Optimizing Crops for Biocontrol of Pests and Disease

Trends in Plant Science

Volumn 20, Issue 11, 2015, Pages 698-712

  Stenberg, Johan A ^a   Heil, Martin ^b   Åhman, Inger ^a   Björkman, Christer ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOLOGICAL PEST CONTROL; CROP; GENETICS; INSECT; MITE; NEMATODE; PLANT BREEDING; PLANT DISEASE; PREVENTION AND CONTROL;

ANIMALS; CROPS, AGRICULTURAL; INSECTS; MITES; NEMATODA; PEST CONTROL, BIOLOGICAL; PLANT BREEDING; PLANT DISEASES;

EID: 84946495646     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2015.08.007     Document Type: Review

References (135)

1. Evans L.T. Crop Evolution, Adaptation and Yield 1996, Cambridge University Press.
2. Hammer K. Das Domestikationssyndrom. Kulturpflanze 1984, 32:11-34.
3. Andersen M.M., et al. Feasibility of new breeding techniques for organic farming. Trends Plant Sci. 2015, 20:426-434.
4. Dangl J.L., et al. Pivoting the plant immune system from dissection to deployment. Science 2013, 341:746-751.
5. Hammond-Kosack K.E., Parker J.E. Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 2003, 14:177-193.
6. Godfray H.C.J., et al. Food security: the challenge of feeding 9 billion people. Science 2010, 327:812-818.
7. Tamiru A., et al. New directions for improving crop resistance to insects by breeding for egg induced defence. Curr. Opin. Insect Sci. 2015, Published online February 28, 2015. 10.1016/j.cois.2015.02.011.
8. Arimura G., et al. Herbivore-induced, indirect plant defences. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2005, 1734:91-111.
9. Walling L.L. The myriad plant responses to herbivores. J. Plant Growth Regul. 2000, 19:195-216.
10. Conrath U., et al. Priming: getting ready for battle. Mol. Plant Microbe Interact. 2006, 19:1062-1071.
11. Frost C., et al. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 2008, 146:818-824.
12. Karban R., Baldwin I.T. Induced Responses to Herbivory 1997, University of Chicago Press.
13. Heil M. Plastic defence expression in plants. Evol. Ecol. 2010, 24:555-569.
14. Karban R. The ecology and evolution of induced resistance against herbivores. Funct. Ecol. 2011, 25:339-347.
15. Heil M. Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol. 2014, 204:297-306.
16. Unsicker S.B., et al. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 2009, 12:479-485.
17. Dudareva N., et al. Plant volatiles: recent advances and future perspectives. Crit. Rev. Plant Sci. 2006, 25:417-440.
18. Heil M. Indirect defence via tritrophic interactions. New Phytol. 2008, 178:41-61.
19. Heil M. Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annu. Rev. Entomol. 2015, 60:213-232.
20. Khan Z.R., et al. Achieving food security for one million sub-Saharan African poor through push-pull innovation by 2020. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2014, 369. 0120284.
21. Atanassov A., Shearer P. Peach extrafloral nectar impacts life span and reproduction of adult Grapholita molesta (Busck) (Lepidoptera: Tortricidae). J. Agric. Urban Entomol. 2005, 22:41-47.
22. Brown M.W., et al. Extrafloral nectar in an apple ecosystem to enhance biological control. J. Econ. Entomol. 2010, 103:1657-1664.
23. Mathews C.R., et al. Interactions between extrafloral nectaries, ants (Hymenoptera: Formicidae), and other natural enemies affect biological control of Grapholita molesta (Lepidoptera: Tortricidae) on Peach (Rosales: Rosaceae). Environ. Entomol. 2011, 40:42-51.
24. James D.G., Price T.S. Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J. Chem. Ecol. 2004, 30:1613-1628.
25. Orre-Gordon G.U.S., et al. 'Attract and reward': combining a herbivore-induced plant volatile with floral resource supplementation - multi-trophic level effects. Biol. Contr. 2013, 64:106-115.
26. Mérey G.v., et al. Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpenes by the plants, but has little effect on the attraction of pest and beneficial insects. Phytochemistry 2011, 72:1838-1847.
27. Åhman I., et al. The potential for modifying plant volatile composition to enhance resistance to arthropod pests. CAB Rev. Perspect. Agricul. Vet. Sci., Nutr. Nat. Res. 2010, 5:006.
28. Bruce T.J.A., et al. The first crop plant genetically engineered to release an insect pheromone for defence. Sci. Rep. 2015, 5:11183.
29. Barrett L.G., Heil M. Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci. 2012, 17:282-292.
30. Dicke M., Sabelis M.W. How plants obtain predatory mites as bodyguards. Netherlands J. Zool. 1988, 38:148-165.
31. Turlings T.C.J., et al. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 1990, 250:1251-1253.
32. Dicke M., Baldwin I.T. The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends Plant Sci. 2010, 15:167-175.
33. Clavijo McCormick A., et al. The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci. 2012, 17:303-310.
34. Dicke M., et al. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 2009, 5:317-324.
35. Kessler A., Baldwin I.T. Defensive function of herbivore-induced plant volatile emissions in nature. Science 2001, 291:2141-2144.
36. Rasmann S., et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 2005, 434:732-737.
37. de Moraes C.M., et al. Herbivore-infested plants selectively attract parasitoids. Nature 1998, 393:570-573.
38. Thaler J.S. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 1999, 399:686-688.
39. Khan Z.R., et al. Intercropping increases parasitism of pests. Nature 1997, 388:631-632.
40. Hassanali A., et al. Integrated pest management: the push-pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2008, 363:611-621.
41. Braasch J., Kaplan I. Over what distance are plant volatiles bioactive? Estimating the spatial dimensions of attraction in an arthropod assemblage. Entomol. Exp. Appl. 2012, 145:115-123.
42. Kaplan I. Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire?. Biol. Contr. 2012, 60:77-89.
43. Turlings T.C.J., Ton J. Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr. Opin. Plant Biol. 2006, 9:421-427.
44. Kelly J.L., et al. Semiochemical lures reduce emigration and enhance pest control services in open-field predator augmentation. Biol. Contr. 2014, 71:70-77.
45. Lundgren J.G. Relationships of Natural Enemies and Non-Prey Foods 2009, Springer.
46. Narvaez A., et al. Effect of different dietary resources on longevity, carbohydrate metabolism, and ovarian dynamics in two fruit fly parasitoids. Arthropod Plant Interact. 2012, 6:361-374.
47. Wäckers F.L., et al. Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications 2005, Cambridge University Press.
48. Stenberg J.A., et al. Uncoupling direct and indirect plant defences: novel opportunities for improving crop security in willow plantations. Agricul. Ecosyst. Environ. 2010, 139:528-533.
49. Stenberg J.A., et al. Host-plant genotype mediates supply and demand of animal food in an omnivorous insect. Ecol. Entomol. 2011, 36:442-449.
50. Ferreira J.A.M., et al. Leaf domatia reduce intraguild predation among predatory mites. Ecol. Entomol. 2011, 36:435-441.
51. Ågren G.I., et al. Omnivores as plant bodyguards - a model of the importance of plant quality. Basic Appl. Ecol. 2012, 13:441-448.
52. Chamberlain S.A., Holland J.N. Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 2009, 90:2384-2392.
53. Romero G.Q., Koricheva J. Contrasting cascade effects of carnivores on plant fitness: a meta-analysis. J. Anim. Ecol. 2011, 80:696-704.
54. Rosumek F.B., et al. Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 2009, 160:537-549.
55. Mathews C.R., et al. Extrafloral nectaries alter arthropod community structure and mediate peach (Prunus persica) plant defense. Ecol. Appl. 2009, 19:722-730.
56. Mathews C.R., et al. Leaf extrafloral nectaries enhance biological control of a key economic pest, Grapholita molesta (Lepidoptera: Tortricidae), in peach (Rosales: Rosaceae). Environ. Entomol. 2007, 36:383-389.
57. Abdala-Roberts L., et al. Plant traits mediate effects of predators across pepper (Capsicum annuum) varieties. Ecol. Entomol. 2014, 39:361-370.
58. Agrawal A.A., Karban R. Domatia mediate plant-arthropod mutualism. Nature 1997, 387:562-563.
59. Agrawal A.A., et al. How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 2000, 89:70-80.
60. Scala A., et al. Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens. Int. J. Mol. Sci. 2013, 14:17781-17811.
61. Turlings T.C.J., et al. Timing of induced volatile emissions in maize seedlings. Planta 1998, 207:146-152.
62. Quintana-Rodriguez E., et al. Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J. Ecol. 2015, 103:250-260.
63. Park S.W., et al. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 2007, 318:113-116.
64. Arimura G-I., et al. Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 2000, 406:512-515.
65. Frost C., et al. Within-plant signalling by volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 2007, 10:490-498.
66. Heil M., Silva Bueno J.C. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5467-5472.
67. Engelberth J., et al. Airborne signals prime plants against insect herbivore attack. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:1781-1785.
68. Heil M., Kost C. Priming of indirect defences. Ecol. Lett. 2006, 9:813-817.
69. Kessler A., et al. Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 2006, 148:280-292.
70. Yi H-S., et al. Airborne induction and priming of plant resistance to a bacterial pathogen. Plant Physiol. 2009, 151:2152-2161.
71. Thaler J.S., et al. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 2012, 17:260-270.
72. Chen Y.H., et al. Crop domestication and its impact on naturally selected trophic interactions. Annu. Rev. Entomol. 2015, 60:35-58.
73. Rodriguez-Saona C., et al. Field responses of predaceous arthropods to methyl salicylate: A meta-analysis and case study in cranberries. Biol. Contr. 2011, 59:294-303.
74. 16 homoterpene TMTT in Lotus japonicus through overexpression of (E,E)-geranyllinalool synthase attracts generalist and specialist predators in different manners. New Phytol. 2013, 200:1200-1211.
75. Shiojiri K., et al. Changing green leaf volatile biosynthesis in plants: An approach for improving plant resistance against both herbivores and pathogens. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:16672-16676.
76. Birkett M.A., Pickett J.A. Prospects of genetic engineering for robust insect resistance. Curr. Opin. Plant Biol. 2014, 19:59-67.
77. Ballhorn D.J., et al. Distance and sex determine host plant choice by herbivorous beetles. PLoS ONE 2013, 8:e55602.
78. Bruce T.J.A., Pickett J.A. Perception of plant volatile blends by herbivorous insects - finding the right mix. Phytochemistry 2011, 72:1605-1611.
79. Halitschke R., et al. Shared signals - 'alarm calls' from plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 2008, 11:24-34.
80. von Merey G.E., et al. Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodoptera frugiperda in Mexican maize fields. Biol. Contr. 2012, 60:7-15.
81. Gouinguené S.P., Turlings T.C.J. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol. 2002, 129:1296-1307.
82. Pichersky E., et al. Biosynthesis of plant volatiles: Nature's diversity and ingenuity. Science 2006, 311:808-811.
83. Holopainen J.K., Gershenzon J. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 2010, 15:176-184.
84. Gish M., et al. Herbivore-induced plant volatiles in natural and agricultural ecosystems: open questions and future prospects. Curr. Opin. Insect Sci. 2015, 9:1-6.
85. Loreto F., et al. Plant volatiles and the environment. Plant Cell Environ. 2014, 37:1905-1908.
86. Kessler A., Heil M. The multiple faces of indirect defences and their agents of natural selection. Funct. Ecol. 2011, 25:348-357.
87. Rodriguez-Saona C., et al. Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. J. Exp. Bot. 2011, 62:2633-2644.
88. Tamiru A., et al. Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol. Lett. 2011, 14:1075-1083.
89. Åhman I. Breeding for inducible resistance. IOBC WPRS Bulletin 2013, 89:311-317.
90. Kanchiswamy C.N., et al. Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends Plant Sci. 2015, 20:206-211.
91. Heil M., Baldwin I.T. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 2002, 7:61-67.
92. Gols R., et al. Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J. Chem. Ecol. 2008, 34:132-143.
93. Bukovinszky T., et al. Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 2009, 160:299-308.
94. Chen Y.H., Welter S.C. Crop domestication creates a refuge from parasitism for a native moth. J. Appl. Ecol. 2007, 44:238-245.
95. Wang X-G., et al. Larger olive fruit size reduces the efficiency of Psyttalia concolor, as a parasitoid of the olive fruit fly. Biol. Contr. 2009, 49:45-51.
96. Collier T., Van Steenwyk R. A critical evaluation of augmentative biological control. Biol. Contr. 2004, 31:245-256.
97. Loughrin J.H., et al. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J. Chem. Ecol. 1995, 21:1217-1227.
98. Beach R.M., et al. Nectaried and nectariless cotton cultivars as nectar sources for the adult soybean looper. J. Entomol. Sci. 1985, 20:233-236.
99. Benrey B., et al. The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biol. Contr. 1998, 11:130-140.
100. Ballhorn D.J., et al. Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus L.). J. Ecol. 2008, 96:971-980.
101. Gouinguené S., et al. Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 2001, 11:9-16.
102. Cortesero A.M., et al. Understanding and manipulating plant attributes to enhance biological control. Biol. Contr. 2000, 17:35-49.
103. Simpson M., et al. Field evaluation of the 'attract and reward' biological control approach in vineyards. Ann. Appl. Biol. 2011, 159:69-78.
104. Hagenbucher S., et al. Resistance mechanisms against arthropod herbivores in cotton and their interactions with natural enemies. Crit. Rev. Plant Sci. 2013, 32:458-482.
105. Hare J.D. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu. Rev. Entomol. 2011, 56:161-180.
106. Rudgers J.A. Enemies of herbivores can shape plant traits: Selection in a facultative ant-plant mutualism. Ecology 2004, 85:192-205.
107. Wooley S.C., et al. Extrafloral nectaries in aspen (Populus tremuloides): heritable genetic variation and herbivore-induced expression. Ann. Bot. 2007, 100:1337-1346.
108. Berlin Kolm S., et al. Nya salixsorter med modern växtförädlingsteknik. Fakta Jordbruk 2011, 1:1-6.
109. Hare J.D. Ontogeny and season constrain the production of herbivore-inducible plant volatiles in the field. J. Chem. Ecol. 2010, 36:1363-1374.
110. Hoballah M.E., et al. Costs of induced volatile production in maize. Oikos 2004, 105:168-180.
111. Dicke M., Sabelis M.W. Does it pay plants to advertize for bodyguards? Towards a cost-benefit analysis of induced synomone production. Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants 1989, 341-358. SPB Publishing. H. Lambers (Ed.).
112. Robert C., et al. A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecol. Lett. 2012, 15:55-64.
113. Gols R., et al. Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 2008, 89:1616-1626.
114. Harvey J.A., et al. Tri-trophic effects of inter- and intra-population variation in defence chemistry of wild cabbage (Brassica oleracea). Oecologia 2011, 166:421-431.
115. Stenberg J.A. Plant-mediated effects of different Salix species on the performance of the braconid parasitoid Perilitus brevicollis. Biol. Contr. 2012, 60:54-58.
116. Fatouros N.E., et al. Synergistic effects of direct and indirect defences on herbivore egg survival in a wild crucifer. Proc. Biol. Sci. 2014, 281:20141254.
117. Stenberg J.A., et al. Plant defence: feeding your bodyguards can be counter-productive. Basic Appl. Ecol. 2011, 12:629-633.
118. Engelberth J., et al. Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Mol. Plant Microbe Interact. 2007, 20:707-716.
119. Heil M. Nectar: generation, regulation and ecological functions. Trends Plant Sci. 2011, 16:191-200.
120. Tamiru A., et al. Oviposition induced volatile emissions from African smallholder farmers' maize varieties. J. Chem. Ecol. 2012, 38:231-234.
121. Ninkovic V., et al. The influence of aphid-induced plant volatiles on ladybird beetle searching behavior. Biol. Contr. 2001, 21:191-195.
122. Mäntylä E., et al. From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE 2008, 3:e2832.
123. Mäntylä E., et al. Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature?. Athrop. Plant Interact. 2014, 8:143-153.
124. Zakir A., et al. Herbivore-induced plant volatiles provide associational resistance against an ovipositing herbivore. J. Ecol. 2013, 101:410-417.
125. Kost C., Heil M. The defensive role of volatile emission and extrafloral nectar secretion for Lima bean in nature. J. Chem. Ecol. 2008, 34:2-13.
126. de Moraes C.M., et al. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 2001, 410:577-580.
127. Tahmasebi Z., et al. Herbivore-induced indirect defense across bean cultivars is independent of their degree of direct resistance. Exp. Appl. Acarol. 2014, 63:217-239.
128. Poelman E.H., et al. Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Funct. Ecol. 2009, 23:951-962.
129. Nissinen A., et al. Influence of carrot psyllid (Trioza apicalis) feeding or exogenous limonene or methyl jasmonate treatment on composition of carrot (Daucus carota) leaf essential oil and headspace volatiles. J. Agric. Food Chem. 2005, 53:8631-8638.
130. Krips O.E., et al. Comparison of cultivars of ornamental crop Gerbera jamesonii on production of spider mite-induced volatiles, and their attractiveness to the predator Phytoseiulus persimilis. J. Chem. Ecol. 2001, 27:1355-1372.
131. Scutareanu P., et al. Constitutive and herbivore-induced volatiles in pear, alder and hawthorn trees. Chemoecology 2003, 13:63-74.
132. Lou Y.G., et al. Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field. J. Chem. Ecol. 2006, 32:2375-2387.
133. Michereff M.F.F., et al. Volatiles mediating a plant-herbivore-natural enemy interaction in resistant and susceptible soybean cultivars. J. Chem. Ecol. 2011, 37:273-285.
134. Himanen S., et al. Effects of cyclamen mite (Phytonemus pallidus) and leaf beetle (Galerucella tenella) damage on volatile emission from strawberry (Fragaria × ananassa Duch.) plants and orientation of predatory mites (Neoseiulus cucumeris, N. californicus, and Euseius finlandicus). J. Agric. Food Chem. 2005, 53:8624-8630.
135. Lehrman A., et al. Constitutive and herbivore-induced systemic volatiles differentially attract an omnivorous biocontrol agent to contrasting Salix clones. AoB Plants 2013, 5:plt005.