A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani

Verwaaijen B, Wibberg D, Winkler A, Zrenner R, Bednarz H, Niehaus K, Grosch R, Pühler A, Schlüter A (2019)
Scientific Reports 9(1): 7221.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA 3.69 MB
Abstract / Bemerkung
The leafy green vegetable Lactuca sativa, L. is susceptible to the soil-born fungus Rhizoctonia solani AG1-IB. In a previous study, we reported on the transcriptional response of R. solani AG1-IB (isolate 7/3/14) during the interspecies interaction with L. sativa cv. Tizian by means of RNA sequencing. Here we present the L. sativa transcriptome and metabolome from the same experimental approach. Three distinct interaction zones were sampled and compared to a blank (non-inoculated) sample: symptomless zone 1, zone 2 showing light brown discoloration, and a dark brown zone 3 characterized by necrotic lesions. Throughout the interaction, we observed a massive reprogramming of the L. sativa transcriptome, with 9231 unique genes matching the threshold criteria for differential expression. The lettuce transcriptome of the light brown zone 2 presents the most dissimilar profile compared to the uninoculated zone 4, marking the main stage of interaction. Transcripts putatively encoding several essential proteins that are involved in maintaining jasmonic acid and auxin homeostasis were found to be negatively regulated. These and other indicator transcripts mark a potentially inadequate defence response, leading to a compatible interaction. KEGG pathway mapping and GC-MS metabolome data revealed large changes in amino acid, lignin and hemicellulose related pathways and related metabolites.
Erscheinungsjahr
2019
Zeitschriftentitel
Scientific Reports
Band
9
Ausgabe
1
Art.-Nr.
7221
ISSN
2045-2322
eISSN
2045-2322
Page URI
https://pub.uni-bielefeld.de/record/2935556

Zitieren

Verwaaijen B, Wibberg D, Winkler A, et al. A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani. Scientific Reports. 2019;9(1): 7221.
Verwaaijen, B., Wibberg, D., Winkler, A., Zrenner, R., Bednarz, H., Niehaus, K., Grosch, R., et al. (2019). A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani. Scientific Reports, 9(1), 7221. doi:10.1038/s41598-019-43706-5
Verwaaijen, Bart, Wibberg, Daniel, Winkler, Anika, Zrenner, Rita, Bednarz, Hanna, Niehaus, Karsten, Grosch, Rita, Pühler, Alfred, and Schlüter, Andreas. 2019. “A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani”. Scientific Reports 9 (1): 7221.
Verwaaijen, B., Wibberg, D., Winkler, A., Zrenner, R., Bednarz, H., Niehaus, K., Grosch, R., Pühler, A., and Schlüter, A. (2019). A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani. Scientific Reports 9:7221.
Verwaaijen, B., et al., 2019. A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani. Scientific Reports, 9(1): 7221.
B. Verwaaijen, et al., “A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani”, Scientific Reports, vol. 9, 2019, : 7221.
Verwaaijen, B., Wibberg, D., Winkler, A., Zrenner, R., Bednarz, H., Niehaus, K., Grosch, R., Pühler, A., Schlüter, A.: A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani. Scientific Reports. 9, : 7221 (2019).
Verwaaijen, Bart, Wibberg, Daniel, Winkler, Anika, Zrenner, Rita, Bednarz, Hanna, Niehaus, Karsten, Grosch, Rita, Pühler, Alfred, and Schlüter, Andreas. “A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani”. Scientific Reports 9.1 (2019): 7221.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Creative Commons Namensnennung 4.0 International Public License (CC-BY 4.0):
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2019-05-13T12:46:23Z
MD5 Prüfsumme
a776d693c1b82f3865d2b1b5843f240f


Link(s) zu Volltext(en)
Access Level
OA Open Access

72 References

Daten bereitgestellt von Europe PubMed Central.

Necrotroph attacks on plants: wanton destruction or covert extortion?
Laluk K, Mengiste T., Arabidopsis Book 8(), 2010
PMID: 22303261
When and how to kill a plant cell: infection strategies of plant pathogenic fungi.
Horbach R, Navarro-Quesada AR, Knogge W, Deising HB., J. Plant Physiol. 168(1), 2010
PMID: 20674079
Plant immunity to necrotrophs.
Mengiste T., Annu Rev Phytopathol 50(), 2012
PMID: 22726121
Introduction — The Genus Rhizoctonia
Ogoshi Akira., 1996
The role of effectors and host immunity in plant-necrotrophic fungal interactions.
Wang X, Jiang N, Liu J, Liu W, Wang GL., Virulence 5(7), 2014
PMID: 25513773
Of PAMPs and effectors: the blurred PTI-ETI dichotomy.
Thomma BP, Nurnberger T, Joosten MH., Plant Cell 23(1), 2011
PMID: 21278123

AUTHOR UNKNOWN, 0
Transcriptome analysis of the phytopathogenic fungus Rhizoctonia solani AG1-IB 7/3/14 applying high-throughput sequencing of expressed sequence tags (ESTs).
Wibberg D, Jelonek L, Rupp O, Krober M, Goesmann A, Grosch R, Puhler A, Schluter A., Fungal Biol 118(9-10), 2014
PMID: 25209639
Improved genome sequence of the phytopathogenic fungus Rhizoctonia solani AG1-IB 7/3/14 as established by deep mate-pair sequencing on the MiSeq (Illumina) system.
Wibberg D, Rupp O, Jelonek L, Krober M, Verwaaijen B, Blom J, Winkler A, Goesmann A, Grosch R, Puhler A, Schluter A., J. Biotechnol. 203(), 2015
PMID: 25801332
Establishment and interpretation of the genome sequence of the phytopathogenic fungus Rhizoctonia solani AG1-IB isolate 7/3/14.
Wibberg D, Jelonek L, Rupp O, Hennig M, Eikmeyer F, Goesmann A, Hartmann A, Borriss R, Grosch R, Puhler A, Schluter A., J. Biotechnol. 167(2), 2012
PMID: 23280342
Development of a Rhizoctonia solani AG1-IB Specific Gene Model Enables Comparative Genome Analyses between Phytopathogenic R. solani AG1-IA, AG1-IB, AG3 and AG8 Isolates.
Wibberg D, Rupp O, Blom J, Jelonek L, Krober M, Verwaaijen B, Goesmann A, Albaum S, Grosch R, Puhler A, Schluter A., PLoS ONE 10(12), 2015
PMID: 26690577
Assembly of the Lactuca sativa, L. cv. Tizian draft genome sequence reveals differences within major resistance complex 1 as compared to the cv. Salinas reference genome.
Verwaaijen B, Wibberg D, Nelkner J, Gordin M, Rupp O, Winkler A, Bremges A, Blom J, Grosch R, Puhler A, Schluter A., J. Biotechnol. 267(), 2017
PMID: 29278726
Genome-Wide Architecture of Disease Resistance Genes in Lettuce.
Christopoulou M, Wo SR, Kozik A, McHale LK, Truco MJ, Wroblewski T, Michelmore RW., G3 (Bethesda) 5(12), 2015
PMID: 26449254
The genomic architecture of disease resistance in lettuce.
McHale LK, Truco MJ, Kozik A, Wroblewski T, Ochoa OE, Lahre KA, Knapp SJ, Michelmore RW., Theor. Appl. Genet. 118(3), 2008
PMID: 19005638
An Ultra-High-Density, Transcript-Based, Genetic Map of Lettuce.
Truco MJ, Ashrafi H, Kozik A, van Leeuwen H, Bowers J, Wo SR, Stoffel K, Xu H, Hill T, Van Deynze A, Michelmore RW., G3 (Bethesda) 3(4), 2013
PMID: 23550116
Resistance to Downy Mildew in Lettuce 'La Brillante' is Conferred by Dm50 Gene and Multiple QTL.
Simko I, Ochoa OE, Pel MA, Tsuchida C, Font I Forcada C, Hayes RJ, Truco MJ, Antonise R, Galeano CH, Michelmore RW., Phytopathology 105(9), 2015
PMID: 25915441

AUTHOR UNKNOWN, 0
The major resistance gene cluster in lettuce is highly duplicated and spans several megabases.
Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW., Plant Cell 10(11), 1998
PMID: 9811791

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL., Genome Biol. 14(4), 2013
PMID: 23618408
ReadXplorer--visualization and analysis of mapped sequences.
Hilker R, Stadermann KB, Doppmeier D, Kalinowski J, Stoye J, Straube J, Winnebald J, Goesmann A., Bioinformatics 30(16), 2014
PMID: 24790157
ReadXplorer 2-detailed read mapping analysis and visualization from one single source.
Hilker R, Stadermann KB, Schwengers O, Anisiforov E, Jaenicke S, Weisshaar B, Zimmermann T, Goesmann A., Bioinformatics 32(24), 2016
PMID: 27540267
An introduction to Docker for reproducible research
Boettiger C., 2015

AUTHOR UNKNOWN, 0
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Author (s): Yoav Benjamini and Yosef Hochberg Source: Journal of the Royal Statistical Society. Series B (Methodological), Vol. 57, No. 1 (1995). Publi
Benjamini Y, Hochberg Y., 2016
UpSet: Visualization of Intersecting Sets.
Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H., IEEE Trans Vis Comput Graph 20(12), 2014
PMID: 26356912
GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists.
Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z., BMC Bioinformatics 10(), 2009
PMID: 19192299
Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data.
Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R, Tohge T, Fernie AR, Stitt M, Usadel B., Plant Cell Environ. 37(5), 2013
PMID: 24237261
A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize.
Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M., Plant Cell Environ. 32(9), 2009
PMID: 19389052
KEGG: kyoto encyclopedia of genes and genomes.
Kanehisa M, Goto S., Nucleic Acids Res. 28(1), 2000
PMID: 10592173
KEGG: new perspectives on genomes, pathways, diseases and drugs.
Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K., Nucleic Acids Res. 45(D1), 2016
PMID: 27899662
New approach for understanding genome variations in KEGG.
Kanehisa M, Sato Y, Furumichi M, Morishima K, Tanabe M., Nucleic Acids Res. 47(D1), 2019
PMID: 30321428
KAAS: an automatic genome annotation and pathway reconstruction server.
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M., Nucleic Acids Res. 35(Web Server issue), 2007
PMID: 17526522
Proposed minimum reporting standards for chemical analysis Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI).
Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TW, Fiehn O, Goodacre R, Griffin JL, Hankemeier T, Hardy N, Harnly J, Higashi R, Kopka J, Lane AN, Lindon JC, Marriott P, Nicholls AW, Reily MD, Thaden JJ, Viant MR., Metabolomics 3(3), 2007
PMID: 24039616
Basic local alignment search tool.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ., J. Mol. Biol. 215(3), 1990
PMID: 2231712
WRKY transcription factors.
Rushton PJ, Somssich IE, Ringler P, Shen QJ., Trends Plant Sci. 15(5), 2010
PMID: 20304701
Evaluation of inhibitory effects of citric and tartaric acids and their combination on the growth of Trichophyton mentagrophytes, Aspergillus fumigatus, Candida albicans, and Malassezia furfur
Shokri H., 2011
In situ immune response and mechanisms of cell damage in central nervous system of fatal cases microcephaly by Zika virus.
Azevedo RSS, de Sousa JR, Araujo MTF, Martins Filho AJ, de Alcantara BN, Araujo FMC, Queiroz MGL, Cruz ACR, Vasconcelos BHB, Chiang JO, Martins LC, Casseb LMN, da Silva EV, Carvalho VL, Vasconcelos BCB, Rodrigues SG, Oliveira CS, Quaresma JAS, Vasconcelos PFC., Sci Rep 8(1), 2018
PMID: 29311619
Salicylic Acid biosynthesis and metabolism.
Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF., Arabidopsis Book 9(), 2011
PMID: 22303280
Abscisic acid biosynthesis and catabolism.
Nambara E, Marion-Poll A., Annu Rev Plant Biol 56(), 2005
PMID: 15862093
Chloroplasts at work during plant innate immunity.
Serrano I, Audran C, Rivas S., J. Exp. Bot. 67(13), 2016
PMID: 26994477
Molecular crosstalk between PAMP-triggered immunity and photosynthesis.
Gohre V, Jones AM, Sklenar J, Robatzek S, Weber AP., Mol. Plant Microbe Interact. 25(8), 2012
PMID: 22550958
Nitric Oxide Ameliorates Zinc Oxide Nanoparticles Phytotoxicity in Wheat Seedlings: Implication of the Ascorbate-Glutathione Cycle.
Tripathi DK, Mishra RK, Singh S, Singh S, Vishwakarma K, Sharma S, Singh VP, Singh PK, Prasad SM, Dubey NK, Pandey AC, Sahi S, Chauhan DK., Front Plant Sci 8(), 2017
PMID: 28220127
CDPKs in immune and stress signaling.
Boudsocq M, Sheen J., Trends Plant Sci. 18(1), 2012
PMID: 22974587
Calcium signaling during reproduction and biotrophic fungal interactions in plants.
Chen J, Gutjahr C, Bleckmann A, Dresselhaus T., Mol Plant 8(4), 2015
PMID: 25660409
Evolution of the rice Xa21 disease resistance gene family.
Song WY, Pi LY, Wang GL, Gardner J, Holsten T, Ronald PC., Plant Cell 9(8), 1997
PMID: 9286106
TMV resistance gene N homologues are linked to Synchytrium endobioticum resistance in potato.
Hehl R, Faurie E, Hesselbach J, Salamini F, Whitham S, Baker B, Gebbardt C., Theor. Appl. Genet. 98(3/4), 1999
PMID: IND22010049

AUTHOR UNKNOWN, 0
A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides.
Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G., Proc. Natl. Acad. Sci. U.S.A. 107(20), 2010
PMID: 20439716
Plant immunity: towards an integrated view of plant-pathogen interactions.
Dodds PN, Rathjen JP., Nat. Rev. Genet. 11(8), 2010
PMID: 20585331
Salicylic acid-dependent immunity contributes to resistance against Rhizoctonia solani, a necrotrophic fungal agent of sheath blight, in rice and Brachypodium distachyon.
Kouzai Y, Kimura M, Watanabe M, Kusunoki K, Osaka D, Suzuki T, Matsui H, Yamamoto M, Ichinose Y, Toyoda K, Matsuura T, Mori IC, Hirayama T, Minami E, Nishizawa Y, Inoue K, Onda Y, Mochida K, Noutoshi Y., New Phytol. 217(2), 2017
PMID: 29048113
Systemic induction of salicylic acid‐related plant defences in potato in response to Rhizoctonia solani AG3PT
Genzel F, P. Franken , K. Witzel , R. Grosch ., Plant Pathol. 67(2), 2018
PMID: IND605885834
Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum.
Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks AA, Shah J., Mol. Plant Microbe Interact. 23(7), 2010
PMID: 20521949
Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses.
Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P., Science 315(5815), 2006
PMID: 17185563
A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions.
Tao Z, Liu H, Qiu D, Zhou Y, Li X, Xu C, Wang S., Plant Physiol. 151(2), 2009
PMID: 19700558
Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato.
Sinha AK, Hofmann MG, Romer U, Kockenberger W, Elling L, Roitsch T., Plant Physiol. 128(4), 2002
PMID: 11950996

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0
Ascorbic Acid Deficiency Activates Cell Death and Disease Resistance Responses in Arabidopsis 1
Pavet V., 2005
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 31076623
PubMed | Europe PMC

Suchen in

Google Scholar