Skip to main content
Log in

Genome-wide in silico identification of LysM-RLK genes in potato (Solanum tuberosum L.)

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The receptor like kinases (RLKs) belong to the RLK/Pelle superfamily, one of the largest gene families in plants. RLKs play an important role in plant development, as well as in response to biotic and abiotic stresses. The lysine motif receptor like kinases (LysM-RLKs) are a subfamily of RLKs containing at least one lysine motif (LysM) that are involved in the perception of elicitors or pathogen-associated molecular patterns (PAMPs). In the present study, 77 putative RLKs genes and three receptor like proteins were identified in potato (Solanum tuberosum) genome, following a genome-wide search. The 77 potato RLK proteins are classified into two major phylogenetic groups based on their kinase domain amino acid sequence similarities. Out of 77 RLKs, 10 proteins had at least one LysM. Among them three RLP proteins were found in potato genome with either 2 or three tandem LysM but these lacked a cytoplasmic kinase domain. Expression analyses of a potato LysM-RLKs (StLysM-RLK05) was carried out by a Real time RT-PCR, following inoculation of potato leaves and immature tubers with late blight and common scab pathogens, respectively. The expression was significantly higher in resistant than in susceptible following S. scabies inoculation. The StLysM-RLK05 sequence was verified and it was polymorphic in scab susceptible cultivar. The present study provides an overview of the StLysM-RLKs gene family in potato genome. This information is helpful for future functional analysis of such an important protein family, in Solanaceae species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

MAPK:

Mitogen activated protein kinases

PAMPs:

Pathogen-associated molecular patterns

RKs:

Receptor kinases

RLKs:

Receptor-like kinases

CEBiP:

Chitin-elicitor binding protein

AUDPC:

Area under the disease progress curve

PDB:

Protein Data Bank

References

  1. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  2. Kushalappa AC, Yogendra KN, Karre S (2016) Plant innate immune response: qualitative and quantitative resistance. Crit Rev Plant Sci 35:38–55

    Article  CAS  Google Scholar 

  3. 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. https://doi.org/10.7554/eLife.03766

    Article  PubMed  PubMed Central  Google Scholar 

  4. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16

    Article  CAS  PubMed  Google Scholar 

  5. Torii KU (2009) Transmembrane receptors in plants: receptor kinases and their ligands. Annu Plant Rev 33:1–29

    Google Scholar 

  6. Kanda Y, Yokotani N, Maeda S, Nishizawa Y, Kamakura T, Mori M (2017) The receptor-like cytoplasmic kinase BSR1 mediates chitin-induced defense signaling in rice cells. Biosci Biotechnol Biochem 81(8):1497–1500

    Article  CAS  PubMed  Google Scholar 

  7. Shiu S-H, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001:re22

    CAS  PubMed  Google Scholar 

  8. Shiu S-H, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Shiu S-H, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 113:re22

    Google Scholar 

  10. 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 5:1003–1011

    Article  PubMed  Google Scholar 

  11. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938

    Article  CAS  PubMed  Google Scholar 

  12. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585

    Article  CAS  PubMed  Google Scholar 

  13. Kaku H, Shibuya N (2016) Molecular mechanisms of chitin recognition and immune signaling by LysM-receptors. Physiol Mol Plant Pathol 95:60–65

    Article  CAS  Google Scholar 

  14. Zhang X-C, Wu X, Findley S, Wan J, Libault M, Nguyen HT, Cannon SB, Stacey G (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144:623–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Buist G, Steen A, Kok J, Kuipers OP (2008) LysM, a widely distributed protein motif for binding to (peptido) glycans. Mol Microbiol 68:838–847

    Article  CAS  PubMed  Google Scholar 

  16. Hohmann U, Lau K, Hothorn M (2017) The structural basis of ligand perception and signal activation by receptor kinases. Annu Rev Plant Biol 68:109–137

    Article  CAS  PubMed  Google Scholar 

  17. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, Lipka V, Maule AJ (2013) LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci USA 110:9166–9170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Liu B, Li JF, Ao Y, Qu J, Li Z, Su J, Zhang Y, Liu J, Feng D, Qi K, He Y, Wang J, Wang HB (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–3419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wan J, Tanaka K, Zhang XC, Son GH, Brechenmacher L, Nguyen TH, Stacey G (2012) LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol 160:396–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Espinoza C, Liang Y, Stacey G (2017) Chitin receptor CERK1 links salt stress and chitin-triggered innate immunity in Arabidopsis. Plant J 89:984–995

    Article  CAS  PubMed  Google Scholar 

  22. Carotenuto G, Chabaud M, Miyata K, Capozzi M, Takeda N, Kaku H, Shibuya N, Nakagawa T, Barker DG, Genre A (2017) The rice LysM receptor-like kinase OsCERK1 is required for the perception of short-chain chitin oligomers in arbuscular mycorrhizal signaling. New Phytol 214:1440–1446

    Article  CAS  PubMed  Google Scholar 

  23. Karre S, Kumar A, Dhokane D, Kushalappa AC (2017) Metabolo-transcriptome profiling of barley reveals induction of chitin elicitor receptor kinase gene (HvCERK1) conferring resistance against Fusarium graminearum. Plant Mol Biol 93:247–267

    Article  CAS  PubMed  Google Scholar 

  24. Bethke PC, Nassar AM, Kubow S, Leclerc YN, Li X-Q, Haroon M, Molen T, Bamberg J, Martin M, Donnelly DJ (2014) History and origin of Russet Burbank (Netted Gem) a sport of Burbank. Am J Potato Res 91:594–609

    Article  Google Scholar 

  25. Yogendra KN, Kushalappa AC, Sarmiento F, Rodriguez E, Mosquera T (2015) Metabolomics deciphers quantitative resistance mechanisms in diploid potato clones against late blight. Funct Plant Biol 42:284–298

    Article  CAS  PubMed  Google Scholar 

  26. Pushpa D, Yogendra KN, Gunnaiah R, Kushalappa AC, Murphy A (2014) Identification of late blight resistance-related metabolites and genes in potato through nontargeted metabolomics. Plant Mol Biol Report 32:584–595

    Article  CAS  Google Scholar 

  27. Yogendra KN, Kushalappa AC (2016) Integrated transcriptomics and metabolomics reveal induction of hierarchies of resistance genes in potato against late blight. Funct Plant Biol 43:766–782

    Article  CAS  PubMed  Google Scholar 

  28. Shirling ET, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  29. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N (2011) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    Article  PubMed  PubMed Central  Google Scholar 

  30. 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 104:19613–19618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dhaliwal AK, Mohan A, Gill KS (2014) Comparative analysis of ABCB1 reveals novel structural and functional conservation between monocots and dicots. Front Firm Knowl Creat Entity. https://doi.org/10.3389/fpls.2014.00657

    Article  Google Scholar 

  32. Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  33. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  35. Zimmermann L, Stephens A, Nam S-Z, Rau D, Kübler J, Lozajic M, Gabler F, Söding J, Lupas AN, Alva V (2017) A completely reimplemented mpi bioinformatics toolkit with a new HHpred server at its core. J Mol Biol 430(15):2237–2243

    Article  PubMed  Google Scholar 

  36. Webb B, Sali A (2016) Comparative protein structure modeling using MODELLER. Curr Protoc Protein Sci 86:2.9.1–2.9.37

    Article  Google Scholar 

  37. Irwin JJ, Sterling T, Mysinger MM, Bolstad ES, Coleman RG (2012) ZINC: a free tool to discover chemistry for biology. J Chem Inf Model 52:1757–1768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 30:2785–2791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31:455–461

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Bouaziz D, Charfeddine M, Jbir R, Saidi MN, Pirrello J, Charfeddine S, Bouzayen M, Gargouri-Bouzid R (2015) Identification and functional characterization of ten AP2/ERF genes in potato. Plant Cell Tissue Organ Cult 123:155–172

    Article  CAS  Google Scholar 

  41. Charfeddine M, Saïdi MN, Charfeddine S, Hammami A, Bouzid RG (2015) Genome-wide analysis and expression profiling of the ERF transcription factor family in potato (Solanum tuberosum L.). Mol Biotechnol 57:348–358

    Article  CAS  PubMed  Google Scholar 

  42. Gromadka R, Cieśla J, Olszak K, Szczegielniak J, Muszyńska G, Polkowska-Kowalczyk L (2018) Genome-wide analysis and expression profiling of calcium-dependent protein kinases in potato (Solanum tuberosum). Plant Growth Regul 84:303–315

    Article  CAS  Google Scholar 

  43. Jupe F, Pritchard L, Etherington GJ, MacKenzie K, Cock PJ, Wright F, Sharma SK, Bolser D, Bryan GJ, Jones JD (2012) Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genom 13:75

    Article  CAS  Google Scholar 

  44. Ma H, Cao X, Shi S, Li S, Gao J, Ma Y, Zhao Q, Chen Q (2016) Genome-wide survey and expression analysis of the amino acid transporter superfamily in potato (Solanum tuberosum L.). Plant Physiol Biochem 107:164–177

    Article  CAS  PubMed  Google Scholar 

  45. Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20:403–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Zhao P, Wang D, Wang R, Kong N, Zhang C, Yang C, Wu W, Ma H, Chen Q (2018) Genome-wide analysis of the potato Hsp20 gene family: identification, genomic organization and expression profiles in response to heat stress. BMC Genom 19:61

    Article  Google Scholar 

  47. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178

    Article  CAS  PubMed  Google Scholar 

  48. Yang X, Tuskan GA (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142:820–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Consortium PGS (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189

    Article  Google Scholar 

  50. Buendia L, Wang T, Girardin A, Lefebvre B (2016) The LysM receptor-like kinase SlLYK10 regulates the arbuscular mycorrhizal symbiosis in tomato. New Phytol 210:184–195

    Article  CAS  PubMed  Google Scholar 

  51. Zeng L, Velásquez AC, Munkvold KR, Zhang J, Martin GB (2012) A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J 69:92–103

    Article  CAS  PubMed  Google Scholar 

  52. Zhang X-C, Cannon SB, Stacey G (2009) Evolutionary genomics of LysM genes in land plants. BMC Evol Biol 9:183

    Article  PubMed  PubMed Central  Google Scholar 

  53. Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, Gough C, Bisseling T (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145:183–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26(17):3923–3935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lohmann GV, Shimoda Y, Nielsen MW, Jørgensen FG, Grossmann C, Sandal N, Sørensen K, Thirup S, Madsen LH, Tabata S (2010) Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol Plant Microbe Interact 23:510–521

    Article  CAS  PubMed  Google Scholar 

  56. Rairdan G, Moffett P (2007) Brothers in arms? Common and contrasting themes in pathogen perception by plant NB-LRR and animal NACHT-LRR proteins. Microbes Infect 9:677–686

    Article  CAS  PubMed  Google Scholar 

  57. Massa AN, Childs KL, Lin H, Bryan GJ, Giuliano G, Buell CR (2011) The transcriptome of the reference potato genome Solanum tuberosum Group Phureja clone DM1-3 516R44. PLoS ONE 6:e26801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Peng K-C, Wang C-W, Wu C-H, Huang C-T, Liou R-F (2015) Tomato SOBIR1/EVR homologs are involved in elicitin perception and plant defense against the oomycete pathogen Phytophthora parasitica. Mol Plant Microbe Interact 28:913–926

    Article  CAS  PubMed  Google Scholar 

  59. Wan J, Zhang X-C, Neece D, Ramonell KM, Clough S, Kim S-y, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kushalappa AC, Yogendra KN, Sarkar K, Kage U, Karre S (2016) Gene discovery and genome editing to develop cisgenic crops with improved resistance against pathogen infection. Can J Plant Path 38:279–295

    Article  CAS  Google Scholar 

Download references

Funding

This work was carried out with the aid of a grant from The Natural Sciences and Engineering Research Council of Canada (NSERC). SJ acknowledges MITACS for funding and Progest2001 Inc. for providing the genotype AG704.10.

Author information

Authors and Affiliations

Authors

Contributions

FN conducted the experiments, bioinformatics analyses and wrote the manuscript; SJ conducted inoculation studies and edited the manuscript; HX conducted scab inoculation studies; AK conceived the idea and edited the manuscript.

Corresponding author

Correspondence to Ajjamada C. Kushalappa.

Ethics declarations

Conflict of interest

Authors declare no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nazarian-Firouzabadi, F., Joshi, S., Xue, H. et al. Genome-wide in silico identification of LysM-RLK genes in potato (Solanum tuberosum L.). Mol Biol Rep 46, 5005–5017 (2019). https://doi.org/10.1007/s11033-019-04951-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-019-04951-z

Keywords

Navigation