Targeted genome editing of plants and plant cells for biomanufacturing.

Chassis Metabolic optimization Modified glycosylation Plant molecular farming Programmable growth and senescence Protease inactivation

Journal

Transgenic research
ISSN: 1573-9368
Titre abrégé: Transgenic Res
Pays: Netherlands
ID NLM: 9209120

Informations de publication

Date de publication:
08 2021
Historique:
received: 02 10 2020
accepted: 03 02 2021
pubmed: 2 3 2021
medline: 5 1 2022
entrez: 1 3 2021
Statut: ppublish

Résumé

Plants have provided humans with useful products since antiquity, but in the last 30 years they have also been developed as production platforms for small molecules and recombinant proteins. This initially niche area has blossomed with the growth of the global bioeconomy, and now includes chemical building blocks, polymers and renewable energy. All these applications can be described as "plant molecular farming" (PMF). Despite its potential to increase the sustainability of biologics manufacturing, PMF has yet to be embraced broadly by industry. This reflects a combination of regulatory uncertainty, limited information on process cost structures, and the absence of trained staff and suitable manufacturing capacity. However, the limited adaptation of plants and plant cells to the requirements of industry-scale manufacturing is an equally important hurdle. For example, the targeted genetic manipulation of yeast has been common practice since the 1980s, whereas reliable site-directed mutagenesis in most plants has only become available with the advent of CRISPR/Cas9 and similar genome editing technologies since around 2010. Here we summarize the applications of new genetic engineering technologies to improve plants as biomanufacturing platforms. We start by identifying current bottlenecks in manufacturing, then illustrate the progress that has already been made and discuss the potential for improvement at the molecular, cellular and organism levels. We discuss the effects of metabolic optimization, adaptation of the endomembrane system, modified glycosylation profiles, programmable growth and senescence, protease inactivation, and the expression of enzymes that promote biodegradation. We outline strategies to achieve these modifications by targeted gene modification, considering case-by-case examples of individual improvements and the combined modifications needed to generate a new general-purpose "chassis" for PMF.

Identifiants

pubmed: 33646510
doi: 10.1007/s11248-021-00236-z
pii: 10.1007/s11248-021-00236-z
pmc: PMC8316201
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

401-426

Subventions

Organisme : Fraunhofer-Gesellschaft
ID : 125-600164
Organisme : Ministerium für Innovation, Wissenschaft und Forschung des Landes Nordrhein-Westfalen
ID : 423
Organisme : H2020 European Research Council
ID : 760331
Organisme : Austrian Science Fund
ID : I2823-B25

Informations de copyright

© 2021. The Author(s).

Références

Plant Physiol. 2013 Feb;161(2):1021-33
pubmed: 23188806
Plant Biotechnol J. 2015 Oct;13(8):1169-79
pubmed: 26286859
Biotechnol Bioeng. 2012 Oct;109(10):2575-88
pubmed: 22511291
Plant Biotechnol J. 2015 Oct;13(8):1106-20
pubmed: 26147010
Biotechnol J. 2014 Aug;9(8):1065-73
pubmed: 24828029
Plant Biotechnol J. 2007 May;5(3):389-401
pubmed: 17359496
Nat Biotechnol. 1996 Aug;14(8):995-8
pubmed: 9631038
Proc Natl Acad Sci U S A. 2011 Jun 21;108(25):10231-6
pubmed: 21646514
Bioresour Technol. 2010 Mar;101(6):2034-42
pubmed: 19932614
Appl Biochem Biotechnol. 2012 Nov;168(6):1608-20
pubmed: 22965305
FEMS Yeast Res. 2007 Oct;7(7):1168-80
pubmed: 17617219
Metab Eng. 2002 Jan;4(1):67-79
pubmed: 11800576
Plant Mol Biol. 2008 Oct;68(3):263-75
pubmed: 18587653
Biotechnol Biofuels. 2013 Apr 16;6(1):53
pubmed: 23587418
Plant Physiol. 2013 Aug;162(4):1881-96
pubmed: 23780897
Plant J. 2009 Feb;57(3):436-45
pubmed: 18939966
Plant Biotechnol J. 2015 Aug;13(6):727-39
pubmed: 25865366
G3 (Bethesda). 2017 Jan 5;7(1):203-219
pubmed: 27852012
Sci Rep. 2017 Apr 21;7(1):1010
pubmed: 28432338
Nucleic Acids Res. 1982 Nov 25;10(22):7055-74
pubmed: 6760125
Int J Mol Sci. 2011;12(8):4975-90
pubmed: 21954339
PLoS One. 2015 Jul 06;10(7):e0130556
pubmed: 26148064
Plant Biotechnol J. 2018 May;16(5):1068-1084
pubmed: 29055088
Nat Methods. 2015 Apr;12(4):326-8
pubmed: 25730490
Front Plant Sci. 2015 Dec 01;6:1047
pubmed: 26648951
Front Bioeng Biotechnol. 2020 Jul 24;8:825
pubmed: 32793574
Plant Biotechnol J. 2015 Oct;13(8):1094-105
pubmed: 26214282
Plant Physiol. 2011 Mar;155(3):1103-12
pubmed: 21233332
J Exp Bot. 2016 Mar;67(5):1433-45
pubmed: 26712824
Front Plant Sci. 2020 Jan 10;10:1666
pubmed: 31998348
PLoS One. 2018 Nov 1;13(11):e0206592
pubmed: 30383825
PLoS One. 2018 Aug 16;13(8):e0202386
pubmed: 30114282
New Phytol. 2012 Jan;193(1):30-50
pubmed: 22085245
Annu Rev Plant Biol. 2013;64:477-99
pubmed: 23330794
Cell. 2010 Apr 16;141(2):355-67
pubmed: 20403329
Plant J. 2012 Dec;72(6):908-21
pubmed: 22889438
Appl Microbiol Biotechnol. 2007 Feb;74(2):381-9
pubmed: 17051412
Microbiol Mol Biol Rev. 2000 Jun;64(2):239-80
pubmed: 10839817
Annu Rev Phytopathol. 2018 Aug 25;56:405-426
pubmed: 30149789
Biotechnol Biofuels. 2019 Jan 9;12:11
pubmed: 30636971
Plant Cell Physiol. 2017 Mar 1;58(3):635-642
pubmed: 28158810
Front Plant Sci. 2017 Mar 27;8:403
pubmed: 28396675
Plant Sci. 2017 Oct;263:201-209
pubmed: 28818376
Adv Biochem Eng Biotechnol. 2021;175:137-166
pubmed: 30069741
J Biol Chem. 2009 Jul 31;284(31):20479-85
pubmed: 19478090
Trends Biotechnol. 2003 Dec;21(12):570-8
pubmed: 14624867
Appl Biochem Biotechnol. 2015 Jan;175(2):841-54
pubmed: 25344434
Nat Plants. 2016 Sep 12;2:16139
pubmed: 27618611
Arch Pharm (Weinheim). 2002 Apr;335(4):143-51
pubmed: 12112034
Biotechnol J. 2019 Mar;14(3):e1800075
pubmed: 29701331
Plant Biotechnol J. 2017 Feb;15(2):197-206
pubmed: 27421111
Plant Biotechnol J. 2012 Dec;10(9):1118-28
pubmed: 22984968
Plant Biotechnol J. 2019 Feb;17(2):350-361
pubmed: 29969180
J Biotechnol. 2003 Dec 5;106(1):15-21
pubmed: 14636706
Nat Biotechnol. 2015 Nov;33(11):1135-7
pubmed: 26544140
Plant Biotechnol J. 2003 Nov;1(6):411-22
pubmed: 17134400
Plant Biotechnol J. 2018 Jun;16(6):1125-1137
pubmed: 29087011
Bioengineered. 2015;6(5):299-302
pubmed: 26186119
Trends Genet. 2006 May;22(5):268-80
pubmed: 16567016
Nat Rev Genet. 2001 Oct;2(10):815-22
pubmed: 11584298
Transgenic Res. 2016 Apr;25(2):173-86
pubmed: 26712321
Plant Cell Environ. 2019 Oct;42(10):2827-2843
pubmed: 31222757
Planta. 2019 Aug;250(2):463-473
pubmed: 31065786
Plant Cell Rep. 2006 Jul;25(7):689-97
pubmed: 16491379
Trends Cell Biol. 2013 Nov;23(11):547-55
pubmed: 23880584
Front Bioeng Biotechnol. 2018 Jun 14;6:81
pubmed: 29963553
Plant Biotechnol J. 2013 Dec;11(9):1058-68
pubmed: 23911079
Plant Biotechnol J. 2016 Apr;14(4):1151-60
pubmed: 26426390
Plant Biotechnol J. 2020 Feb 24;:
pubmed: 32096288
Plant Biotechnol J. 2019 Dec;17(12):2228-2230
pubmed: 31206994
Plant Biotechnol J. 2008 Sep;6(7):702-21
pubmed: 18498310
Biotechnol J. 2020 Mar;15(3):e1900308
pubmed: 31657528
Plant J. 2018 Jun;94(5):767-775
pubmed: 29575326
Transgenic Res. 2019 Dec;28(5-6):537-547
pubmed: 31264021
Front Microbiol. 2019 Feb 27;10:335
pubmed: 30873140
Plant Biotechnol J. 2008 May;6(4):392-402
pubmed: 18346095
Plant Biotechnol J. 2010 Aug;8(6):691-718
pubmed: 20331531
Plant Biotechnol J. 2012 Sep;10(7):851-61
pubmed: 22621344
Methods Mol Biol. 2016;1482:103-10
pubmed: 27557763
Semin Cell Dev Biol. 2018 Aug;80:133-141
pubmed: 28688929
Plant Biotechnol J. 2018 Apr;16(4):902-910
pubmed: 28921815
Vaccine. 2012 Jun 13;30(28):4160-6
pubmed: 22554467
Appl Microbiol Biotechnol. 2016 Apr;100(8):3451-61
pubmed: 26936774
Plant Biotechnol J. 2007 Sep;5(5):579-90
pubmed: 17524049
Front Plant Sci. 2019 Jun 26;10:777
pubmed: 31316529
Biotechnol J. 2016 Jan;11(1):107-16
pubmed: 26632507
Angew Chem Int Ed Engl. 2019 Jul 8;58(28):9565-9569
pubmed: 30892798
Plant Physiol. 2004 Jan;134(1):510-9
pubmed: 14718674
Influenza Other Respir Viruses. 2012 May;6(3):204-10
pubmed: 21974811
Front Plant Sci. 2020 Mar 11;11:282
pubmed: 32218797
J Integr Plant Biol. 2017 Mar;59(3):205-224
pubmed: 28009482
Plant Biotechnol J. 2016 Aug;14(8):1682-94
pubmed: 26868756
Proc Natl Acad Sci U S A. 2016 Aug 23;113(34):9498-503
pubmed: 27444013
Plant Cell Environ. 2006 Jan;29(1):126-37
pubmed: 17086759
MAbs. 2016 Nov/Dec;8(8):1456-1466
pubmed: 27559626
Appl Microbiol Biotechnol. 2015 Aug;99(16):6753-64
pubmed: 25957150
Wiley Interdiscip Rev RNA. 2020 Nov;11(6):e1597
pubmed: 32367681
Plant Biol (Stuttg). 2015 Mar;17(2):484-92
pubmed: 25243954
J Biosci. 2009 Dec;34(6):953-62
pubmed: 20093748
Plant Physiol. 1991 Jul;96(3):775-85
pubmed: 16668254
Nat Plants. 2019 Jul;5(7):715-721
pubmed: 31285558
Biotechnol Adv. 2012 Mar-Apr;30(2):434-9
pubmed: 21856403
Bioengineered. 2017 May 4;8(3):203-211
pubmed: 27644793
Nat Commun. 2018 May 17;9(1):1967
pubmed: 29773790
Front Plant Sci. 2019 Oct 08;10:1245
pubmed: 31649707
Front Plant Sci. 2019 Jan 18;9:1893
pubmed: 30713542
Curr Pharm Biotechnol. 2015;16(11):966-82
pubmed: 26343135
Sci Rep. 2018 Mar 19;8(1):4755
pubmed: 29555968
Curr Biol. 2007 Sep 18;17(18):1609-14
pubmed: 17869110
Cell. 2016 Apr 21;165(3):535-50
pubmed: 27104977
Front Plant Sci. 2016 Jan 29;7:18
pubmed: 26858738
Plant Cell Rep. 2015 Oct;34(10):1707-16
pubmed: 26082433
Plant Biotechnol J. 2010 Jun;8(5):564-87
pubmed: 20233335
J Biosci Bioeng. 2017 Aug;124(2):215-220
pubmed: 28336416
Plant Biotechnol J. 2013 Oct;11(8):933-41
pubmed: 23777410
Microb Cell Fact. 2016 May 23;15:87
pubmed: 27216259
Front Plant Sci. 2020 Jun 11;11:809
pubmed: 32595683
Environ Sci Pollut Res Int. 2004;11(3):152-7
pubmed: 15259697
J Proteome Res. 2018 Nov 2;17(11):3749-3760
pubmed: 30226384
Plant Biol (Stuttg). 2004 Mar-Apr;6(2):201-5
pubmed: 15045672
Appl Microbiol Biotechnol. 2019 Dec;103(23-24):9479-9491
pubmed: 31701198
Biotechnol Adv. 2020 May - Jun;40:107519
pubmed: 31954848
Angew Chem Int Ed Engl. 2014 Oct 6;53(41):10876-93
pubmed: 25136976
J Food Sci. 2016 Oct;81(10):C2425-C2430
pubmed: 27649517
Biotechnol Biofuels. 2018 Aug 16;11:225
pubmed: 30147748
RNA Biol. 2021 Jan;18(1):64-78
pubmed: 32715941
Front Bioeng Biotechnol. 2020 Apr 09;8:296
pubmed: 32328483
PLoS One. 2016 Nov 28;11(11):e0167086
pubmed: 27893815
Science. 2016 Nov 18;354(6314):857-861
pubmed: 27856901
Curr Biol. 2015 May 4;25(9):R384-9
pubmed: 25942556
Nat Biotechnol. 2006 Dec;24(12):1591-7
pubmed: 17128273
Philos Trans R Soc Lond B Biol Sci. 2014 Mar 03;369(1640):20130243
pubmed: 24591723
Plant Biotechnol J. 2008 Apr;6(3):246-63
pubmed: 18086234
Nat Plants. 2020 Jul;6(7):766-772
pubmed: 32601420
Enzyme Microb Technol. 2020 Feb;133:109442
pubmed: 31874688
Plant Biotechnol J. 2018 Oct;16(10):1797-1810
pubmed: 29509983
Microb Cell Fact. 2020 Jul 23;19(1):148
pubmed: 32703203
Glycobiology. 2016 Sep;26(9):926-939
pubmed: 26911286
Microb Cell Fact. 2014 Dec 19;13:177
pubmed: 25523647
Plant Cell. 1999 Apr;11(4):601-14
pubmed: 10213781
Front Genet. 2019 Feb 20;10:96
pubmed: 30842788
New Phytol. 2016 May;210(3):794-807
pubmed: 26800491
Plant Cell Rep. 2012 Mar;31(3):539-49
pubmed: 22108719
Curr Opin Biotechnol. 2020 Feb;61:15-20
pubmed: 31593785
Trends Biotechnol. 2004 Jul;22(7):346-53
pubmed: 15245907
J Vis Exp. 2016 Aug 08;(114):
pubmed: 27584939
Plant Cell Rep. 2015 Feb;34(2):179-87
pubmed: 25187294
Proc Natl Acad Sci U S A. 2019 Jul 2;116(27):13384-13393
pubmed: 31213543
Plant J. 2015 Nov;84(4):704-17
pubmed: 26402748
Plant Direct. 2019 Jul 19;3(7):e00153
pubmed: 31360827
Nat Commun. 2019 Mar 6;10(1):1084
pubmed: 30842412
Protein Expr Purif. 2010 Feb;69(2):159-67
pubmed: 19733669
Plant Cell Physiol. 2020 Jun 1;61(6):1041-1053
pubmed: 32191315
Nucleic Acids Res. 2001 Dec 15;29(24):5226-32
pubmed: 11812856
Front Plant Sci. 2018 Nov 13;9:1607
pubmed: 30483283
Plant Physiol. 2020 Feb;182(2):739-755
pubmed: 31792147
Trends Biochem Sci. 2020 Feb;45(2):123-136
pubmed: 31753702
PLoS Genet. 2014 Jan;10(1):e1004084
pubmed: 24453985
Science. 2019 Jan 4;363(6422):
pubmed: 30606819
Cell. 2015 Jun 18;161(7):1606-18
pubmed: 26052047
Plant Biotechnol J. 2004 Nov;2(6):517-23
pubmed: 17147624
Front Bioeng Biotechnol. 2019 Jan 09;6:206
pubmed: 30687700
Mol Biol Rep. 2020 Jun;47(6):4427-4438
pubmed: 32424521
PLoS One. 2013;8(1):e54836
pubmed: 23372778
Front Bioeng Biotechnol. 2018 Jul 24;6:102
pubmed: 30087892
Front Plant Sci. 2016 Oct 25;7:1572
pubmed: 27826306
Arch Virol. 2017 Dec;162(12):3717-3726
pubmed: 28864903
Sci Signal. 2018 Sep 04;11(546):
pubmed: 30181241
Annu Rev Plant Biol. 2018 Apr 29;69:147-172
pubmed: 29570364
Biotechnol Bioeng. 2017 Mar;114(3):492-502
pubmed: 27618314
Nat Rev Mol Cell Biol. 2018 Jan;19(1):20-30
pubmed: 29018283
BMC Plant Biol. 2015 Feb 13;15:54
pubmed: 25849300
Plant Biotechnol J. 2016 Dec;14(12):2265-2275
pubmed: 27159528
Cell. 2015 Mar 26;161(1):56-66
pubmed: 25815985
IUBMB Life. 2019 Aug;71(8):1099-1108
pubmed: 31241827
Biotechnol J. 2014 Apr;9(4):566-77
pubmed: 24478119
Front Plant Sci. 2020 Jan 09;10:1649
pubmed: 31998338
Plant Cell Physiol. 2004 Nov;45(11):1566-77
pubmed: 15574832
Plant Biotechnol J. 2017 Sep;15(9):1120-1129
pubmed: 28160363
Front Plant Sci. 2020 Oct 20;11:594019
pubmed: 33193552
Planta. 2016 Nov;244(5):1157-1166
pubmed: 27663725
Science. 2014 Nov 28;346(6213):1258096
pubmed: 25430774
Plant Biotechnol J. 2019 Apr;17(4):750-761
pubmed: 30220095
Plant Physiol. 2013 May;162(1):390-400
pubmed: 23509176
Nat Commun. 2018 Mar 6;9(1):868
pubmed: 29511193
Plant Physiol. 2002 Jul;129(3):943-8
pubmed: 12114549
Plant Cell Environ. 2017 Nov;40(11):2469-2486
pubmed: 28010046
Plant Cell. 1999 Apr;11(4):587-600
pubmed: 10213780
J Cell Biol. 2009 Nov 16;187(4):525-36
pubmed: 19948500
J Biotechnol. 2016 Jan 10;217:1-11
pubmed: 26521697
Plant Signal Behav. 2015;10(10):e1065367
pubmed: 26225871
Sci Total Environ. 2020 Jul 10;725:138495
pubmed: 32298900
Sci Rep. 2013 Oct 22;3:3019
pubmed: 24145658
Methods Mol Biol. 2017;1629:167-184
pubmed: 28623586
Front Plant Sci. 2015 Sep 10;6:693
pubmed: 26442010
Plant Biotechnol J. 2020 Jul;18(7):1537-1549
pubmed: 31837192
Nat Rev Mol Cell Biol. 2010 Feb;11(2):113-27
pubmed: 20094052
BMC Plant Biol. 2019 Jul 4;19(1):292
pubmed: 31272394
Plant Biotechnol J. 2012 Dec;10(9):1035-45
pubmed: 22882653
Sci Rep. 2012;2:944
pubmed: 23230509
Proc Natl Acad Sci U S A. 2013 May 28;110(22):9171-6
pubmed: 23686579
Front Plant Sci. 2014 Sep 03;5:439
pubmed: 25232360
Methods Enzymol. 2014;546:459-72
pubmed: 25398353
Nature. 1989 Nov 2;342(6245):76-8
pubmed: 2509938
Immunol Cell Biol. 2020 Apr;98(4):287-304
pubmed: 32157732
Front Plant Sci. 2016 Mar 08;7:267
pubmed: 27014293
Biotechnol Prog. 2020 Jan;36(1):e2896
pubmed: 31443134
Biotechnol Adv. 2015 Nov 1;33(6 Pt 1):902-13
pubmed: 25922318
Biotechnol Lett. 2014 Aug;36(8):1581-93
pubmed: 24752815
Environ Pollut. 2017 Dec;231(Pt 1):845-853
pubmed: 28869831
Extremophiles. 2019 Jul;23(4):479-486
pubmed: 31119430
Cell. 2010 Apr 16;141(2):344-54
pubmed: 20403328
Biotechnol Bioeng. 2013 Feb;110(2):471-82
pubmed: 22948957
Gene X. 2019 Mar 06;2:100012
pubmed: 32550546
Bioengineered. 2013 May-Jun;4(3):136-9
pubmed: 23563599
Plant J. 2001 Oct;28(2):225-35
pubmed: 11722766
Plant Physiol. 2018 Aug;177(4):1425-1438
pubmed: 29925584
Plant J. 2011 Mar;65(5):675-89
pubmed: 21223397
Regul Toxicol Pharmacol. 2016 Mar;75:27-34
pubmed: 26739812
Environ Sci Pollut Res Int. 2016 May;23(9):8890-901
pubmed: 26810792
Plant Physiol. 2015 Oct;169(2):931-45
pubmed: 26269544
Plant Signal Behav. 2012 Nov;7(11):1402-3
pubmed: 22960759
Plant Physiol. 2014 Dec;166(4):1682-3
pubmed: 25467437
Proc Natl Acad Sci U S A. 1980 May;77(5):2455-9
pubmed: 6248849
Annu Rev Plant Biol. 2008;59:191-223
pubmed: 18257708
Curr Opin Biotechnol. 2016 Feb;37:36-44
pubmed: 26524248
J Food Sci. 2010 Apr;75(3):C297-304
pubmed: 20492283
Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):6297-302
pubmed: 15079073

Auteurs

J F Buyel (JF)

Fraunhofer Institute for Molecular Biology and Applied Ecology IME, Forckenbeckstrasse 6, 52074, Aachen, Germany. johannes.buyel@rwth-aachen.de.
Institute for Molecular Biotechnology, RWTH Aachen University, Worringerweg 1, 52074, Aachen, Germany. johannes.buyel@rwth-aachen.de.

E Stöger (E)

Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, Austria.

L Bortesi (L)

Aachen-Maastricht Institute for Biobased Materials (AMIBM), Maastricht University, Brightlands Chemelot Campus, Urmonderbaan 22, 6167 RD, Geleen, The Netherlands.

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Classifications MeSH