Lignin biosynthesis and its integration into metabolism

Vanholme, Ruben; De Meester, Barbara; Ralph, John; Boerjan, Wout

doi:10.1016/j.copbio.2019.02.018

Lignin biosynthesis and its integration into metabolism

Journal Article · Sat Mar 23 00:00:00 EDT 2019 · Current Opinion in Biotechnology

DOI:https://doi.org/10.1016/j.copbio.2019.02.018· OSTI ID:1556084

Vanholme, Ruben ^[1]; De Meester, Barbara ^[2]; ^[3]; Boerjan, Wout ^[2]

Ghent Univ. (Belgium); VIB Center for Plant Systems Biology, Ghent (Belgium); Vlaams Instituut voor Biotechnologie Department of Plant Systems Biology
Ghent Univ. (Belgium); VIB Center for Plant Systems Biology, Ghent (Belgium)
Univ. of Wisconsin, Madison, WI (United States)

Lignin is a principal structural component of cell walls in higher terrestrial plants. It reinforces the cell walls, facilitates water transport, and acts as a physical barrier to pathogens. Lignin is typically described as being composed of p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) units that derive from the polymerization of the hydroxycinnamyl alcohols, p-coumaryl, coniferyl, and sinapyl alcohol, respectively. Yet, lignin also derives from various other aromatic monomers. In this work, we review the biosynthetic pathway to the lignin monomers, and how flux through the pathway is regulated. Upon perturbation of the phenylpropanoid pathway, pathway intermediates may successfully incorporate into the lignin polymer, thereby affecting its physicochemical properties, or may remain soluble as such or as derivatized molecules that might interfere with physiological processes.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Great Lakes Bioenergy Research Center, Madison, WI (United States)

Sponsoring Organization:: Research Foundation Flanders (FWO); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0018409

OSTI ID:: 1556084

Journal Information:: Current Opinion in Biotechnology, Journal Name: Current Opinion in Biotechnology Journal Issue: C Vol. 56; ISSN 0958-1669

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (73)

Evidence that stilbene synthases have developed from chalcone synthases several times in the course of evolution Tropf, S.; Lanz, T.; Rensing, S. A. Journal of Molecular Evolution, Vol. 38, Issue 6 https://doi.org/10.1007/BF00175881	journal	June 1994
A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation Hatfield, Ronald; Ralph, John; Grabber, John H. Planta, Vol. 228, Issue 6, p. 919-928 https://doi.org/10.1007/s00425-008-0791-4	journal	July 2008
Hydroxycinnamates in lignification Ralph, John Phytochemistry Reviews, Vol. 9, Issue 1, p. 65-83 https://doi.org/10.1007/s11101-009-9141-9	journal	August 2009
Naturally p-Hydroxybenzoylated Lignins in Palms Lu, Fachuang; Karlen, Steven D.; Regner, Matt BioEnergy Research, Vol. 8, Issue 3 https://doi.org/10.1007/s12155-015-9583-4	journal	February 2015
Can genetic engineering of lignin deposition be accomplished without an unacceptable yield penalty? Bonawitz, Nicholas D.; Chapple, Clint Current Opinion in Biotechnology, Vol. 24, Issue 2 https://doi.org/10.1016/j.copbio.2012.11.004	journal	April 2013
The quest for transcriptional hubs of lignin biosynthesis: beyond the NAC-MYB-gene regulatory network model Ohtani, Misato; Demura, Taku Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2018.10.002	journal	April 2019
Tailor-made trees: engineering lignin for ease of processing and tomorrow’s bioeconomy Mahon, Elizabeth L.; Mansfield, Shawn D. Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2018.10.014	journal	April 2019
Bioactivity: phenylpropanoids’ best kept secret Vanholme, Bartel; El Houari, Ilias; Boerjan, Wout Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2018.11.012	journal	April 2019
Flux modeling for monolignol biosynthesis Wang, Jack P.; Matthews, Megan L.; Naik, Punith P. Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2018.12.003	journal	April 2019
Lignin structure and its engineering Ralph, John; Lapierre, Catherine; Boerjan, Wout Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2019.02.019	journal	April 2019
4-Coumaroyl and Caffeoyl Shikimic Acids Inhibit 4-Coumaric Acid:Coenzyme A Ligases and Modulate Metabolic Flux for 3-Hydroxylation in Monolignol Biosynthesis of Populus trichocarpa Lin, Chien-Yuan; Wang, Jack P.; Li, Quanzi Molecular Plant, Vol. 8, Issue 1 https://doi.org/10.1016/j.molp.2014.12.003	journal	January 2015
Down-regulation of hydroxycinnamoyl CoA: Shikimate hydroxycinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality Shadle, Gail; Chen, Fang; Srinivasa Reddy, M. S. Phytochemistry, Vol. 68, Issue 11 https://doi.org/10.1016/j.phytochem.2007.03.022	journal	June 2007
Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua Trends in Plant Science, Vol. 15, Issue 11, p. 625-632 https://doi.org/10.1016/j.tplants.2010.08.007	journal	November 2010
Dynamic modeling of subcellular phenylpropanoid metabolism in Arabidopsis lignifying cells Guo, Longyun; Wang, Peng; Jaini, Rohit Metabolic Engineering, Vol. 49 https://doi.org/10.1016/j.ymben.2018.07.003	journal	September 2018
Structural Characterization of Lignin from Maize ( Zea mays L.) Fibers: Evidence for Diferuloylputrescine Incorporated into the Lignin Polymer in Maize Kernels del Río, José C.; Rencoret, Jorge; Gutiérrez, Ana Journal of Agricultural and Food Chemistry, Vol. 66, Issue 17 https://doi.org/10.1021/acs.jafc.8b00880	journal	April 2018
Occurrence of Naturally Acetylated Lignin Units Del Río, José C.; Marques, Gisela; Rencoret, Jorge Journal of Agricultural and Food Chemistry, Vol. 55, Issue 14 https://doi.org/10.1021/jf0705264	journal	July 2007
Detection and Determination of p-Coumaroylated Units in Lignins Lu, Fachuang; Ralph, John Journal of Agricultural and Food Chemistry, Vol. 47, Issue 5, p. 1988-1992 https://doi.org/10.1021/jf981140j	journal	May 1999
Arylpropane-1,3-diols in Lignins from Normal and CAD-Deficient Pines Ralph, John; Kim, Hoon; Peng, Junpeng Organic Letters, Vol. 1, Issue 2 https://doi.org/10.1021/ol9906559	journal	July 1999
Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki Nature, Vol. 509, Issue 7500, p. 376-380 https://doi.org/10.1038/nature13084	journal	March 2014
Identification of a plastidial phenylalanine exporter that influences flux distribution through the phenylalanine biosynthetic network Widhalm, Joshua R.; Gutensohn, Michael; Yoo, Heejin Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9142	journal	September 2015
Role of bifunctional ammonia-lyase in grass cell wall biosynthesis Barros, Jaime; Serrani-Yarce, Juan C.; Chen, Fang Nature Plants, Vol. 2, Issue 6 https://doi.org/10.1038/nplants.2016.50	journal	May 2016
The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes Gou, Mingyue; Ran, Xiuzhi; Martin, Dwight W. Nature Plants, Vol. 4, Issue 5 https://doi.org/10.1038/s41477-018-0142-9	journal	April 2018
Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing Oyarce, Paula; De Meester, Barbara; Fonseca, Fernando Nature Plants, Vol. 5, Issue 2 https://doi.org/10.1038/s41477-018-0350-3	journal	January 2019
Identification and characterization of cDNA clones encoding hydroxycinnamoyl-CoA:tyramine N-hydroxycinnamoyltransferase from tobacco Farmer, Mary Jo; Czernic, Pierre; Michael, Anthony European Journal of Biochemistry, Vol. 263, Issue 3 https://doi.org/10.1046/j.1432-1327.1999.00538.x	journal	August 1999
Lignin content in natural Populus variants affects sugar release Studer, M. H.; DeMartini, J. D.; Davis, M. F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305 https://doi.org/10.1073/pnas.1009252108	journal	March 2011
Membrane protein complexes catalyze both 4- and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis Chen, H. -C.; Li, Q.; Shuford, C. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1116416109	journal	December 2011
A polymer of caffeyl alcohol in plant seeds Chen, F.; Tobimatsu, Y.; Havkin-Frenkel, D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 5 https://doi.org/10.1073/pnas.1120992109	journal	January 2012
Completion of the core -oxidative pathway of benzoic acid biosynthesis in plants Qualley, A. V.; Widhalm, J. R.; Adebesin, F. Proceedings of the National Academy of Sciences, Vol. 109, Issue 40 https://doi.org/10.1073/pnas.1211001109	journal	September 2012
Loss of function of cinnamyl alcohol dehydrogenase 1 leads to unconventional lignin and a temperature-sensitive growth defect in Medicago truncatula Zhao, Q.; Tobimatsu, Y.; Zhou, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 33 https://doi.org/10.1073/pnas.1312234110	journal	July 2013
Phosphorylation is an on/off switch for 5-hydroxyconiferaldehyde O -methyltransferase activity in poplar monolignol biosynthesis Wang, Jack P.; Chuang, Ling; Loziuk, Philip L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 27 https://doi.org/10.1073/pnas.1510473112	journal	June 2015
NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamylalcohol dehydrogenase and cinnamoyl-CoA reductase Ralph, J.; Hatfield, R. D.; Piquemal, J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 22 https://doi.org/10.1073/pnas.95.22.12803	journal	October 1998
Identification of Grass-specific Enzyme That Acylates Monolignols with p-Coumarate Withers, Saunia; Lu, Fachuang; Kim, Hoon Journal of Biological Chemistry, Vol. 287, Issue 11, p. 8347-8355 https://doi.org/10.1074/jbc.M111.284497	journal	January 2012
Effects of Coumarate 3-Hydroxylase Down-regulation on Lignin Structure Ralph, John; Akiyama, Takuya; Kim, Hoon Journal of Biological Chemistry, Vol. 281, Issue 13, p. 8843-8853 https://doi.org/10.1074/jbc.M511598200	journal	January 2006
Mutation in Brachypodium caffeic acid O -methyltransferase 6 alters stem and grain lignins and improves straw saccharification without deteriorating grain quality Ho-Yue-Kuang, Séverine; Alvarado, Camille; Antelme, Sébastien Journal of Experimental Botany, Vol. 67, Issue 1 https://doi.org/10.1093/jxb/erv446	journal	October 2015
Altered Lignin Biosynthesis Improves Cellulosic Bioethanol Production in Transgenic Maize Plants Down-Regulated for Cinnamyl Alcohol Dehydrogenase Fornalé, Silvia; Capellades, Montserrat; Encina, Antonio Molecular Plant, Vol. 5, Issue 4 https://doi.org/10.1093/mp/ssr097	journal	July 2012
Exploiting the Substrate Promiscuity of Hydroxycinnamoyl-CoA:Shikimate Hydroxycinnamoyl Transferase to Reduce Lignin Eudes, Aymerick; Pereira, Jose H.; Yogiswara, Sasha Plant and Cell Physiology, Vol. 57, Issue 3 https://doi.org/10.1093/pcp/pcw016	journal	February 2016
The Effects on Lignin Structure of Overexpression of Ferulate 5-Hydroxylase in Hybrid Poplar ¹ Stewart, Jaclyn J.; Akiyama, Takuya; Chapple, Clint Plant Physiology, Vol. 150, Issue 2 https://doi.org/10.1104/pp.109.137059	journal	April 2009
Mass Spectrometry-Based Sequencing of Lignin Oligomers Morreel, Kris; Dima, Oana; Kim, Hoon Plant Physiology, Vol. 153, Issue 4 https://doi.org/10.1104/pp.110.156489	journal	June 2010
MYB8 Controls Inducible Phenolamide Levels by Activating Three Novel Hydroxycinnamoyl-Coenzyme A:Polyamine Transferases in Nicotiana attenuata Onkokesung, Nawaporn; Gaquerel, Emmanuel; Kotkar, Hemlata Plant Physiology, Vol. 158, Issue 1 https://doi.org/10.1104/pp.111.187229	journal	November 2011
Completion of Tricin Biosynthesis Pathway in Rice: Cytochrome P450 75B4 Is a Unique Chrysoeriol 5′-Hydroxylase Lam, Pui Ying; Liu, Hongjia; Lo, Clive Plant Physiology, Vol. 168, Issue 4 https://doi.org/10.1104/pp.15.00566	journal	June 2015
cis-Cinnamic Acid Is a Novel, Natural Auxin Efflux Inhibitor That Promotes Lateral Root Formation Steenackers, Ward; Klíma, Petr; Quareshy, Mussa Plant Physiology, Vol. 173, Issue 1 https://doi.org/10.1104/pp.16.00943	journal	November 2016
Disrupting Flavone Synthase II Alters Lignin and Improves Biomass Digestibility Lam, Pui Ying; Tobimatsu, Yuki; Takeda, Yuri Plant Physiology, Vol. 174, Issue 2 https://doi.org/10.1104/pp.16.01973	journal	April 2017
Hydroxystilbenes Are Monomers in Palm Fruit Endocarp Lignins Carlos del Río, José; Rencoret, Jorge; Gutiérrez, Ana Plant Physiology, Vol. 174, Issue 4 https://doi.org/10.1104/pp.17.00362	journal	June 2017
Different Routes for Conifer- and Sinapaldehyde and Higher Saccharification upon Deficiency in the Dehydrogenase CAD1 Van Acker, Rebecca; Déjardin, Annabelle; Desmet, Sandrien Plant Physiology, Vol. 175, Issue 3 https://doi.org/10.1104/pp.17.00834	journal	September 2017
Silencing CAFFEOYL SHIKIMATE ESTERASE Affects Lignification and Improves Saccharification in Poplar Saleme, Marina de Lyra Soriano; Cesarino, Igor; Vargas, Lívia Plant Physiology, Vol. 175, Issue 3 https://doi.org/10.1104/pp.17.00920	journal	September 2017
Vessel-Specific Reintroduction of CINNAMOYL-COA REDUCTASE1 (CCR1) in Dwarfed ccr1 Mutants Restores Vessel and Xylary Fiber Integrity and Increases Biomass De Meester, Barbara; de Vries, Lisanne; Özparpucu, Merve Plant Physiology, Vol. 176, Issue 1 https://doi.org/10.1104/pp.17.01462	journal	November 2017
CINNAMYL ALCOHOL DEHYDROGENASE-C and -D Are the Primary Genes Involved in Lignin Biosynthesis in the Floral Stem of Arabidopsis Sibout, Richard; Eudes, Aymerick; Mouille, Gregory The Plant Cell, Vol. 17, Issue 7 https://doi.org/10.1105/tpc.105.030767	journal	June 2005
A Systems Biology View of Responses to Lignin Biosynthesis Perturbations in Arabidopsis Vanholme, Ruben; Storme, Véronique; Vanholme, Bartel The Plant Cell, Vol. 24, Issue 9 https://doi.org/10.1105/tpc.112.102574	journal	September 2012
Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans Pesquet, Edouard; Zhang, Bo; Gorzsás, András The Plant Cell, Vol. 25, Issue 4 https://doi.org/10.1105/tpc.113.110593	journal	April 2013
Complete Proteomic-Based Enzyme Reaction and Inhibition Kinetics Reveal How Monolignol Biosynthetic Enzyme Families Affect Metabolic Flux and Lignin in Populus trichocarpa Wang, Jack P.; Naik, Punith P.; Chen, Hsi-Chuan The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.113.120881	journal	March 2014
Small Glycosylated Lignin Oligomers Are Stored in Arabidopsis Leaf Vacuoles Dima, Oana; Morreel, Kris; Vanholme, Bartel The Plant Cell, Vol. 27, Issue 3 https://doi.org/10.1105/tpc.114.134643	journal	February 2015
Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency): Marker for ferulic acid incorporation into lignins Ralph, John; Kim, Hoon; Lu, Fachuang The Plant Journal, Vol. 53, Issue 2 https://doi.org/10.1111/j.1365-313X.2007.03345.x	journal	October 2007
Engineering traditional monolignols out of lignin by concomitant up-regulation of F5H1 and down-regulation of COMT in Arabidopsis: Concomitant F5H1 up-regulation and COMT down-regulation in Arabidopsis Vanholme, Ruben; Ralph, John; Akiyama, Takuya The Plant Journal, Vol. 64, Issue 6 https://doi.org/10.1111/j.1365-313X.2010.04353.x	journal	October 2010
Over-expression of F5H in COMT-deficient Arabidopsis leads to enrichment of an unusual lignin and disruption of pollen wall formation: Lignin modification leads to male sterility Weng, Jing-Ke; Mo, Huaping; Chapple, Clint The Plant Journal, Vol. 64, Issue 6 https://doi.org/10.1111/j.1365-313X.2010.04391.x	journal	November 2010
Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification: Reduction in lignin DP enhances saccharification Eudes, Aymerick; George, Anthe; Mukerjee, Purba Plant Biotechnology Journal, Vol. 10, Issue 5 https://doi.org/10.1111/j.1467-7652.2012.00692.x	journal	March 2012
Metabolic engineering of novel lignin in biomass crops Vanholme, Ruben; Morreel, Kris; Darrah, Chiarina New Phytologist, Vol. 196, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04337.x	journal	October 2012
Elicitors and defense gene induction in plants with altered lignin compositions Gallego-Giraldo, Lina; Posé, Sara; Pattathil, Sivakumar New Phytologist, Vol. 219, Issue 4 https://doi.org/10.1111/nph.15258	journal	June 2018
CAD 1 and CCR 2 protein complex formation in monolignol biosynthesis in Populus trichocarpa Yan, Xiaojing; Liu, Jie; Kim, Hoon New Phytologist, Vol. 222, Issue 1 https://doi.org/10.1111/nph.15505	journal	October 2018
The maize brown midrib2 ( bm2 ) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation Tang, Ho Man; Liu, Sanzhen; Hill-Skinner, Sarah The Plant Journal, Vol. 77, Issue 3 https://doi.org/10.1111/tpj.12394	journal	January 2014
p -Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon Petrik, Deborah L.; Karlen, Steven D.; Cass, Cynthia L. The Plant Journal, Vol. 77, Issue 5 https://doi.org/10.1111/tpj.12420	journal	February 2014
Tricin-lignins: occurrence and quantitation of tricin in relation to phylogeny Lan, Wu; Rencoret, Jorge; Lu, Fachuang The Plant Journal, Vol. 88, Issue 6 https://doi.org/10.1111/tpj.13315	journal	November 2016
Downregulation of p‐ COUMAROYL ESTER 3‐ HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification Takeda, Yuri; Tobimatsu, Yuki; Karlen, Steven D. The Plant Journal, Vol. 95, Issue 5 https://doi.org/10.1111/tpj.13988	journal	July 2018
Monolignol ferulate conjugates are naturally incorporated into plant lignins Karlen, Steven D.; Zhang, Chengcheng; Peck, Matthew L. Science Advances, Vol. 2, Issue 10 https://doi.org/10.1126/sciadv.1600393	journal	October 2016
Caffeoyl Shikimate Esterase (CSE) Is an Enzyme in the Lignin Biosynthetic Pathway in Arabidopsis Vanholme, R.; Cesarino, I.; Rataj, K. Science, Vol. 341, Issue 6150 https://doi.org/10.1126/science.1241602	journal	August 2013
Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone Wilkerson, C. G.; Mansfield, S. D.; Lu, F. Science, Vol. 344, Issue 6179, p. 90-93 https://doi.org/10.1126/science.1250161	journal	April 2014
Abnormal Lignin in a Loblolly Pine Mutant Ralph, J. Science, Vol. 277, Issue 5323 https://doi.org/10.1126/science.277.5323.235	journal	July 1997
Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique Biotechnology for Biofuels, Vol. 6, Article No. 46 https://doi.org/10.1186/1754-6834-6-46	journal	January 2013
Suppression of CINNAMOYL-CoA REDUCTASE increases the level of monolignol ferulates incorporated into maize lignins Smith, Rebecca A.; Cass, Cynthia L.; Mazaheri, Mona Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0793-1	journal	May 2017
Evaluation of Lignin Syringyl/Guaiacyl Ratio in Eucalyptus Camaldulensis across Three Diverse Sites Based on near Infrared Spectroscopic Calibration Modelling with Five Eucalyptus Species and its Impact on Kraft Pulp Yield Ramadevi, Payyavula; Hegde, Deepak V.; Varghese, Mohan Journal of Near Infrared Spectroscopy, Vol. 24, Issue 6 https://doi.org/10.1255/jnirs.1251	journal	January 2016
Integrative Analysis of Transgenic Alfalfa (Medicago sativa L.) Suggests New Metabolic Control Mechanisms for Monolignol Biosynthesis Lee, Yun; Chen, Fang; Gallego-Giraldo, Lina PLoS Computational Biology, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pcbi.1002047	journal	May 2011
SbCOMT (Bmr12) is involved in the biosynthesis of tricin-lignin in sorghum Eudes, Aymerick; Dutta, Tanmoy; Deng, Kai PLOS ONE, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pone.0178160	journal	June 2017
Clonal Selection for Lignin and Etherified Ferulates in Three Perennial Grasses Casler, M. D.; Jung, H. G.; Coblentz, W. K. Crop Science, Vol. 48, Issue 2 https://doi.org/10.2135/cropsci2007.04.0229	journal	March 2008
Glycosylation Is a Major Regulator of Phenylpropanoid Availability and Biological Activity in Plants Le Roy, Julien; Huss, Brigitte; Creach, Anne Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00735	journal	May 2016

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