Transcriptome dynamics associated with resistance and susceptibility against fusarium head blight in four wheat genotypes

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Abstract

Background

Fusarium head blight (FHB) of wheat in North America is caused mostly by the fungal pathogen Fusarium graminearum ( Fg). Upon exposure to Fg, wheat initiates a series of cellular responses involving massive transcriptional reprogramming. In this study, we analyzed transcriptomics data of four wheat genotypes (Nyubai, Wuhan 1, HC374, and Shaw), at 2 and 4 days post inoculation (dpi) with Fg, using RNA-seq technology.

Results

A total of 37,772 differentially expressed genes (DEGs) were identified, 28,961 from wheat and 8811 from the pathogen. The susceptible genotype Shaw exhibited the highest number of host and pathogen DEGs, including 2270 DEGs associating with FHB susceptibility. Protein serine/threonine kinases and LRR-RK were associated with susceptibility at 2 dpi, while several ethylene-responsive, WRKY, Myb, bZIP and NAC-domain containing transcription factors were associated with susceptibility at 4 dpi. In the three resistant genotypes, 220 DEGs were associated with resistance. Glutathione S-transferase ( GST), membrane proteins and distinct LRR-RKs were associated with FHB resistance across the three genotypes. Genes with unique, high up-regulation by Fg in Wuhan 1 were mostly transiently expressed at 2 dpi, while many defense-associated genes were up-regulated at both 2 and 4 dpi in Nyubai; the majority of unique genes up-regulated in HC374 were detected at 4 dpi only. In the pathogen, most genes showed increased expression between 2 and 4 dpi in all genotypes, with stronger levels in the susceptible host; however two pectate lyases and a hydrolase were expressed higher at 2 dpi, and acetyltransferase activity was highly enriched at 4 dpi.

Conclusions

There was an early up-regulation of LRR-RKs, different between susceptible and resistant genotypes; subsequently, distinct sets of genes associated with defense response were up-regulated. Differences in expression profiles among the resistant genotypes indicate genotype-specific defense mechanisms. This study also shows a greater resemblance in transcriptomics of HC374 to Nyubai, consistent with their sharing of two FHB resistance QTLs on 3BS and 5AS, compared to Wuhan 1 which carries one QTL on 2DL in common with HC374.

Electronic supplementary material

The online version of this article (10.1186/s12864-018-5012-3) contains supplementary material, which is available to authorized users.

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Most cited references 83

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Programmed cell death in the plant immune system.

N S Coll, P Epple, J L Dangl (2011)

Cell death has a central role in innate immune responses in both plants and animals. Besides sharing striking convergences and similarities in the overall evolutionary organization of their innate immune systems, both plants and animals can respond to infection and pathogen recognition with programmed cell death. The fact that plant and animal pathogens have evolved strategies to subvert specific cell death modalities emphasizes the essential role of cell death during immune responses. The hypersensitive response (HR) cell death in plants displays morphological features, molecular architectures and mechanisms reminiscent of different inflammatory cell death types in animals (pyroptosis and necroptosis). In this review, we describe the molecular pathways leading to cell death during innate immune responses. Additionally, we present recently discovered caspase and caspase-like networks regulating cell death that have revealed fascinating analogies between cell death control across both kingdoms.

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Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens.

Zuyu Zheng, Synan Abu Qamar, Zhixiang Chen … (2006)

Plant WRKY transcription factors are key regulatory components of plant responses to microbial infection. In addition to regulating the expression of defense-related genes, WRKY transcription factors have also been shown to regulate cross-talk between jasmonate- and salicylate-regulated disease response pathways. The two pathways mediate resistance against different types of microbial pathogens, and there are numerous reports of antagonistic interactions between them. Here we show that mutations of the Arabidopsis WRKY33 gene encoding a WRKY transcription factor cause enhanced susceptibility to the necrotrophic fungal pathogens Botrytis cinerea and Alternaria brassicicola concomitant with reduced expression of the jasmonate-regulated plant defensin PDF1.2 gene. Ectopic over-expression of WRKY33, on the other hand, increases resistance to the two necrotrophic fungal pathogens. The wrky33 mutants do not show altered responses to a virulent strain of the bacterial pathogen Pseudomonas syringae, although the ectopic expression of WRKY33 results in enhanced susceptibility to this pathogen. The susceptibility of WRKY33-over-expressing plants to P. syringae is associated with reduced expression of the salicylate-regulated PR-1 gene. The WRKY33 transcript is induced in response to pathogen infection, or treatment with salicylate or the paraquat herbicide that generates activated oxygen species in exposed cells. WRKY33 is localized to the nucleus of plant cells and recognizes DNA molecules containing the TTGACC W-box sequence. Together, these results indicate that pathogen-induced WRKY33 is an important transcription factor that regulates the antagonistic relationship between defense pathways mediating responses to P. syringae and necrotrophic pathogens.

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Primary metabolism and plant defense--fuel for the fire.

Melvin D Bolton (2009)

Plants have the ability to recognize and respond to a multitude of microorganisms. Recognition of pathogens results in a massive reprogramming of the plant cell to activate and deploy defense responses to halt pathogen growth. Such responses are associated with increased demands for energy, reducing equivalents, and carbon skeletons that are provided by primary metabolic pathways. Although pathogen recognition and downstream resistance responses have been the focus of major study, an intriguing and comparatively understudied phenomenon is how plants are able to recruit energy for the defense response. To that end, this review will summarize current research on energy-producing primary metabolism pathways and their role in fueling the resistance response.

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Author and article information

Contributors

Youlian Pan:

ORCID: http://orcid.org/0000-0002-0158-0081

youlian.pan@nrc-cnrc.gc.ca

Ziying Liu: ziying.liu@nrc-cnrc.gc.ca

Hélène Rocheleau: helene.rocheleau@agr.gc.ca

François Fauteux: francois.fauteux@nrc-cnrc.gc.ca

Yunli Wang: yunli.wang@nrc-cnrc.gc.ca

Curt McCartney: curt.mccartney@agr.gc.ca

Thérèse Ouellet: therese.ouellet@agr.gc.ca

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 29 August 2018

Publication date PMC-release: 29 August 2018

Publication date Collection: 2018

Volume: 19

Electronic Location Identifier: 642

Affiliations

[1 ]ISNI 0000 0004 0449 7958, GRID grid.24433.32, Digital Technologies Research Centre, NRC, ; 1200 Montreal Road, Ottawa, ON K1A 0R6 Canada

[2 ]ISNI 0000 0001 1302 4958, GRID grid.55614.33, Ottawa Research and Development Centre, AAFC, ; 960 Carling Ave, Ottawa, ON K1A 0C6 Canada

[3 ]Morden Research and Development Centre, AAFC, 101 Route 100, Morden, MB R6M 1Y5 Canada

Author information

Youlian Pan http://orcid.org/0000-0002-0158-0081

Article

Publisher ID: 5012

DOI: 10.1186/s12864-018-5012-3

PMC ID: 6116500

PubMed ID: 30157778

SO-VID: 97cfec9b-0dd0-4a0a-8730-171d3a4e672b

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 19 April 2018

Date accepted : 14 August 2018

Funding

Funded by: Canadian Agriculture and Agri-Food Growing Forward 2 program

Award ID: project J-000412

Award Recipient : Thérèse Ouellet

Funded by: Genomics Research and Development Initiative

Award ID: projects J-000008 and J-001580

Award Recipient : Thérèse Ouellet

Funded by: Western Grains Research Foundation and Agriculture and Agri-Food Canada

Award ID: National Wheat Improvement Program

Award Recipient : Curt McCartney

Funded by: FundRef http://dx.doi.org/10.13039/501100000046, National Research Council Canada;

Award ID: “Canadian Wheat Improvement” project A1-011652

Award Recipient : Youlian Pan

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: fusarium head blight,differentially expressed genes,rna-seq,triticum aestivum,fusarium graminearum,pathogenesis,plant defense

Data availability:

ScienceOpen disciplines: Genetics

Keywords: fusarium head blight, differentially expressed genes, rna-seq, triticum aestivum, fusarium graminearum, pathogenesis, plant defense

Transcriptome dynamics associated with resistance and susceptibility against fusarium head blight in four wheat genotypes

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Abstract

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Decoding Infection and Transmission

Most cited references 83

Programmed cell death in the plant immune system.

Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens.

Primary metabolism and plant defense--fuel for the fire.

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