Dynamic transcriptomes of resistant and susceptible peach lines after infestation by green peach aphids ( Myzus persicae  Sülzer) reveal defence responses controlled by the  Rm3  locus

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Abstract

Background

The green peach aphid (GPA), Myzus persicae (Sülzer), is a widespread phloem-feeding insect that significantly influences the yield and visual quality of peach [ Prunus persica (L.) Batsch]. Single dominant gene ( Rm3)-based resistance provides effective management of this invasive pest, although little is known about the molecular responses of plants to GPA feeding.

Results

To illustrate the molecular mechanisms of monogenic resistance in peach to young tissue-infecting GPAs, aphid-resistant/aphid-susceptible peach lines from a segregating population with Rm3/rm3 and rm3/rm3 genotypes were infested with GPAs for 3 to 72 h. Transcriptome analysis of the infested tissues identified 3854 differentially expressed genes (DEGs). Although the majority of the DEGs in the resistant line also responded to aphid attack in the susceptible line, the overall magnitude of change was greater in the resistant line than in the susceptible line. The enriched gene ontology of the 3854 DEGs involved in plant defence responses included redox situation, calcium-mediated signalling, transcription factor (e.g., WRKY, MYB, and ERF), MAPK signalling cascade, phytohormone signalling, pathogenesis-related protein, and secondary metabolite terms. Of the 53 genes annotated in a 460 kb interval of the rm3 locus, seven genes were differentially expressed between the aphid-resistant and aphid-susceptible peach lines following aphid infestation.

Conclusions

Together, these results suggest that the Rm3-dependent resistance relies mainly on the inducible expression of defence-related pathways and signalling elements within hours after the initiation of aphid feeding and that the production of specific secondary metabolites from phenylpropanoid/flavonoid pathways can have major effects on peach-aphid interactions.

Electronic supplementary material

The online version of this article (10.1186/s12864-018-5215-7) contains supplementary material, which is available to authorized users.

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Most cited references 40

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Mechanisms of plant defense against insect herbivores.

Abdul Rashid War, Michael Paulraj, Tariq Ahmad … (2014)

Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production.

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MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.

Oliver Thimm, Oliver Bläsing, Yves Gibon … (2004)

MAPMAN is a user-driven tool that displays large data sets onto diagrams of metabolic pathways or other processes. SCAVENGER modules assign the measured parameters to hierarchical categories (formed 'BINs', 'subBINs'). A first build of TRANSCRIPTSCAVENGER groups genes on the Arabidopsis Affymetrix 22K array into >200 hierarchical categories, providing a breakdown of central metabolism (for several pathways, down to the single enzyme level), and an overview of secondary metabolism and cellular processes. METABOLITESCAVENGER groups hundreds of metabolites into pathways or groups of structurally related compounds. An IMAGEANNOTATOR module uses these groupings to organise and display experimental data sets onto diagrams of the users' choice. A modular structure allows users to edit existing categories, add new categories and develop SCAVENGER modules for other sorts of data. MAPMAN is used to analyse two sets of 22K Affymetrix arrays that investigate the response of Arabidopsis rosettes to low sugar: one investigates the response to a 6-h extension of the night, and the other compares wild-type Columbia-0 (Col-0) and the starchless pgm mutant (plastid phosphoglucomutase) at the end of the night. There were qualitatively similar responses in both treatments. Many genes involved in photosynthesis, nutrient acquisition, amino acid, nucleotide, lipid and cell wall synthesis, cell wall modification, and RNA and protein synthesis were repressed. Many genes assigned to amino acid, nucleotide, lipid and cell wall breakdown were induced. Changed expression of genes for trehalose metabolism point to a role for trehalose-6-phosphate (Tre6P) as a starvation signal. Widespread changes in the expression of genes encoding receptor kinases, transcription factors, components of signalling pathways, proteins involved in post-translational modification and turnover, and proteins involved in the synthesis and sensing of cytokinins, abscisic acid (ABA) and ethylene revealing large-scale rewiring of the regulatory network is an early response to sugar depletion.

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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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Author and article information

Contributors

Liang Niu: niuliang@caas.cn

Lei Pan: panlei@caas.cn

Wenfang Zeng: zengwenfang@caas.cn

Zhenhua Lu: luzhenhua@caas.cn

Guochao Cui: cuiguochao@caas.cn

Meili Fan: 1670271313@qq.com

Qiang Xu: xuqiang@mail.hzau.edu.cn

Zhiqiang Wang: wangzhiqiang@caas.cn

Guohuai Li: liguohuai@mail.hzau.edu.cn

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): 28 November 2018

Publication date PMC-release: 28 November 2018

Publication date Collection: 2018

Volume: 19

Electronic Location Identifier: 846

Affiliations

[1 ]ISNI 0000 0004 1790 4137, GRID grid.35155.37, Key Laboratory of Horticultural Plant Biology, Ministry of Education, , Huazhong Agricultural University, ; Wuhan, 430070 China

[2 ]ISNI 0000 0001 0526 1937, GRID grid.410727.7, Key Laboratory of Fruit Breeding Technology of Ministry of Agriculture, Zhengzhou Fruit Research Institute, , Chinese Academy of Agricultural Sciences, ; Zhengzhou, 450009 China

Article

Publisher ID: 5215

DOI: 10.1186/s12864-018-5215-7

PMC ID: 6264056

PubMed ID: 30486776

SO-VID: 6732e37a-8831-4989-8a44-9d0f494f8b08

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 : 3 May 2018

Date accepted : 31 October 2018

Funding

Funded by: the Agricultural Science and Technology Innovation Program

Award ID: CAAS-ASTIP-2018-ZFRI

Award Recipient : Zhiqiang Wang

Funded by: the National Natural Science Foundation of China

Award ID: 31701880

Award Recipient : Lei Pan

Funded by: the Central Public-interest Scientific Institution Basal Research Fund

Award ID: 1610192017703

Award Recipient : Lei Pan

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: rm3 locus,peach,myzus persicae (sülzer),innate immunity,transcriptome analysis,aphid resistance

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ScienceOpen disciplines: Genetics

Keywords: rm3 locus, peach, myzus persicae (sülzer), innate immunity, transcriptome analysis, aphid resistance

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Dynamic transcriptomes of resistant and susceptible peach lines after infestation by green peach aphids ( Myzus persicae Sülzer) reveal defence responses controlled by the Rm3 locus

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Abstract

Background

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Electronic supplementary material

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Genes & Diseases

Most cited references 40

Mechanisms of plant defense against insect herbivores.

MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.

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

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Cited by 14

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