Alternative splicing creates a pseudo-strictosidine β-d-glucosidase modulating alkaloid synthesis in Catharanthus roseus.
Journal
Plant physiology
ISSN: 1532-2548
Titre abrégé: Plant Physiol
Pays: United States
ID NLM: 0401224
Informations de publication
Date de publication:
02 04 2021
02 04 2021
Historique:
received:
16
07
2020
accepted:
24
11
2020
pubmed:
2
4
2021
medline:
6
8
2021
entrez:
1
4
2021
Statut:
ppublish
Résumé
Deglycosylation is a key step in the activation of specialized metabolites involved in plant defense mechanisms. This reaction is notably catalyzed by β-glucosidases of the glycosyl hydrolase 1 (GH1) family such as strictosidine β-d-glucosidase (SGD) from Catharanthus roseus. SGD catalyzes the deglycosylation of strictosidine, forming a highly reactive aglycone involved in the synthesis of cytotoxic monoterpene indole alkaloids (MIAs) and in the crosslinking of aggressor proteins. By exploring C. roseus transcriptomic resources, we identified an alternative splicing event of the SGD gene leading to the formation of a shorter isoform of this enzyme (shSGD) that lacks the last 71-residues and whose transcript ratio with SGD ranges from 1.7% up to 42.8%, depending on organs and conditions. Whereas it completely lacks β-glucosidase activity, shSGD interacts with SGD and causes the disruption of SGD multimers. Such disorganization drastically inhibits SGD activity and impacts downstream MIA synthesis. In addition, shSGD disrupts the metabolic channeling of downstream biosynthetic steps by hampering the recruitment of tetrahydroalstonine synthase in cell nuclei. shSGD thus corresponds to a pseudo-enzyme acting as a regulator of MIA biosynthesis. These data shed light on a peculiar control mechanism of β-glucosidase multimerization, an organization common to many defensive GH1 members.
Identifiants
pubmed: 33793899
pii: 6054813
doi: 10.1093/plphys/kiaa075
pmc: PMC8133614
doi:
Substances chimiques
Plant Proteins
0
Vinca Alkaloids
0
strictosidine
20824-29-7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
836-856Informations de copyright
© American Society of Plant Biologists 2020. All rights reserved. For permissions, please email: journals.permissions@oup.com.
Références
J Biol Chem. 2001 Apr 13;276(15):11895-901
pubmed: 11096099
Planta. 1991 Sep;185(2):148-52
pubmed: 24186336
Plant Physiol. 2006 Aug;141(4):1237-47
pubmed: 16751439
Plant Cell. 2003 Oct;15(10):2333-42
pubmed: 14523247
Leuk Lymphoma. 2005 Oct;46(10):1489-96
pubmed: 16194895
Arch Biochem Biophys. 2009 Sep;489(1-2):92-8
pubmed: 19664588
Planta. 1988 Dec;173(4):474-81
pubmed: 24226684
J Biol Chem. 2014 Mar 21;289(12):8203-16
pubmed: 24505140
Plant Physiol. 2007 Dec;145(4):1577-87
pubmed: 17951452
Chem Biol. 2015 Mar 19;22(3):336-41
pubmed: 25772467
J Chem Ecol. 2008 Oct;34(10):1311-21
pubmed: 18787901
Plant Cell Physiol. 2005 Jul;46(7):1140-8
pubmed: 15919674
Curr Opin Plant Biol. 2005 Jun;8(3):264-71
pubmed: 15860423
Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):22020-5
pubmed: 19996170
Nat Protoc. 2015 Jun;10(6):845-58
pubmed: 25950237
Plant Mol Biol. 2012 Mar;78(4-5):361-75
pubmed: 22228407
J Exp Bot. 2015 Apr;66(7):2093-106
pubmed: 25697790
Nat Commun. 2017 Aug 22;8(1):316
pubmed: 28827772
Curr Opin Plant Biol. 2014 Jun;19:43-50
pubmed: 24727073
Plant Physiol. 2013 Oct;163(2):1047-58
pubmed: 23929720
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Front Plant Sci. 2017 Dec 06;8:2082
pubmed: 29270185
J Chem Ecol. 1996 Aug;22(8):1355-66
pubmed: 24226242
J Mol Biol. 2000 Nov 10;303(5):831-42
pubmed: 11061978
Plant Sci. 2018 Nov;276:163-170
pubmed: 30348315
Nucleic Acids Res. 2017 Jul 3;45(W1):W320-W324
pubmed: 28387820
Biol Direct. 2008 May 21;3:20
pubmed: 18495041
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Nat Plants. 2017 Jan 13;3:16208
pubmed: 28085153
Biochem Biophys Res Commun. 2007 Aug 17;360(1):188-93
pubmed: 17586462
Nat Commun. 2019 May 13;10(1):2142
pubmed: 31086174
Nat Commun. 2016 Jul 15;7:12116
pubmed: 27418042
J Plant Physiol. 2011 Apr 15;168(6):549-57
pubmed: 21047699
Plant J. 2018 May;94(3):469-484
pubmed: 29438577
BMC Biol. 2016 Nov 11;14(1):98
pubmed: 27835992
Curr Opin Struct Biol. 2017 Dec;47:95-104
pubmed: 28787627
Plant J. 2015 May;82(4):680-92
pubmed: 25759247
Plant Cell Rep. 2009 Aug;28(8):1215-34
pubmed: 19504099
Nat Biotechnol. 2003 May;21(5):539-45
pubmed: 12692560
Plant Cell Rep. 1993 Aug;12(10):573-6
pubmed: 24201788
Metab Eng. 2018 Jul;48:150-162
pubmed: 29852273
Science. 2018 Jun 15;360(6394):1235-1239
pubmed: 29724909
Plant Cell. 2013 Oct;25(10):3640-56
pubmed: 24179132
Plant Mol Biol. 2007 Sep;65(1-2):13-30
pubmed: 17611800
BMC Genomics. 2015 Aug 19;16:619
pubmed: 26285573
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
BMC Plant Biol. 2010 Aug 19;10:182
pubmed: 20723215
Biochim Biophys Acta. 2009 Mar;1794(3):526-31
pubmed: 19100871
Plant Cell. 2007 Sep;19(9):2886-97
pubmed: 17890378
Plant Physiol. 2013 Dec;163(4):1792-803
pubmed: 24108213
Sci Rep. 2017 Jan 17;7:40453
pubmed: 28094274
J Biol Chem. 2004 Jul 23;279(30):31796-803
pubmed: 15148317
Methods Enzymol. 2016;576:167-206
pubmed: 27480687
Plant Biol (Stuttg). 2015 Nov;17(6):1242-6
pubmed: 26284695
Nat Prod Rep. 2006 Aug;23(4):532-47
pubmed: 16874388
Plant Cell. 2008 Mar;20(3):524-42
pubmed: 18326827
Phytochemistry. 2009 Jul-Aug;70(11-12):1355-65
pubmed: 19712949
Plant Cell Physiol. 2013 May;54(5):673-85
pubmed: 23493402
J Struct Biol. 2005 Apr;150(1):1-10
pubmed: 15797725
Nucleic Acids Res. 2001 Jan 1;29(1):221-2
pubmed: 11125097
Proc Natl Acad Sci U S A. 2018 Mar 20;115(12):3180-3185
pubmed: 29511102
Eur J Biochem. 2002 Apr;269(8):2204-13
pubmed: 11985599
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
J Mol Biol. 2004 Jul 9;340(3):399-404
pubmed: 15210342
Plant Physiol. 2013 Jun;162(2):1006-17
pubmed: 23632853
Plant J. 2016 Dec;88(6):1058-1070
pubmed: 27549386
Plant Physiol. 2017 Aug;174(4):2098-2112
pubmed: 28550206
Biochem Soc Trans. 2017 Apr 15;45(2):537-544
pubmed: 28408493
J Biol Chem. 2000 Feb 4;275(5):3051-6
pubmed: 10652285
FEBS Lett. 1980 Feb 11;110(2):187-91
pubmed: 6768587
Plant Physiol. 2016 Nov;172(3):1563-1577
pubmed: 27688619
Plant Physiol. 2017 Jul;174(3):1371-1383
pubmed: 28483880