pp 1-15 | Cite as

The Role of the Shikimate and the Phenylpropanoid Pathways in Root-Knot Nematode Infection

  • Noureddine Hamamouch
  • Essarioui Adil
Part of the Progress in Botany book series


Plant-parasitic nematodes are costly burdens to crop production because of their intricate relationship with the host plants, wide host range, and the level of postinfection damage. Limitations on the use of chemical pesticides have brought increasing attention in studies on alternative methods for nematode control. Among the strategies of nonchemical nematode management is the identification and implementation of host resistance. Plant resistance involves the production of morphological barriers to prevent pathogens from entry into host cells or may include the synthesis of certain biochemicals that interfere with the subsequent development of pathogens. Among plant biochemical responses to infection is the synthesis of important and diverse compounds from the shikimate and the phenylpropanoid pathways. Many of these compounds are bioactive, playing important roles in defense against biotic and abiotic tresses. This review gathers information from across a large body of studies focusing on the role of the shikimate and the phenylpropanoid pathways in plant-nematode interactions.


Parasitic nematodes Host resistance Shikimate pathway Phenylpropanoid pathway 


  1. Alkharouf NW, Klink VP, Chouikha IB, Beard HS, MacDonald MH, Meyer S, Knap HT, Khan R, Matthews BF (2006) Time course microarray analyses reveals global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224:838–852Google Scholar
  2. Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, Favery B, Garcia-Casado G, Solano R, Fenoll C, Escobar C (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 61:698–712Google Scholar
  3. Bekal S, Niblack TL, Lambert KN (2003) A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol Plant-Microbe Interact 16:439–449Google Scholar
  4. Bird DM, Kaloshian I (2003) Are roots special? Nematodes have their say. Physiol Mol Plant Pathol 62:115–123Google Scholar
  5. Bohm BA (1998) Introduction to flavonoids. Harwood, AmsterdamGoogle Scholar
  6. Braca A, Bader A, Siciliano T, Morelli I, De Tommasi N (2003) New pyrrolizidine alkaloids and glycosides from Anchusa strigosa. Planta Med 69:835–841Google Scholar
  7. Breuske CH (1980) Phenylalanine ammonia lyase activity in tomato roots infected and resistant to the root-knot nematode, Meloidogyne incognita. Physiol Plant Pathol 16:409–414Google Scholar
  8. Brooker NL, Kuzimichev Y, Laas J, Pavlis L (2007) Evaluation of coumarin derivatives as anti-fungal agents against soil-borne fungal pathogens. Commun Agric Appl Biol Sci 72:785–793Google Scholar
  9. Brooker N, Windorski J, Blumi E (2008) Halogenated coumarins derivatives as novel seed protectants. Commun Agric Appl Biol Sci 73(2):81–89Google Scholar
  10. Caponi P, Saba M, Oplos C, Aissani N, Maxia A, Menkissoglu-Spiroudi U, Casu L, Ntalli N (2015) Nematicidal activity of furanocoumarins from parsley against Meloidogyne spp. Pest Manag Sci 71(8):1099–1105Google Scholar
  11. Chen S, Dickson DW, Hewlett TE (1997) Tannic acid effects on hatching of Heterodera glycines in vitro. J Nematol 29:742–745Google Scholar
  12. Chin S, Behm C, Mathesius U (2018) Functions of flavonoids in plant-nematode interactions. Plan Theory 7(4):85Google Scholar
  13. Christensen AB, Gregersen PL, Schroder J, Collinge DB (1998) A chalcone synthase with an unusual substrate preference is expressed in barley leaves in response to UV light and pathogen attack. Plant Mol Biol 37:849–857Google Scholar
  14. Cook R, Tiller SA, Mizen KA, Edwards R (1995) Isoflavonoid metabolism in resistant and susceptible cultivars of white clover infected with the stem nematode Ditylenchus dipsaci. J Plant Physiol 146:348–354Google Scholar
  15. D’Auria JC, Gershenzon J (2005) The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol 8(3):308–316Google Scholar
  16. D’Errico G, Lois Woo S, Lombardi N, Manganiello G, Roversi PF (2018) Activity of chestnut tannins against the southern root-knot nematode Meloidogyne incognita. Redia 101:53–59Google Scholar
  17. Davis EL, Hussey RS, Baum TJ (2004) Getting to the roots of parasitism by nematodes. Trends Parasitol 20:134–141Google Scholar
  18. Decraemer W, Hunt DJ (2006) Structure and classification. In: Perry RN, Moens M (eds) Plant nematology. CAB International, Wallingford, pp 3–32Google Scholar
  19. Dhakshinamoorthy S, Mariama K, Elsen A, De Waele D (2014) Phenols and lignin are involved in the defence response of banana (Musa) plants to Radopholus similis infection. Nematology 16:565–576Google Scholar
  20. Diaz Napal GN, Defago MT, Valladares GR, Palacios SM (2010) Response of Epilachna paenulata to two flavonoids, pinocembrin and quercetin, in a comparative study. J Chem Ecol 36(8):898–904Google Scholar
  21. Doyle EA, Lambert KN (2003) Meloidogyne javanica chorismate mutase1 alters plant cell development. Mol Plant-Microbe Interact 16:123–131Google Scholar
  22. Edens RM, Anand SC, Bolla RI (1995) Enzymes of the phenylpropanoid pathway in soybean infected with Meloidogyne incognita or Heterodera glycines. J Nematol 27(3):292–303Google Scholar
  23. Faizi S, Fayyaz S, Bano S, Yawar Iqbal E, Lubna Siddiqi H, Naz A (2011) Isolation of nematicidal compounds from Tagetes patula L. yellow flowers: structure–activity relationship studies against cyst nematode Heterodera zeae infective stage larvae. J Agric Food Chem 59:9080–9093Google Scholar
  24. Gao BL, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2003) The parasitome of the phytonematode Heterodera glycines. Mol Plant-Microbe Interact 16:720–726Google Scholar
  25. Gheysen G, Mitchum MG (2009) Molecular insights in the susceptible plant response to nematode infection. Plant Cell 15:45–81Google Scholar
  26. Gheysen G, Mitchum MG (2011) How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol 14:1–7Google Scholar
  27. Giebel J (1973) Phenylalanine and tyrosine ammonia-lyase activities in potato roots and their significance in potato resistance to Heterodera Rostochiensis. Nematologica 19(1):3–6Google Scholar
  28. Goddijn O, Lindsey K, van der Lee F, Klap J, Sijmons P (1993) Differential gene expression in nematode induced feeding structures of transgenic plants harbouring promoter-gus A fusion constructs. Plant J 4:863873Google Scholar
  29. Golinowski W, Grundler FMW, Sobczak M (1996) Changes in the structure of Arabidopsis thaliana during female development of the plant-parasitic nematode Heterodera schachtii. Protoplasma 194:103–116Google Scholar
  30. Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 13:1121–1129Google Scholar
  31. Grundler FMW, Sobczak M, Golinowski W (1998) Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii. Eur J Plant Pathol 104:545–551Google Scholar
  32. Guo Q, Du G, Li Y, Liang C, Wang C, Zhang Y, Li R (2018) Nematotoxin coumarins from Angelica pubescens Maxim. f. biserrata Shan et Yuan roots and their physiological effect so Bursaphelenchus xylophilus. J Nematol 50(4):2018–2045Google Scholar
  33. Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55(6):481–504Google Scholar
  34. Hassan S, Mathesius U (2012) The role of flavonoids in root-rhizosphere signaling: opportunities and challenges for improving plant-microbe interactions. J Exp Bot 63:3429–3444Google Scholar
  35. Hewlett TE, Hewlett EM, Dickson DW (1997) Response of Meloidogyne spp., Heterodera glycines, and Radopholus similis to tannic acid. J Nematol 29:737–741Google Scholar
  36. Hoffmann-Campo CB, Neto JA, de Oliveira MC, Oliveira LJ (2006) Detrimental effect of rutin on Anticarsia gemmatalis Pesqui. Agropec Bras 41:1453–1459Google Scholar
  37. Huang JS, Barker KR (1991) Glyceollin I in soybean-cyst nematode interactions: spatial and temporal distribution in roots of resistant and susceptible soybeans. Plant Physiol 96:1302–1307Google Scholar
  38. Huang G, Dong R, Allen R, Davis EL, Baum TJ, Hussey RS (2005) Two chorismate mutase genes from the root-knot nematode Meloidogyne incognita. Mol Plant Pathol 6:23–30Google Scholar
  39. Hutangura P, Mathesius U, Jones MGK, Rolfe BG (1999) Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Aust J Plant Physiol 26:221–231Google Scholar
  40. Ibrahim H, Hosseini P, Alkharouf N, Hussein E, Gaml El-Din A, Aly M, Matthews BF (2011) Analysis of gene expression in soybean (Glycine max) roots in response to the root knot nematode Meloidogyne incognita using microarrays and KEGG pathways. BMC Genomics 12:220Google Scholar
  41. Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant Microbe Interact 20:293–305Google Scholar
  42. Jakobek L (2015) Interactions of polyphenols with carbohydrates, lipids and proteins. Food Chem 175:556–567Google Scholar
  43. Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette ML, Renou JP, Abbad P, Favery B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44:447–458Google Scholar
  44. Jones MGK (1981) Host cell responses to endoparasitic nematode attack: structure and function of giant cells and syncytia. Ann Appl Biol 97:353–372Google Scholar
  45. Jones JT, Furlanetto C, Bakker E, Banks B, Blok V, Chen Q et al (2003) Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol Plant Pathol 4:43–50Google Scholar
  46. Jones JT, Furlanetto C, Phillips MS (2007) The role of flavonoid produced in response to cyst nematode infection of Arabidopsis thaliana. Nematology 9:671–677Google Scholar
  47. Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961Google Scholar
  48. Karczmarek A, Overmars H, Helder J, Goverse A (2004) Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Mol Plant Pathol 5:343–346Google Scholar
  49. Kennedy MJ, Niblack TL, Krishnan HB (1999) Infection by Heterodera glycines elevates isoflavonoid production and influences soybean nodulation. J Nematol 31:341–347Google Scholar
  50. Kikuchi T, Eves-van den Akker S, Jones JT (2017) Genome evolution of plant-parasitic nematodes. Annu Rev Phytopathol 55:333–354Google Scholar
  51. Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF (2007a) A timecourse comparative microarray analysis of an incompatible and compatible response by Glycine max (soybean) to Heterodera glycines (soybean cyst nematode). Planta 226:1423–1447Google Scholar
  52. Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF (2007b) Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean roots infected by soybean cyst nematode (Heterodera glycines). Planta 226:1389–1409Google Scholar
  53. Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982Google Scholar
  54. Lambert KN, Allen KD, Sussex IM (1999) Cloning and characterization of an esophageal-gland specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol Plant-Microbe Interact 12:328–336Google Scholar
  55. Maistrello L, Vaccari G, Sasanelli N (2010) Effect of chestnut tannins on the root-knot nematode Meloidogyne javanica. Helminthologia 47(1):48–75Google Scholar
  56. McCarter JP (2009) Molecular approaches toward resistance to plant-parasitic nematodes. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Springer, Berlin, pp 239–268Google Scholar
  57. Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T (2006) Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root-knot nematode interactions. New Phytol 170:501–512Google Scholar
  58. Mian IH, Rodriguez-Kabana R (1982a) Organic amendments with high tannin and phenolic contents for control of Meloidogyne arenaria in infested soil. Nematropica 12:221–234Google Scholar
  59. Mian IH, Rodriguez-Kabana R (1982b) Survey of the nematicidal properties of some organic materials available in Alabama as amendments to soil for control of Meloidogyne arenaria. Nematropica 12:205–220Google Scholar
  60. Misra P, Pandey A, Tiwari M, Chandrashekar K, Sidhu OP, Asif MH, Chakrabarty D, Singh PK, Trivedi PK, Nath P et al (2010) Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol 152:2258–2268Google Scholar
  61. Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben M, Davis E (2013) Nematode effector proteins: an emerging paradigm of parasitism. New Phytol 199:879–894Google Scholar
  62. Nax I, Palomares-Rius JE, Blok V, Khan MR, Ali S (2013) In vitro and in planta nematicidal activity of Fumaria parviflora (Fumariaceae) against the southern root-knot nematode Meloidogyne incognita. Plant Pathol 62:943–952Google Scholar
  63. Nicol JM, Turner SJ, Coyne DL, Nijs LD, Hockland S, Maafi ZT (2011) Current nematode threats to world agriculture. In: Genomics and molecular genetics of plant-nematode interactions. Springer, Dordrecht, pp 21–44Google Scholar
  64. Olson MM, Roseland CR (1991) Induction of the coumarins scopoletin and ayapin in sunflower by insect-feeding stress and effects of coumarins on the feeding of sunflower beetle (Coleontara chrysomelidae). Environ Entomol 20:1166–1172Google Scholar
  65. Popeijus H, Blok V, Cardle L, Bakker E, Phillips M, Helder J, Smant G, Jones J (2000) Analysis of genes expressed in second stage juveniles of the potato cyst nematodes Globodera rostochiensis and Globodera pallida using the expressed sequence tag approach. Nematology 2:567–574Google Scholar
  66. Puthoff DP, Nettleton D, Rodermel SR, Baum TJ (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant J 33:911–921Google Scholar
  67. Quentin M, Allasia V, Pegard A, Allais F, Ducrot PH, Favery B, Levis C, Martinet S, Masur C, Ponchet M, Roby D, Schlaich NL, Jouanin L, Keller H (2009) Imbalanced lignin biosynthesis promotes the sexual reproduction of homothallic oomycete pathogens. PLoS Pathog 5(1):e1000264. Scholar
  68. Rahman AU (2000) Studies in natural product chemistry, vol 24. Elsevier, Amsterdam, pp 860–861Google Scholar
  69. Razavi SM, Imanzadeh GH, Davari M (2010) Coumarins from Zosima absinthifolia seeds, with allelopatic effects. EurAsia J Biosci 4:17–22Google Scholar
  70. Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883Google Scholar
  71. Schofield P, Mbugua DM, Pell AN (2001) Analysis of condensed tannins: a review. Anim Feed Sci Technol 91:21–40Google Scholar
  72. Sharma R, Negi DS, Shiu WK, Gibbons S (2006) Characterization of an insecticidal coumarin from Boenninghausenia albiflora. Phytother Res 20:607–609Google Scholar
  73. Shirley BW (1996) Flavonoid biosynthesis: “new” functions for an “old” pathway. Trends Plant Sci 1:377–382Google Scholar
  74. Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P, Rozanska E, Sobczak M, Torres MA, Grundler FM (2014) Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Sci Signal 7:320–333Google Scholar
  75. Sijmons PC, Atkinson HJ, Wyss U (1994) Parasitic strategies of root nematodes and associated host cell responses. Annu Rev Phytopathol 32:235–259Google Scholar
  76. Silverman P, Nuckles E, Ye XS, Kuc J, Raskin I (1993) Salicylic acid, ethylene, and pathogen resistance in tobacco. Mol Plant Microbe Interact 6:775–781Google Scholar
  77. Simmonds MSJ (2003) Flavonoid-insect interactions: recent advances in our knowledge. Phytochemistry 64:21–30Google Scholar
  78. Starr JL, Yang W, Yan Y, Crutcher F, Kolomiets K (2014) Expression of phenylalanine ammonia lyase gene in maize lines differing in susceptibility to Meloidogyne incognita. J Nematol 46:360–364Google Scholar
  79. Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, Kreil D, Sykacek P, Grundler FMW, Bohlmann H (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57:771–784Google Scholar
  80. Thoison O, Sévenet T, Niemeyer HM, Russell GB (2004) Insect antifeedant compounds from Nothofagus dombeyi and N. pumilio. Phytochemistry 65:2173–2176Google Scholar
  81. Tytgat T, De Meutter J, Gheysen G, Coomans A (2000) Sedentary endoparasitic nematodes as a model for other plant parasitic nematodes. Nematology 2:113–121Google Scholar
  82. Uehara T, Sugiyama S, Matsuura H, Arie T, Masuta CR (2010) Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid. Plant Cell Physiol 51:1524–1536Google Scholar
  83. Vanholme B, Kast P, Haegeman A, Jacob J, Grunewald W, Gheysen G (2009) Structural and functional investigation of a secreted chorismate mutase from the plant-parasitic nematode Heterodera schachtii in the context of related enzymes from diverse origins. Mol Plant Pathol 10:189–200Google Scholar
  84. Vasyukova NI, Pridvorova SM, Gerasimova NG, Chalenko GI, Ozeretskovskaya OL, Udalova ZV, Zinov’eva SV (2007) The involvement of phenylalanine ammonia-lyase and salicylic acid in the induction of resistance to tomato plants infested with gall nematode Meloidogyne incognita. Dokl Biol Sci 416:382–385Google Scholar
  85. Vernooij B, Uknes S, Ward E, Ryals J (1994) Salicylic acid as a signal molecule in plant pathogen interactions. Curr Opin Cell Biol 6:275–279Google Scholar
  86. Veronico P, Paciolla C, Pomar F, De Leonardis S, García-Ulloa A, Melillo MT (2018) Changes in lignin biosynthesis and monomer composition in response to benzothiadiazole and root-knot nematode Meloidogyne incognita infection in tomato. J Plant Physiol 230:40–50Google Scholar
  87. Wang X-B, Li G-H, Li L, Zheng L-J, Huang R, Zhang K-Q (2008) Nematicidal coumarins from Heracleum candicans wall. Nat Prod Res 22:666–671Google Scholar
  88. Wasson AP, Ramsay K, Jones MG, Mathesius U (2009) Differing requirements for flavonoids during the formation of lateral roots, nodules and root knot nematode galls in Medicago truncatula. New Phytol 183:167–179Google Scholar
  89. Winkel-Shirley B (2001) Flavonoid biosynthesis: a colourful model for genetics, biochemistry, cell biology and biotechnology. Plant Physiol 126:485–493Google Scholar
  90. Wuyts N, Lognay G, Swennen R, De Waele D (2006) Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J Exp Bot 57:2825–2835Google Scholar
  91. Wyss U, Grundler FMW (1992) Feeding behavior of sedentary plant parasitic nematodes. Eur J Plant Pathol 98:165–173Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Noureddine Hamamouch
    • 1
  • Essarioui Adil
    • 2
  1. 1.Laboratory of Biotechnology and Sustainable Development of Natural Resources, Polydisciplinary FacultyUniversity Sultan Moulay SlimaneBeni MellalMorocco
  2. 2.National Institute for Agricultural ResearchErrachidiaMorocco

Personalised recommendations