Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches' broom disease.
Defense responses
Lignans and coumarins
Linoleic acid
MAPK-signaling cascade
Nerium spp
Phenolic acids
Plant-pathogen interaction
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
14 Jun 2022
14 Jun 2022
Historique:
received:
13
11
2021
accepted:
27
05
2022
entrez:
14
6
2022
pubmed:
15
6
2022
medline:
18
6
2022
Statut:
epublish
Résumé
Nerium indicum Mill. is an ornamental plant that is found in parks, riversides, lakesides, and scenic areas in China and other parts of the world. Our recent survey indicated the prevalence of witches' broom disease (WBD) in Guangdong, China. To find out the possible defense strategies against WBD, we performed a MiSeq based ITS sequencing to identify the possible casual organism, then did a de novo transcriptome sequencing and metabolome profiling in the phloem and stem tip of N. indicum plants suffering from WBD compared to healthy ones. The survey showed that Wengyuen county and Zengcheng district had the highest disease incidence rates. The most prevalent microbial species in the diseased tissues was Cophinforma mamane. The transcriptome sequencing resulted in the identification of 191,224 unigenes of which 142,396 could be annotated. There were 19,031 and 13,284 differentially expressed genes (DEGs) between diseased phloem (NOWP) and healthy phloem (NOHP), and diseased stem (NOWS) and healthy stem (NOHS), respectively. The DEGs were enriched in MAPK-signaling (plant), plant-pathogen interaction, plant-hormone signal transduction, phenylpropanoid and flavonoid biosynthesis, linoleic acid and α-linoleic acid metabolism pathways. Particularly, we found that N. indicum plants activated the phytohormone signaling, MAPK-signaling cascade, defense related proteins, and the biosynthesis of phenylpropanoids and flavonoids as defense responses to the pathogenic infection. The metabolome profiling identified 586 metabolites of which 386 and 324 metabolites were differentially accumulated in NOHP vs NOWP and NOHS and NOWS, respectively. The differential accumulation of metabolites related to phytohormone signaling, linoleic acid metabolism, phenylpropanoid and flavonoid biosynthesis, nicotinate and nicotinamide metabolism, and citrate cycle was observed, indicating the role of these pathways in defense responses against the pathogenic infection. Our results showed that Guangdong province has a high incidence of WBD in most of the surveyed areas. C. mamane is suspected to be the causing pathogen of WBD in N. indicum. N. indicum initiated the MAPK-signaling cascade and phytohormone signaling, leading to the activation of pathogen-associated molecular patterns and hypersensitive response. Furthermore, N. indicum accumulated high concentrations of phenolic acids, coumarins and lignans, and flavonoids under WBD. These results provide scientific tools for the formulation of control strategies of WBD in N. indicum.
Sections du résumé
BACKGROUND
BACKGROUND
Nerium indicum Mill. is an ornamental plant that is found in parks, riversides, lakesides, and scenic areas in China and other parts of the world. Our recent survey indicated the prevalence of witches' broom disease (WBD) in Guangdong, China. To find out the possible defense strategies against WBD, we performed a MiSeq based ITS sequencing to identify the possible casual organism, then did a de novo transcriptome sequencing and metabolome profiling in the phloem and stem tip of N. indicum plants suffering from WBD compared to healthy ones.
RESULTS
RESULTS
The survey showed that Wengyuen county and Zengcheng district had the highest disease incidence rates. The most prevalent microbial species in the diseased tissues was Cophinforma mamane. The transcriptome sequencing resulted in the identification of 191,224 unigenes of which 142,396 could be annotated. There were 19,031 and 13,284 differentially expressed genes (DEGs) between diseased phloem (NOWP) and healthy phloem (NOHP), and diseased stem (NOWS) and healthy stem (NOHS), respectively. The DEGs were enriched in MAPK-signaling (plant), plant-pathogen interaction, plant-hormone signal transduction, phenylpropanoid and flavonoid biosynthesis, linoleic acid and α-linoleic acid metabolism pathways. Particularly, we found that N. indicum plants activated the phytohormone signaling, MAPK-signaling cascade, defense related proteins, and the biosynthesis of phenylpropanoids and flavonoids as defense responses to the pathogenic infection. The metabolome profiling identified 586 metabolites of which 386 and 324 metabolites were differentially accumulated in NOHP vs NOWP and NOHS and NOWS, respectively. The differential accumulation of metabolites related to phytohormone signaling, linoleic acid metabolism, phenylpropanoid and flavonoid biosynthesis, nicotinate and nicotinamide metabolism, and citrate cycle was observed, indicating the role of these pathways in defense responses against the pathogenic infection.
CONCLUSION
CONCLUSIONS
Our results showed that Guangdong province has a high incidence of WBD in most of the surveyed areas. C. mamane is suspected to be the causing pathogen of WBD in N. indicum. N. indicum initiated the MAPK-signaling cascade and phytohormone signaling, leading to the activation of pathogen-associated molecular patterns and hypersensitive response. Furthermore, N. indicum accumulated high concentrations of phenolic acids, coumarins and lignans, and flavonoids under WBD. These results provide scientific tools for the formulation of control strategies of WBD in N. indicum.
Identifiants
pubmed: 35701735
doi: 10.1186/s12870-022-03672-z
pii: 10.1186/s12870-022-03672-z
pmc: PMC9199210
doi:
Substances chimiques
Flavonoids
0
Linoleic Acids
0
Plant Growth Regulators
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
291Informations de copyright
© 2022. The Author(s).
Références
PLoS One. 2015 Jul 01;10(7):e0130425
pubmed: 26132073
Nucleic Acids Res. 2002 Jan 1;30(1):276-80
pubmed: 11752314
BMC Bioinformatics. 2011 Aug 04;12:323
pubmed: 21816040
Brief Bioinform. 2019 Jul 19;20(4):1160-1166
pubmed: 28968734
Pharmacogn Rev. 2014 Jul;8(16):156-62
pubmed: 25125887
Plant Physiol. 2001 Jan;125(1):73-6
pubmed: 11154300
Genome Biol. 2004;5(2):R7
pubmed: 14759257
FEMS Microbiol Ecol. 2013 Apr;84(1):165-75
pubmed: 23176677
Curr Opin Plant Biol. 2003 Aug;6(4):365-71
pubmed: 12873532
Sci Rep. 2019 Nov 19;9(1):17030
pubmed: 31745110
Appl Environ Microbiol. 2000 Dec;66(12):5488-91
pubmed: 11097934
Micron. 2021 Sep;148:103108
pubmed: 34237476
Biochim Biophys Acta. 1972 Jul 13;276(1):85-93
pubmed: 5047712
Int J Mol Sci. 2018 Feb 27;19(3):
pubmed: 29495448
Curr Opin Plant Biol. 2004 Jun;7(3):254-61
pubmed: 15134745
J Biol Chem. 1956 Feb;218(2):753-68
pubmed: 13295228
Front Plant Sci. 2017 Apr 18;8:545
pubmed: 28458676
PLoS One. 2016 Jun 09;11(6):e0157022
pubmed: 27280887
BMC Bioinformatics. 2015 May 22;16:169
pubmed: 25994840
Front Plant Sci. 2018 May 22;9:655
pubmed: 29872444
Plant Dis. 1999 Mar;83(3):302
pubmed: 30845521
J Mol Biol. 1995 Jun 23;249(5):843-56
pubmed: 7540694
Mol Plant Pathol. 2010 Jan;11(1):83-92
pubmed: 20078778
Brief Bioinform. 2001 Mar;2(1):9-18
pubmed: 11465066
PLoS One. 2013 Nov 21;8(11):e80238
pubmed: 24278262
Nucleic Acids Res. 2011 Jul;39(Web Server issue):W316-22
pubmed: 21715386
Front Plant Sci. 2015 May 12;6:322
pubmed: 26029224
Gene. 2014 Aug 10;546(2):398-402
pubmed: 24853202
Mol Plant Microbe Interact. 2011 Aug;24(8):888-96
pubmed: 21751851
J Exp Bot. 2020 Jan 7;71(2):470-479
pubmed: 31644801
Front Plant Sci. 2015 Mar 17;6:122
pubmed: 25852698
Mol Biosyst. 2012 Apr;8(5):1507-19
pubmed: 22373587
Nat Methods. 2013 Oct;10(10):996-8
pubmed: 23955772
J Exp Bot. 2017 Jul 10;68(15):4013-4028
pubmed: 28922752
Plant J. 2000 Aug;23(4):481-8
pubmed: 10972874
Nat Genet. 2000 May;25(1):25-9
pubmed: 10802651
Dev Dyn. 2008 Nov;237(11):3102-14
pubmed: 18855897
Redox Biol. 2017 Apr;11:192-204
pubmed: 27984790
J Exp Bot. 2005 Mar;56(413):865-77
pubmed: 15642708
J Exp Bot. 2013 Sep;64(12):3855-67
pubmed: 23888068
Mol Plant. 2010 Sep;3(5):783-93
pubmed: 20713980
New Phytol. 2016 Dec;212(4):902-907
pubmed: 27488095
Front Plant Sci. 2018 Nov 27;9:1674
pubmed: 30538711
Mol Ecol. 1993 Apr;2(2):113-8
pubmed: 8180733
Insect Sci. 2015 Apr;22(2):157-64
pubmed: 24753304
Bioinformatics. 2010 Oct 1;26(19):2460-1
pubmed: 20709691
Plant J. 2013 Apr;74(2):267-79
pubmed: 23331961
Front Biosci. 2004 May 01;9:1577-86
pubmed: 14977569
BMC Plant Biol. 2019 Jan 15;19(1):26
pubmed: 30646861
Annu Rev Phytopathol. 2013;51:245-66
pubmed: 23663002
Bioinformatics. 2011 Nov 1;27(21):2957-63
pubmed: 21903629
Int J Syst Evol Microbiol. 2013 Feb;63(Pt 2):636-640
pubmed: 22544788
Plant Mol Biol. 2011 Nov;77(4-5):323-36
pubmed: 21818683
J Cell Biol. 2005 Jan 3;168(1):17-20
pubmed: 15631987
Trends Plant Sci. 2010 Aug;15(8):462-70
pubmed: 20554469
BMC Plant Biol. 2020 Jan 2;20(1):1
pubmed: 31898482
Plant J. 2003 Jan;33(2):221-33
pubmed: 12535337
Plant J. 2010 May 1;62(4):663-73
pubmed: 20202164
Nucleic Acids Res. 2004 Jan 1;32(Database issue):D115-9
pubmed: 14681372
Plant J. 2012 May;70(4):650-65
pubmed: 22268572
Hortic Res. 2022 Jan 5;9:
pubmed: 35043187
Plant Biol (Stuttg). 2005 Nov;7(6):581-91
pubmed: 16388461
Mol Genet Genomics. 2002 Apr;267(2):154-61
pubmed: 11976958
J Am Chem Soc. 2016 Mar 23;138(11):3639-42
pubmed: 26928142
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
BMC Plant Biol. 2014 Jun 15;14:166
pubmed: 24930014
Mol Plant Microbe Interact. 2007 May;20(5):589-96
pubmed: 17506336
Mol Biol Evol. 2020 May 1;37(5):1530-1534
pubmed: 32011700
Front Plant Sci. 2019 Oct 01;10:1183
pubmed: 31632422
Plant Dis. 2005 May;89(5):530
pubmed: 30795447
Plant Signal Behav. 2014;9(11):e973818
pubmed: 25482778
Plant Dis. 2007 Feb;91(2):227
pubmed: 30781014
Int J Mol Sci. 2018 Feb 23;19(2):
pubmed: 29473858
Plants (Basel). 2019 Sep 06;8(9):
pubmed: 31489878
Front Genet. 2020 Sep 11;11:788
pubmed: 33061930
PLoS One. 2012;7(3):e32491
pubmed: 22403664
Plant J. 2009 Jan;57(2):302-12
pubmed: 18798871
Sci Rep. 2017 Sep 7;7(1):10862
pubmed: 28883533
Nature. 2006 Nov 16;444(7117):323-9
pubmed: 17108957
Mol Plant. 2016 Dec 5;9(12):1667-1670
pubmed: 27717919
Plant Physiol. 2006 Nov;142(3):1329-39
pubmed: 17012408
BMC Genomics. 2020 Oct 22;21(1):734
pubmed: 33092530
Stud Mycol. 2013 Sep 30;76(1):51-167
pubmed: 24302790
Nat Genet. 2017 Apr;49(4):537-549
pubmed: 28191891
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Physiol Plant. 2018 Nov;164(3):337-348
pubmed: 29604096
Plant Physiol. 2015 Nov;169(3):1557-67
pubmed: 26048881
Mol Plant Pathol. 2002 Sep 1;3(5):371-90
pubmed: 20569344
Biochem J. 1989 Jan 15;257(2):529-34
pubmed: 2649077
Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W5-9
pubmed: 18440982
Sci Rep. 2017 Jul 25;7(1):6389
pubmed: 28743869
New Phytol. 2017 Aug;215(3):958-964
pubmed: 28574164
Int J Mol Sci. 2019 Dec 12;20(24):
pubmed: 31842411
Hortic Res. 2017 Dec 27;4:17080
pubmed: 29285398
Front Plant Sci. 2017 Jul 19;8:1257
pubmed: 28769960
Front Plant Sci. 2021 Jul 28;12:691838
pubmed: 34394145
Front Plant Sci. 2021 May 24;12:678959
pubmed: 34108985