Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects

Frontiers in Plant Science

Volumn 4, Issue APR, 2013, Pages

  Wondafrash, Mesfin ^a,b   Van Dam, Nicole M ^a   Tytgat, Tom O G ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b HARAMAYA UNIVERSITY   (Ethiopia)

Author keywords

Aboveground belowground interactions; Herbivores; Secondary plant compounds; Signaling interactions; Systemic induced plant defense

Indexed keywords

EID: 84884368314     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00087     Document Type: Review

References (165)

1. Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchi, E. G. J., Deleury, E., et al. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26, 909-915.
2. Ahn, J. H., and Lee, J. S. (2003). Sugar acts as a regulatory signal on the wound-inducible expression of SbHRGP3::GUS in transgenic plants. Plant Cell Rep. 22, 286-293.
3. Alkharouf, N. W., Klink, V. P., Chouikha, I. B., Beard, H. S., Macdonald, M. H., Meyer, S., et al. (2006). Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224, 838-852.
4. Alston, D. G., Bradley, J. R., Schmitt, D. P., and Coble, H. D. (1991). Response of Helicoverpa zea (Lepidoptera, Noctuidae) populations to canopy development in soybean as influenced by Heterodera glycines (Nematode, Heteroderidae) and annual weed population densities. J. Econ. Entomol. 84, 267-276.
5. Alston, D. G., Schmitt, D. P., Bradley, J. R., and Coble, H. D. (1993). Multiple pest interactions in soybean-Effects on Heterodera glycines egg populations and crop yield. J. Nematol. 25, 42-49.
6. Angot, A., Vergunst, A., Genin, S., and Peeters, N. (2007). Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog. 3:e3. doi: 10.1371/journal.ppat.0030003
7. Antolin-Llovera, M., Ried, M. K., Binder, A., and Parniske, M. (2012). Receptor kinase signaling pathways in plant-microbe interactions, Annu. Rev. Phytopathol. 50, 451-473.
8. Arimura, G. I., Ozawa, R., and Maffei, M. E. (2011). Recent advances in plant early signaling in response to herbivory. Int. J. Mol. Sci. 12, 3723-3739.
9. Babst, B. A., Ferrieri, R. A., Gray, D. W., Lerdau, M., Schlyer, D. J., Schueller, M., et al. (2005). Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol. 167, 63-72.
10. Bagatto, G., Paquette, L. C., and Shorthouse, J. D. (1996). Influence of galls of Phanacis taraxaci on carbon partitioning within common dandelion, Taraxacum officinale. Entomol. Exp. Appl. 79, 111-117.
11. Bakker, E., Dees, R., Bakker, J., and Goverse, A. (2006). "Mechanisms involved in plant resistance to nematodes, " in Multigenic and Induced Systemic Resistance in Plants, eds T. Sadik and B. Elizabeth (Berlin: Springer), 314-334.
12. Bellafiore, S., and Briggs, S. P. (2010). Nematode effectors and plant responses to infection. Curr. Opin. Plant Biol. 13, 442-448.
13. Bellafiore, S., Shen, Z. X., Rosso, M. N., Abad, P., Shih, P., and Briggs, S. P. (2008). Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog. 4:e1000192. doi: 10.1371/journal.ppat.1000192
14. Bezemer, T. M., De Deyn, G. B., Bossinga, T. M., Van Dam, N. M., Harvey, J. A., and Van Der Putten, W. H. (2005). Soil community composition drives aboveground plant-herbivore-parasitoid interactions. Ecol. Lett. 8, 652-661.
15. Bezemer, T. M., and van Dam, N. M. (2005). Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol. Evol. 20, 617-624.
16. Bezemer, T. M., Wagenaar, R., Van Dam, N. M., Van Der Putten, W. H., and Wackers, F. L. (2004). Above-and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury. J. Chem. Ecol. 30, 53-67.
17. Bhattarai, K. K., Xie, Q. G., Mantelin, S., Bishnoi, U., Girke, T., Navarre, D. A., et al. (2008). Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol. Plant Microbe Interact. 21, 1205-1214.
18. Bhattarai, K. K., Xie, Q. G., Pourshalimi, D., Younglove, T., and Kaloshian, I. (2007). Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Mol. Plant Microbe Interact. 20, 276-282.
19. Bidart-Bouzat, M. G., and Kliebenstein, D. (2011). An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167, 677-689.
20. Blaxter, M. (1998). Caenorhabditis elegans is a nematode. Science 282, 2041-2046.
21. Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., et al. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71-75.
22. Blaxter, M. L., Page, A. P., Rudin, W., and Maizels, R. M. (1992). Nematode surface coats-actively evading immunity. Parasitol. Today 8, 243-247.
23. Boller, T., and 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.
24. Bolton, M. D. (2009). Primary metabolism and plant defense-fuel for the fire. Mol. Plant Microbe Interact. 22, 487-497.
25. Bonaventure, G., Vandoorn, A., and Baldwin, I. T. (2011). Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci. 16, 294-299.
26. Bonte, D., De Roissart, A., Vandegehuchte, M. L., Ballhorn, D. J., Van Leeuwen, T., and De La Pena, E. (2010). Local adaptation of aboveground herbivores towards plant phenotypes induced by soil biota. PLoS ONE 5:e11174. doi: 10.1371/journal.pone.0011174
27. Bostock, R. M. (2005). Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu. Rev. Phytopathol. 43, 545-580.
28. Branch, C., Hwang, C. F., Navarre, D. A., and Williamson, V. M. (2004). Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato. Mol. Plant Microbe Interact. 17, 351-356.
29. Bruce, T. J. A., Matthes, M. C., Napier, J. A., and Pickett, J. A. (2007). Stressful "memories" of plants: evidence and possible mechanisms. Plant Sci. 173, 603-608.
30. Caillaud, M. C., Dubreuil, G., Quentin, M., Perfus-Barbeoch, L., Lecornte, P., Engler, J. D., et al. (2008). Root-knot nematodes manipulate plant cell functions during a compatible interaction. J. Plant Physiol. 165, 104-113.
31. Carter-Wientjes, C. H., Russin, J. S., Boethel, D. J., Griffin, J. L., and Mcgawley, E. C. (2004). Feeding and maturation by soybean looper (Lepidoptera: Noctuidae) larvae on soybean affected by weed, fungus, and nematode pests. J. Econ. Entomol. 97, 14-20.
32. Chitwood, D. J. (2003). Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest. Manag. Sci. 59, 748-753.
33. Connor, E. F., and Taverner, M. P. (1997). The evolution and adaptive significance of the leaf-mining habit. Oikos 79, 6-25.
34. Conrath, U., Beckers, G. J. M., Flors, V., Garcia-Agustin, P., Jakab, G., Mauch, F., et al. (2006). Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062-1071.
35. Conrath, U., Pieterse, C. M. J., and Mauch-Mani, B. (2002). Priming in plant-pathogen interactions. Trends Plant Sci. 7, 210-216.
36. Davies, K. G., and Curtis, R. H. C. (2011). Cuticle surface coat of plant-parasitic nematodes. Annu. Rev. Phytopathol. 49, 135-156.
37. Davis, E. L., Hussey, R. S., Mitchum, M. G., and Baum, T. J. (2008). Parasitism proteins in nematode-plant interactions. Curr. Opin. Plant Biol. 11, 360-366.
38. Davis, E. L., and Mitchum, M. G. (2005). Nematodes. Sophisticated parasites of legumes. Plant Physiol. 137, 1182-1188.
39. De Deyn, G. B., Raaijmakers, C. E., Zoomer, H. R., Berg, M. P., De Ruiter, P. C., Verhoef, H. A., et al. (2003). Soil invertebrate fauna enhances grassland succession and diversity. Nature 422, 711-713.
40. De Deyn, G. B., Van Ruijven, J., Raaijmakers, C. E., De Ruiter, P. C., and Van Der Putten, W. H. (2007). Above-and belowground insect herbivores differentially affect soil nematode communities in species-rich plant communities. Oikos 116, 923-930.
41. De Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., et al. (2005). Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Microbe Interact. 18, 923-937.
42. Dicke, M., Van Loon, J. J. A., and Soler, R. (2009). Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5, 317-324.
43. Diezel, C., Von Dahl, C. C., Gaquerel, E., and Baldwin, I. T. (2009). Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150, 1576-1586.
44. Dubreuil, G., Deleury, E., Magliano, M., Jaouannet, M., Abad, P., and Rosso, M.-N. (2011). Peroxiredoxins from the plant parasitic root-knot nematode, Meloidogyne incognita, are required for successful development within the host. Int. J. Parasitol. 41, 385-396.
45. Erb, M., Meldau, S., and Howe, G. A. (2012). Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17, 250-259.
46. Fu, S., Kisselle, K. W., Coleman, D. C., Hendrix, P. F., and Crossley D. A. Jr. (2001). Short-term impacts of aboveground herbivory (grasshopper) on the abundance and 14C activity of soil nematodes in conventional tillage and no-till agroecosytems. Soil Biol. Biochem. 33, 1253-1258.
47. Fujimoto, T., Tomitaka, Y., Abe, H., Tsuda, S., Futai, K., and Mizukubo, T. (2011). Expression profile of jasmonic acid-induced genes and the induced resistance against the root-knot nematode (Meloidogyne incognita) in tomato plants (Solanum lycopersicum) after foliar treatment with methyl jasmonate. J. Plant Physiol. 168, 1084-1097.
48. Gheysen, G., and Fenoll, C. (2002). Gene expression in nematode feeding sites. Annu. Rev. Phytopathol. 40, 191-219.
49. Gheysen, G., and Mitchum, M. G. (2011). How nematodes manipulate plant development pathways for infection. Curr. Opin. Plant Biol. 14, 415-421.
50. Goff, S. A., Ricke, D., Lan, T.-H., Presting, G., Wang, R., Dunn, M., et al. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92-100.
51. Gómez, S., Ferrieri, R. A., Schueller, M., and Orians, C. M. (2010). Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol. 188, 835-844.
52. Gullan, P. J., and Cranston, P. S. (2010). The Insects: An Outline of Entomology. Hoboken: Wiley-Blackwell.
53. Haegeman, A., Mantelin, S., Jones, J. T., and Gheysen, G. (2012). Functional roles of effectors of plant-parasitic nematodes. Gene 492, 19-31.
54. Hamamouch, N., Li, C. Y., Seo, P. J., Park, C. M., and Davis, E. L. (2011). Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol. Plant Pathol. 12, 355-364.
55. Heming, B. S. (1993). "Structure, function, ontogeny, and evolution of feeding in thrips (Thysanoptera), " in Functionaql Morphology of Insect Feeding, eds C. W. Schaefer and R. A. B. Leschen (Lanham: Entomological Society of America), 3-41.
56. Hilker, M., and Meiners, T. (2010). How do plants "notice" attack by herbivorous arthropods? Biol. Rev. 85, 267-280.
57. Hofmann, J., El Ashry, A., Anwar, S., Erban, A., Kopka, J., and Grundler, F. (2010). Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. Plant J. 62, 1058-1071.
58. Hogenhout, S. A., and Bos, J. I. B. (2011). Effector proteins that modulate plant-insect interactions. Curr. Opin. Plant Biol. 14, 422-428.
59. Hol, W. H. G., De Boer, W., Termorshuizen, A. J., Meyer, K. M., Schneider, J. H. M., Van Dam, N. M., et al. (2010). Reduction of rare soil microbes modifies plant-herbivore interactions. Ecol. Lett. 13, 292-301.
60. Hong, S. C., Donaldson, J., and Gratton, C. (2010). Soybean cyst nematode effects on soybean aphid preference and performance in the laboratory. Environ. Entomol. 39, 1561-1569.
61. Hong, S. C., Macguidwin, A., and Gratton, C. (2011). Soybean aphid and soybean cyst nematode interactions in the field and effects on soybean yield. J. Econ. Entomol. 104, 1568-1574.
62. Hoth, S., Schneidereit, A., Lauterbach, C., Scholz-Starke, J., and Sauer, N. (2005). Nematode infection triggers the de novo formation of unloading phloem that allows macromolecular trafficking of green fluorescent protein into syncytia. Plant Physiol. 138, 383-392.
63. Hoth, S., Stadler, R., Sauer, N., and Hammes, U. Z. (2008). Differential vascularization of nematode-induced feeding sites. Proc. Natl. Acad. Sci. U.S.A. 105, 12617-12622.
64. Hunter, M. D. (2001). Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agric. For. Entomol. 3, 3-9.
65. Hussey, R. S. (1989). Disease-inducing secretions of plant-parasitic nematodes. Annu. Rev. Phytopathol. 27, 123-141.
66. Ithal, N., Recknor, J., Nettleton, D., Hearne, L., Maier, T., Baum, T. J., et al. (2007a). Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol. Plant Microbe Interact. 20, 293-305.
67. Ithal, N., Recknor, J., Nettleton, D., Maier, T., Baum, T. J., and Mitchum, M. G. (2007b). Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol. Plant Microbe Interact. 20, 510-525.
68. Johnson, S. N., Birch, A. N. E., Gregory, P. J., and Murray, P. J. (2006). The 'mother knows best' principle: should soil insects be included in the preference-performance debate? Ecol. Entomol. 31, 395-401.
69. Jones, D. A., and Takemoto, D. (2004). Plant innate immunity-direct and indirect recognition of general and specific pathogen-associated molecules. Curr. Opin. Immunol. 16, 48-62.
70. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329.
71. Jones, J. T., Reavy, B., Smant, G., and Prior, A. E. (2004). Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324, 47-54.
72. Kabouw, P., Kos, M., Kleine, S., Vockenhuber, E. A., Van Loon, J. J. A., Van Der Putten, W. H., et al. (2011). Effects of soil organisms on aboveground multitrophic interactions are consistent between plant genotypes mediating the interaction. Entomol. Exp. Appl. 139, 197-206.
73. Kaloshian, I. (2004). Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem. Ecol. 30, 2419-2438.
74. Kaloshian, I., and Walling, L. L. (2005). Hemipterans as plant pathogens. Annu. Rev. Phytopathol. 43, 491-521.
75. Kaplan, I., Halitschke, R., Kessler, A., Rehill, B. J., Sardanelli, S., and Denno, R. F. (2008a). Physiological integration of roots and shoots in plant defense strategies links above-and belowground herbivory. Ecol. Lett. 11, 841-851.
76. Kaplan, I., Halitschke, R., Kessler, A., Sardanelli, S., and Denno, R. F. (2008b). Constitutive and induced defenses to herbivory in above-and belowground plant tissues. Ecology 89, 392-406.
77. Kaplan, I., Sardanelli, S., and Denno, R. F. (2009). Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum. Ecol. Entomol. 34, 262-270.
78. Kaplan, I., Sardanelli, S., Rehill, B. J., and Denno, R. F. (2011). Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis. Oecologia 166, 627-636.
79. Katagiri, F., and Tsuda, K. (2010). Understanding the plant immune system. Mol. Plant Microbe Interact. 23, 1531-1536.
80. Kerchev, P. I., Fenton, B., Foyer, C. H., and Hancock, R. D. (2012). Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ. 35, 441-453.
81. Kim, J., Quaghebeur, H., and Felton, G. W. (2011). Reiterative and interruptive signaling in induced plant resistance to chewing insects. Phytochemistry 72, 1624-1634.
82. Koo, A. J. K., and Howe, G. A. (2009). The wound hormone jasmonate. Phytochemistry 70, 1571-1580.
83. Koornneef, A., Leon-Reyes, A., Ritsema, T., Verhage, A., Den Otter, F. C., Van Loon, L. C., et al. (2008). Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147, 1358-1368.
84. Koyama, Y., Yao, I., and Akimoto, S.-I. (2004). Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation. Entomol. Exp. Appl. 113, 35-44.
85. Kutyniok, M., and Muller, C. (2012). Crosstalk between above-and belowground herbivores is mediated by minute metabolic responses of the host Arabidopsis thaliana. J. Exp. Bot. 63, 6199-6210.
86. Kyndt, T., Nahar, K., Haegeman, A., De Vleesschauwer, D., Hofte, M., and Gheysen, G. (2012). Comparing systemic defence-related gene expression changes upon migratory and sedentary nematode attack in rice. Plant Biol. 14, 73-82.
87. Labandeira, C. C. (1997). Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annu. Rev. Ecol. Syst. 28, 153-193.
88. Leon-Reyes, A., Du, Y. J., Koornneef, A., Proietti, S., Korbes, A. P., Memelink, J., et al. (2010). Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol. Plant Microbe Interact. 23, 187-197.
89. Li, Q., Xie, Q. G., Smith-Becker, J., Navarre, D. A., and Kaloshian, I. (2006). Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant Microbe Interact. 19, 655-664.
90. Lohmann, M., Scheu, S., and Muller, C. (2009). Decomposers and root feeders interactively affect plant defence in Sinapis alba. Oecologia 160, 289-298.
91. Lou, Y. G., and Baldwin, I. T. (2004). Nitrogen supply influences herbivore-induced direct and indirect defenses and transcriptional responses to Nicotiana attenuata. Plant Physiol. 135, 496-506.
92. Maizels, R. M., Gomez-Escobar, N., Gregory, W. F., Murray, J., and Zang, X. X. (2001). Immune evasion genes from filarial nematodes. Int. J. Parasitol. 31, 889-898.
93. Manninen, A. M., Vuorinen, M., and Holopainen, J. K. (1998). Variation in growth, chemical defense, and herbivore resistance in scots pine provenances. J. Chem. Ecol. 24, 1315-1331.
94. Mateille, T. (1994). Biology of the plant nematode relationship-physiological changes and the defense mehanism of plants. Nematologica 40, 276-311.
95. Mathur, V., Tytgat, T. G., Graaf, R., Kalia, V., Sankara Reddy, A., Vet, L. M., et al. (2012). Dealing with double trouble: consequences of single and double herbivory in Brassica juncea. Chemoecology 1-12.
96. Meyers, B. C., Kozik, A., Griego, A., Kuang, H., and Michelmore, R. W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell Online 15, 809-834.
97. Mithöfer, A., and Boland, W. (2008). Recognition of herbivory-associated molecular patterns. Plant Physiol. 146, 825-831.
98. Mithofer, A., and Boland, W. (2012). "Plant defense against herbivores: chemical aspects, " in Annual Review of Plant Biology, Vol 63. ed. S. S. Merchant, 431-450.
99. Monaghan, J., and Zipfel, C. (2012). Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15, 349-357.
100. Mukhtar, M. S., Carvunis, A.-R., Dreze, M., Epple, P., Steinbrenner, J., Moore, J., et al. (2011). Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596-601.
101. Mur, L. A. J., Kenton, P., Atzorn, R., Miersch, O., and Wasternack, C. (2006). The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 140, 249-262.
102. Nahar, K., Kyndt, T., De Vleesschauwer, D., Hofte, M., and Gheysen, G. (2011). The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol. 157, 305-316.
103. Nahar, K., Kyndt, T., Nzogela, Y. B., and Gheysen, G. (2012). Abscisic acid interacts antagonistically with classical defense pathways in rice-migratory nematode interaction. New Phytol. 196, 901-913.
104. Nobre, M. J. G., and Evans, K. (1998). Plant and nematode surfaces: their structure and importance in host-parasite interactions. Nematologica 44, 103-124.
105. Nombela, G., Williamson, V. M., and Muniz, M. (2003). The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant Microbe Interact. 16, 645-649.
106. Nurnberger, T., and Kemmerling, B. (2006). Receptor protein kinases-pattern recognition receptors in plant immunity. Trends Plant Sci. 11, 519-522.
107. Offler, C. E., Mccurdy, D. W., Patrick, J. W., and Talbot, M. J. (2003). Tansfer cells: cells specialized for a special purpose. Annu. Rev. Plant Biol. 54, 431-454.
108. Olson, D. M., Davis, R. F., Wackers, F. L., Rains, G. C., and Potter, T. (2008). Plant-herbivore-carnivore interactions in cotton, Gossypium hirsutum: linking belowground and aboveground. J. Chem. Ecol. 34, 1341-1348.
109. Opperman, C. H., Bird, D. M., Williamson, V. M., Rokhsar, D. S., Burke, M., Cohn, J., et al. (2008). Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proc. Natl. Acad. Sci. U.S.A. 105, 14802-14807.
110. Pieterse, C. M. J., Van Der Does, D., Zamioudis, C., Leon-Reyes, A., and Van Wees, S. C. M. (2012). Hormonal Modulation of Plant Immunity. Annu. Rev. Cell Dev. Biol. 28, 489-521.
111. Pieterse, C. M. J., and van Loon, L. C. (1999). Salicylic acid-independent plant defence pathways. Trends Plant Sci. 4, 52-58.
112. Postma, W. J., Slootweg, E. J., Rehman, S., Finkers-Tomczak, A., Tytgat, T. O. G., Van Gelderen, K., et al. (2012). The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiol. 160, 944-954.
113. Puthoff, D. P., Nettleton, D., Rodermel, S. R., and Baum, T. J. (2003). Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant J. 33, 911-921.
114. Raman, A. (2012). Gall induction by hemipteroid insects. J. Plant Interact. 7, 29-44.
115. Rasmann, S., Bauerle, T. L., Poveda, K., and Vannette, R. (2011). Predicting root defence against herbivores during succession. Funct. Ecol. 25, 368-379.
116. Redfern, M. (1997). Plant galls: an intimate association between animals and plants. Antenna 21, 55-63.
117. Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E., and Williamson, V. M. (1998). The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. U.S.A. 95, 9750-9754.
118. Russin, J. S., Layton, M. B., Boethel, D. J., Mcgawley, E. C., Snow, J. P., and Berggren, G. T. (1989). Development of Heterodera glycines on soybean damaged by soybean looper and stem canker. J. Nematol. 21, 108-114.
119. Russin, J. S., Mcgawley, E. C., and Boethel, D. J. (1993). Population development of Meloidogyne incognita on soybean defoliated by Pseudoplusia includens. J. Nematol. 25, 50-54.
120. Schoonhoven, L. M., Van Loon, J. J. A., and Dicke, M. (2005). Insect-Plant Biology. Wallingford: Cab publishing.
121. Schwachtje, J., and Baldwin, I. T. (2008). Why does herbivore attack reconfigure primary metabolism? Plant Physiol. 146, 845-851.
122. Schwachtje, J., Minchin, P. E. H., Jahnke, S., Van Dongen, J. T., Schittko, U., and Baldwin, I. T. (2006). SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl. Acad. Sci. U.S.A. 103, 12935-12940.
123. Schwessinger, B., and Ronald, P. C. (2012). Plant innate immunity: perception of conserved microbial signatures. Annu. Rev. Plant Biol. 63, 451-482.
124. Schwessinger, B., and Zipfel, C. (2008). News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11, 389-395.
125. Sijmons, P. C., Atkinson, H. J., and Wyss, U. (1994). Parasitic strategies of root nematodes and associated host-cell responses. Annu. Rev. Phytopathol. 32, 235-259.
126. Sinclair, R. J., and Hughes, L. (2010). Leaf miners: the hidden herbivores. Austral Ecol. 35, 300-313.
127. Smith, A. M., and Stitt, M. (2007). Coordination of carbon supply and plant growth. Plant Cell Environ. 30, 1126-1149.
128. Smith, C. M., and Clement, S. L. (2012). Molecular bases of plant resistance to arthropods. Annu. Rev. Entomol. 57, 309-328.
129. Sohlenius, B. (1980). Abundance, biomass and contribution to energy-flow by soil nematodes in terrestrial ecosystems. Oikos 34, 186-194.
130. Spiegel, Y., Inbar, J., Kahane, I., and Sharon, E. (1995). Carbohydrate-recognition domains on the surface of phytophagous nematodes. Exp. Parasitol. 80, 220-227.
131. Spoel, S. H., and Dong, X. N. (2012). How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12, 89-100.
132. Spoel, S. H., Koornneef, A., Claessens, S. M. C., Korzelius, J. P., Van Pelt, J. A., Mueller, M. J., et al. (2003). NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15, 760-770.
133. Steinbrenner, A., Gómez, S., Osorio, S., Fernie, A., and Orians, C. (2011). Herbivore-induced changes in tomato (Solanum lycopersicum) primary metabolism: a whole plant perspective. J. Chem. Ecol. 37, 1294-1303.
134. Steppuhn, A., Gase, K., Krock, B., Halitschke, R., and Baldwin, I. T. (2004). Nicotine's defensive function in nature. PLoS Biol. 2:e217. doi: 10.1371/journal.pbio.0020217
135. Stone, G. N., and Schönrogge, K. (2003). The adaptive significance of insect gall morphology. Trends Ecol. Evol. 18, 512-522.
136. Tiwari, S., Youngman, R. R., Lewis, E. E., and Eisenback, J. D. (2009). European corn borer (Lepidoptera: Crambidae) stalk tunneling on root-knot nematode (Tylenchida: Heteroderidae) fitness on corn. J. Econ. Entomol. 102, 602-609.
137. Tomczak, A., Koropacka, K., Smant, G., Goverse, A., and Bakker, E. (2009). "Resistant plant responses", in Plant Cell Monographs, Vol. 15, eds R. H. Berg and C. G. Taylor (New York: Springer), 83-113.
138. Trudgill, D. L., and Blok, V. C. (2001). Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu. Rev. Phytopathol. 39, 53-77.
139. Tsuda, K., and Katagiri, F. (2010). Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13, 459-465.
140. Turlings, T. C. J., Hiltpold, I., and Rasmann, S. (2012). The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358, 47-56.
141. Tytgat, T., De Meutter, J., Gheysen, G., and Coomans, A. (2000). Sedentary endoparasitic nematodes as a model for other plant parasitic nematodes. Nematology 2, 113-121.
142. Tytgat, T., De Meutter, J., Vanholme, B., Claeys, M., Verreijdt, L., Gheysen, G., et al. (2002). Development and pharyngeal gland activities of Heterodera schachtii infecting Arabidopsis thaliana roots. Nematology 4, 899-908.
143. Utsumi, S., and Ohgushi, T. (2007). Plant regrowth response to a stem-boring insect: a swift moth-willow system. Popul. Ecol. 49, 241-248.
144. van Dam, N. M. (2009). Belowground herbivory and plant defenses. Annu. Rev. Ecol. Evol. Syst. 40, 373-392.
145. van Dam, N. M., Harvey, J. A., Wackers, F. L., Bezemer, T. M., Van Der Putten, W. H., and Vet, L. E. M. (2003). Interactions between aboveground and belowground induced responses against phytophages. Basic Appl. Ecol. 4, 63-77.
146. van Dam, N. M., and Oomen, M. W. A. T. (2008). Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth. Plant Signal. Behav. 3, 91-98.
147. van Dam, N. M., Raaijmakers, C. E., and Van Der Putten, W. H. (2005). Root herbivory reduces growth and survival of the shoot feeding specialist Pieris rapae on Brassica nigra. Entomol. Exp. Appl. 115, 161-170.
148. van Dam, N. M., Tytgat, T. O. G., and Kirkegaard, J. A. (2009). Root and shoot glucosinolates: a comparison of their diversity, function and interactions in natural and managed ecosystems. Phytochem. Rev. 8, 171-186.
149. van den Burg, H. A., and Takken, F. L. W. (2009). Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci. 14, 286-294.
150. van der Hoorn, R. A. L., and Kamoun, S. (2008). From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009-2017.
151. Vandegehuchte, M. L., De La Pena, E., and Bonte, D. (2010). Interactions between root and shoot herbivores of Ammophila arenaria in the laboratory do not translate into correlated abundances in the field. Oikos 119, 1011-1019.
152. Vanholme, B., De Meutter, J., Tytgat, T., Van Montagu, M., Coomans, A., and Gheysen, G. (2004). Secretions of plant-parasitic nematodes: a molecular update. Gene 332, 13-27.
153. van Ooijen, G., Van Den Burg, H. A., Cornelissen, B. J. C., and Takken, F. L. W. (2007). Structure and function of resistance proteins in solanaceous plants. Annu. Rev. Phytopathol. 45, 43-72.
154. Van Wees, S. C. M., Van Der Ent, S., and Pieterse, C. M. J. (2008). Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11, 443-448.
155. Verhage, A., Vlaardingerbroek, I., Raaijmakers, C., Van Dam, N., Dicke, M., Van Wees, S. C. M., et al. (2011). Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Front. Plant Sci. 2:47. doi: 10.3389/fpls.2011.00047
156. Vos, P., Simons, G., Jesse, T., Wijbrandi, J., Heinen, L., Hogers, R., et al. (1998). The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16, 1365-1369.
157. Waetzig, G. H., Sobczak, M., and Grundler, F. M. W. (1999). Localization of hydrogen peroxide during the defence response of Arabidopsis thaliana against the plant-parasitic nematode Heterodera glycines. Nematology 1, 681-686.
158. Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Setala, H., Van Der Putten, W. H., and Wall, D. H. (2004). Ecological linkages between aboveground and belowground biota. Science 304, 1629-1633.
159. Wubben, M. J. E., Jin, J., and Baum, T. J. (2008). Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol. Plant Microbe Interact. 21, 424-432.
160. Wu, J. Q., and Baldwin, I. T. (2010). New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44, 1-24.
161. Wurst, S., and van der Putten, W. H. (2007). Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores. Basic Appl. Ecol. 8, 491-499.
162. Wyss, U. (2002). "Feeding behaviour of plant-parasitic nematodes, " in The Biology of Nematodes, ed. D.L. Lee (London: Taylor and Francis), 233-259.
163. Wyss, U., Grundler, F. M. W., and Munch, A. (1992). The Parasitic behavior of 2nd-stage juveniles of Meloidogyne-incognita in Roots of Arabidopsis-thaliana. Nematologica 38, 98-111.
164. Zinov'eva, S. V., Vasyukova, N. I., and Ozeretskovskaya, O. L. (2004). Biochemical aspects of plant interactions with phytoparasitic nematodes: a review. Appl. Biochem. Microbiol. 40, 111-119.
165. Zipfel, C. (2008). Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20, 10-16.