Advertisement

Journal of Plant Biochemistry and Biotechnology

, Volume 26, Issue 4, pp 371–386 | Cite as

Advances in proteomic technologies and their scope of application in understanding plant–pathogen interactions

  • N. M. R. Ashwin
  • Leonard Barnabas
  • A. Ramesh Sundar
  • P. Malathi
  • R. Viswanathan
  • Antonio Masi
  • Ganesh Kumar Agrawal
  • Randeep Rakwal
Review Article

Abstract

Proteomics, one of the major tools of ‘omics’ is evolving phenomenally since the development and application of two-dimensional gel electrophoresis coupled with mass spectrometry at the end of twentieth century. However, the adoption and application of advanced proteomic technologies in understanding plant–pathogen interactions are far less, when compared to their application in other related fields of systems biology. Hence, this review is diligently focused on the advances in various proteomic approaches and their gamut of applications in different facets of phyto-pathoproteomics. Especially, the scope and application of proteomics in understanding fundamental concepts of plant–pathogen interactions such as identification of pathogenicity determinants (effector proteins), disease resistance proteins (resistance and pathogenesis-related proteins) and their regulation by post-translational modifications have been portrayed. This review, for the first time, presents a critical appraisal of various proteomic applications by assessing all phyto-pathoproteomics-related research publications that were published in peer-reviewed journals, during the period 2000–2016. This assessment has revealed the present status and contribution of proteomic applications in different categories of phyto-pathoproteomics, namely, cellular components, host–pathogen interactions, model and non-model plants, and utilization of different proteomic approaches. Comprehensively, the analysis highlights the burgeoning application of global proteome approaches in various crop diseases, and demand for acceleration in deploying advanced proteomic technologies to thoroughly comprehend the intricacies of complex and rapidly evolving plant–pathogen interactions.

Keywords

Phyto-pathoproteomics Plant–pathogen interactions Global proteome analysis Targeted proteome analysis 

Abbreviations

2DGE–MS

Two-dimensional gel electrophoresis–mass spectrometry

ETI

Effector-triggered immunity

LAPs

Low abundant peptides

PAMPs

Pathogen associated molecular patterns

PRRs

Pattern recognition receptors

PTI

PAMP-triggered immunity

PTM

Post-translational modification

Notes

Acknowledgements

The authors would like to express their gratitude to Indian Council of Agricultural Research (ICAR), New Delhi. The authors thank Director, ICAR-Sugarcane Breeding Institute for providing facilities and continuous encouragement. We also place on record our sincere thanks to Department of Science and Technology, Govt. of India for the support. The authors are indebted to INPPO (http://www.inppo.com/) for their support and encouragement.

Compliance with ethical standards

Conflict of interest

The authors declare that they do not have any conflict of interest.

Supplementary material

13562_2017_402_MOESM1_ESM.xlsx (32.6 mb)
Online resource Supp. ESM_1 a) List of research and review articles published in peer-reviewed journals on or related to plant-pathogen interactions using core proteomic strategies during the period 2000–2016*. b) An overview on the status of application of proteomics in understanding plant-pathogen interactions in terms of number of publications under different categories in peer-reviewed journals between 2000 and 2016*. * Only publications until August, 2016 were considered for analysis (XLSX 33399 kb)
13562_2017_402_MOESM2_ESM.docx (17 kb)
Online resource Supp. ESM_2 List of review articles that summarizes significant findings of individual research publications under specific categories of phyto-pathoproteomics (DOCX 16 kb)

References

  1. Agrawal GK, Bourguignon J, Rolland N, Ephritikhine G, Myriam F, Jaquinod M, Alexiou KG, Chardot T, Chakraborty N, Jolivet P, Doonan JH, Rakwal R (2011) Plant organelle proteomics: collaborating for optimal cell function. Mass Spectrom Rev 30:772–853. doi: 10.1002/mas.20301 PubMedGoogle Scholar
  2. Agrawal GK, Sarkar A, Righetti PG, Pedreschi R, Carpentier S, Wang T, Barkla BJ, Kohli A, Ndimba BK, Bykova NV, Rampitch C, Zolla L, Rafudeen MS, Cramer R, Bindschedler LV, Tsakirpaloglou N, Ndimba RJ, Farrant JM, Renaut J, Job D, Kikuchi S, Rakwal R (2013) A decade of plant proteomics and mass spectrometry: translation of technical advancements to food security and safety issues. Mass Spectrom Rev 32:335–365. doi: 10.1002/mas.21365 CrossRefPubMedGoogle Scholar
  3. Agrios GN (2005) Plant pathology. Elsevier Academic Press, New YorkGoogle Scholar
  4. Alexander MM, Cilia M (2016) A molecular tug-of-war: global plant proteome changes during viral infection. Curr Plant Biol 5:13–24. doi: 10.1016/j.cpb.2015.10.003 CrossRefGoogle Scholar
  5. Altenbach D, Robatzek S (2007) Pattern recognition receptors: from the cell surface to intracellular dynamics. Mol Plant Microbe Interact 20:1031–1039. doi: 10.1094/MPMI-20-9-1031 CrossRefPubMedGoogle Scholar
  6. Amalraj RS, Selvaraj N, Veluswamy GK, Ramanujan RP, Muthurajan R, Palaniyandi M, Agrawal GK, Rakwal R, Viswanathan R (2010) Sugarcane proteomics: establishment of a protein extraction method for 2-DE in stalk tissues and initiation of sugarcane proteome reference map. Electrophoresis 31:1959–1974. doi: 10.1002/elps.200900779 CrossRefPubMedGoogle Scholar
  7. Atanassov I, Urlaub H (2013) Increased proteome coverage by combining PAGE and peptide isoelectric focusing: comparative study of gel-based separation approaches. Proteomics 13:2947–2955. doi: 10.1002/pmic.201300035 PubMedPubMedCentralGoogle Scholar
  8. Barnabas L, Ramadass A, Amalraj RS, Palaniyandi M, Rasappa V (2015) Sugarcane proteomics: an update on current status, challenges, and future prospects. Proteomics 15:1658–1670. doi: 10.1002/pmic.201400463 CrossRefPubMedGoogle Scholar
  9. Barnabas L, Ashwin NMR, Kaverinathan K, Trentin AR, Pivato M, Sundar AR, Malathi P, Viswanathan R, Rosana OB, Neethukrishna K, Carletti P (2016) Proteomic analysis of a compatible interaction between sugarcane and Sporisorium scitamineum. Proteomics 16:1111–1122. doi: 10.1002/pmic.201500245 CrossRefPubMedGoogle Scholar
  10. Bodzon-Kulakowska A, Bierczynska-Krzysik A, Dylag T, Drabik A, Suder P, Noga M, Jarzebinska J, Silberring J (2007) Methods for samples preparation in proteomic research. J Chromatogr B 849:1–31. doi: 10.1016/j.jchromb.2006.10.040 CrossRefGoogle Scholar
  11. Bohm H, Albert I, Fan L, Reinhard A, Nürnberger T (2014) Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol 20C:47–54. doi: 10.1016/j.pbi.2014.04.007 CrossRefGoogle Scholar
  12. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406. doi: 10.1146/annurev.arplant.57.032905.105346 CrossRefPubMedGoogle Scholar
  13. Brewis IA, Brennan P (2010) Proteomics technologies for the global identification and quantification of proteins. Adv Protein Chem Struct Biol 80:1–44. doi: 10.1016/B978-0-12-381264-3.00001-1 CrossRefPubMedGoogle Scholar
  14. Brun V, Masselon C, Garin J, Dupuis A (2009) Isotope dilution strategies for absolute quantitative proteomics. J Proteomics 72:740–749. doi: 10.1016/j.jprot.2009.03.007 CrossRefPubMedGoogle Scholar
  15. Burgyan J (2008) Role of silencing suppressor proteins. Methods Mol Biol 451:69–79CrossRefPubMedGoogle Scholar
  16. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814. doi: 10.1016/j.cell.2006.02.008 CrossRefPubMedGoogle Scholar
  17. Colignon B, Raes M, Dieu M, Delaive E, Mauro S (2013) Evaluation of three-dimensional gel electrophoresis to improve quantitative profiling of complex proteomes. Proteomics 13:2077–2082. doi: 10.1002/pmic.201200494 CrossRefPubMedGoogle Scholar
  18. Da Silva ACR, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NA, Alves LM (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459–463. doi: 10.1038/417459a CrossRefPubMedGoogle Scholar
  19. Delaunois B, Jeandet P, Clement C, Baillieul F, Dorey S, Cordelier S (2014) Uncovering plant-pathogen crosstalk through apoplastic proteomic studies. Front Plant Sci 5:249. doi: 10.3389/fpls.2014.00249 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dou D, Zhou J-M (2012) Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–495. doi: 10.1016/j.chom.2012.09.003 CrossRefPubMedGoogle Scholar
  21. Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13:472–477. doi: 10.1016/j.pbi.2010.04.007 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Evans C, Noirel J, Ow SY, Salim M, Pereira-Medrano AG, Couto N, Pandhal J, Smith D, Pham TK, Karunakaran E, Zou X (2012) An insight into iTRAQ: where do we stand now? Anal Bioanal Chem 404:1011–1027. doi: 10.1007/s00216-012-5918-6 CrossRefPubMedGoogle Scholar
  23. Faulkner C, Robatzek S (2012) Plants and pathogens: putting infection strategies and defence mechanisms on the map. Curr Opin Plant Biol 15:699–707. doi: 10.1016/j.pbi.2012.08.009 CrossRefPubMedGoogle Scholar
  24. Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, Shabanowitz J, Hunt DF, White FM (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20:301–305CrossRefPubMedGoogle Scholar
  25. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194. doi: 10.1038/nature10947 CrossRefPubMedGoogle Scholar
  26. Florens L, Washburn MP (2006) Proteomic analysis by multidimensional protein identification technology. Methods Mol Biol 328:159–175PubMedGoogle Scholar
  27. Gallien S, Bourmaud A, Kim SY, Domon B (2014) Technical considerations for large-scale parallel reaction monitoring analysis. J Proteom 100:147–159. doi: 10.1016/j.jprot.2013.10.029 CrossRefGoogle Scholar
  28. Geiger T, Wisniewski JR, Cox J, Zanivan S, Kruger M, Ishihama Y, Mann M (2011) Use of stable isotope labeling by amino acids in cell culture as a spike-in standard in quantitative proteomics. Nat Protoc 6:147–157. doi: 10.1038/nprot.2010.192 CrossRefPubMedGoogle Scholar
  29. Giraldo MC, Valent B (2013) Filamentous plant pathogen effectors in action. Nat Rev Microbiol 11:800–814. doi: 10.1038/nrmicro3119 CrossRefPubMedGoogle Scholar
  30. Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:79–92. doi: 10.1126/science.1068275 CrossRefGoogle Scholar
  31. Gohre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215. doi: 10.1146/annurev.phyto.46.120407.110050 CrossRefPubMedGoogle Scholar
  32. Gonzalez-Fernandez R, Prats E, Jorrín-Novo JV (2010) Proteomics of plant pathogenic fungi. J Biomed Biotechnol 2010:932527. doi: 10.1155/2010/932527 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B, Goldman BS, Cao Y, Askenazi M, Halling C, Mullin L (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323–2328. doi: 10.1126/science.1066803 CrossRefPubMedGoogle Scholar
  34. Gupta R, Wang Y, Agrawal GK, Rakwal R, Jo IH, Bang KH, Kim ST (2015) Time to dig deep into the plant proteome: a hunt for low-abundance proteins. Front Plant Sci 6:1–3. doi: 10.3389/fpls.2015.00022 Google Scholar
  35. Halligan BD, Ruotti V, Jin W, Laffoon S, Twigger SN, Dratz EA (2004) ProMoST (Protein Modification Screening Tool): a web-based tool for mapping protein modifications on two-dimensional gels. Nucleic Acids Res 32:638–644. doi: 10.1093/nar/gkh356 CrossRefGoogle Scholar
  36. Harsha HC, Molina H, Pandey A (2008) Quantitative proteomics using stable isotope labeling with amino acids in cell culture. Nat Protoc 3:505–516. doi: 10.1038/nprot.2008.2 CrossRefPubMedGoogle Scholar
  37. Hiller K, Schobert M, Hundertmark C, Jahn D, Münch R (2003) JVirGel: calculation of virtual two-dimensional protein gels. Nucleic Acids Res 31:3862–3865. doi: 10.1093/nar/gkg536 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22:115–122. doi: 10.1094/MPMI-22-2-0115 CrossRefPubMedGoogle Scholar
  39. Howden AJM, Huitema E (2012) Effector-triggered post-translational modifications and their role in suppression of plant immunity. Front Plant Sci 3:160. doi: 10.3389/fpls.2012.00160 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hull R (2013) Plant virology. Elsevier Academic Press, New YorkGoogle Scholar
  41. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi: 10.1038/nature05286 CrossRefPubMedGoogle Scholar
  42. Jorrin-Novo JV, Pascual J, Lucas RS, Romero-Rodríguez MC, Rodríguez-Ortega MJ, Lenz C, Valledor L (2015) Fourteen years of plant proteomics reflected in “Proteomics”: moving from model species and 2-DE based approaches to orphan species and gel-free platforms. Proteomics 15:1–45. doi: 10.1002/pmic.201400349 CrossRefGoogle Scholar
  43. Kaboord B, Perr M (2008) Isolation of proteins and protein complexes by immunoprecipitation. In: Posch A (ed) Methods in molecular biology—2D PAGE: sample preparation and fractionation, vol 424. Humana Pre, Clifton, pp 349–364. doi: 10.1007/978-1-60327-064-9_27 CrossRefGoogle Scholar
  44. Katagiri F, Tsuda K (2010) Understanding the plant immune system. Mol Plant Microbe Interact 23:1531–1536. doi: 10.1094/MPMI-04-10-0099 CrossRefPubMedGoogle Scholar
  45. Klose J (1975) Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues. A novel approach to testing for induced point mutations in mammals. Humangenetik 26:231–243PubMedGoogle Scholar
  46. Kockmann T, Trachsel C, Panse C, Wahlander A, Selevsek N, Grossmann J, Wolski WE, Schlapbach R (2016) Targeted proteomics coming of age—SRM, PRM and DIA performance evaluated from a core facility perspective. Proteomics. doi: 10.1002/pmic.201500502 PubMedGoogle Scholar
  47. Lapin D, Van den Ackerveken G (2013) Susceptibility to plant disease: more than a failure of host immunity. Trends Plant Sci 18:546–554. doi: 10.1016/j.tplants.2013.05.005 CrossRefPubMedGoogle Scholar
  48. Liebler DC, Zimmerman LJ (2013) Targeted quantitation of proteins by mass spectrometry. Biochemistry 52:3797–3806. doi: 10.1021/bi400110b CrossRefPubMedPubMedCentralGoogle Scholar
  49. Macek B, Mann M, Olsen JV (2009) Global and site-specific quantitative phosphoproteomics: principles and applications. Annu Rev Pharmacol Toxicol 49:199–221. doi: 10.1146/annurev.pharmtox.011008.145606 CrossRefPubMedGoogle Scholar
  50. Mann M, Jensen ON (2003) Proteomic analysis of post-translational modifications. Nat Biotechnol 21:255–261. doi: 10.1038/nbt0303-255 CrossRefPubMedGoogle Scholar
  51. McLachlin DT, Chait BT (2003) Improved β-elimination-based affinity purification strategy for enrichment of phosphopeptides. Anal Chem 75:6826–6836. doi: 10.1021/ac034989u CrossRefPubMedGoogle Scholar
  52. Mohammed S, Heck AJR (2011) Strong cation exchange (SCX) based analytical methods for the targeted analysis of protein post-translational modifications. Curr Opin Biotechnol 22:9–16. doi: 10.1016/j.copbio.2010.09.005 CrossRefPubMedGoogle Scholar
  53. Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15:349–357. doi: 10.1016/j.pbi.2012.05.006 CrossRefPubMedGoogle Scholar
  54. O’Farrell PF (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021PubMedPubMedCentralGoogle Scholar
  55. Patterson SD, Aebersold RH (2003) Proteomics: the first decade and beyond. Nat Genet 33:311–323. doi: 10.1038/ng1106 CrossRefPubMedGoogle Scholar
  56. Phillips CM, Iavarone AT, Marletta MA (2011) Quantitative proteomic approach for cellulose degradation by Neurospora crassa. J Proteome Res 10:4177–4185. doi: 10.1021/pr200329b CrossRefPubMedGoogle Scholar
  57. Rabilloud T (2013) When 2D is not enough, go for an extra dimension. Proteomics 13:2065–2068. doi: 10.1002/pmic.201300215 CrossRefPubMedGoogle Scholar
  58. Rauniyar N (2015) Parallel reaction monitoring: a targeted experiment performed using high resolution and high mass accuracy mass spectrometry. Int J Mol Sci 16:28566–28581. doi: 10.3390/ijms161226120 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Righetti PG, Boschetti E (2016) Global proteome analysis in plants by means of peptide libraries and applications. J Proteom 143:3–14. doi: 10.1016/j.jprot.2016.02.033 CrossRefGoogle Scholar
  60. Rowland E, Kim J, Bhuiyan NH, van Wijk KJ (2015) The Arabidopsis chloroplast stromal N-terminome: complexities of amino-terminal protein maturation and stability. Plant Physiol 169:1881–1896. doi: 10.1104/pp.15.01214 PubMedPubMedCentralGoogle Scholar
  61. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, Billault A, Brottier P, Camus JC, Cattolico L, Chandler M, Choisne N, Claudel-Renard C, Cunnac S, Demange N, Gaspin C, Lavie M, Moisan A, Robert C, Saurin W, Schiex T, Siguier P, Thebault P, Whalen M, Wincker P, Levy M, Weissenbach J, Boucher CA (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497. doi: 10.1038/415497a CrossRefPubMedGoogle Scholar
  62. Scheele GA (1975) Two-dimensional gel analysis of soluble proteins. Characterization of guinea pig exocrine pancreatic proteins. J Biol Chem 250:5375–5385PubMedGoogle Scholar
  63. Sergeant K, Renaut J (2010) Plant biotic stress and proteomics. Curr Proteom 7:275–297. doi: 10.2174/157016410793611765 CrossRefGoogle Scholar
  64. Shiio Y, Aebersold R (2006) Quantitative proteome analysis using isotope-coded affinity tags and mass spectrometry. Nat Protoc 1:139–145. doi: 10.1038/nprot.2006.22 CrossRefPubMedGoogle Scholar
  65. Simpson AJ, Reinach FC, Arruda P, Abreu FA, Acencio M, Alvarenga R, Alves LC, Araya JE, Baia GS, Baptista CS, Barros MH (2000) The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa consortium of the organization for nucleotide sequencing and analysis. Nature 406:151–159. doi: 10.1038/35018003 CrossRefPubMedGoogle Scholar
  66. Song J, Sun R, Li D, Tan F, Li X, Jiang P, Huang X, Lin L, Deng Z, Zhang Y (2012) An improvement of shotgun proteomics analysis by adding next-generation sequencing transcriptome data in orange. PLoS ONE 7:5–10. doi: 10.1371/journal.pone.0039494 Google Scholar
  67. Stergiopoulos I, de Wit PJGM (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263. doi: 10.1146/annurev.phyto.112408.132637 CrossRefPubMedGoogle Scholar
  68. Stergiopoulos I, De Kock MJD, Lindhout P, De Wit PJGM (2007) Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol Plant Microbe Interact 20:1271–1283. doi: 10.1094/MPMI-20-10-1271 CrossRefPubMedGoogle Scholar
  69. Takken FL, Albrecht M, Tameling WI (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9:383–390. doi: 10.1016/j.pbi.2006.05.009 CrossRefPubMedGoogle Scholar
  70. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815. doi: 10.1038/35048692 CrossRefGoogle Scholar
  71. Thelen JJ (2007) Ch 1: introduction to proteomics: a brief historical perspective on contemporary approaches. In: Samaj J, Thelen JJ (eds) Plant proteomics. Springer, Berlin, Heidelberg, pp 1–13. doi: 10.1007/978-3-540-72617-3_1
  72. Thingholm TE, Jensen ON, Larsen MR (2009) Analytical strategies for phosphoproteomics. Proteomics 9:1451–1468. doi: 10.1002/pmic.200800454 CrossRefPubMedGoogle Scholar
  73. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet. doi: 10.1371/journal.pgen.1000772 PubMedPubMedCentralGoogle Scholar
  74. Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis. A single gel method for detecting changes in protein extracts. Electrophoresis 18:2071–2077CrossRefPubMedGoogle Scholar
  75. Villen J, Beausoleil SA, Gerber SA, Gygi SP (2007) Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci USA 104:1488–1493. doi: 10.1073/pnas.0609836104 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Walsh CT, Garneau-Tsodikova S, Gatto GJ (2005) Protein posttranslational modifications: the chemistry of proteome diversifications. Angew Chem Int Ed Engl 44:7342–7372. doi: 10.1002/anie.200501023 CrossRefPubMedGoogle Scholar
  77. Washburn MP, Wolters D, Yates JR (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19:242–247CrossRefPubMedGoogle Scholar
  78. Wilkins MR, Sanchez JC, Gooley AA, Appel RD, Humphery-Smith I, Hochstrasser DF, Williams KL (1995) Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotechnol Genet Eng Rev 13:19–50CrossRefGoogle Scholar
  79. Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K, Dong S, Schornack S, Zipfel C, Robatzek S, Hogenhout SA, Kamoun S (2012) Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb Symp Quant Biol 77:235–247. doi: 10.1101/sqb.2012.77.015933 CrossRefPubMedGoogle Scholar
  80. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Almeida NF, Woo L (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317–2323. doi: 10.1126/science.1066804 CrossRefPubMedGoogle Scholar
  81. Wu L, Chen H, Curtis C, Fu ZQ (2014) How plants deploy effector-triggered immunity to combat pathogens. Virulence 5:710–721. doi: 10.4161/viru.29755 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Yamagata A, Kristensen DB, Takeda Y, Miyamoto Y, Okada K, Inamatsu M, Yoshizato K (2002) Mapping of phosphorylated proteins on two-dimensional polyacrylamide gels using protein phosphatase. Proteomics 2:1267–1276. doi: 10.1002/1615-9861(200209)2:9<1267:AID-PROT1267>3.0.CO;2-R CrossRefPubMedGoogle Scholar
  83. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92. doi: 10.1126/science.1068037 CrossRefPubMedGoogle Scholar
  84. Zhang J, Zhou J-M (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793. doi: 10.1093/mp/ssq035 CrossRefPubMedGoogle Scholar
  85. Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420. doi: 10.1016/j.pbi.2009.06.003 CrossRefPubMedGoogle Scholar

Copyright information

© Society for Plant Biochemistry and Biotechnology 2017

Authors and Affiliations

  1. 1.Plant Pathology Section, Division of Crop ProtectionIndian Council of Agricultural Research - Sugarcane Breeding InstituteCoimbatoreIndia
  2. 2.Department of Agronomy, Food, Natural Resources, Animals and EnvironmentUniversity of PadovaPaduaItaly
  3. 3.Research Laboratory for Biotechnology and BiochemistryKathmanduNepal
  4. 4.GRADE (Global Research Arch for Developing Education) Academy Private LimitedBirgunjNepal
  5. 5.Faculty of Health and Sport Sciences, and Tsukuba International Academy for Sport Studies (TIAS)University of TsukubaTsukubaJapan

Personalised recommendations