Advertisement

Plant Cell Reports

, Volume 38, Issue 2, pp 173–182 | Cite as

The oomycete microbe-associated molecular pattern Pep-13 triggers SERK3/BAK1-independent plant immunity

  • Haixia Wang
  • Huan He
  • Yetong Qi
  • Hazel McLellan
  • Zhejuan Tian
  • Paul R. J. Birch
  • Zhendong TianEmail author
Original Article

Abstract

Key message

Oomycetes MAMP Pep-13 can trigger SERK3/BAK1-independent PTI. Silencing of SERK3/BAK1 in solanaceous plants resulted in reduced expression of brassinosteroid marker genes and enhanced PTI transcriptional responses to Pep-13 treatment.

Abstract

To prevent disease, pattern recognition receptors (PRRs) are responsible for detecting microbe-associated molecular patterns (MAMPs) to switch on plant innate immunity. SOMATIC EMBROYOGENESIS KINASE 3 (SERK3)/BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) is a well-characterized receptor-like kinase (RLK) that serves as a pivotal co-receptor with PRRs to activate immunity following recognition of MAMPs including flg22, EF-Tu, INF1 and XEG1. However, the requirement for SERK3/BAK1 in many pattern-triggered immune (PTI) signaling pathways is not yet known. Pep-13 is an oomycete MAMP that consists of a highly conserved motif (an oligopeptide of 13 amino acids) shared in Phytophthora transglutaminases. Quantitative RT-PCR analysis reveals that the transcripts of three PTI marker genes (WRKY7, WRKY8 and ACRE31) rapidly accumulate in response to three different MAMPs: flg22, chitin and Pep-13. Whereas silencing of SERK3/BAK1 in Nicotiana benthamiana or potato compromised transcript accumulation in response to flg22, it did not attenuate WRKY7, WRKY8 and ACRE31 up-regulation in response to chitin or Pep-13. This indicates that Pep-13 triggers immunity in a SERK3/BAK1-independent manner, similar to chitin. Surprisingly, silencing of SERK3/BAK1 led to significantly increased accumulation of PTI marker gene transcripts following Pep-13 or chitin treatment, compared to controls. This was accompanied by reduced expression of brassinosteroid (BR) marker genes StSTDH, StEXP8 and StCAB50 and StCHL1, which is a negative regulator of PTI, supporting previous reports that SERK3/BAK1-dependent BR signaling attenuates plant immunity. We provide Pep-13 as an alternative to chitin as a trigger of SERK3/BAK1-independent immunity.

Keywords

MAMP Disease resistance Transcriptome Flagellin Late blight 

Abbreviations

PRRs

Pattern recognition receptors

MAMPs

Microbe-associated molecular patterns

BAK1

BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1

PTI

Pattern-triggered immune

ETI

Effector-triggered immunity

RLK

Receptor-like kinase

Notes

Acknowledgements

This work was support by the National Natural Science Foundation of China (31761143007, 31171603) and the Fundamental Research Funds for the Central Universities (2662017PY069) for funding ZT’s lab. We thank the Biotechnology and Biological Sciences Research Council (BBSRC) for funding PRJB’s lab (BB/L026880/1).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2018_2359_MOESM1_ESM.docx (2.7 mb)
Figure S1 Expression time courses of flg22 induced transcripts in potato and Nicotiana benthamiana. Figure S2 Expression time course of chitin induced transcripts in potato and N. benthamiana. Figure S3 Expression time courses of Pep13 induced transcripts in potato and N. benthamiana. Figure S4 Alignment of Solanum tuberosum (potato) and Nicotiana benthamiana SERK3/BAK1 full-length nucleotide sequences. Figure S5 The silencing of BAK1 in Solanum tuberosum. Figure S6 Virus-induced gene silencing (VIGS) of BAK1 in Nicotiana benthamiana. Table S1. Primer sequences used in this study (DOCX 2759 KB)

References

  1. Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S, Chinchilla D, Rathjen JP, de Vries SC, Zipfel C (2012) Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci USA 109:303–308CrossRefGoogle Scholar
  2. Antolin-Llovera M, Ried MK, Parniske M (2014) Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE ectodomain promotes complex formation with Nod factor receptor 5. Curr Biol 24:422–427CrossRefGoogle Scholar
  3. Belkhadir Y, Yang L, Hetzel J, Dangl JL, Chory J (2014) The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem Sci 39:447–456CrossRefGoogle Scholar
  4. Ben Khaled S, Postma J, Robatzek S (2015) A moving view: subcellular trafficking processes in pattern recognition receptor-triggered plant immunity. Annu Rev Phytopathol 53:379–402CrossRefGoogle Scholar
  5. Bohm H, Albert I, Oome S, Raaymakers TM, Van den Ackerveken G, Nurnberger T (2014) A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis. PLoS Pathog 10:e1004491CrossRefGoogle Scholar
  6. Brodaczewska K, Donskow-Lysoniewska K, Doligalska M (2015) Chitin, a key factor in immune regulation: lesson from infection with fungi and chitin bearing parasites. Acta Parasitol 60:337–344CrossRefGoogle Scholar
  7. Brunner F, Rosahl S, Lee J, Rudd JJ, Geiler C, Kauppinen S, Rasmussen G, Scheel D, Nurnberger T (2002) Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J 21:6681–6688CrossRefGoogle Scholar
  8. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:e03766CrossRefGoogle Scholar
  9. Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008) Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3:126–135CrossRefGoogle Scholar
  10. Chaparro-Garcia A, Wilkinson RC, Gimenez-Ibanez S, Findlay K, Coffey MD, Zipfel C, Rathjen JP, Kamoun S, Schornack S (2011) The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PloS One 6:e16608CrossRefGoogle Scholar
  11. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin induced complex of the receptor FLS2 and BAK1 initiates plant defense. Nature 448:497–500CrossRefGoogle Scholar
  12. Cikos S, Bukovska A, Koppel J (2007) Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis. BMC Mol Biol 8:113CrossRefGoogle Scholar
  13. Couto D, Zipfel C (2016) Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16:537–552CrossRefGoogle Scholar
  14. Desaki Y, Miyata K, Suzuki M, Shibuya N, Kaku H (2018) Plant immunity and symbiosis signaling mediated by LysM receptors. Innate Immun 24:92–100CrossRefGoogle Scholar
  15. Du J, Verzaux E, Chaparro-Garcia A, Bijsterbosch G, Keizer LC, Zhou J, Liebrand TW, Xie C, Govers F, Robatzek S, van der Vossen EA, Jacobsen E, Visser RG, Kamoun S, Vleeshouwers VG (2015) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat Plants 1:15034CrossRefGoogle Scholar
  16. Elieh Ali Komi D, Sharma L, Dela Cruz CS (2018) Chitin and its effects on inflammatory and immune responses. Clin Rev Allergy Immun 54:213–223CrossRefGoogle Scholar
  17. Fellbrich G, Romanski A, Varet A, Blume B, Brunner F, Engelhardt S, Felix G, Kemmerling B, Krzymowska M, Nürnberger T (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J 32:375–390CrossRefGoogle Scholar
  18. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011CrossRefGoogle Scholar
  19. Gopalakannan A, Aru V (2006) Immunomodulatory effects of dietary intake of chitin, chitosan and levamisole on the immune system of Cyprinus carpio and control of Aeromonas hydrophila infection in pond. Aquaculture 255:179–187CrossRefGoogle Scholar
  20. Halim VA, Altmann S, Ellinger D, Eschen-Lippold L, Miersch O, Scheel D, Rosahl S (2009) PAMP-induced defense responses in potato require both salicylic acid and jasmonic acid. Plant J 57:230–242CrossRefGoogle Scholar
  21. He Q, McLellan H, Boevink PC, Sadanandom A, Xie C, Birch PR, Tian Z (2015) U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans. J Exp Bot 66:3189–3199CrossRefGoogle Scholar
  22. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222CrossRefGoogle Scholar
  23. Hein I, Gilroy EM, Armstrong MR, Birch PR (2009) The zig-zag-zig in oomycete-plant interactions. Mol Plant Pathol 10:547–562CrossRefGoogle Scholar
  24. Jones J, Dangl J (2006) The plant immune system. Nature 444:323–329CrossRefGoogle Scholar
  25. Jones JD, Vance RE, Dangl JL (2016) Intracellular innate immune surveillance devices in plants and animals. Science 354:6316CrossRefGoogle Scholar
  26. Jung WJ, Park RD (2014) Bioproduction of chitooligosaccharides: present and perspectives. Mar Drugs 12:5328–5356CrossRefGoogle Scholar
  27. Kemmerling B, Halter T, Mazzotta S, Mosher S, Nurnberger T (2011) A genome-wide survey for Arabidopsis leucine-rich repeat receptor kinases implicated in plant immunity. Front Plant Sci 2:88CrossRefGoogle Scholar
  28. Kroj T, Rudd JJ, Nürnberger T, Gäbler Y, Lee J, Scheel D (2003) Mitogen-activated protein kinases play an essential role in oxidative burst-independent expression of pathogenesis-related genes in parsley. J Biol Chem 278:2256–2264CrossRefGoogle Scholar
  29. Lee J, Rudd JJ, Macioszek VK, Scheel D (2004) Dynamic changes in the localization of MAPK cascade components controlling pathogenesis-related (PR) gene expression during innate immunity in parsley. J Biol Chem 279:22440–22448CrossRefGoogle Scholar
  30. Lee CG, Da Silva CA, Lee JY, Hartl D, Elias JA (2008) Chitin regulation of immune responses: an old molecule with new roles. Curr Opin Immunol 20:684–689CrossRefGoogle Scholar
  31. Li J, Wen J, Lease KA, Dorke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222CrossRefGoogle Scholar
  32. Liu T, Liu Z, Song C, Hu Y, Han Z, She J, Fan F, Wang J, Jin C, Chang J, Zhou JM, Chai J (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–1164CrossRefGoogle Scholar
  33. Lozano-Duran R, Macho AP, Boutrot F, Segonzac C, Somssich IE, Zipfel C (2013) The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. eLife 2:e00983CrossRefGoogle Scholar
  34. Ma Z, Song T, Zhu L, Ye W, Wang Y, Shao Y, Dong S, Zhang Z, Dou D, Zheng X, Tyler BM, Wang Y (2015) A Phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. Plant Cell 27:2057–2072CrossRefGoogle Scholar
  35. McLellan H, Boevink PC, Armstrong MR, Pritchard L, Gomez S, Morales J, Whisson SC, Beynon JL, Birch PRJ (2013) An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. PLoS Pathog 9:e1003670CrossRefGoogle Scholar
  36. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618CrossRefGoogle Scholar
  37. Nam KH, Li (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212CrossRefGoogle Scholar
  38. Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449–460CrossRefGoogle Scholar
  39. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J 68:100–113CrossRefGoogle Scholar
  40. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, Zipfel C (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet 7:e1002046CrossRefGoogle Scholar
  41. Shan L, He P, Li J, Heese A, Peck SC, Nurnberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27CrossRefGoogle Scholar
  42. Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–628CrossRefGoogle Scholar
  43. Tang D, Wang G, Zhou JM (2017) Receptor kinases in plant–pathogen interactions: more than pattern recognition. Plant Cell 29:618–637CrossRefGoogle Scholar
  44. Turnbull D, Yang L, Naqvi S, Breen S, Welsh L, Stephens J, Morris J, Boevink PC, Hedley PE, Zhan J, Birch PRJ, Gilroy EM (2017) RXLR Effector AVR2 up-regulates a brassinosteroid-responsive bHLH transcription factor to suppress immunity. Plant Physiol 174:356–369CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture and Rural AffairsHuazhong Agricultural University (HZAU)WuhanPeople’s Republic of China
  2. 2.Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of EducationHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  3. 3.Division of Plant Sciences, School of Life ScienceUniversity of Dundee (at James Hutton Institute)DundeeUK
  4. 4.Cell and Molecular SciencesJames Hutton InstituteDundeeUK

Personalised recommendations