Soil abiotic factors influence interactions between belowground herbivores and plant roots

Journal of Experimental Botany

Volumn 64, Issue 5, 2013, Pages 1295-1303

  Erb, Matthias ^a   Lu, Jing ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Drought; Induced resistance; Moisture; Plant immunity; Root herbivores; Soil texture.

Indexed keywords

ANIMAL; DROUGHT; HERBIVORY; HOST PARASITE INTERACTION; IMMUNOLOGY; LARVA; PARASITOLOGY; PHYSIOLOGY; PLANT ROOT; REVIEW; SOIL;

ANIMALS; DROUGHTS; HERBIVORY; HOST-PARASITE INTERACTIONS; LARVA; PLANT ROOTS; SOIL;

EID: 84875161454     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert007     Document Type: Review

References (83)

1. Baldwin IT. 1988. Damage-induced alkaloids in tobacco-pot-bound plants are not inducible. Journal of Chemical Ecology 14, 1113-1120.
2. Baldwin IT, Hamilton W. 2000. Jasmonate-induced responses of Nicotiana sylvestris results in fitness costs due to impaired competitive ability for nitrogen. Journal of Chemical Ecology 26, 915-952.
3. Beeckman T, Friml J. 2010. Nitrate contra auxin: nutrient sensing by roots. Developmental Cell 18, 877-878.
4. Blossey B, Hunt-Joshi TR. 2003. Belowground herbivory by insects: influence on plants and aboveground herbivores. Annual Review of Entomology 48, 521-547.
5. Breuillin F, Schramm J, Hajirezaei M, et al. 2010. Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. The Plant Journal 64, 1002-1017.
6. Brown VK, Gange AC. 1990. Insect herbivory insect below ground. Advances in Ecological Research 20, 1-58.
7. Chaves MM, Maroco JP, Pereira JS. 2003. Understanding plant responses to drought-from genes to the whole plant. Functional Plant Biology 30, 239-264.
8. Chen YG, Ruberson JR, Olson DM. 2008. Nitrogen fertilization rate affects feeding, larval performance, and oviposition preference of the beet armyworm, Spodoptera exigua, on cotton. Entomologia Experimentalis et Applicata 126, 244-255.
9. Davis PM, Brenes N, Allee LL. 1996. Temperature dependent models to predict regional differences in corn rootworm (Coleoptera: Chrysomelidae) phenology. Environmental Entomology 25, 767-775.
10. Dunn JP, Frommelt K. 1998. Effects of below-ground herbivory by Diabrotica virgifera virgifera (Col, Chrysomelidea) and soil moisture on leaf gas exchange of maize. Journal of Applied Entomology-Zeitschrift für Angewandte Entomologie 122, 179-183.
11. Ellsbury MM, Schumacher TE, Gustin RD, Woodson WD. 1994. Soil compaction effect on corn-rootworm populations in maize artificially infested with eggs of western corn-rootworm (Coleoptera, Chrysomelidae). Environmental Entomology 23, 943-948.
12. Erb M, Flors V, Karlen D, de Lange E, Planchamp C, D'Alessandro M, Turlings TCJ, Ton J. 2009. Signal signature of aboveground-induced resistance upon belowground herbivory in maize. The Plant Journal 59, 292-302.
13. Erb M, Glauser G, Robert CAM. 2012. Induced immunity against belowground insect herbivores-activation of defenses in the absence of a jasmonate burst. Journal of Chemical Ecology 38, 629-640.
14. Erb M, Köllner TG, Degenhardt J, Zwahlen C, Hibbard BE, Turlings TCJ. 2011. The role of abscisic acid and water stress in root herbivore-induced leaf resistance. New Phytologist 189, 308-320.
15. Fierer N, Jackson RB. 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences, USA 103, 626-631.
16. Gange A, Brown V, Sinclair G. 1994. Reduction of black vine weevil larval growth by vesicular-arbuscular mycorrhizal infection. Entomologia Experimentalis et Applicata 70, 115-119.
17. Gao JP, Chao DY, Lin HX. 2007. Understanding abiotic stress tolerance mechanisms: recent studies on stress response in rice. Journal of Integrative Plant Biology 49, 742-750.
18. Gouinguene SP, Turlings TCJ. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiology 129, 1296-1307.
19. Grant JA, Villani MG. 2003. Soil moisture effects on entomopathogenic nematodes. Environmental Entomology 32, 80-87.
20. Gray ME, Steffey KL. 1998. Corn rootworm (Coleoptera: Chrysomelidae) larval injury and root compensation of 12 maize hybrids: an assessment of the economic injury index. Journal of Economic Entomology 91, 723-740.
21. Gutbrodt B, Mody K, Dorn S. 2011. Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores. Oikos 120, 1732-1740.
22. Hattori Y, Nagai K, Ashikari M. 2011. Rice growth adapting to deepwater. Current Opinion in Plant Biology 14, 100-105.
23. Hibbard BE, Duran DP, Ellersieck MR, Ellsbury MM. 2003. Post-establishment movement of western corn rootworm larvae (Coleoptera: Chrysomelidae) in Central Missouri corn. Journal of Economic Entomology 96, 599-608.
24. Hiltpold I, Turlings TCJ. 2008. Belowground chemical signaling in maize: when simplicity rhymes with efficiency. Journal of Chemical Ecology 34, 628-635.
25. Hoback WW, Clark TL, Meinke LJ, Higley LG, Scalzitti JM. 2002. Immersion survival differs among three Diabrotica species. Entomologia Experimentalis et Applicata 105, 29-34.
26. Hol WHG. 2011. The effect of nutrients on pyrrolizidine alkaloids in Senecio plants and their interactions with herbivores and pathogens. Phytochemistry Reviews 10, 119-126.
27. Huberty AF, Denno RF. 2004. Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85, 1383-1398.
28. Hunter MD. 2001. Out of sight, out of mind: the impacts of rootfeeding insects in natural and managed systems. Agricultural and Forest Entomology 3, 3-9.
29. Ibrahim MA, Stewart-Jones A, Pulkkinen J, Poppy GM, Holopainen JK. 2008. The influence of different nutrient levels on insect-induced plant volatiles in Bt and conventional oilseed rape plants. Plant Biology 10, 97-107.
30. Jasper DA, Davy JA. 1993. Root characteristics of native plantspecies in relation to the benefit of mycorrhizal colonization for phosphorus uptake. Plant and Soil 155, 281-284.
31. Johnson SN, Barton AT, Clark KE, Gregory PJ, McMenemy LS, Hancock RD. 2011. Elevated atmospheric carbon dioxide impairs the performance of root-feeding vine weevils by modifying root growth and secondary metabolites. Global Change Biology 17, 688-695.
32. Johnson SN, Crawford JW, Gregory PJ, Grinev DV, Mankin RW, Masters GJ, Murray PJ, Wall DH, Zhang X. 2007. Non-invasive techniques for investigating and modelling root-feeding insects in managed and natural systems. Agricultural and Forest Entomology 9, 39-46.
33. Johnson SN, Gregory PJ, McNicol JW, Oodally Y, Zhang XX, Murray PJ. 2010a. Effects of soil conditions and drought on egg hatching and larval survival of the clover root weevil (Sitona lepidus). Applied Soil Ecology 44, 75-79.
34. Johnson SN, Hallett PD, Gillespie TL, Halpin C. 2010b. Belowground herbivory and root toughness: a potential model system using lignin-modified tobacco. Physiological Entomology 35, 186-191.
35. Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF. 2008. Constitutive and induced defenses to herbivory in above-and belowground plant tissues. Ecology 89, 392-406.
36. Koricheva J, Gange AC, Jones T. 2009. Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90, 2088-2097.
37. Laan P, Berrevoets MJ, Lythe S, Armstrong W, Blom CWPM. 1989. Root morphology and aerenchyma formation as indicators of the flood-tolerance of rumex species. Journal of Ecology 77, 693-703.
38. Landgraf R, Schaarschmidt S, Hause B. 2012. Repeated leaf wounding alters the colonization of Medicago truncatula roots by beneficial and pathogenic microorganisms. Plant, Cell and Environment 35, 1344-1357.
39. Lepage MP, Bourgeois G, Brodeur J, Boivin G. 2012. Effect of soil temperature and moisture on survival of eggs and first-instar larvae of Delia radicum. Environmental Entomology 41, 159-165.
40. Li H, Futch SH, Syvertsen JP, McCoy CW. 2007a. Time series forecast and soil characteristics-based simple and multivariate linear models for management of Diaprepes abbreviatus root weevil in citrus. Soil Biology and Biochemistry 39, 2436-2447.
41. Li H, McCoy CW, Syvertsen JP. 2007b. Controlling factors of environmental flooding, soil pH and Diaprepes abbreviatus (L.) root weevil feeding in citrus: larval survival and larval growth. Applied Soil Ecology 35, 553-565.
42. Li H, Syvertsen JP, McCoy CW, Stuart RJ, Schumann AW. 2006. Water stress and root injury from simulated flooding and Diaprepes abbreviatus root weevil larval feeding in citrus. Soil Science 171, 138-151.
43. MacEwan RJ, Crawford DM, Newton PJ, Clune TS. 2010. High clay contents, dense soils, and spatial variability are the principal subsoil constraints to cropping the higher rainfall land in south-eastern Australia. Australian Journal of Soil Research 48, 150-166.
44. Martin CG, Mannion C, Schaffer B. 2011. Leaf gas exchange and growth responses of green buttonwood and swingle citrumelo to Diaprepes abbreviatus (Coleoptera: Curculionidae) larval feeding and flooding. Florida Entomologist 94, 279-289.
45. McKey D. 1974. Adaptive patterns in alkaloid physiology. American Naturalist 108, 305-320.
46. Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM. 2010. Innate immune responses activated in arabidopsis roots by microbe-associated molecular patterns. The Plant Cell 22, 973-990.
47. Monshausen GB, Gilroy S. 2009. Feeling green: mechanosensing in plants. Trends in Cell Biology 19, 228-235.
48. Nell M, Votsch M, Vierheilig H, Steinkellner S, Zitterl-Eglseer K, Franz C, Novak J. 2009. Effect of phosphorus uptake on growth and secondary metabolites of garden sage (Salvia officinalis L.). Journal of the Science of Food and Agriculture 89, 1090-1096.
49. Neveu N, Grandgirard J, Nenon JP, Cortesero AM. 2002. Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. Journal of Chemical Ecology 28, 1717-1732.
50. Pacchioli MA, Hower AA. 2004. Soil and moisture effects on the dynamics of early instar clover root curculio (Coleoptera: Curculionidae) and biomass of alfalfa root nodules. Environmental Entomology 33, 119-127.
51. Quisenberry S, Heinrichs E. 1998. Germplasm evaluation and utilization for insect resistance in rice. In: Global plant genetic resources for insect-resistant crops. CRC Press.
52. Rasmann S, Bauerle TL, Poveda K, Vannette R. 2011a. Predicting root defence against herbivores during succession. Functional Ecology 25, 368-379.
53. Rasmann S, Erwin AC, Halitschke R, Agrawal AA. 2011b. Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. Journal of Ecology 99, 16-25.
54. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732-737.
55. Richardson MD, Bacon CW. 1993. Cyclic hydroxamic acid accumulation in corn seedlings exposed to reduced water potentials before, during, and after germination. Journal of Chemical Ecology 19, 1613-1624.
56. Robert CAM, Erb M, Duployer M, Zwahlen C, Doyen GR, Turlings TCJ. 2012a. Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytologist 194, 1061-1069.
57. Robert CAM, Veyrat N, Glauser G, et al. 2012b. A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecology Letters 15, 55-64.
58. Sampedro L, Moreira X, Martins P, Zas R. 2009. Growth and nutritional response of Pinus pinaster after a large pine weevil (Hylobius abietis) attack. Trees-Structure and Function 23, 1189-1197.
59. Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH. 2003. Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiology 133, 295-306.
60. Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PEA. 2009. Phytohormone-based activity mapping of insect herbivoreproduced elicitors. Proceedings of the National Academy of Sciences, USA 106, 653-657.
61. Schroeder WJ, Beavers JB. 1987. Movement of the entomogenous nematodes of the families heterorhabditidae and steinernematidae in soil. Journal of Nematology 19, 257-259.
62. Seki M, Umezawa T, Urano K, Shinozaki K. 2007. Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology 10, 296-302.
63. Shao HB, Chu LY, Jaleel CA, Manivannan P, Panneerselvam R, Shao MA. 2009. Understanding water deficit stress-induced changes in the basic metabolism of higher plants-biotechnologically and sustainably improving agriculture and the ecoenvironment in arid regions of the globe. Critical Reviews in Biotechnology 29, 131-151.
64. Smaoui A, Jouini J, Rabhi M, Bouzaien G, Albouchi A, Abdelly C. 2011. Physiological and anatomical adaptations induced by flooding in Cotula coronopifolia. Acta Biologica Hungarica 62, 182-193.
65. Soler R, van der Putten WH, Harvey JA, Vet LEM, Dicke M, Bezemer TM. 2012. Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. Journal of Chemical Ecology 38, 755-767.
66. Soukup A, Armstrong W, Schreiber L, Franke R, Votrubova O. 2007. Apoplastic barriers to radial oxygen loss and solute penetration: a chemical and functional comparison of the exodermis of two wetland species, Phragmites australis and Glyceria maxima. New Phytologist 173, 264-278.
67. Stout MJ, Brovont RA, Duffey SS. 1998. Effect of nitrogen availability on expression of constitutive and inducible chemical defenses in tomato, Lycopersicon esculentum. Journal of Chemical Ecology 24, 945-963.
68. Strnad SP, Bergman MK. 1987. Movement of 1st-instar western corn rootworms (Coleoptera, Chrysomelidae) in soil. Environmental Entomology 16, 975-978.
69. Takahashi H, Scott TK. 1993. Intensity of hydrostimulation for the induction of root hydrotropism and its sensing by the root cap. Plant, Cell and Environment 16, 99-103.
70. Thaler JS, Bostock RM. 2004. Interactions between abscisic-acidmediated responses and plant resistance to pathogens and insects. Ecology 85, 48-58.
71. Troufflard S, Mullen W, Larson TR, Graham IA, Crozier A, Amtmann A, Armengaud P. 2010. Potassium deficiency induces the biosynthesis of oxylipins and glucosinolates in Arabidopsis thaliana. BMC Plant Biology 10, 172.
72. Van Der Putten WH. 2003. Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84, 2269-2280.
73. Vernon MK. 1979. Drought cracks as oviposition sites for western and northern corn rootworms (Diabrotica: Coleoptera). Journal of the Kansas Entomological Society 52, 769-776.
74. Villani MG, Wright RJ. 1988. Use of radiography in behavioral studies of turfgrass-infesting scarab grub species (Coleoptera: Scarabaeidae). Bulletin of the Entomological Society of America 34, 132-144.
75. Villani MG, Wright RJ. 1990. Environmental influences on soil macroarthropod behavior in agricultural systems. Annual Review of Entomology 35, 249-269.
76. Way MO, Reay-Jones FPF, Stout MJ, Tarpley L. 2006. Effects of nitrogen fertilizer applied before permanent flood on the interaction between rice and rice water weevil (Coleoptera: Curculionidae). Journal of Economic Entomology 99, 2030-2037.
77. Wilkinson S, Davies WJ. 2002. ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant, Cell and Environment 25, 195-210.
78. Yang JW, Yi HS, Kim H, Lee B, Lee S, Ghim SY, Ryu CM. 2011. Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the belowground microflora. Journal of Ecology 99, 46-56.
79. Yi H-S, Yang JW, Ghim S-Y, Ryu C-M. 2011. A cry for help from leaf to root: above ground insect feeding leads to the recruitment of rhizosphere microbes for plant self-protection against subsequent diverse attacks. Plant Signaling and Behavior 6, 1192-1194.
80. Zamioudis C, Pieterse CMJ. 2012. Modulation of host immunity by beneficial microbes. Molecular Plant-Microbe Interactions 25, 139-150.
81. Zhang H, Schonhof I, Krurnbein A, Gutezeit B, Li L, Stuzel H, Schreiner M. 2008. Water supply and growing season influence glucosinolate concentration and composition in turnip root (Brassica rapa ssp rapifera L.). Journal of Plant Nutrition and Soil Science-Zeitschrift für Pflanzenernahrung und Bodenkunde 171, 255-265.
82. Zhang Z, Stout MJ, Shang H, Pousson RC. 2006. Adaptations of larvae and pupae of the rice water weevil, Lissorhoptrus oryzophilus Kuschel (Coleoptera: Curculionidae), to living in flooded soils. Journal of the Kansas Entomological Society 79, 176-183.
83. Zvereva EL, Kozlov MV. 2012. Sources of variation in plant responses to belowground insect herbivory: a meta-analysis. Oecologia 169, 441-452.