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Fungal and Bacterial Biotrophy and Necrotrophy

  • Geeta
  • Reema Mishra
Chapter

Abstract

Plant pathogens have been divided into two classes, namely, biotrophs and necrotrophs. These pathogens lead to significant economic losses by infecting various crops. Biotrophs complete their life cycle by using the living host cell machinery, while necrotrophs feed on the host cell after killing them. Hemibiotrophs, a third group, show both the forms for obtaining nutrition i.e., early biotrophic stage to later necrotrophic phase. After infecting the plants, both the groups of plant pathogens can trigger and suppress plant immune responses by synthesizing and secreting effector proteins. In case of biotrophic pathogens, effector proteins were found to be Avr proteins (identified by resistance proteins), hrp genes, and cell wall-degrading enzymes, while necrotrophic pathogen has additional effectors called as host-selective toxins. Significant differences have been observed between these two groups in the disease symptoms they cause, their host range, morphogenesis of the infection, production of secondary metabolites and hormones, and nature of plant resistance. Biotrophs possess a sophisticated way of infection, i.e., it enters the host cell using the haustoria, colonizes the intercellular space, and overpowers the host defenses. Necrotrophs have been further grouped into host-specific and broad host range necrotrophs depending on the toxins they secrete. In case of necrotrophic infections, host cell death has been shown to trigger production of hormones like ethylene, abscisic acid, salicylic acid, and jasmonic acid. Both bacterial and fungal plant pathogens belonging to the above mentioned category have been identified. In this chapter we are going to discuss the current state of knowledge about bacterial and fungal biotrophs and necrotrophs.

Keywords

Bacteria Biotrophs Effector proteins Fungal Necrotrophs Pathogen 

Notes

Glossary

Appressorial pegs

It is a specialized cell characteristic of fungal plant pathogens and is used during infection process.

Effector proteins

Proteins secreted by bacterial pathogens during the infection process and help in suppressing the immune system of host.

Extracellular polysaccharides

High molecular weight sugar polymers synthesized by microorganisms. They play important roles in protecting the microorganism and also mediate their pathogenicity.

Hypersensitive response

It is a defense mechanism evoked by pathogens and involves localized cell death to stop the spread of infection.

Phytohormone

Chemicals or signal molecules synthesized by plants and play an important role in their growth and development.

Phytopathogens

Pathogenic bacteria, viruses, or fungi which infect plants and cause many plant diseases.

Quorum sensing

It is a phenomenon of cell-cell communication which helps bacteria to sense the cell density and coordinate their behavior accordingly.

Small RNAs

Noncoding RNA molecules which are less than 200 nucleotide in length and have a role in RNA silencing and regulation of gene expression.

Virulence

The extent of injury caused by pathogen to its host.

References

  1. Abbas HK, Tanaka T, Duke SO, Porter JK, Wray EM, Hodges L, Sessions AE, Wang E, Merrill AH, Riley RT (1994) Fumonisin- and AAL-toxin-induced disruption of sphingolipid metabolism with accumulation of free sphingoid bases. Plant Physiol 106:1085–1093PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agrios GN (2005) Plant pathology (5). Elsevier Academic Press, San FranciscoGoogle Scholar
  3. Ahmad S, Soanes DM, Barooah MC, Talbot NJ (2006) Investigating the evolution of fungal virulence by functional genomics. In: Brown AJP (ed) The mycota vol XII. Fungal genomics. Springer, Berlin, pp 35–49CrossRefGoogle Scholar
  4. Alfano JR, Collmer A (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683–1698PubMedPubMedCentralCrossRefGoogle Scholar
  5. Alfano JR, Collmer A (1997) The type III (hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179:5655–5662PubMedPubMedCentralCrossRefGoogle Scholar
  6. Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414PubMedCrossRefGoogle Scholar
  7. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479PubMedPubMedCentralCrossRefGoogle Scholar
  8. Arlat M, Van Gijsegem F, Huet JC, Pernollet JC, Boucher CA (1994) PopA1, a protein which induces a hypersensitive like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J 13:543–553PubMedPubMedCentralGoogle Scholar
  9. Audenaert K, De Meyer GB, Höfte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128:491–501PubMedPubMedCentralCrossRefGoogle Scholar
  10. Barras F, Van Gijsegem F, Chatterjee AK (1994) Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu Rev Phytopathol 32:201–234CrossRefGoogle Scholar
  11. Bauer DW, Wei Z-M, Beer SV, Collmer A (1995) Erwinia chrysanthemi harpinEChA: an elicitor of the hypersensitive response that contributes to soft-rot pathogenesis. Mol Plant-Microbe Interact 8:484–491PubMedCrossRefGoogle Scholar
  12. Bent AF, Mackey D (2007) Elicitors, effectors and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436PubMedCrossRefGoogle Scholar
  13. Berestetskiy AO (2008) A review of fungal phytotoxins: from basic studies to practical use. Appl Biochem Microbiol 44:453–465CrossRefGoogle Scholar
  14. Boch J, Joardar V, Gao L, Robertson TL, Lim M, Kunkel BN (2002) Identification of Pseudomonas syringae genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44:73–88PubMedCrossRefGoogle Scholar
  15. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bolton MD, Thomma BP, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7:1–16PubMedCrossRefGoogle Scholar
  17. Bos JI, Kanneganti TD, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PR, Kamoun S (2006) The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 48:165–176PubMedCrossRefGoogle Scholar
  18. Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R (2009) Ustilago maydis as a pathogen. Annu Rev Phytopathol 47:423–445PubMedCrossRefGoogle Scholar
  19. Brodhun F, Cristobal-Sarramian A, Zabel S, Newie J, Hamberg M, Feussner I (2013) An iron 13S-lipoxygenase with an a-linolenic acid specific hydroperoxidase activity from Fusarium oxysporum. PLoS One 8:e64919PubMedPubMedCentralCrossRefGoogle Scholar
  20. Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defenses in Arabidopsis thaliana. Mol Plant Pathol 6:629–639PubMedCrossRefGoogle Scholar
  21. Büttner D, Bonas U (2006) Who comes first? How plant pathogenic bacteria orchestrate type III secretion. Curr Opin Microbiol 9:193–200PubMedCrossRefGoogle Scholar
  22. Chang JH, Urbach JM, Law TF, Arnold LW, Hu A, Gombar S et al (2005) A high-throughput, near saturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci U S A 102:2549–2554PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cheng Q, Wang H, Xu B, Zhu S, Hu L, Huang M (2014) Discovery of a novel small secreted protein family with conserved N-terminal IGY motif in Dikarya fungi. BMC Genomics 15:1151PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cho Y (2015) How the necrotrophic fungus Alternaria brassicicola kills plant cells remains an enigma. Eukaryot Cell 14:335–344PubMedPubMedCentralCrossRefGoogle Scholar
  25. Collmer A, Bauer DW (1994) Erwinia chrysanthemi and Pseudomonas syringae: plant pathogens trafficking in virulence proteins. Curr Top Microbiol Immunol 192:43–78PubMedGoogle Scholar
  26. Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR (2002) Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol 10:462–469PubMedCrossRefGoogle Scholar
  27. Cornelis GR, Van Gijsegem F (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54:735–774PubMedCrossRefGoogle Scholar
  28. Corsaro MM, Evidente A, Lanzetta R, Lavermicocca P, Molinaro A (2001) Structure determination of the phytotoxic mannan exopysaccharide from Pseudomonas syringae pv. ciccaronei. Carbohydr Res 330:6208–6215CrossRefGoogle Scholar
  29. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y et al (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955PubMedCrossRefGoogle Scholar
  30. Denny TP (1995) Involvement of bacterial polysaccharide in plant pathogenesis. Annu Rev Phytopathol 33:173–197PubMedCrossRefGoogle Scholar
  31. Desjardins AE, McCormick SP, Appell M (2007) Structure−activity relationships of trichothecene toxins in an Arabidopsis thaliana leaf assay. J Agric Food Chem 55:6487–6492PubMedCrossRefGoogle Scholar
  32. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M et al (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci U S A 100:8024–8029PubMedPubMedCentralCrossRefGoogle Scholar
  33. Di X, Takken FLW, Tintor N (2016) How phytohormones shape interactions between plants and the soil-borne fungus Fusarium oxysporum. Front Plant Sci 7:170. https://doi.org/10.3389/fpls.2016.00170 PubMedPubMedCentralGoogle Scholar
  34. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V et al (2011) Metabolic priming by a secreted fungal effector. Nature 478:395–398PubMedCrossRefGoogle Scholar
  35. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant pathogen interactions. Nat Rev Genet 11:539–548PubMedCrossRefGoogle Scholar
  36. Dodds PN, Rafiqi M, Gan PHP, Hardham AR, Jones DA, Ellis JG (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance. New Phytol 183:993–1000PubMedCrossRefGoogle Scholar
  37. Doehlemann G, van der Linde K, Amann D, Schwammbach D, Hof A, Mohanty A et al (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5:e1000290PubMedPubMedCentralCrossRefGoogle Scholar
  38. Dou D, Kale SD, Wang X, Chen Y, Wang Q, Wang X, Jiang RHY, Arredondo FD, Anderson R, Thakur P, McDowell J, Wang Y, Tyler BM (2008) Carboxy-terminal motifs common to many oomycete RXLR effectors are required for avirulence and suppression of BAX-mediated programmed cell death by Phytophthora sojae effector Avr1b. Plant Cell 20:118–1133Google Scholar
  39. Evangelisti E, Govetto B, Minet-Kebdani N, Kuhn ML, Attard A, Ponchet M, Panabières F, Gourgues M (2013) The Phytophthora parasitica RXLR effector penetration-specific effector 1 favours Arabidopsis thaliana infection by interfering with auxin physiology. New Phytol 199:476–489PubMedCrossRefGoogle Scholar
  40. Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR (2007) The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 8:677–700PubMedCrossRefGoogle Scholar
  41. Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296CrossRefGoogle Scholar
  42. Glazebrook J (2005) Contrasting mechanisms of defence against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227PubMedCrossRefGoogle Scholar
  43. Göhre V, Robatzek S (2009) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215CrossRefGoogle Scholar
  44. Gross DC (1991) Molecular and genetic analysis of toxin production by pathovars of Pseudomonas syringae. Annu Rev Phytopathol 29:247–278CrossRefGoogle Scholar
  45. Guimarães RL, Stotz HU (2004) Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol 136:3703–3711PubMedPubMedCentralCrossRefGoogle Scholar
  46. Haas BJ, Kamoun S, Zody MC, Jiang RH et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398PubMedCrossRefGoogle Scholar
  47. Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95:641–655CrossRefGoogle Scholar
  48. Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Ann Bot 80:713–720CrossRefGoogle Scholar
  49. Heath MC (1998) Apoptosis, programmed cell death and the hypersensitive response. Eur J Plant Pathol 104:117–124CrossRefGoogle Scholar
  50. Heath MC (2000a) Nonhost resistance and non-specific plant defences. Curr Opin Plant Biol 3:315–319PubMedCrossRefGoogle Scholar
  51. Heath MC (2000b) Hypersensitive response-related death. Plant Mol Biol 44:321–334PubMedCrossRefGoogle Scholar
  52. Heath MC (2002) Cellular interactions between biotrophic fungal pathogens and host or nonhost plants. Can J Plant Pathol 24:259–264CrossRefGoogle Scholar
  53. Hemetsberger C, Mueller AN, Matei A, Herrberger C, Hensel G, Kumlehn J, Mishra B, Sharma R, Thines M, Hückelhoven R, Doehlemann G (2015) The fungal core effector Pep1 is conserved across smuts of dicots and monocots. New Phytol 206:1116–1126PubMedCrossRefGoogle Scholar
  54. Horbach R, Navarro-Quesada AR, Knogge W et al (2011) When and how to kill a plant cell: infection strategies of plant pathogenic fungi. J Plant Physiol 168:51–62PubMedCrossRefGoogle Scholar
  55. Howlett BJ (2006) Secondary metabolite toxins and nutrition of plant pathogenic fungi. Curr Opin Plant Biol 9:371–375PubMedCrossRefGoogle Scholar
  56. Hückelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45:101–127PubMedCrossRefGoogle Scholar
  57. Idnurm A, Howlett BJ (2001) Pathogenicity genes of phytopathogenic fungi. Mol Plant Pathol 2:241–255PubMedCrossRefGoogle Scholar
  58. Inomata M, Hirai N, Yoshida R, Ohigashi H (2004) The biosynthetic pathway to abscisic acid via ionylideneethane in the fungus Botrytis cinerea. Phytochemistry 65:2667–2678PubMedCrossRefGoogle Scholar
  59. Jiang RHY, Tripathy S, Govers F, Tyler BM (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc Natl Acad Sci U S A 105:4874–4879PubMedPubMedCentralCrossRefGoogle Scholar
  60. Jin Q, Thilmony R, Zwiesler-Vollick J, He SY (2003) Type III protein secretion in Pseudomonas syringae. Microbes Infect 5:301–310PubMedCrossRefGoogle Scholar
  61. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  62. Kaffarnik FA, Jones AM, Rathjen JP, Peck SC (2009) Effector proteins of the bacterial pathogen Pseudomonas syringae alter the extracellular proteome of the host plant, Arabidopsis thaliana. Mol Cell Proteomics 8:145–156PubMedCrossRefGoogle Scholar
  63. Kahmann R, Basse C (2001) Fungal gene expression during pathogenesis-related development and host plant colonization. Curr Opin Microbiol 4:374–380PubMedCrossRefGoogle Scholar
  64. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N et al (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A 103:11086–11091PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kale SD, Gu B, Capelluto DGS, Dou D, Feldman E et al (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–295PubMedCrossRefGoogle Scholar
  66. Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ et al (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101PubMedCrossRefGoogle Scholar
  67. Kars I, McCalman M, Wagemakers L, van Kan JAL (2005) Functional analysis of Botrytis cinerea pectin methylesterase genes by PCR-based targeted mutagenesis: Bcpme1 and Bcpme2 are dispensable for virulence of strain B05.10. Mol Plant Pathol 6:641–652PubMedCrossRefGoogle Scholar
  68. Kazan K, Lyons R (2014) Intervention of phytohormone pathways by pathogen effectors. Plant Cell 26:2285–2309PubMedPubMedCentralCrossRefGoogle Scholar
  69. Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–463PubMedCrossRefGoogle Scholar
  70. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, Czymmek K et al (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388–1403PubMedPubMedCentralCrossRefGoogle Scholar
  71. Kim K, Jeon J, Choi J, Cheong K, Song H, Choi G, Kang S, Lee Y (2016) Kingdom-wide analysis of fungal small secreted proteins (SSPs) reveals their potential role in host association. Front Plant Sci 7:186. https://doi.org/10.3389/fpls.2016.00186 PubMedPubMedCentralGoogle Scholar
  72. Koeck M, Hardham AR, Dodds PN (2011) The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell Microbiol 13:1849–1857PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kraepiel Y, Barny M (2016) Gram-negative phytopathogenic bacteria, all hemibiotrophs after all? Mol Plant Pathol 17:313–316PubMedCrossRefGoogle Scholar
  74. Laluk K, Mengiste T (2010) Necrotroph attacks on plants: wanton destruction or covert extortion? In: The Arabidopsis book. The American Society of Plant Biologists, Rockville, pp 1–34Google Scholar
  75. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275PubMedCrossRefGoogle Scholar
  76. Lee S-J, Rose JK (2010) Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins. Plant Signal Behav 5:769–772PubMedPubMedCentralCrossRefGoogle Scholar
  77. Liao C-H, Hung HY, Chatterjee AK (1988) An extracellular pectate lyase is the pathogenicity factor of the soft-rotting bacterium Pseudomonas viridiflava. Mol Plant-Microbe Interact 1:199–206CrossRefGoogle Scholar
  78. Lindgren PB, Peet RC, Panopoulos NJ (1986) Gene cluster of Pseudomonas syringae pv.phaseolicola” controls pathogenicity of bean plants and hypersensitivity on nonhost plants. J Bacteriol 168:512–522PubMedPubMedCentralCrossRefGoogle Scholar
  79. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, Humphris S, Burr T, Takle G, Brurberg MB, Birch PR et al (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4:e1000093–e1000010PubMedPubMedCentralCrossRefGoogle Scholar
  80. Liu T, Ye W, Ru Y, Yang X, Gu B, Tao K et al (2011) Two host cytoplasmic effectors are required for pathogenesis of Phytophthora sojae by suppression of host defenses. Plant Physiol 155:490–501PubMedCrossRefGoogle Scholar
  81. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, Devera ME, Liang X, Tör M, Billiar T (2007) The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220:60–81PubMedCrossRefGoogle Scholar
  82. Mattoo S, Lee YM, Dixon JE (2007) Interactions of bacterial effector proteins with host proteins. Curr Opin Immunol 19:392–401PubMedCrossRefGoogle Scholar
  83. Matzinger P (2007) Friendly and dangerous signals: is the tissue in control? Nat Immunol 8:11–13PubMedCrossRefGoogle Scholar
  84. Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 7:352–356PubMedCrossRefGoogle Scholar
  85. Mendgen K, Hahn M (2004) Plant infection and the establishment of fungal biotrophy. Curr Opin Plant Biol 7:356–364CrossRefGoogle Scholar
  86. Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267–294PubMedCrossRefGoogle Scholar
  87. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K et al (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104:19613–19618PubMedPubMedCentralCrossRefGoogle Scholar
  88. Mobius N, Hertweck C (2009) Fungal phytotoxins as mediators of virulence. Curr Opin Plant Biol 12:390–398PubMedCrossRefGoogle Scholar
  89. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1–4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21:1273–1290PubMedPubMedCentralCrossRefGoogle Scholar
  90. Muller O, Schreier PH, Uhrig JF (2008) Identification and characterization of secreted and pathogenesis related proteins in Ustilago maydis. Mol Gen Genomics 279:27–39CrossRefGoogle Scholar
  91. Niepold F, Anderson D, Mills D (1985) Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae. Proc Natl Acad Sci U S A 82:406–410PubMedPubMedCentralCrossRefGoogle Scholar
  92. Noel L, Thieme F, Nennstie D, Bonas U (2001) cDNA-AFLP analysis unravels a genome-wide hrpG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol Microbiol 41:1271–1281PubMedCrossRefGoogle Scholar
  93. Oliver RP, Ipcho SVS (2004) Arabidopsis pathology breathes new life into necrotrophs vs.- biotrophs classification of fungal pathogens. Mol Plant Pathol 5:347–352PubMedCrossRefGoogle Scholar
  94. Pedras MS, Ahiahonu PW (2004) Phytotoxin production and phytoalexin elicitation by the phytopathogenic fungus Sclerotinia sclerotiorum. J Chem Ecol 30:2163–2179PubMedCrossRefGoogle Scholar
  95. Pemberton CL, Salmond GPC (2004) The Nep1-like proteins – a growing family of microbial elicitors of plant necrosis. Mol Plant Pathol 5:353–359PubMedCrossRefGoogle Scholar
  96. Penn CD, Daniel SL (2013) Salicylate degradation by the fungal plant pathogen Sclerotinia sclerotiorum. Curr Microbiol 67:218–225PubMedCrossRefGoogle Scholar
  97. Pennington HG, Gheorghe DM, Damerum A, Pliego C, Spanu PD, Cramer R, Bindschedler LV (2016) Interactions between the powdery mildew effector BEC1054 and barley proteins identify candidate host targets. J Proteome Res 15:826–839PubMedCrossRefGoogle Scholar
  98. Perombelon MCM, Kelman A (1980) Ecology of the soft rot Erwinias. Annu Rev Phytopathol 18:361–387CrossRefGoogle Scholar
  99. Prell HH, Day PR (2001) Plant–fungal pathogen interaction: a classical and molecular view. Springer, BerlinCrossRefGoogle Scholar
  100. Prins TW, Tudzynski P, Tiedemann AV, Tudzynski B, ten Have A, Hansen ME, Tenberge K, van Kan JAL (2000) Infection strategies of Botrytis cinerea and related necrotrophic pathogens. In: Kronstad JW (ed) Fungal pathology. Kluwer Academic Publishers, Dordrecht, pp 33–64CrossRefGoogle Scholar
  101. Redkar A, Hoser R, Schilling L, Zechmann B, Krzymowska M, Walbot V, Doehlemann G (2015) A secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors. Plant Cell 27:1332–1351PubMedPubMedCentralCrossRefGoogle Scholar
  102. Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615PubMedPubMedCentralCrossRefGoogle Scholar
  103. Sánchez-Vallet A, Saleem-Batcha R, Kombrink A, Hansen G, Valkenburg DJ, Thomma BP, Mesters JR (2013) Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. elife 2:e00790PubMedPubMedCentralCrossRefGoogle Scholar
  104. Schulze-Lefert P (2004) Knocking in the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall. Curr Opin Plant Biol 7:377–383PubMedCrossRefGoogle Scholar
  105. Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41:641–667PubMedCrossRefGoogle Scholar
  106. Shames SR, Finlay BB (2012) Bacterial effector interplay: a new way to view effector function. Trends Microbiol 20:214–219PubMedCrossRefGoogle Scholar
  107. Shi L, Bielawski J, Mu J, Dong H, Teng C, Zhang J, Yang X, Tomishige N, Hanada K, Hannun YA, Zuo J (2007) Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res 17:1030–1040PubMedCrossRefGoogle Scholar
  108. Silverstein KA, Graham MA, Paape TD, VandenBosch KA (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 138:600–610PubMedPubMedCentralCrossRefGoogle Scholar
  109. Singh R, Dangol S, Chen Y, Choi J, Cho YS, Lee JE, Choi MO, Jwa NS (2016) Magnaporthe oryzae effector AVR-Pii helps to establish compatibility by inhibition of the rice NADP-malic enzyme resulting in disruption of oxidative burst and host innate immunity. Mol Cell 39:426–438CrossRefGoogle Scholar
  110. Snoeijers SS, Pérez-García A, Joosten MHAJ, De Wit PJGM (2000) The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. Eur J Plant Pathol 106:493–506CrossRefGoogle Scholar
  111. Stam R, Jupe J, Howden AJ, Morris JA, Boevink PC, Hedley PE, Huitema E (2013) Identification and characterization CRN effectors in Phytophthora capsici shows modularity and functional diversity. PLoS One 8:e59517PubMedPubMedCentralCrossRefGoogle Scholar
  112. Stergiopoulos I, de Wit PJGM (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263PubMedCrossRefGoogle Scholar
  113. Stergiopoulos I, van den Burg HA, Ökmen B, Beenen HG, van Liere S, Kema GHJ, de Wit PJGM (2010) Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc Natl Acad Sci U S A 107:7610–7615PubMedPubMedCentralCrossRefGoogle Scholar
  114. Stergiopoulos I, Collemare J, Mehrabi R, De Wit PJ (2013) Phytotoxic secondary metabolites and peptides produced by plant pathogenic Dothideomycete fungi. FEMS Microbiol Rev 37:67–93PubMedCrossRefGoogle Scholar
  115. Stone JK (2001) Necrotroph. In: Maloy OC, Murray TD (eds) Encyclopedia of plant pathology. Wiley, New York, pp 676–677Google Scholar
  116. Thomma B, Van Esse HP, Crous PW, De Wit P (2005) Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Mol Plant Pathol 6:379–393PubMedCrossRefGoogle Scholar
  117. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403PubMedCrossRefGoogle Scholar
  118. Torto TA, Li S, Styer A, Huitema E, Testa A, Gow NA, van West P, Kamoun S (2003) EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Res 13:1675–1685PubMedPubMedCentralCrossRefGoogle Scholar
  119. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H (2013) Host selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37:44–66PubMedCrossRefGoogle Scholar
  120. Tudzynski P, Sharon A (2003) Fungal pathogenicity genes. In: Arora DDK, Khachatourians GG (eds) Applied mycology and biotechnology vol. 3: fungal genomics. Elsevier, Berlin, pp 187–212Google Scholar
  121. Tyler BM (2009) Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell Microbiol 11:13–20PubMedCrossRefGoogle Scholar
  122. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL (2007) The phytotoxin coronatine contribute to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol Plant-Microbe Interact 20:955–965PubMedCrossRefGoogle Scholar
  123. van Damme M, Bozkurt TO, Cakir C, Schornack S, Sklenar J et al (2012) The Irish potato famine pathogen Phytophthora infestans translocates the CRN8 kinase into host plant cells. PLoS Pathog 8:e1002875PubMedPubMedCentralCrossRefGoogle Scholar
  124. van Esse HP, Bolton MD, Stergiopoulos L, de Wit P, Thomma B (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interac 20:1092–1101CrossRefGoogle Scholar
  125. van Esse HP, van’t Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, Boeren S et al (2008) The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20:1948–1963PubMedPubMedCentralCrossRefGoogle Scholar
  126. Van Gijsegem F, Genin S, Boucher C (1993) Evolutionary conservation of pathogenicity determinants among plant and animal pathogenic bacteria. Trends Microbiol 1:175–180PubMedCrossRefGoogle Scholar
  127. Van Kan JA (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247–253PubMedCrossRefGoogle Scholar
  128. van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162PubMedCrossRefGoogle Scholar
  129. Vleeshouwers VGAA, Oliver RP (2014) Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol Plant-Microbe Interact 27:196–206PubMedCrossRefGoogle Scholar
  130. Vleeshouwers VGAA, Rietman H, Krenek P, Champouret N, Young C, Oh S-K, Wang M, Bouwmeester K, Vosman B, Visser R (2008) Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS One 3:e2875PubMedPubMedCentralCrossRefGoogle Scholar
  131. Vleeshouwers VGAA, Finkers R, Budding DJ, Visser M, Jacobs MMJ, van Berloo R, Pel M, Champouret N, Bakker E, Krenek P, Rietman H, Huigen DJ, Hoekstra R, Goverse A, Vosman B, Jacobsen E, Visser RGF (2011) SolRgene: an online database to explore disease resistance genes in tuber-bearing Solanum species. BMC Plant Biol 11:116PubMedPubMedCentralCrossRefGoogle Scholar
  132. Walton JD (1996) Host-selective toxins: agents of compatibility. Plant Cell 8:1723–1733PubMedPubMedCentralCrossRefGoogle Scholar
  133. Wang X, Jiang N, Liu J, Liu W, Wang G-L (2014) The role of effectors and host immunity in plant–necrotrophic fungal interactions. Virulence 5:722–732PubMedPubMedCentralCrossRefGoogle Scholar
  134. Wang M, Weiberg A, Jin H (2015) Pathogen small RNAs: a new class of effectors for pathogen attacks. Mol Plant Pathol 16:219–223PubMedCrossRefGoogle Scholar
  135. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123PubMedPubMedCentralCrossRefGoogle Scholar
  136. Weiberg A, Wang M, Bellinger M, Jin H (2014) Small RNAs: a new paradigm in plant–microbe interactions. Annu Rev Phytopathol 52:495–516PubMedCrossRefGoogle Scholar
  137. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG et al (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115–119PubMedCrossRefGoogle Scholar
  138. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404PubMedCrossRefGoogle Scholar
  139. Willment JA, Brown GD (2007) C-type lectin receptors in antifungal immunity. Trends Microbiol 16:27–32PubMedCrossRefGoogle Scholar
  140. Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro-Garcia A, Ammar R, Staskawicz BJ, Kamoun S (2007) Adaptive evolution has targeted the c-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19:2349–2369PubMedPubMedCentralCrossRefGoogle Scholar
  141. Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285PubMedCrossRefGoogle Scholar
  142. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W et al (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80PubMedCrossRefGoogle Scholar
  143. Yang Y, Gabriel DW (1995) Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. Mol Plant-Microbe Interact 8:627–631PubMedCrossRefGoogle Scholar
  144. Zhu W, Wei W, Fu Y, Cheng J, Xie J, Li G, Yi X, Kang Z, Dickman MB, Jiang D (2013) A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS One 8:e53901PubMedPubMedCentralCrossRefGoogle Scholar
  145. Zipfel C (2008) Pattern recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16PubMedCrossRefGoogle Scholar
  146. Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420PubMedCrossRefGoogle Scholar
  147. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767PubMedCrossRefGoogle Scholar
  148. Zong N, Xiang T, Zou Y, Chai J, Zhou J-M (2008) Blocking and triggering of plant immunity by Pseudomonas syringae effector AvrPto. Plant Signal Behav 3:583–585PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zwiesler-Vollick J, Plovanich-Jones AE, Nomura K, Brandyopadhyay S, Joardar V et al (2002) Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol Microbiol 45:1207–1218PubMedCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of BotanyGargi College, University of DelhiNew DelhiIndia

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