Clathrin-mediated endocytosis facilitates the internalization of Magnaporthe oryzae effectors into rice cells.
Journal
The Plant cell
ISSN: 1532-298X
Titre abrégé: Plant Cell
Pays: England
ID NLM: 9208688
Informations de publication
Date de publication:
26 06 2023
26 06 2023
Historique:
received:
08
12
2022
accepted:
02
03
2023
medline:
27
6
2023
pubmed:
29
3
2023
entrez:
28
3
2023
Statut:
ppublish
Résumé
Fungi and oomycetes deliver effectors into living plant cells to suppress defenses and control plant processes needed for infection. Little is known about the mechanism by which these pathogens translocate effector proteins across the plasma membrane into the plant cytoplasm. The blast fungus Magnaporthe oryzae secretes cytoplasmic effectors into a specialized biotrophic interfacial complex (BIC) before translocation. Here, we show that cytoplasmic effectors within BICs are packaged into punctate membranous effector compartments that are occasionally observed in the host cytoplasm. Live cell imaging with fluorescently labeled proteins in rice (Oryza sativa) showed that these effector puncta colocalize with the plant plasma membrane and with CLATHRIN LIGHT CHAIN 1, a component of clathrin-mediated endocytosis (CME). Inhibiting CME using virus-induced gene silencing and chemical treatments resulted in cytoplasmic effectors in swollen BICs lacking effector puncta. By contrast, fluorescent marker colocalization, gene silencing, and chemical inhibitor studies failed to support a major role for clathrin-independent endocytosis in effector translocation. Effector localization patterns indicated that cytoplasmic effector translocation occurs underneath appressoria before invasive hyphal growth. Taken together, this study provides evidence that cytoplasmic effector translocation is mediated by CME in BICs and suggests a role for M. oryzae effectors in coopting plant endocytosis.
Identifiants
pubmed: 36976907
pii: 7091728
doi: 10.1093/plcell/koad094
pmc: PMC10291035
doi:
Substances chimiques
Fungal Proteins
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2527-2551Commentaires et corrections
Type : CommentIn
Informations de copyright
© The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.
Déclaration de conflit d'intérêts
Conflict of interest statement. The authors declare no competing interests.
Références
Mol Biol Cell. 1999 Apr;10(4):961-74
pubmed: 10198050
Methods Mol Biol. 2021;2356:69-77
pubmed: 34236677
Cold Spring Harb Perspect Biol. 2011 Aug 01;3(8):a004721
pubmed: 21576253
Plant Cell. 1995 Aug;7(8):1221-33
pubmed: 7549480
Plant Cell. 2012 May;24(5):2105-22
pubmed: 22589463
Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15967-72
pubmed: 19717456
Nat Commun. 2013;4:1996
pubmed: 23774898
Plant Physiol. 2017 May;174(1):5-20
pubmed: 28275150
J Cell Biol. 1993 Dec;123(5):1107-17
pubmed: 8245121
Fungal Genet Biol. 2002 Dec;37(3):233-44
pubmed: 12431458
PLoS Genet. 2013;9(12):e1004035
pubmed: 24385929
Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12713-8
pubmed: 9770551
Plant Cell. 2005 Nov;17(11):3203-12
pubmed: 16199615
Mol Gen Genet. 1978 Jul 11;163(2):181-7
pubmed: 355847
Front Plant Sci. 2021 Jun 18;12:685187
pubmed: 34220905
Trends Plant Sci. 2015 Jun;20(6):388-97
pubmed: 25914086
Plant Cell. 2010 Apr;22(4):1388-403
pubmed: 20435900
Plant Physiol. 2017 Oct;175(2):708-720
pubmed: 28830938
Curr Opin Plant Biol. 2017 Aug;38:19-24
pubmed: 28460240
Nat Rev Mol Cell Biol. 2018 May;19(5):313-326
pubmed: 29410531
Plant Cell. 2022 Jan 20;34(1):146-173
pubmed: 34550393
Methods Mol Biol. 2006;344:403-20
pubmed: 17033082
Plant Physiol. 2008 Aug;147(4):1482-92
pubmed: 18678740
Plant Cell. 2008 May;20(5):1363-80
pubmed: 18502847
Elife. 2018 Jun 22;7:
pubmed: 29932422
New Phytol. 2017 Oct;216(1):8-10
pubmed: 28850183
Nat Microbiol. 2021 Jun;6(6):722-730
pubmed: 33941900
J Biol Chem. 2001 May 25;276(21):18540-50
pubmed: 11278939
Traffic. 2001 Sep;2(9):631-42
pubmed: 11555417
Science. 2018 Mar 23;359(6382):1399-1403
pubmed: 29567712
Nature. 2014 Jul 31;511(7511):587-91
pubmed: 25043043
Genetics. 1991 Jan;127(1):87-101
pubmed: 2016048
Nat Rev Microbiol. 2013 Nov;11(11):800-14
pubmed: 24129511
Nat Chem Biol. 2019 Jun;15(6):641-649
pubmed: 31011214
Int J Mol Sci. 2020 Feb 25;21(5):
pubmed: 32106431
mBio. 2018 Feb 27;9(1):
pubmed: 29487238
Plant Cell. 2021 Jul 2;33(5):1447-1471
pubmed: 33677602
Elife. 2020 Jan 23;9:
pubmed: 31971511
Traffic. 2015 Feb;16(2):204-26
pubmed: 25430691
J Cell Sci. 2020 Aug 6;133(15):
pubmed: 32616560
J Biol Chem. 2007 Mar 2;282(9):6803-11
pubmed: 17166839
J Cell Sci. 2018 Sep 3;131(17):
pubmed: 30177507
Fungal Genet Biol. 2005 Jun;42(6):483-92
pubmed: 15893252
Trends Plant Sci. 2000 Oct;5(10):446-51
pubmed: 11044722
Front Cell Dev Biol. 2021 Jan 21;8:615447
pubmed: 33553150
PLoS One. 2016 Aug 25;11(8):e0160637
pubmed: 27560664
PLoS Pathog. 2016 Oct 6;12(10):e1005921
pubmed: 27711180
Plant Cell. 2012 Jan;24(1):322-35
pubmed: 22267486
Plant Cell. 2017 Jun;29(6):1184-1195
pubmed: 28522546
Curr Opin Plant Biol. 2010 Dec;13(6):706-13
pubmed: 20851666
Cell. 2010 Jul 23;142(2):284-95
pubmed: 20655469
New Phytol. 2017 Jan;213(2):956-964
pubmed: 27716942
Microbiologyopen. 2015 Dec;4(6):952-66
pubmed: 26472068
Nat Commun. 2018 Jun 14;9(1):2347
pubmed: 29904064
Plant Physiol. 2007 Dec;145(4):1192-200
pubmed: 17981986
Plant Cell. 2013 Aug;25(8):2986-97
pubmed: 23975899
PLoS One. 2015 Sep 08;10(9):e0137071
pubmed: 26348328
Nat Rev Genet. 2010 Aug;11(8):539-48
pubmed: 20585331
J Cell Sci. 2011 Dec 1;124(Pt 23):3933-40
pubmed: 22194304
Microbiol Mol Biol Rev. 2015 Sep;79(3):263-80
pubmed: 26041933
New Phytol. 2017 Oct;216(1):205-215
pubmed: 28758684
Plant Cell. 2023 Apr 20;35(5):1360-1385
pubmed: 36808541
Plant Mol Biol. 2013 Jan;81(1-2):41-56
pubmed: 23103994
Curr Opin Plant Biol. 2011 Dec;14(6):674-82
pubmed: 21945181
New Phytol. 2008;179(1):196-208
pubmed: 18433432
Curr Opin Plant Biol. 2012 Aug;15(4):367-74
pubmed: 22664220
Annu Rev Plant Biol. 2015;66:513-45
pubmed: 25923844
J Cell Biol. 2014 Jun 9;205(5):721-35
pubmed: 24891602
New Phytol. 2006;171(4):699-718
pubmed: 16918543
PLoS Biol. 2014 Feb 25;12(2):e1001801
pubmed: 24586116
Eukaryot Cell. 2007 Mar;6(3):546-54
pubmed: 17142568
Nat Cell Biol. 2011 Oct 09;13(12):1431-6
pubmed: 21983562
Plant Cell. 2009 Apr;21(4):1273-90
pubmed: 19357089
PLoS Pathog. 2012;8(4):e1002643
pubmed: 22496661
Plant Physiol. 2018 Jan;176(1):208-218
pubmed: 29074601
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
Front Cell Dev Biol. 2021 Jun 17;9:681734
pubmed: 34222251
J Microsc. 2004 May;214(Pt 2):159-73
pubmed: 15102063
Nat Commun. 2016 Jun 08;7:11710
pubmed: 27271794
Annu Rev Microbiol. 1996;50:491-512
pubmed: 8905089
Proc Natl Acad Sci U S A. 2016 Sep 27;113(39):11034-9
pubmed: 27651493
Cell Logist. 2012 Oct 1;2(4):203-208
pubmed: 23538558
New Phytol. 2016 Apr;210(2):627-42
pubmed: 26765243
Mol Biol Cell. 2002 Apr;13(4):1313-28
pubmed: 11950941
Plant Cell. 2007 Feb;19(2):706-24
pubmed: 17322409