overexpressed in a transgenic line of A. thaliana producing C18-HFA, respectively. Only the overexpression of RcpPLAIIIβ resulted in a significant reduction in seed HFA content with concomitant changes in fatty acid composition. Reductions in HFA content occurred in both PC and TAG indicating that HFAs released from PC were not incorporated into TAG. These results suggest that RcpPLAIIIβ may catalyze the removal of HFAs from PC in the developing seeds synthesizing these unusual fatty acids.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adhikari ND, Bates PD, Browse J (2016) WRINKLED1 rescues feedback inhibition of fatty acid synthesis in hydroxylase-expressing seeds. Plant Physiol 171(1):179–191. https://doi.org/10.1104/pp.15.01906
Bafor M, Smith MA, Jonsson L, Stobart K, Stymne S (1991) Ricinoleic acid biosynthesis and triacylglycerol assembly in microsomal preparations from developing castor-bean (Ricinus communis) endosperm. Biochem J 280(2):507–514. https://doi.org/10.1042/bj2800507
Bates D, Browse J (2011) The pathway of triacylglycerol synthesis through phosphatidylcholine in Arabidopsis produces a bottleneck for the accumulation of unusual fatty acids in transgenic seeds. Plant J 68(3):387–399. https://doi.org/10.1111/j.1365-313X.2011.04693.x
Bates PD, Browse J (2012) The significance of different diacylgycerol synthesis pathways on plant oil composition and bioengineering. Front Plant Sci 3:147. https://doi.org/10.3389/fpls.2012.00147
Bates PD, Fatihi A, Snappp AR, Carlsson AS, Browse J, Lu C (2012) Acyl editing and headgroup exchange are the major mechanisms that direct polyunsaturated fatty acid flux into triacylglycerols. Plant Physiol 160(3):1530–1539. https://doi.org/10.1104/pp.112.204438
Bates PD, Stymne S, Ohlrogge J (2013) Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol 16(3):358–364. https://doi.org/10.1016/j.pbi.2013.02.015
Bates PD, Johnson SR, Cao X, Li J, Nam J-W, Jaworski JG, Ohlrogge JB, Browse J (2014) Fatty acid synthesis is inhibited by inefficient utilization of unusual fatty acids for glycerolipid assembly. Proc Natl Acad Sci USA 111(3):1204–1209. https://doi.org/10.1073/pnas.1318511111
Bayon S, Chen G, Weselake RJ, Browse J (2015) A small phospholipase A2-α from castor catalyzes the removal of hydroxy fatty acids from phosphatidylcholine in transgenic Arabidopsis seeds. Plant Physiol 167(4):1259–1270. https://doi.org/10.1104/pp.114.253641
Bent A (2006) Arabidopsis thaliana floral dip transformation method. Methods Mol Biol 343:87–103. https://doi.org/10.1385/1-59745-130-4:87
Broun P, Somerville C (1997) Accumulation of ricinoleic, lesquerolic, and densipolic acids in seeds of transgenic Arabidopsis plants that express a fatty acyl hydroxylase cDNA from castor bean. Plant Physiol 113(3):933–942. https://doi.org/10.1104/pp.113.3.933
Broun P, Boddupalli S, Somerville C (1998) A bifunctional oleate 12-hydroxylase: desaturase from Lesquerella fendleri. Plant J 13(2):201–210
Brown AP, Kroon JT, Swarbreck D, Febrer M, Larson TR, Graham IA, Caccamo M, Slabas AR (2012) Tissue-specific whole transcriptome sequencing in castor, directed at understanding triacylglycerol lipid biosynthetic pathways. PLoS ONE 7(2):e30100. https://doi.org/10.1371/journal.pone.0030100
Burgal J, Shockey J, Lu C, Dyer J, Larson T, Graham I, Browse J (2008) Metabolic engineering of hydroxy fatty acid production in plants: RcDGAT2 drives dramatic increases in ricinoleate levels in seed oil. Plant Biotechnol J 6(8):819–831. https://doi.org/10.1111/j.1467-7652.2008.00361.x
Chen G (2016) Lesquerella (Physaria spp.). In: McKeon T, Hayes DH, Hildebrand DF, Weselake RJ (eds) Industrial oil crops. Elsevier/AOCS Press, New York/Urbana, pp 313–316
Chen GQ, He X, Liao LP, McKeon TA (2004) 2S albumin gene expression in castor plant (Ricinus communis L.). J Am Oil Chem Soc 81(9):867–872. https://doi.org/10.1007/s11746-004-0993-5
Chen GQ, Lin J-T, Lu C (2011a) Hydroxy fatty acid synthesis and lipid gene expression during seed development in Lesquerella fendleri. Ind Crops Prod 34(2):1286–1292. https://doi.org/10.1016/j.indcrop.2010.08.003
Chen G, Snyder CL, Greer MS, Weselake RJ (2011b) Biology and biochemistry of plant phospholipases. Crit Rev Plant Sci 30(3):239–258. https://doi.org/10.1080/07352689.2011.572033
Chen G, Greer MS, Lager I, Yilmaz JL, Mietkiewska E, Carlsson AS, Stymne S, Weselake RJ (2012) Identification and characterization of an LCAT-like Arabidopsis thaliana gene encoding a novel phospholipase A. FEBS Lett 586(4):373–377. https://doi.org/10.1016/j.febslet.2011.12.034
Chen G, Greer MS, Weselake RJ (2013) Plant phospholipase A: advances in molecular biology, biochemistry, and cellular function. Biomol Concepts 4(5):527–532. https://doi.org/10.1515/bmc-2013-0011
Chen G, Woodfield HK, Pan X, Harwood JL, Weselake RJ (2015) Acyl-trafficking during plant oil accumulation. Lipids 50(11):1057–1068. https://doi.org/10.1007/s11745-015-4069-x
Chen GQ, van Erp H, Martin-Moreno J, Johnson K, Morales E, Eastmond PJ, Lin J-T (2016) Expression of castor LPAT2 enhances ricinoleic acid content at the sn-2 position of triacylglycerols in Lesquerella seed. Int J Mol Sci 17(4):507. https://doi.org/10.3390/ijms17040507
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Dauk M, Lam P, Kunst L, Smith MA (2007) A FAD2 homologue from Lesquerella lindheimeri has predominantly fatty acid hydroxylase activity. Plant Sci 73(1):43–49. https://doi.org/10.1016/j.plantsci.2007.03.015
Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne S (2000) Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci USA 97(12):6487–6492. https://doi.org/10.1073/pnas.120067297
de Marcos Lousa C, van Roermund CW, Postis VL, Dietrich D, Kerr ID, Wanders RJ, Baldwin SA, Baker A, Theodoulou FL (2013) Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporter is required for transport and metabolism of fatty acids. Proc Natl Acad Sci USA 110(4):1279–1284. https://doi.org/10.1073/pnas.1218034110
Dierig D, Tomasi PM, Dahlqvist GH (2006) Registration of WCL-LY2 high oil Lesquerella fendleri germplasm. Crop Sci 46(4):604–605. https://doi.org/10.2135/cropsci2006.02-0103
Dierig D, Wang G, McCloskey W, Thorp K, Isbell T, Ray D, Foster MA (2011) Lesquerella: new crop development and commercialization in the US. Ind Crops Prod 34(2):1381–1385. https://doi.org/10.1016/j.indcrop.2010.12.023
Dong Y, Li M, Zhang P, Wang X, Fan C, Zhou Y (2014) Patatin-related phospholipase pPLAIIIδ influences auxin-responsive cell morphology and organ size in Arabidopsis and Brassica napus. BMC Plant Biol. https://doi.org/10.1186/s12870-014-0332-1
Goderis IJ, de Bolle MF, François IE, Wouters PF, Broekaert WF, Cammue BP (2002) A set of modular plant transformation vectors allowing flexible insertion of up to six expression units. Plant Mol Biol 50(1):17–27. https://doi.org/10.1023/A:1016052416053
He X, Chen GQ, Kang ST, McKeon TA (2007) Ricinus communis contains an acyl-CoA synthetase that preferentially activates ricinoleate to its CoA thioester. Lipids 42(10):931–938. https://doi.org/10.1007/s11745-007-3090-0
Horn PJ, Liu J, Cocuron J-C, McGlew K, Thrower NA, Larson M, Lu C, Alonso AP, Ohlrogge J (2016) Identification of multiple lipid genes with modifications in expression and sequence associated with the evolution of hydroxyl fatty acid accumulation in Physaria fendleri. Plant J 86(4):322–348. https://doi.org/10.1111/tpj.13163
Hu Z, Ren Z, Lu C (2012) The phosphatidylcholine diacylglycerol cholinephosphotransferase is required for efficient hydroxyl fatty acid accumulation in transgenic Arabidopsis. Plant Physiol 158(4):1944–1954. https://doi.org/10.1104/pp.111.192153
Jaworski J, Cahoon EB (2003) Industrial oils from transgenic plants. Curr Opin Plant Biol 6(2):178–184. https://doi.org/10.1016/s1369-5266(03)00013-x
Jayawardhane KN, Singer SD, Weselake RJ, Chen G (2018) Plant sn-glycerol-3-phosphate acyltransferases: biocatalysts involved in the biosynthesis of intracellular and extracellular lipids. Lipids 53(5):469–480. https://doi.org/10.1002/lipd.12049
Jessen D, Roth C, Wiermer M, Fulda M (2015) Two activities of long-chain acyl-coenzyme A synthetase are involved in lipid trafficking between the endoplasmic reticulum and the plastid in arabidopsis. Plant Physiol 167(2):351–366. https://doi.org/10.1104/pp.114.250365
Kennedy EP (1961) Biosynthesis of complex lipids. Fed Proc 20:934–940
Kim HU, Chen GQ (2015) Identification of hydroxyl fatty acid and triacyglycerol metabolism-related genes in lesquerella through seed transcriptome analysis. BMC Genom 16:230. https://doi.org/10.1186/s12864-015-1413-8
Kim HU, Lee K-R, Go YS, Jung JH, Suh M-C, Kim JB (2011) Endoplasmic reticulum-located PDAT1-2 from castor bean enhances hydroxyl fatty acid accumulation in transgenic plants. Plant Cell Physiol 52(6):983–993. https://doi.org/10.1093/pcp/pcr051
Kroon JT, Wei W, Simon WJ, Slabas AR (2006) Identification and functional expression of a type 2 acyl-CoA: diacylglycerol acyltransferase (DGAT2) in developing castor bean seeds which has high homology to the major triglyceride biosynthetic enzyme of fungi and animals. Phytochemistry 67(23):2541–2549. https://doi.org/10.1016/j.phytochem.2006.09.020
Kumar R, Wallis JG, Skidmore C, Browse J (2006) A mutation in Arabidopsis cytochrome b5 reductase identified by high-throughput screening differentially affects hydroxylation and desaturation. Plant J 48(6):920–932. https://doi.org/10.1111/j.1365-313X.2006.02925.x
Kunst L, Taylor DC, Underhill EW (1992) Fatty acid elongation in developing seeds of Arabidopsis thaliana. Plant Physiol Biochem 30(4):425–434
Lager I, Yilmaz JL, Zhou XR et al (2013) Plant acyl-CoA: lysophosphatidylcholine acyltransferases (LPCATs) have different specificities in their forward and reverse reactions. J Biol Chem 288(52):36902–36914. https://doi.org/10.1074/jbc.M113.521815J
Lands WEM (1960) Metabolism of glycerolipids. 2. The enzymatic acylation of lyolecithin. J Biol Chem 235(8):2233–2237
Lee K, Chen GQ, Kim HU (2015) Current progress towards the metabolic engineering of plant seed oil for hydroxy fatty acids production. Plant Cell Rep 34(4):603–615. https://doi.org/10.1007/s00299-015-1736-6
Li M, Bahn SC, Guo L, Musgrave W, Berg H, Welti R, Wang X (2011) Patatin-related phospholipase pPLAIIIβ-induced changes in lipid metabolism alter cellulose content and cell elongation in Arabidopsis. Plant Cell 23(3):1107–1123. https://doi.org/10.1105/tpc.110.081240
Li M, Bahn SC, Fan C, Li J, Phan T, Ortiz M, Roth MR, Welti R, Jaworski J, Wang X (2013) Patatin-related phospholipase pPLAIII δ increases seed oil content with long-chain fatty acids in Arabidopsis. Plant Physiol 162(1):39–51. https://doi.org/10.1104/pp.113.216994
Li M, Wei F, Tawfall A, Tang M, Saettele A, Wang X (2015) Overexpression of patatin-related phospholipase AIIIδ altered plant growth and increased seed oil content in camelina. Plant Biotechnol J 13(6):766–778. https://doi.org/10.1111/pbi.12304
Lin J, Woodruff CL, Lagouche OJ, McKeon TA, Stafford AE, Goodrich-Tanrikulu M, Singleton JA, Haney CA (1998) Biosynthesis of triacylglycerols containing ricinoleate in castor microsomes using 1-acyl-2-oleoyl-sn-glycero-3-phosphocholine as the substrate of oleoyl-12-hydroxylase. Lipids 33(1):59–69
Lin J, Turner C, Liao LP, McKeon TA (2003) Identification and quantification of the molecular species of acylglycerols in castor oil by HPLC using ELSD. J Liq Chromatogr Relat Technol 26(5):773–780. https://doi.org/10.1081/JLC-120018421
Liu Q, Siloto RM, Lehner R, Storne SJ, Weselake RJ (2012) Acyl-CoA: diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Prog Lipid Res 51(4):350–377. https://doi.org/10.1016/j.plipres.2012.06.001
Liu G, Zhang K, Ai J, Deng X, Hong Y, Wang X (2015) Patatin-related phospholipase A, pPLAIIIα, modulates the longitudinal growth of vegetative tissues and seeds in rice. J Exp Bot 66(21):6945–6955. https://doi.org/10.1093/jxb/erv402
Lu C, Fulda M, Wallis JG, Browse J (2006) A high-throughput screen for genes from castor that boost hydroxy fatty acid accumulation in seed oils of transgenic Arabidopsis. Plant J 45(5):847–856. https://doi.org/10.1111/j.1365-313X.2005.02636.x
Lu C, Xin Z, Ren Z, Miquel M, Browse J (2009) An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis. Proc Natl Acad Sci USA 106(44):18837–18842. https://doi.org/10.1073/pnas.0908848106
Lunn D, Wallis JG, Browse J (2018a) Overexpression of Seipin 1 increases oil in hydroxyl fatty acid-accumulating seeds. Plant Cell Physiol 59(1):205–214. https://doi.org/10.1093/pcp/pcx177
Lunn D, Smith GA, Wallis JG, Browse J (2018b) Development defects of hydroxyl-fatty acid-accumulating seeds are reduced by castor acyltransferases. Plant Physiol 177(2):553–564. https://doi.org/10.1104/pp.17.01805
Lunn D, Wallis JG, Browse J (2019) Tri-hydroxy-triacylglycerol is efficiently produced by position-specific castor acyltransferases. Plant Physiol 179(3):1050–1063. https://doi.org/10.1104/pp.18.01409
Mavraganis I, Meesapyodsuk D, Vrinten P, Smith M, Qiu X (2010) Type II diacylglycerol acyltransferase from Claviceps purpurea with ricinoleic acid, a hydroxyl fatty acid of industrial importance, as preferred substrate. Appl Environ Microbiol 76(4):1135–1142. https://doi.org/10.1128/aem.02297-09
McKeon TA (2016) Castor (Ricinus communis L.). In: McKeon T, Hayes DH, Hildebrand DF, Weselake RJ (eds) Industrial oil crops. Elsevier/AOCS Press, New York/Urbana, pp 75–112
McKeon TA, He X (2015) Castor diacylglycerol acyltransferase type 1 (DGAT1) displays greater activity with diricinolein than Arabidopsis DGAT1. Biocat Agri Biotechnol 4(2):276–278. https://doi.org/10.1016/j.bcab.2015.01.005
Meesapyodsuk D, Qiu X (2008) An oleate hydroxylase from the fungus Claviceps purpurea: cloning, functional analysis, and expression in Arabidopsis. Plant Physiol 147(3):1325–1333. https://doi.org/10.1104/pp.108.117168
Mietkiewska E, Miles R, Wickramarathna A, Sahibollah AF, Greer MS, Chen G, Weselake RJ (2014) Combined transgenic expression of Punica granatum conjugase (FADX) and FAD2 desaturase in high linoleic acid Arabidopsis thaliana mutant leads to increased accumulation of punicic acid. Planta 240(3):575–583. https://doi.org/10.1007/s00425-014-2109-z
Millar AA, Smith MA, Kunst L (2000) All fatty acids are not equal: discrimination in plant membrane lipids. Trends Plant Sci 5(3):95–101
Moire L, Rezzenico E, Goepfert S, Poirier Y (2004) Impact of unusual fatty acid synthesis on futile cycling through beta-oxidation and on gene expression in transgenic plants. Plant Physiol 134(1):432–442. https://doi.org/10.1104/pp.103.032938
Moon H, Smith MA, Kunst L (2001) A condensing enzyme from the seeds of Lesquerella fendleri that specifically elongates hydroxy fatty acids. Plant Physiol 127(4):1635–1643. https://doi.org/10.1104/pp.010544
Mutlu H, Meier MAR (2010) Castor oil as a renewable resource for the chemical industry. Eur J Lipid Sci Technol 112(1):10–30. https://doi.org/10.1002/ejlt.200900138
Ogunniyi DS (2006) Castor oil: a vital industrial raw material. Bioresour Biotechnol 97(9):1086–1091. https://doi.org/10.1016/j.biortech.2005.03.028
Shockey J, Regmi A, Cotton K, Adhikari N, Browse J, Bates PD (2016) Identification of Arabidopsis GPAT9 (At5g60620) as an essential gene involved in triacylglycerol biosynthesis. Plant Physiol 170(1):163–179. https://doi.org/10.1104/pp.15.01563
Shockey J, Lager I, Stymne S, Kotapati HK, Sheffield J, Mason C, Bates PD (2019) Specialized lysophosphatidic acid acyltransferases contribute to unusual fatty acid accumulation in exotic Euphorbiaceae seed oils. Planta 249(5):1285–1299. https://doi.org/10.1007/s00425-018-03086-y
Singer SD, Weselake RJ (2018) Production of other bioproducts from plant oils. In: Chen G, Weselake RJ, Singer SD (eds) Plant Bioproducts. Springer Science + Business Media,LLC part of Springer Nature, New York, pp 59–85
Singer S, Chen G, Mietkiewska E, Tomasi P, Jayawardhane K, Dyer J, Weselake RJ (2016) Arabidopsis GPAT9 contributes to synthesis of intracellular glycerolipids but not surface lipids. J Exp Bot 67(15):4627–4638. https://doi.org/10.1093/jxb/erw242
Smith MA, Moon H, Chowrira G, Kunst L (2003) Heterologous expression of a fatty acid hydroxylase gene in developing seeds of Arabidopsis thaliana. Planta 217(3):507–516. https://doi.org/10.1007/s00425-003-1015-6
Snapp AR, Kang J, Qi X, Lu C (2014) A fatty acid condensing enzyme from Physaria fendleri increases hydroxy fatty acid accumulation in transgenic oilseeds of Camelina sativa. Planta 240(3):599–610. https://doi.org/10.1007/s00425-014-2122-2
Ståhl U, Banas A, Stymne S (1995) Plant microsomal phospholipid acyl hydrolases have selectivities for uncommon fatty acids. Plant Physiol 107(3):953–962. https://doi.org/10.1104/pp.107.3.953
Thomæus S, Carlsson AS, Stymne S (2001) Distribution of fatty acids in polar and neutral lipids during seed development in Arabidopsis thaliana genetically engineered to produce acetylenic, epoxy and hydroxy fatty acids. Plant Sci 161(5):997–1003. https://doi.org/10.1016/S0168-9452(01)00500-3
Van De Loo PJ, Broun P, Turner S, Somerville C (1995) An oleate-12 hydroxylase from Ricinus communis L. is a fatty acyl desaturase homolog. Proc Natl Acad Sci USA 92(15):6743–6747
van Erp H, Bates PD, Burgal J, Shockey J, Browse J (2011) Castor phospholipid: diacylglycerol acyltransferase facilitates efficient metabolism of hydroxy fatty acids in transgenic Arabidopsis. Plant Physiol 155(2):683–693. https://doi.org/10.1104/pp.110.167239
van Erp H, Shockey J, Zhang M, Adhikari ND, Browse J (2015) Reducing isozyme competition increases target fatty acid accumulation in seed triacylglycerols of transgenic Arabidopsis. Plant Physiol 168(1):36–46. https://doi.org/10.1104/pp.114.254110
Vanhercke T, Wool CC, Stymne S, Singh SP, Green AG (2013) Metabolic engineering of plant oils and waxes for use as industrial feedstocks. Plant Biotechnol J 11(2):197–210. https://doi.org/10.1111/pbi.12023
Wang L, Shen W, Kazachkov M, Chen G, Chen Q, Carlsson AS, Stymne S, Weselake RJ, Zou J (2012) Metabolic interactions between the lands cycle and the Kennedy pathway of glycerolipid synthesis in Arabidopsis developing seeds. Plant Cell 24(11):4652–4669. https://doi.org/10.1105/tpc.112.104604
Waschburger E, Kulcheski FR, Veto NM, Margis R, Margis-Pinheiro M, Turchetto-Zolet AC (2018) Genome-wide analysis of the glycerol-3-phosphate acyltransferase (GPAT) gene family reveals the evolution and diversification of plant GPATs. Genet Mol Biol 41(1 suppl 1):355–370. https://doi.org/10.1590/1678-4685-GMB-2017-0076
Xu Y, Caldo KMP, Pal-Nath D, Ozga J, Lemieux MJ, Weselake RJ, Chen G (2018) Properties and biotechnological applications of acyl-CoA: diacylglycerol acyltransferases and phospholipid: diacylglycerol acyltransferases from terrestrial plants and microalgae. Lipids 53(7):663–688. https://doi.org/10.1002/lipd.12081
Yurchenko OP, Nykiforuk CL, Moloney MM, Ståhl U, Banaś A, Stymne S, Weselake RJ (2009) A 10-kDa acyl-CoA-binding protein (ACBP) from Brassica napus enhances acyl exchange between acyl-CoA and phosphatidylcholine. Plant Biotechnol J 7(7):602–610. https://doi.org/10.1111/j.1467-7652.2009.00427.x
Acknowledgements
The authors thank Dr. John Browse of Washington State University for kindly providing Arabidopsis CL7 line. This work was supported by the Canada Research Chairs (R.J.W. and G.C.), Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants (RGPIN-2016-05926 to G.C. and RGPIN-2014-04585 to R.J.W.), and Alberta Innovates Bio Solutions (R.J.W.). The infrastructure used in this work was funded by the Canadian Foundation for Innovation and Research Capacity Program of Alberta Enterprise and Advanced Education.
Author information
Authors and Affiliations
Contributions
R.J.W. oversaw the project; R.J.W. and G.C. conceived the project; Y.L., G.C., E.M. and R.J.W. designed the experiments; R.J.W., G.C. and S.D.S. supervised the experiments; Y.L. performed most of the experiments and data analysis; G.C. conducted some of the experiments and data analysis; Z.S. performed qRT-PCR, K.C. and Y.L. made constructs for gene transformation; J.D., M.S., and T.M. generated important plant materials, genes, and gene libraries. Y.L. and G.C. wrote the initial draft of the article. All authors participated in interpretation of the data and were instrumental in the preparation of the final article.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
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.
Rights and permissions
About this article
Cite this article
Lin, Y., Chen, G., Mietkiewska, E. et al. Castor patatin-like phospholipase A IIIβ facilitates removal of hydroxy fatty acids from phosphatidylcholine in transgenic Arabidopsis seeds. Plant Mol Biol 101, 521–536 (2019). https://doi.org/10.1007/s11103-019-00915-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-019-00915-w