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Resistance Mechanisms Against Arthropod Herbivores in Cotton and Their Interactions with Natural Enemies

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Resistance Mechanisms Against Arthropod Herbivores in Cotton and Their Interactions with Natural Enemies Critical Reviews in Plant Sciences, 32:458–482, 2013 Copyright C Taylor & Francis Group, LLC ISSN: 0735-2689 print / 1549-7836 online DOI: 10.1080/07352689.2013.809293 Resistance Mechanisms Against Arthropod Herbivores in Cotton and Their Interactions with Natural Enemies S. Hagenbucher,1 D. M. Olson,2 J. R. Ruberson,3 F. L. Wackers,¨ 4 and J. Romeis1 1Agroscope Reckenholz-Tanikon¨ Research Station ART, Reckenholzstr. 191, 8046 Zurich, Switzerland 2Crop Protection and Management Research Unit, USDA-ARS, Tifton, Georgia, USA 3Department of Entomology, University of Georgia, Tifton, Georgia, USA 4Lancaster Environment Centre, Lancaster University, LA1 4YQ Lancaster, United Kingdom Table of Contents I. INTRODUCTION ..................................................................................................................................................................................................459 II. DIRECT RESISTANCE MECHANISMS ..................................................................................................................................................461 A. Morphological Traits ........................................................................................................................................................................................461 1. Impact of trichomes on herbivores .......................................................................................................................................................462 2. Impact of trichomes on natural enemies .............................................................................................................................................462 B. Plant Secondary Metabolites .........................................................................................................................................................................463 1. Terpenoids .....................................................................................................................................................................................................463 1.1. Terpenoid distribution .....................................................................................................................................................................463 1.2. Impact of terpenoids on herbivores ............................................................................................................................................464 1.3. Induction of glands and terpenoids ............................................................................................................................................466 2. Impact of other plant metabolites on herbivores ..............................................................................................................................468 3. Impact of secondary plant metabolites on natural enemies .........................................................................................................469 III. INDIRECT RESISTANCE MECHANISMS .............................................................................................................................................469 A. Volatiles ................................................................................................................................................................................................................469 1. Release of volatile compounds ..............................................................................................................................................................469 2. Arthropod response to cotton volatiles ...............................................................................................................................................470 B. Extrafloral Nectaries ........................................................................................................................................................................................471 IV. INSECT-RESISTANT TRANSGENIC COTTON ..................................................................................................................................472 V. INFLUENCE OF ENVIRONMENTAL CONDITIONS ON COTTON ARTHROPOD RESISTANCE .....................473 Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 VI. CONCLUSIONS .....................................................................................................................................................................................................474 ACKNOWLEDGMENTS ..............................................................................................................................................................................................475 REFERENCES ...................................................................................................................................................................................................................475 Address correspondence to J. Romeis, Agroscope ART, Reckenholzstrasse 59, 8046 Zurich, Switzerland. E-mail: joerg.romeis@ agroscope.admin.ch 458 ARTHROPOD HERBIVORES IN COTTON 459 cluding specialists like the boll weevil, Anthonomus grandis Cotton plants (genus Gossypium)aregrownonmorethan30 (Coleoptera: Curculionidae) and polyphagous insects like He- million hectares worldwide and are a major source of fiber. The liothis/Helicoverpa spp. (Lepidoptera: Noctuidae) (Matthews plants possess a wide range of direct and indirect resistance mech- and Tunstall, 1994). Additionally, cotton supports a high diver- anisms against herbivorous arthropods. Direct resistance mecha- sity of entomophagous arthropods: over 600 species of preda- nisms include morphological traits such as trichomes and a range of secondary metabolites. The best known insecticidal compounds tors, including dragonflies, beetles, and spiders were reported are the terpenoid gossypol and its precursors and related com- from cotton fields in Arkansas (U.S.) alone (Whitcomb and Bell, pounds. Indirect resistance mechanisms include herbivore-induced 1964). volatiles and extrafloral nectaries that allow plants to attract and Despite intensive pest management, the many arthropod her- sustain natural enemy populations. We discuss these resistance bivores of cotton cause considerable damage (Matthews and traits of cotton, their induction by herbivores, and their impact on herbivores and natural enemies. In addition, we discuss the use of Tunstall, 1994; King et al., 1996). For example, in the United genetically engineered cotton plants to control pest Lepidoptera States, yield losses due to arthropod pests averaged 3.1% be- and the influence of environmental factors on the resistance traits. tween 2006 and 2012 (Figure 1). It needs to be taken into account that even a small percentage of yield loss translates Keywords Bt-cotton, Gossypium, gossypol, host plant resistance, op- into a high economic loss. In 2012 total yield reduction from timal defense theory, plant defense arthropod pests in the United States was 2.04%, represent- ing a loss of >700,000 bales of cotton valued at >381 mil- I. INTRODUCTION lion US$. If management costs are included, the total eco- Cotton (Gossypium spp.) is one of the most important natu- nomic damage was >1 billion US$ (http://www.biochemistry. ral sources of textile fiber, accounting for around 50% of all msstate.edu/resources/cottoncrop.asp). fibers used by humans (Matthews and Tunstall, 1994). The Many key pests of cotton are in the order Lepidoptera, a genus Gossypium belongs to the tribe Gossypiae, together with number of which damage the reproductive organs, and thereby the genera Cephalohibiscus, Cienfuegosia, Gossypioides, Ham- causing severe losses to fiber production. Some of the most pea, Kokia, Lebronnecia and Thespesia (Fryxell, 1979). Among notorious pest species belong to the family Noctuidae, namely other traits, this tribe is characterized by small lysigenous glands the polyphagous New World species Heliothis virescens and (glands formed through cell lysis) on the plants’ surface. The Helicoverpa zea and the Old World and Australasia species genus Gossypium contains around 50 species (Wendell et al., Helicoverpa armigera and Helicoverpa punctigera (the latter 2010) that have evolved in tropical and subtropical parts of occurring only in Australia). The globally distributed pink boll- South and Central America, the Caribbean, Australasia, Africa worm Pectinophora gossypiella (Gelechiidae) is a highly spe- and Oceania (Fryxell, 1979). A distinct group of six Gossyp- cialized cotton herbivore and a serious pest. In the United States, ium species (G. hirsutum, G. barbadense, G. tomentosum, G. however, this species has been nearly eradicated (section IV). lancelotum, G. darwinii and, G. mustelinum) in South and Cen- Other important pests include Earias species, such as E. vitella, tral America are tetraploid, whereas all other cotton species are E. fabia, E. insulana, E. biplaga, and E. cupreoviridis (Noc- diploid (Fryxell, 1979). tuidae), which also act as stem borers, and Diparopsis species Four species of Gossypium are of economic importance: (Noctuidae), which are major cotton pests in Africa. Defoliat- G. hirsutum, G. barbadense, G. arboreum and G. herbaceum. ing caterpillars can also contribute to yield losses, although a They were most likely domesticated independently of one an- healthy cotton plant can tolerate losses of up to 20% of its total other (Fryxell, 1979). Whereas the dominant
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