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Plant Ecology pp 257-299 | Cite as

Biotic Stress

  • Ernst-Detlef Schulze
  • Erwin Beck
  • Nina Buchmann
  • Stephan Clemens
  • Klaus Müller-Hohenstein
  • Michael Scherer-Lorenzen
Chapter

Abstract

This chapter explores the reasons why plants rarely succumb to pathogens or herbivores. Even though plants are constantly under attack from viruses, bacteria, fungi, oomycetes or nematodes, the occurrence of disease is the exception. Similarly, plant defences effectively limit the damage caused by chewing or sucking insects. After a discussion of pathogenicity determinants and preformed defences, this chapter describes a concept unifying the inducible local immune responses to non-adapted and adapted pathogens. Perception and signal transduction events are explored. Next, systemic resistance is explained—that is, the activation of defence mechanisms in tissues distant from the site of a pathogen attack. Also covered is gene silencing as a defence against phytopathogenic viruses. Like pathogen defences, herbivore defences are both constitutive and inducible. In addition, they can be not only direct but also indirect, meaning that the enemies of herbivores are attracted and recruited for defence by the plant. Recognition of herbivore attack and the ensuing chain of signalling events are described. Plant defences are often chemical—that is, based on complex mixtures of bioactive secondary metabolites. The synthesis of glucosinolates is elaborated on to illustrate how herbivory acts as a driver of genetic diversity. Finally, parasitic plants and allelopathy are discussed as two additional forms of biotic stress.

References

  1. Acevedo FE, Rivera-Vega LJ, Chung SH et al (2015) Cues from chewing insects—the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86PubMedCrossRefGoogle Scholar
  2. Agrawal AA, Hastings AP, Johnson MTJ et al (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116PubMedCrossRefGoogle Scholar
  3. Agrawal AA, Konno K (2009) Latex: a model for understanding mechanisms, ecology, and evolution of plant defence against herbivory. Annu Rev Ecol Evol Syst 40:311–331CrossRefGoogle Scholar
  4. Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defence against pathogens. Trends Plant Sci 17:73–90PubMedCrossRefGoogle Scholar
  5. Alborn HT, Turlings TCJ, Jones TH et al (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949CrossRefGoogle Scholar
  6. Arimura G, Ozawa R, Shimoda T et al (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515PubMedCrossRefGoogle Scholar
  7. Bär W, Pfeifer P, Dettner K (2000) Biochemische Interaktionen zwischen Kalanchoe-Pflanzen. Biologie in unserer Zeit 30:228–234CrossRefGoogle Scholar
  8. Barbehenn RV, Peter Constabel C (2011) Tannins in plant–herbivore interactions. Phytochemistry 72:1551–1565PubMedCrossRefGoogle Scholar
  9. Bartels S, Boller T (2015) Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. J Exp Bot 66:5183–5193PubMedCrossRefGoogle Scholar
  10. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363PubMedCrossRefGoogle Scholar
  11. Bednarek P, Osbourn A (2009) Plant–microbe interactions: chemical diversity in plant defence. Science 324:746–748PubMedCrossRefGoogle Scholar
  12. Benderoth M, Pfalz M, Kroymann J (2009) Methylthioalkylmalate synthases: genetics, ecology and evolution. Phytochem Rev 8:255–268CrossRefGoogle Scholar
  13. 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 60:379–406PubMedCrossRefGoogle Scholar
  14. Bouarab K, Melton R, Peart J et al (2002) A saponin-detoxifying enzyme mediates suppression of plant defences. Nature 418:889–892PubMedCrossRefGoogle Scholar
  15. Browse J (2009) Jasmonate passes muster: a receptor and targets for the defence hormone. Annu Rev Plant Biol 60:183–205PubMedCrossRefGoogle Scholar
  16. Buchanan B, Gruissem W, Jones R (2015) Biochemistry and molecular biology of plants, 2nd edn. Wiley, ChichesterGoogle Scholar
  17. Campos ML, Kang J-H, Howe GA (2014) Jasmonate-triggered plant immunity. J Chem Ecol 40:657–675PubMedPubMedCentralCrossRefGoogle Scholar
  18. Caplan A, Herrera-Estrella L, Inzé D et al (1983) Introduction of genetic material into plant cells. Science 222:815–821PubMedCrossRefGoogle Scholar
  19. Cappa JJ, Pilon-Smits EAH (2013) Evolutionary aspects of elemental hyperaccumulation. Planta 239(2):267–275PubMedCrossRefGoogle Scholar
  20. Choi J, Tanaka K, Cao Y et al (2014) Identification of a plant receptor for extracellular ATP. Science 343:290–294PubMedCrossRefGoogle Scholar
  21. Conn CE, Bythell-Douglas R, Neumann D et al (2015) Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349:540–543PubMedCrossRefGoogle Scholar
  22. Conrath U, Kauss H (2000) Das “Immunsystem” der Pflanze. Biologie in unserer Zeit 30:202–208CrossRefGoogle Scholar
  23. Crous PW, Hawksworth DL, Wingfield MJ (2015) Identifying and naming plant-pathogenic fungi: past, present, and future. Annu Rev Phytopathol 53:247–267PubMedCrossRefGoogle Scholar
  24. Davis EL, Mitchum MG (2005) Nematodes. Sophisticated parasites of legumes. Plant Physiol 137:1182–1188PubMedPubMedCentralCrossRefGoogle Scholar
  25. de Jonge R, van Esse H, Kombrink A et al (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955PubMedCrossRefGoogle Scholar
  26. Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847PubMedCrossRefGoogle Scholar
  27. Djamei A, Schipper K, Rabe F et al (2011) Metabolic priming by a secreted fungal effector. Nature 478:395–398PubMedCrossRefGoogle Scholar
  28. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548PubMedCrossRefGoogle Scholar
  29. Dou D, Zhou J-M (2012) Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–495PubMedCrossRefGoogle Scholar
  30. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci U S A 101:1781–1785PubMedPubMedCentralCrossRefGoogle Scholar
  31. Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296. https://doi.org/10.1146/annurev.py.09.090171.001423 CrossRefGoogle Scholar
  32. Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defence. Annu Rev Plant Biol 64:839–863PubMedCrossRefGoogle Scholar
  33. Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defence mechanism against insects. Science 175:776–777PubMedCrossRefGoogle Scholar
  34. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952PubMedCrossRefGoogle Scholar
  35. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61PubMedCrossRefGoogle Scholar
  36. Hopkins RJ, Van Dam NM, Van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83PubMedCrossRefGoogle Scholar
  37. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefGoogle Scholar
  38. Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defence against insect attack. Plant Cell 8:2067–2077PubMedPubMedCentralGoogle Scholar
  39. Huang T, Jander G, de Vos M (2011) Non-protein amino acids in plant defence against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72:1531–1537PubMedCrossRefGoogle Scholar
  40. Incarbone M, Dunoyer P (2013) RNA silencing and its suppression: novel insights from in planta analyses. Trends Plant Sci 18:382–392PubMedCrossRefGoogle Scholar
  41. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  42. Jung HW, Tschaplinski TJ, Wang L et al (2009) Priming in systemic plant immunity. Science 324:89–91PubMedCrossRefGoogle Scholar
  43. Kallenbach M, Bonaventure G, Gilardoni PA et al (2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations. Proc Natl Acad Sci U S A 109:E1548–E1557PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kay S, Bonas U (2009) How Xanthomonas type III effectors manipulate the host plant. Curr Opin Microbiol 12:37–43PubMedCrossRefGoogle Scholar
  45. Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defences and insect populations. Science 305:665–668PubMedCrossRefGoogle Scholar
  46. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202PubMedCrossRefGoogle Scholar
  47. Konno K, Ono H, Nakamura M et al (2006) Mulberry latex rich in antidiabetic sugar-mimic alkaloids forces dieting on caterpillars. Proc Natl Acad Sci U S A 103:1337–1341PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jürgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451(7180):835–840. https://doi.org/10.1038/nature06545 PubMedCrossRefGoogle Scholar
  49. Lozano-Torres JL, Wilbers RHP, Gawronski P et al (2012) Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc Natl Acad Sci U S A 109:10119–10124PubMedPubMedCentralCrossRefGoogle Scholar
  50. Melotto M, Underwood W, Koczan J et al (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  51. Mithöfer A, Boland W (2012) Plant defence against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450PubMedCrossRefGoogle Scholar
  52. Mousavi SAR, Chauvin A, Pascaud F et al (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422–426PubMedCrossRefGoogle Scholar
  53. Mukhtar MS, Carvunis A-R, Dreze M et al (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601PubMedPubMedCentralCrossRefGoogle Scholar
  54. Návarová H, Bernsdorff F, Döring A-C, Zeier J (2012) Pipecolic acid, an endogenous mediator of defence amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123–5141PubMedPubMedCentralCrossRefGoogle Scholar
  55. Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266PubMedCrossRefGoogle Scholar
  56. Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–897PubMedCrossRefGoogle Scholar
  57. Periyannan S, Moore J, Ayliffe M et al (2013) The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341:786–788PubMedCrossRefGoogle Scholar
  58. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811PubMedPubMedCentralCrossRefGoogle Scholar
  59. Römer P, Hahn S, Jordan T et al (2007) Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:645–648PubMedCrossRefGoogle Scholar
  60. Saintenac C, Zhang W, Salcedo A et al (2013) Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science 341:783–786PubMedPubMedCentralCrossRefGoogle Scholar
  61. Schnee C, Köllner TG, Held M et al (2006) The products of a single maize sesquiterpene synthase form a volatile defence signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci U S A 103:1129–1134CrossRefGoogle Scholar
  62. Schwach F, Vaistij FE, Jones L, Baulcombe DC (2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–1852PubMedPubMedCentralCrossRefGoogle Scholar
  63. Snyder BA, Nicholson RL (1990) Synthesis of phytoalexins in Sorghum as a site-specific response to fungal ingress. Science 248:1637–1639PubMedCrossRefGoogle Scholar
  64. Soosaar JLM, Burch-Smith TM, Dinesh-Kumar SP (2005) Mechanisms of plant resistance to viruses. Nat Rev Micro 3:789–798CrossRefGoogle Scholar
  65. Stinson KA, Campbell SA, Powell JR et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:e140PubMedPubMedCentralCrossRefGoogle Scholar
  66. Tsuda K, Somssich IE (2015) Transcriptional networks in plant immunity. New Phytol 206:932–947PubMedCrossRefGoogle Scholar
  67. Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253PubMedCrossRefGoogle Scholar
  68. Uknes S, Mauch-Mani B, Moyer M et al (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656PubMedPubMedCentralGoogle Scholar
  69. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defence against herbivores. Curr Opin Plant Biol 12:479–485PubMedCrossRefGoogle Scholar
  70. Weir TL, Park S-W, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479PubMedCrossRefGoogle Scholar
  71. Westwood JH, Yoder JI, Timko MP, dePamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235PubMedCrossRefGoogle Scholar
  72. Whitham TG, Bailey JK, Schweitzer JA et al (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523PubMedCrossRefGoogle Scholar
  73. Whitham TG, Difazio SP, Schweitzer JA et al (2008) Perspective—extending genomics to natural communities and ecosystems. Science 320:492–495PubMedCrossRefGoogle Scholar
  74. Wu J, Baldwin I (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44(44):1–24PubMedCrossRefGoogle Scholar
  75. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J et al (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80PubMedCrossRefGoogle Scholar
  76. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117PubMedCrossRefGoogle Scholar
  77. Yoshida S, Cui S, Ichihashi Y, Shirasu K (2016) The haustorium, a specialized invasive organ in parasitic plants. In: Merchant SS (ed) Annual review of plant biology, vol 67. Annual Reviews, Palo Alto, pp 643–667PubMedCrossRefGoogle Scholar
  78. Yoshida S, Shirasu K (2012) Plants that attack plants: molecular elucidation of plant parasitism. Curr Opin Plant Biol 15:708–713PubMedCrossRefGoogle Scholar
  79. Züst T, Heichinger C, Grossniklaus U et al (2012) Natural enemies drive geographic variation in plant defences. Science 338:116–119PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Ernst-Detlef Schulze
    • 1
  • Erwin Beck
    • 2
  • Nina Buchmann
    • 3
  • Stephan Clemens
    • 2
  • Klaus Müller-Hohenstein
    • 4
  • Michael Scherer-Lorenzen
    • 5
  1. 1.Max Planck Institute for BiogeochemistryJenaGermany
  2. 2.Department of Plant PhysiologyUniversity of BayreuthBayreuthGermany
  3. 3.Department of Environmental Systems ScienceETH ZurichZurichSwitzerland
  4. 4.Department of BiogeographyUniversity of BayreuthBayreuthGermany
  5. 5.Chair of Geobotany, Faculty of BiologyUniversity of FreiburgFreiburgGermany

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