title: Transcriptional dynamics of Phytophthora infestans during sequential stages of hemibiotrophic infection of tomato.
abstract: Hemibiotrophic plant pathogens, such as the oomycete Phytophthora infestans, employ a biphasic infection strategy, initially behaving as biotrophs, where minimal symptoms are exhibited by the plant, and subsequently as necrotrophs, feeding on dead plant tissue. The regulation of this transition and the breadth of molecular mechanisms that modulate plant defences are not well understood, although effector proteins secreted by the pathogen are thought to play a key role. We examined the transcriptional dynamics of P. infestans in a compatible interaction with its host tomato (Solanum lycopersicum) at three infection stages: biotrophy; the transition from biotrophy to necrotrophy; and necrotrophy. The expression data suggest a tight temporal regulation of many pathways associated with the suppression of plant defence mechanisms and pathogenicity, including the induction of putative cytoplasmic and apoplastic effectors. Twelve of these were experimentally evaluated to determine their ability to suppress necrosis caused by the P. infestans necrosis-inducing protein PiNPP1.1 in Nicotiana benthamiana. Four effectors suppressed necrosis, suggesting that they might prolong the biotrophic phase. This study suggests that a complex regulation of effector expression modulates the outcome of the interaction.
authors.affiliation: Section of Plant Pathology and Plant Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.
authors.forename: Andrea P
authors.initials: AP
authors.lastname: Zuluaga
authors.affiliation: Section of Plant Pathology and Plant Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.|Laboratory of Agrigenomics, Universidad Nacional Autónoma de México (UNAM), ENES-León, 37684, Guanajuato, Mexico.
authors.forename: Julio C
authors.initials: JC
authors.lastname: Vega-Arreguín
authors.affiliation: Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY, 14853, USA.|Robert W. Holly Center for Agriculture and Health, USDA-ARS, Tower Road, Ithaca, NY, 14853, USA.
authors.forename: Zhangjun
authors.initials: Z
authors.lastname: Fei
authors.affiliation: Institute for Biotechnology and Life Science Technologies, Cornell University, Ithaca, NY, 14853, USA.
authors.forename: Lalit
authors.initials: L
authors.lastname: Ponnala
authors.affiliation: Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.|Biotechnology Institute, Nongwoo Bio Co., Ltd, Gyeonggi, South Korea.
authors.forename: Sang Jik
authors.initials: SJ
authors.lastname: Lee
authors.affiliation: Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.|Departamento de Biología Vegetal, Campus de Teatinos, Universidad de Málaga, 29071, Málaga, Spain.
authors.forename: Antonio J
authors.initials: AJ
authors.lastname: Matas
authors.affiliation: Section of Plant Pathology and Plant Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.
authors.forename: Sean
authors.initials: S
authors.lastname: Patev
authors.affiliation: Section of Plant Pathology and Plant Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.
authors.forename: William E
authors.initials: WE
authors.lastname: Fry
authors.affiliation: Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.
authors.forename: Jocelyn K C
authors.initials: JK
authors.lastname: Rose
mesh_terms: D016000:Cluster Analysis; D020869:Gene Expression Profiling; D005786:Gene Expression Regulation; D018551:Solanum lycopersicum / Q000382:microbiology*; D055750:Phytophthora infestans / Q000235:genetics* / Q000472:pathogenicity*; D010935:Plant Diseases / Q000382:microbiology*; D018515:Plant Leaves / Q000382:microbiology; D011506:Proteins / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D017422:Sequence Analysis, DNA; D013997:Time Factors; D014026:Nicotiana / Q000382:microbiology; D014158:Transcription, Genetic; D059467:Transcriptome / Q000235:genetics
chemical_list: D011506:Proteins; D012333:RNA, Messenger
keywords: Phytophthora infestans; hemibiotroph; in planta effectors; transcriptome
references.citation: Proc Int Conf Intell Syst Mol Biol. 1999;:138-48
references.pmid: 10786296
references.citation: Plant Cell. 2000 May;12(5):771-86
references.pmid: 10810149
references.citation: EMBO J. 2000 May 15;19(10):2257-69
references.pmid: 10811617
references.citation: Genome Res. 2000 Dec;10(12):2055-61
references.pmid: 11116099
references.citation: Curr Opin Plant Biol. 2001 Aug;4(4):322-7
references.pmid: 11418342
references.citation: Bioinformatics. 2001 Dec;17(12):1093-104
references.pmid: 11751217
references.citation: Genome Res. 2002 Apr;12(4):656-64
references.pmid: 11932250
references.citation: Plant Cell. 2002 Jun;14(6):1329-45
references.pmid: 12084830
references.citation: Appl Environ Microbiol. 2002 Oct;68(10):4996-5004
references.pmid: 12324349
references.citation: Mol Plant Microbe Interact. 2003 Feb;16(2):141-8
references.pmid: 12575748
references.citation: Cell. 2003 Feb 7;112(3):369-77
references.pmid: 12581526
references.citation: Cell. 2003 Feb 7;112(3):379-89
references.pmid: 12581527
references.citation: Fungal Genet Biol. 2003 Mar;38(2):250-63
references.pmid: 12620261
references.citation: Mol Genet Genomics. 2003 Jul;269(4):499-507
references.pmid: 12768412
references.citation: Genome Res. 2003 Jul;13(7):1675-85
references.pmid: 12840044
references.citation: Nucleic Acids Res. 2004 Jan 1;32(Database issue):D262-6
references.pmid: 14681408
references.citation: J Biol Chem. 2004 Jun 18;279(25):26370-7
references.pmid: 15096512
references.citation: J Mol Biol. 2004 Jul 16;340(4):783-95
references.pmid: 15223320
references.citation: Curr Opin Plant Biol. 2004 Aug;7(4):356-64
references.pmid: 15231256
references.citation: Bioinformatics. 2004 Dec 12;20(18):3710-5
references.pmid: 15297299
references.citation: Fungal Genet Biol. 2005 Mar;42(3):244-56
references.pmid: 15707845
references.citation: Annu Rev Phytopathol. 2005;43:205-27
references.pmid: 16078883
references.citation: Mol Plant Microbe Interact. 2005 Sep;18(9):913-22
references.pmid: 16167762
references.citation: Fungal Genet Biol. 2006 Jan;43(1):20-33
references.pmid: 16380277
references.citation: J Gen Virol. 1992 Aug;73 ( Pt 8):2105-14
references.pmid: 1645147
references.citation: Mol Plant Microbe Interact. 2006 Aug;19(8):854-63
references.pmid: 16903351
references.citation: Plant J. 2006 Oct;48(2):165-76
references.pmid: 16965554
references.citation: Plant Physiol. 2007 Jan;143(1):364-77
references.pmid: 17085509
references.citation: Plant Physiol. 2007 May;144(1):32-42
references.pmid: 17351049
references.citation: Mol Plant Microbe Interact. 2007 Jul;20(7):781-93
references.pmid: 17601166
references.citation: Nature. 2007 Nov 1;450(7166):115-8
references.pmid: 17914356
references.citation: Nat Methods. 2008 Feb;5(2):179-81
references.pmid: 18193056
references.citation: Nucleic Acids Res. 2008 May;36(8):2630-8
references.pmid: 18344523
references.citation: Plant Cell. 2008 Jul;20(7):1930-47
references.pmid: 18621946
references.citation: Mol Plant Microbe Interact. 2008 Jun;21(6):820-30
references.pmid: 18624645
references.citation: PLoS One. 2008 Aug 06;3(8):e2875
references.pmid: 18682852
references.citation: Phytopathology. 2000 Jan;90(1):78-84
references.pmid: 18944575
references.citation: J Mol Biol. 2009 Jan 30;385(4):1207-20
references.pmid: 19071134
references.citation: PLoS One. 2009;4(5):e5556
references.pmid: 19440541
references.citation: BMC Genomics. 2009 Jun 12;10:264
references.pmid: 19523228
references.citation: BMC Genomics. 2009 Jul 06;10:299
references.pmid: 19580677
references.citation: Nature. 2009 Sep 17;461(7262):393-8
references.pmid: 19741609
references.citation: Plant Cell. 2009 Sep;21(9):2928-47
references.pmid: 19794118
references.citation: Plant J. 2010 May;62(3):357-66
references.pmid: 20128886
references.citation: Plant Signal Behav. 2010 Jun;5(6):769-72
references.pmid: 20400849
references.citation: PLoS One. 2010 May 07;5(5):e10536
references.pmid: 20479869
references.citation: BMC Plant Biol. 2010 Jun 08;10:103
references.pmid: 20529319
references.citation: BMC Genomics. 2010 Jun 17;11:384
references.pmid: 20565788
references.citation: Plant Physiol. 2011 Jan;155(1):490-501
references.pmid: 21071601
references.citation: Mol Plant Microbe Interact. 2011 Mar;24(3):368-76
references.pmid: 21077772
references.citation: BMC Genomics. 2010 Nov 16;11:637
references.pmid: 21080964
references.citation: PLoS One. 2011 Mar 14;6(3):e17767
references.pmid: 21423760
references.citation: Mol Plant Microbe Interact. 2011 Jul;24(7):808-18
references.pmid: 21644839
references.citation: Plant Cell. 2011 Jun;23(6):2064-86
references.pmid: 21653195
references.citation: Mol Plant Pathol. 2012 Jan;13(1):17-37
references.pmid: 21726390
references.citation: BMC Genomics. 2011 Oct 11;12:498
references.pmid: 21988821
references.citation: BMC Bioinformatics. 2011 Nov 23;12:453
references.pmid: 22111509
references.citation: Cell Microbiol. 2012 May;14(5):669-81
references.pmid: 22233353
references.citation: Mol Plant Microbe Interact. 2012 Jul;25(7):896-909
references.pmid: 22397404
references.citation: Mol Plant Microbe Interact. 2012 Jul;25(7):910-9
references.pmid: 22414442
references.citation: Nat Genet. 2012 Sep;44(9):1060-5
references.pmid: 22885923
references.citation: PLoS Pathog. 2012;8(8):e1002875
references.pmid: 22927814
references.citation: Mol Plant Pathol. 2013 Feb;14(2):171-84
references.pmid: 23127185
references.citation: New Phytol. 2013 Mar;197(4):1236-49
references.pmid: 23252678
references.citation: Genome Biol. 2013 Jun 25;14(6):R63
references.pmid: 23799990
references.citation: Plant Cell. 2014 Mar;26(3):1345-59
references.pmid: 24632534
references.citation: New Phytol. 2014 Aug;203(3):926-38
references.pmid: 24889686
references.citation: Mol Plant Pathol. 2016 Jan;17(1):42-54
references.pmid: 25808779
references.citation: Plant Dis. 2000 Jul;84(7):731-735
references.pmid: 30832099
references.citation: Arch Biochem Biophys. 1983 Jul 15;224(2):494-505
references.pmid: 6870275
references.citation: Mol Plant Microbe Interact. 1997 Nov;10(8):1028-30
references.pmid: 9353948
references.citation: Biochem Biophys Res Commun. 1998 Apr 7;245(1):133-9
references.pmid: 9535796
references.citation: Fungal Genet Biol. 1998 Mar;23(2):126-38
references.pmid: 9578626