A polyketide synthase from Verticillium dahliae modulates melanin biosynthesis and hyphal growth to promote virulence.
Hyphal growth
Melanin
Microsclerotia
Polyketide synthase
Verticillium dahliae
Virulence
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
30 05 2022
30 05 2022
Historique:
received:
21
03
2022
accepted:
13
05
2022
entrez:
31
5
2022
pubmed:
1
6
2022
medline:
3
6
2022
Statut:
epublish
Résumé
During the disease cycle, plant pathogenic fungi exhibit a morphological transition between hyphal growth (the phase of active infection) and the production of long-term survival structures that remain dormant during "overwintering." Verticillium dahliae is a major plant pathogen that produces heavily melanized microsclerotia (MS) that survive in the soil for 14 or more years. These MS are multicellular structures produced during the necrotrophic phase of the disease cycle. Polyketide synthases (PKSs) are responsible for catalyzing production of many secondary metabolites including melanin. While MS contribute to long-term survival, hyphal growth is key for infection and virulence, but the signaling mechanisms by which the pathogen maintains hyphal growth are unclear. We analyzed the VdPKSs that contain at least one conserved domain potentially involved in secondary metabolism (SM), and screened the effect of VdPKS deletions in the virulent strain AT13. Among the five VdPKSs whose deletion affected virulence on cotton, we found that VdPKS9 acted epistatically to the VdPKS1-associated melanin pathway to promote hyphal growth. The decreased hyphal growth in VdPKS9 mutants was accompanied by the up-regulation of melanin biosynthesis and MS formation. Overexpression of VdPKS9 transformed melanized hyphal-type (MH-type) into the albinistic hyaline hyphal-type (AH-type), and VdPKS9 was upregulated in the AH-type population, which also exhibited higher virulence than the MH-type. We show that VdPKS9 is a powerful negative regulator of both melanin biosynthesis and MS formation in V. dahliae. These findings provide insight into the mechanism of how plant pathogens promote their virulence by the maintenance of vegetative hyphal growth during infection and colonization of plant hosts, and may provide novel targets for the control of melanin-producing filamentous fungi.
Sections du résumé
BACKGROUND
During the disease cycle, plant pathogenic fungi exhibit a morphological transition between hyphal growth (the phase of active infection) and the production of long-term survival structures that remain dormant during "overwintering." Verticillium dahliae is a major plant pathogen that produces heavily melanized microsclerotia (MS) that survive in the soil for 14 or more years. These MS are multicellular structures produced during the necrotrophic phase of the disease cycle. Polyketide synthases (PKSs) are responsible for catalyzing production of many secondary metabolites including melanin. While MS contribute to long-term survival, hyphal growth is key for infection and virulence, but the signaling mechanisms by which the pathogen maintains hyphal growth are unclear.
RESULTS
We analyzed the VdPKSs that contain at least one conserved domain potentially involved in secondary metabolism (SM), and screened the effect of VdPKS deletions in the virulent strain AT13. Among the five VdPKSs whose deletion affected virulence on cotton, we found that VdPKS9 acted epistatically to the VdPKS1-associated melanin pathway to promote hyphal growth. The decreased hyphal growth in VdPKS9 mutants was accompanied by the up-regulation of melanin biosynthesis and MS formation. Overexpression of VdPKS9 transformed melanized hyphal-type (MH-type) into the albinistic hyaline hyphal-type (AH-type), and VdPKS9 was upregulated in the AH-type population, which also exhibited higher virulence than the MH-type.
CONCLUSIONS
We show that VdPKS9 is a powerful negative regulator of both melanin biosynthesis and MS formation in V. dahliae. These findings provide insight into the mechanism of how plant pathogens promote their virulence by the maintenance of vegetative hyphal growth during infection and colonization of plant hosts, and may provide novel targets for the control of melanin-producing filamentous fungi.
Identifiants
pubmed: 35637443
doi: 10.1186/s12915-022-01330-2
pii: 10.1186/s12915-022-01330-2
pmc: PMC9153097
doi:
Substances chimiques
Fungal Proteins
0
Melanins
0
Polyketide Synthases
79956-01-7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
125Informations de copyright
© 2022. The Author(s).
Références
Mol Plant Pathol. 2018 Jun;19(6):1444-1453
pubmed: 29024255
Annu Rev Phytopathol. 2021 Aug 25;59:31-51
pubmed: 33891830
Mol Plant Microbe Interact. 2006 Feb;19(2):139-49
pubmed: 16529376
Annu Rev Phytopathol. 2009;47:39-62
pubmed: 19385730
Philos Trans R Soc Lond B Biol Sci. 2007 Jul 29;362(1483):1195-200
pubmed: 17360275
New Phytol. 2021 May;230(4):1578-1593
pubmed: 33570748
mBio. 2021 Mar 23;12(2):
pubmed: 33758088
Fungal Biol. 2017 Jun - Jul;121(6-7):589-601
pubmed: 28606354
Pest Manag Sci. 2013 Feb;69(2):278-84
pubmed: 22933369
FEMS Yeast Res. 2019 Sep 1;19(6):
pubmed: 31374572
PLoS Pathog. 2011 Jul;7(7):e1002137
pubmed: 21829347
New Phytol. 2019 Apr;222(2):1012-1029
pubmed: 30609067
Prikl Biokhim Mikrobiol. 2014 Mar-Apr;50(2):125-34
pubmed: 25272728
Nat Plants. 2019 Nov;5(11):1167-1176
pubmed: 31636399
Mol Plant Microbe Interact. 2015 Oct;28(10):1091-101
pubmed: 26035129
Annu Rev Phytopathol. 2015;53:181-98
pubmed: 26047557
Curr Opin Microbiol. 2010 Aug;13(4):431-6
pubmed: 20627806
RSC Adv. 2019 Nov 4;9(61):35797-35802
pubmed: 35528102
PLoS Pathog. 2017 Mar 10;13(3):e1006275
pubmed: 28282450
Can J Microbiol. 1976 May;22(5):702-11
pubmed: 945119
Fungal Genet Biol. 2017 Jan;98:1-11
pubmed: 27866941
Methods Mol Biol. 2011;722:199-212
pubmed: 21590423
FEMS Microbiol Lett. 2004 Mar 19;232(2):203-9
pubmed: 15033240
PLoS One. 2011;6(12):e28341
pubmed: 22174791
Fungal Genet Biol. 2016 Mar;88:13-23
pubmed: 26812120
Front Microbiol. 2016 Sep 27;7:1532
pubmed: 27729908
Fungal Biol. 2013 May;117(5):368-79
pubmed: 23719222
Can J Microbiol. 1976 Jun;22(6):787-99
pubmed: 945120
Appl Microbiol Biotechnol. 2018 Dec;102(23):9873-9880
pubmed: 30255231
New Phytol. 2019 Mar;221(4):2138-2159
pubmed: 30290010
Nat Rev Microbiol. 2005 Dec;3(12):937-47
pubmed: 16322742
Fungal Genet Biol. 2013 Jan;50:55-62
pubmed: 23174282
Environ Microbiol. 2019 Aug;21(8):2977-2996
pubmed: 31136051
Cell Death Discov. 2021 Mar 29;7(1):62
pubmed: 33782397
Appl Microbiol Biotechnol. 2014 Feb;98(4):1749-62
pubmed: 24389666
Fungal Genet Biol. 2012 Apr;49(4):271-83
pubmed: 22387367
J Bacteriol. 1998 Jun;180(12):3031-8
pubmed: 9620950
Mol Plant Pathol. 2018 Apr;19(4):841-857
pubmed: 28520093
PLoS Genet. 2008 Apr 11;4(4):e1000046
pubmed: 18404212
Gene. 2014 Oct 25;550(2):238-44
pubmed: 25151308
Fungal Biol. 2020 May;124(5):490-500
pubmed: 32389312
Mol Biotechnol. 2011 Nov;49(3):209-21
pubmed: 21424547
Int J Mol Sci. 2020 Nov 18;21(22):
pubmed: 33218033
J Biol Chem. 2009 Jun 19;284(25):17194-17205
pubmed: 19349281
FEMS Microbiol Lett. 2019 Apr 1;366(7):
pubmed: 31004487
Phytopathology. 2008 Aug;98(8):871-85
pubmed: 18943205
New Phytol. 2018 Jan;217(2):756-770
pubmed: 29084346
Mol Microbiol. 2016 Feb;99(4):729-48
pubmed: 26514268
Microbiol Spectr. 2017 Mar;5(2):
pubmed: 28256187
Mol Plant Microbe Interact. 2020 Nov;33(11):1315-1329
pubmed: 32815478
Biomol Ther (Seoul). 2017 Jul 1;25(4):396-403
pubmed: 28605833
Microbiol Mol Biol Rev. 2002 Sep;66(3):447-59, table of contents
pubmed: 12208999
Fungal Biol. 2017 Dec;121(12):1001-1010
pubmed: 29122172
Front Microbiol. 2016 Aug 03;7:1192
pubmed: 27536281
Mycology. 2018 Mar 07;9(3):166-175
pubmed: 30181923
Biol Chem. 2014 Dec;395(12):1389-99
pubmed: 25205724
Mol Plant Pathol. 2020 Nov;21(11):1451-1466
pubmed: 32954659
Microbiol Res. 2019 Dec;229:126326
pubmed: 31493702
mSphere. 2019 Jul 10;4(4):
pubmed: 31292234
Nat Prod Rep. 2012 Oct;29(10):1050-73
pubmed: 22858605
Microbiol Res. 2021 Jan;242:126620
pubmed: 33189072
Environ Microbiol. 2019 Dec;21(12):4875-4886
pubmed: 31698543
Antonie Van Leeuwenhoek. 2019 Jul;112(7):1095-1104
pubmed: 30725325
J Genet Genomics. 2013 Aug 20;40(8):421-31
pubmed: 23969251
Environ Microbiol. 2019 Dec;21(12):4852-4874
pubmed: 31667948
Cell Microbiol. 2003 Apr;5(4):203-23
pubmed: 12675679
BMC Genomics. 2013 Sep 09;14:607
pubmed: 24015849
Nat Rev Microbiol. 2019 Mar;17(3):167-180
pubmed: 30531948
Mol Microbiol. 2022 Feb;117(2):261-273
pubmed: 34278632
Front Microbiol. 2013 Jan 18;3:440
pubmed: 23346079
BMC Genomics. 2014 May 01;15:324
pubmed: 24884698
Microbiology (Reading). 2018 Apr;164(4):685-696
pubmed: 29485393
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
Fungal Genet Biol. 2010 May;47(5):406-15
pubmed: 20144723
Sci Rep. 2016 Jun 22;6:27979
pubmed: 27329129
Genes Dev. 2004 Jul 15;18(14):1695-708
pubmed: 15256499
Phytopathology. 2020 Aug;110(8):1465-1475
pubmed: 32286920
Mol Microbiol. 2019 Aug;112(2):649-666
pubmed: 31116900
Mol Plant Pathol. 2016 Dec;17(9):1364-1381
pubmed: 26857810
FEMS Microbiol Rev. 2009 Mar;33(2):376-93
pubmed: 19178566
Curr Genet. 2005 Aug;48(2):109-16
pubmed: 16003535
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Mol Plant Microbe Interact. 2013 Feb;26(2):249-56
pubmed: 22970788
Fungal Biol. 2012 Feb;116(2):318-31
pubmed: 22289777
Fungal Genet Biol. 2005 May;42(5):420-33
pubmed: 15809006
Mol Microbiol. 2000 Dec;38(5):940-54
pubmed: 11123670