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RNA sequencing analysis provides new insights into dynamic molecular responses to Valsa mali pathogenicity in apple ‘Changfu No. 2’

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Abstract

Valsa canker caused by the necrotrophic pathogen Valsa mali (Vm) severely affects apple production in Eastern Asia. The molecular basis underlying the apple response to Vm infection is poorly understood. Hence, we performed RNA sequencing (RNA-seq) to investigate the dynamic gene expression profiles of a major apple cultivar, ‘Changfu No.2’, during Vm infection. Compared with the control (C), 104, 313, and 1059 differentially expressed genes (DEGs) were detected from the phloem tissue within the range of 0.9–1.3 cm (T1), 0.5–0.9 cm (T2), and 0.1–0.5 cm (T3) beyond the lesion periphery, respectively. Gene ontology (GO) enrichment analysis revealed that the DEGs associated with plant growth and development were down-regulated, whereas those related to defense responses were up-regulated. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that hormonal and Ca2+ signaling and phenylpropanoid biosynthesis were involved in the defense responses. In conclusion, multiple defense responses associated with ABA, JA, ET, Ca2+, and cell wall signals contributed to the defense against Vm infection in ‘Changfu No.2’. In contrast, the DEGs with inhibited expression were involved in plant growth and development; auxin signaling and several resistance genes might weaken the resistance of ‘Changfu No.2’ to pathogens. Our results offer a new insight into plant responses against necrotrophs and could benefit programs aimed at breeding for Vm resistance.

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Abbreviations

AzA:

Azelaic acid

Ca2+ :

Calcium ion

CWDEs:

Cell wall degrading enzymes

DEGs:

Differentially expressed genes

ET:

Ethylene

ETI:

Effector-triggered immunity

G3P:

Glycerol-3-phosphate

IAA:

Auxin

JA:

Jasmonic acid

MeS:

Methyl salicylic acid

PAMP:

Pathogen-associated molecular pattern

PRR:

Pattern-recognition receptor

PTI:

PAMP-triggered immunity

RT-qPCR:

Real-time quantitative PCR

RNA-seq:

RNA sequencing

SA:

Salicylic acid

SAR:

Systemic acquired resistance

TF:

Transcription factor

Vm :

Valsa mali

References

  • Abe K, Kotoda N, Kato H, Soejima J (2007) Resistance sources to Valsa canker (Valsa ceratosperma) in a germplasm collection of diverse Malus species. Plant Breed 126:449–453

    Article  Google Scholar 

  • Bacete L, Mélida H, Miedes E, Molina A (2018) Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J 93:614–636

    Article  CAS  PubMed  Google Scholar 

  • Bellincampi D, Cervone F, Lionetti V (2014) Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Front Plant Sci 5:228

    Article  PubMed  PubMed Central  Google Scholar 

  • Berens ML, Berry HM, Mine A, Argueso CT, Tsuda K (2016) Evolution of hormone signaling networks in plant defense. Annu Rev Phytopathol 55:401–425

    Article  CAS  Google Scholar 

  • Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58:4019–4026

    Article  CAS  PubMed  Google Scholar 

  • Berrocal-Lobo M, Molina A (2008) Arabidopsis defense response against Fusarium oxysporum. Trends Plant Sci 13:145–150

    Article  CAS  PubMed  Google Scholar 

  • Cantu D, Vicente AR, Labavitch JM, Bennett AB, Powell AL (2008) Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends Plant Sci 13:610–617

    Article  CAS  PubMed  Google Scholar 

  • Cao K, Guo L, Li B, Sun G, Chen H (2009) Investigations on the occurrence and control of apple canker in China. Plant Prot 35:114–116 (In Chinese)

    Google Scholar 

  • Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao QM, Selote D, Hu YL, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43:421–427

    Article  CAS  PubMed  Google Scholar 

  • Chaturvedi R, Venables B, Petros RA, Nalam V, Li M, Wang X, Takemoto LJ, Shah J (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J 71:161–172

    Article  CAS  PubMed  Google Scholar 

  • Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, Geest H, Bianco L, Micheletti D, Velasco R, Pierro E, Gouzy J, Rees D, Guérif P, Muranty H, Durel CE, Laurens F, Lespinasse Y, Gaillard S, Aubourg S, Quesneville H, Weigel D, Weg E, Troggio M, Bucher E (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49:1099–1106

    Article  CAS  PubMed  Google Scholar 

  • Dörmann P, Kim H, Ott T, Schulze-Lefert P, Trujillo M, Wewer V, Hückelhoven R (2014) Cell-autonomous defense, re-organization and trafficking of membranes in plant-microbe interactions. New Phytol 204:815–822

    Article  CAS  PubMed  Google Scholar 

  • Fu Z, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863

    Article  CAS  PubMed  Google Scholar 

  • Gao Q, Zhu S, Kachroo P, Kachroo A (2015) Signal regulators of systemic acquired resistance. Front Plant Sci 6:228

    PubMed  PubMed Central  Google Scholar 

  • Genger RK, Jurkowski GI, McDowell JM, Lu H, Jung HW, Greenberg JT, Bent AF (2008) Signaling pathways that regulate the enhanced disease resistance of Arabidopsis “defense, no death” mutants. Mol Plant Microbe Interact 21:1285–1296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Harwood J (2012) Lipids in plants and microbes. Springer Science & Business Media, Berlin

    Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  PubMed  Google Scholar 

  • Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14:373–382

    Article  CAS  PubMed  Google Scholar 

  • Kepley JB, Jacobi WR (2000) Pathogenicity of Cytospora fungi on six hardwood species. J Arboric 26:326–332

    Google Scholar 

  • Kidd BN, Kadoo NY, Dombrecht B, Tekeoglu M, Gardiner DM, Thatcher LF, Aitken E, Schenk P, Manners J, Kazan K (2011) Auxin signaling and transport promote susceptibility to the root-infecting fungal pathogen Fusarium oxysporum in Arabidopsis. Mol Plant Microbe Interact 24:733–748

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative and the 2-ΔΔCt method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Llorente F, Alonso-Blanco C, Sánchez-Rodriguez C, Jorda L, Molina A (2005) ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43:165–180

    Article  CAS  PubMed  Google Scholar 

  • Llorente F, Muskett P, Sánchez-Vallet A, López G, Ramos B, Sánchez-Rodríguez C, Jordá L, Parker J, Molina A (2008) Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Mol Plant 1:496–509

    Article  CAS  PubMed  Google Scholar 

  • López-Berges MS, Rispail N, Prados-Rosales RC, Di Pietro A (2010) A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell 22:2459–2475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magnin-Robert M, Le BD, Markham J, Dorey S, Clément C, Baillieul F, Dhondt-Cordelier S (2015) Modifications of sphingolipid content affect tolerance to hemibiotrophic and necrotrophic pathogens by modulating plant defense responses in arabidopsis. Plant Physiol 169:2255–2274

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267–294

    Article  CAS  PubMed  Google Scholar 

  • Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–2565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moeder W, Urquhart W, Ung H, Yoshioka K (2011) The role of cyclic nucleotide-gated ion channels in plant immunity. Mol Plant 4:442–452

    Article  CAS  PubMed  Google Scholar 

  • Naseem M, Srivastava M, Tehseen M, Ahmed N (2015) Auxin crosstalk to plant immune networks: a plant-pathogen interaction perspective. Curr Protein Pept Sci 16:389–394

    Article  CAS  PubMed  Google Scholar 

  • Oliver RP, Ipcho SV (2004) Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol Plant Pathol 5:347–352

    Article  CAS  PubMed  Google Scholar 

  • Pré M, Atallah M, Champion A, De Vos M, Pieterse CM, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranty B, Aldon D, Cotelle V, Galaud JP, Thuleau P, Mazars C (2016) Calcium sensors as key hubs in plant responses to biotic and abiotic stresses. Front Plant Sci 7:327

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasabe M, Takeuchi K, Kamoun S, Ichinose Y, Govers F, Toyoda K, Shiraishi T, Yamada T (2000) Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. FEBS J 267:5005–5013

    CAS  Google Scholar 

  • Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263

    Article  CAS  PubMed  Google Scholar 

  • Suzaki K (2008) Population structure of Valsa ceratosperma, causal fungus of Valsa canker, in apple and pear orchards. J Gen Plant Pathol 74:128–132

    Article  CAS  Google Scholar 

  • Tarazona S, García F, Ferrer A, Dopazo J, Conesa A (2012) Noiseq: a rna-seq differential expression method robust for sequencing depth biases. University of Southampton 17:18

    Google Scholar 

  • Tsegaye Y, Richardson CG, Bravo JE, Mulcahy BJ, Lynch DV, Markham JE, Jaworski JG, Chen M, Cahoon EB, Dunn TM (2007) Arabidopsis mutants lacking long chain base phosphate lyase are fumonisin-sensitive and accumulate trihydroxy-18:1 long chain base phosphate. J Biol Chem 282:28195–28206

    Article  CAS  PubMed  Google Scholar 

  • Tsuda K, Katagiri F, Parker J E, Ellis J G (2010) Comparing signaling mechanisms engaged in patterntriggered and effector-triggered immunity. Curr Opin Plant Biol 13:459-465

    Article  CAS  PubMed  Google Scholar 

  • Vlot AC, Klessig DF, Park SW (2008) Systemic acquired resistance: the elusive signal (s). Curr Opin Plant Biol 11:436–442

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Hu T, Wang Y, Luo Y, Michailides TJ, Cao K (2016) New understanding on infection processes of Valsa canker of apple in China. Eur J Plant Pathol 146:531–540

    Article  Google Scholar 

  • Wei J, Huang L, Gao Z, Ke X, Kang Z (2010) Laboratory evaluation methods of apple Valsa canker disease caused by Valsa ceratosperma sensu Kobayashi. Acta Phytopathologica Sinica 40:14–20 (In Chinese)

    Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Z, Ke X, Kang Z, Huang L (2016) Apple resistance responses against Valsa mali revealed by transcriptomics analyses. Physiol Mol Plant Pathol 93:85–92

    Article  CAS  Google Scholar 

  • Zhai L, Zhang M, Lv G, Chen X, Jia N, Hong N, Wang G (2014) Biological and molecular characterization of four Botryosphaeria species isolated from pear plants showing stem wart and stem canker in China. Plant Dis 98:716–726

    Article  Google Scholar 

  • Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605

    Article  CAS  PubMed  Google Scholar 

  • Zuo C, Zhang W, Mao J, Jiang X, Ma Z, Su J, Chen B (2017a) Genome wide identification and expression analysis of LysM receptor like kinase in apple. Acta Horticulturae Sinica 44:733–742 (In Chinese)

    Google Scholar 

  • Zuo C, Zhang W, Chen Z, Chen B, Huang Y (2017b) RNA sequencing reveals that endoplasmic reticulum stress and disruption of membrane integrity underlie dimethyl Trisulfide toxicity against Fusarium oxysporum f. sp. cubense tropical race 4. Front Microbiol 8:1365

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank Ph.D Lijun Bai (GeneBang Inc., Chengdu, China, www.genebang.com) for technical assistance with RNA sequencing and bioinformatic analysis.

Funding

This work was supported by the Talent introduction Project of Gansu Agricultural University (GSAU-RCZX201712) and the Natural Science Foundation of China No. 31501728.

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Authors and Affiliations

  1. College of Horticulture, Gansu Agricultural University, Lanzhou, 730070, China

    Cunwu Zuo, Juan Mao, Mingyu Chu, Hu Duo & Baihong Chen

  2. Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou, China

    Zhongjian Chen

Authors
  1. Cunwu Zuo
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  2. Juan Mao
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  3. Zhongjian Chen
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  4. Mingyu Chu
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  5. Hu Duo
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  6. Baihong Chen
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Contributions

ZC and CB conceived, designed, and coordinated the study. ZC, MJ, CM, and DH performed the experiments and collected, analyzed, and deposited the data. CZ proofread the final draft and revised the manuscript. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Baihong Chen.

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Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Data Archiving Statement

The raw data has been deposited in the National Center for Biotechnology information (NCBI) Short Read Archive (SPA) under accession number SRP160545.

Additional information

Communicated by M. Troggio

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Zuo, C., Mao, J., Chen, Z. et al. RNA sequencing analysis provides new insights into dynamic molecular responses to Valsa mali pathogenicity in apple ‘Changfu No. 2’. Tree Genetics & Genomes 14, 75 (2018). https://doi.org/10.1007/s11295-018-1288-3

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