Plant Defence Against Herbivory and Insect Adaptations

Review SPECIAL ISSUE: Using Non-Model Systems to Explore

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Plant defence against herbivory and insect adaptations

Abdul Rasheed War1*, Gaurav Kumar Taggar2, Barkat Hussain3, Monica Sachdeva Taggar4, Ramakrishnan M. Nair1 and Hari C. Sharma5* 1World Vegetable Center, South Asia, Hyderabad 502324, Andhra Pradesh, India 2Department of Plant Breeding & Genetics, Punjab Agricultural University, Ludhiana 141004, Punjab, India 3Division of Entomology, SKUAST-K, Shalimar 190001, Srinagar, Jammu and Kashmir, India 4School of Renewable Energy Engineering, Punjab Agricultural University, Ludhiana 141004, Punjab, India 5YSP University of Horticulture and Forestry, Nauni 173230, Solan, Himachal Pradesh, India Received: 10 November 2017 Editorial decision: 31 May 2018 Accepted: 9 June 2018 Published: 12 June 2018 Guest Editor: Rupesh Kariyat Citation: War AR, Taggar GK, Hussain B, Taggar MS, Nair RM, Sharma HC. 2018. Plant defence against herbivory and insect adaptations. AoB PLANTS 10: ply037; doi: 10.1093/aobpla/ply037

Abstract. There is always a silent war between plants and herbivorous insects that we are rarely privy to. In this silent war, chemicals act as both weapons and messengers. Insect–plant co-evolution is going on for millions of years. Plants always look for new strategies to avoid insect pests and insects, in turn, are always ready to develop counter-adaptations. This intricate interaction has led to the development of a number of plant defensive traits and the counter-adaptive features in insects as well. Both plants and insects have developed morphological and biochemical defensive traits to dodge each other’s strategies. However, biochemical interactions are considered more important and effective than morphological ones because of their dynamic nature. Some of the plant defensive traits evolved during this evolution include toxic furanocoumarins, toxic amino acids, trichomes, lignin and latex. Since there is an increasing focus on improving crop production through safe and sustainable means by reducing the reliance on pesticides, it is highly important to understand the plant defensive traits against insect herbivory. It is equally important to understand the adaptations by insect pests to these defensive traits in order to develop and deploy management strategies to outsmart the insect pests. Here we discuss the plant defence traits against insect herbivory, their induction by elicitors and/or insect damage, and the counter-adaptation by insect pests.

Keywords: Adaptations; induced resistance; insect pests; plant secondary metabolites; plant volatiles.

Introduction plants have developed an array of defensive strategies (Zhao et al. 2009; Karban 2011; War et al. 2012) by produc- Plants and insects have co-evolved continuously since ing various morphological and biochemical defences that the first appearance of phytophagous insects in the his- restrict the insect pests (Fig. 1; Howe and Jander 2008; War tory of life. Insect herbivory forms a critical component in et al. 2012). The morphological defensive responses include insect–plant co-evolution (Howe and Jander 2008; Zhao increase in the trichomes, sclerophylly, latex deposition, et al. 2009; Karban 2011). To avoid damage by insect pests,

*Corresponding author’s e-mail address: [email protected]; [email protected]; [email protected]

© The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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etc. (Dalin and Björkman 2003; War et al. 2013a, b) and the to their offspring as reported in wild radish, Raphanus biochemical traits include various toxic secondary metab- raphanistrum infested by Pieris rapae (Agrawal 2002). olites produced in plants on account of insect herbivory The transgenerational effect of induced resistance (Karban 2011; Taggar et al. 2012; Holopainen and Blande makes plants more vigorous and reduces insect infest- 2013; War et al. 2013b; Kaur et al. 2015). ation in progeny (Agrawal 2002). However, insects pre- Plant defence may directly affect insect growth and cisely adapt to the plant defensive traits that allow them Downloaded from https://academic.oup.com/aobpla/article-abstract/10/4/ply037/5036447 by University of Bologna user on 09 April 2019 development through toxic secondary metabolites or to feed successfully on the otherwise hostile and unpre- indirectly by recruiting the natural enemies of the insect dictable host (Zhu-Salzman et al. 2003; Ahn et al. 2007; pest through herbivore-induced plant volatiles (HIPVs) Després et al. 2007; War and Sharma 2014). This con- and extrafloral nectar (Arimura et al. 2009; Karban tinuous race between the two entities to outsmart each 2011; War et al. 2012). Induced resistance in response to other has led to the development of more defensive herbivore attack makes host plants phenotypically plas- traits in plants and strong counter-adaptive strategies tic and plant tissues less nutritious, thus making them a in insect pests (Zhu-Salzman et al. 2003; Sharma et al. less attractive food choice and practically unpalatable 2009; War and Sharma 2014). to insect pests (Karban 2011). Induced resistance is also sensed in the undamaged parts of the same plant and the neighbouring plants as well (Holopainen and Blande Co-evolution between plants and insects 2013). Further, induced resistance may also show a Insect–plant co-evolution has been ongoing for 400 transgenerational effect, i.e. transferring from parents million years (Labandeira 2013). In response to insect

Figure 1. Plant defence against insect pests (EPF = extrafloral nectar; HIPV = herbivore induced plant volatiles; JA = jasmonic acid; SA = salicylic acid).

herbivory, natural selection has resulted in the evolution leaf-chewing herbivores, showed the lowest genetic cor- of morphological, behavioural and biochemical diver- relation (Leimu and Koricheva 2006). sity among plants and insect pests. The plant defensive Both morphological and biochemical defences traits confer direct resistance against insect pests and in plants are important to withstand insect attack. also provide high competitive ability in the absence of Although morphological defence is primarily used by insect pests (Agrawal et al. 2012; Hare 2012). The gen- plants against insect pests, the biochemical-based Downloaded from https://academic.oup.com/aobpla/article-abstract/10/4/ply037/5036447 by University of Bologna user on 09 April 2019 eralist and specialist insect herbivores show an evo- defence is considered more effective as it directly affects lution of some candidate genes responsible for their insect growth and development (Kariyat et al. 2013). adaptation to host plants as reported in the pea aphid, The HIPVs indirectly defend plants by recruiting the nat- Acyrthosiphon pisum (Jaquiery et al. 2012). Also, another ural enemies of the insect pests, such as parasitoids specialist insect pest, Drosophila sechellia, evolved on and predators (Arimura et al. 2009; War et al. 2011). Morinda citrifolia shows higher expression levels of Induced resistance in plants against biotic stresses is neurons ab3 and ab3B. These neurons are sensitive to attributed to the phenylpropanoid and octadecanoid hexanoate esters and 2-heptanone, respectively, and pathways mediated by salicylic acid (SA) and jasmonic enable the pest to recognize the odours from Morinda acid (JA), respectively (Zhao et al. 2009; Scott et al. 2010; fruit (Ibba et al. 2010). Similarly, grubs of the bruchid He et al. 2011). These pathways produce a number of beetle Caryedes brasiliensis feed on the seeds of Dioclea plant defensive secondary metabolites in intermediate megacarpa, which contain a toxic non-protein amino steps, which affect insect growth and development and acid L-canavanine. A modified tRNA synthetase in these also release volatiles that attracts the insect’s natural grubs distinguishes between L-canavanine and arginine enemies (Howe and Jander 2008; He et al. 2011). (Rosenthal et al. 1976). Eco-genomic tools have been implicated in studying the genetic basis of plant defensive traits in many plant systems (Schranz et al. 2009). Plant defence elicitors They can further be used to study the constitutive and Plants recognize cues in the insect’s oral secretion/saliva inducible defences by focusing on the polymorphic traits and in the ovipositional fluid (Schmelz et al. 2006; Alborn or follow the transgenic approaches to study the gene et al. 2007; Wu et al. 2007; Howe and Jander 2008). Insect function and ecological consequences (Schranz et al. oral secretions contain specific elicitors such as fatty 2009). acid conjugates (FACs), which stimulate plant defence. The first plant defence elicitor identified from the oral secretions of beet armyworm, Spodoptera exigua, was Plant defence against insect herbivory volicitin (N-(17-hydroxylinolenoyl)-L-glutamine), whose Host plant resistance is an important form of plant application on maize wounds resulted in the emission defence against insect herbivory and is widely implicated of a blend of volatiles that attracted natural enemies in crop protection against insect pests and diseases of the pest (Alborn et al. 1997). N-linolenoyl-glu, a (Sharma et al. 2009; Maffei et al. 2012; Pieterse et al. potential elicitor of volatiles in tobacco plants isolated 2012; War et al. 2012). The constitutive plant defence from tobacco hornworm, Manduca sexta regurgitate is present in plants irrespective of the external stimuli, (Halitschke et al. 2001), when applied to the wounded while the induced defence is stimulated by insect feed- leaves of tobacco activates mitogen-activated protein ing and/or the elicitor application (Sharma et al. 2009; kinase (MAPK), wound-induced protein kinase (WIPK), War et al. 2012). Moreover, plants manage the resources SA-induced protein kinase (SIPK), JA, SA, ethylene (ET) between defence and growth by eliciting anti-herbivore and JA-isoleucine conjugate (JA-Ile) (Wu et al. 2007). defence only when necessary (Karban 2011). The MAPK pathway is involved in plant growth and devel- A meta-analysis of genetic correlation between plant opment and activates various signalling pathways in the resistance to multiple enemies has shown positive cor- host plant in response to biotic and abiotic stresses such relations if both the compared species are generalist as cold, drought, pathogens and insect attack (Wu et al. herbivores or both are specialist herbivores (Leimu and 2007). Further, 7-epi-JA induced by FACs elicits plant Koricheva 2006). Plant resistance to herbivores showed defensive genes against herbivory (Halitschke et al. positive genetic correlation from herbivores with differ- 2001). ent feeding habits, such as gall inducers and leaf min- Inceptins and caeliferins in the oral secretions of ers, miners and leaf folders, and leaf folders and gall many insects also activate plant defensive pathways inducers (Leimu and Koricheva 2006). Mechanism of against insect pests (Schmelz et al. 2006; Alborn et al. resistance in the pairwise comparison between insects 2007). Plastidic ATP synthase, γ-subunit gives rise to of different feeding guilds, such as phloem-feeding and inceptins, whereas the caeliferins are sulfated fatty

acids (Schmelz et al. 2006; Alborn et al. 2007). The glu- (Thines et al. 2007). The removal of repression of JAZ cose oxidase (GOX) in the saliva of Ostrinia nubilalis proteins activates the JA-responsive genes such as the and Helicoverpa zea mediates the defensive signalling genes encoding JAZ proteins (Thines et al. 2007). The pathways in tomato (Tian et al. 2012; Louis et al. 2013). JA signalling pathway has two branches, MYC2 branch Further, salivary components of O. nubilalis induce the that regulates defence against insect herbivores and expression of Proteinase Inhibitor 2 (PIN2) and maize pro- the ethylene response factor (ERF) branch that regu- Downloaded from https://academic.oup.com/aobpla/article-abstract/10/4/ply037/5036447 by University of Bologna user on 09 April 2019 tease inhibitor genes in tomato and maize, respectively lates plant defence against necrotrophic pathogens (Louis et al. 2013). Some reports show the suppression (Pieterse et al. 2012). The expression of wound-inducible of plant defensive responses by insect oral secretions. vegetative storage protein 2 (VSP2) and lipoxygenase 2 For example, oral secretions of the African cotton leaf- (LOX2) genes is regulated by the MYC2 branch, while as worm, Spodoptera littoralis and cabbage butterfly, Pieris ERF branch regulates the expression of ERF1 and octa- brassicae cause suppression of plant defence responses decanoid-responsive Arabidopsis 59 (ORA59). These, in in Arabidopsis resulting in increased larval weights turn, regulate plant defensin genes such as plant defen- (Consales et al. 2012). sin 1.2 (PDF1.2) (Dombrecht et al. 2007). Under multiple herbivore attacks, crosstalk occurs between signalling Mechanism of signal transduction pathways to induce specific responses against insect herbivores (Pieterse et al. 2012). Jasmonic acid and SA pathways crosstalk antagonistically and the process is mediated Plants respond to herbivory by induction of signal trans- by the MAPKs, WRKY, NPR1 and ET (Pieterse et al. 2012; duction pathways, which lead to changes in the expres- Thaler et al. 2012). Herbivores are sometimes bene- sion of defence-related genes and finally, the induction fited by the crosstalk between signalling pathways. For of biosynthesis pathways (Howe and Jander 2008; example, M. sexta feeding suppresses the nicotine but Maffei et al. 2012; Thaler et al. 2012). Plants recognize induces ET accumulation in nicotine plants (Kahl et al. the plant defence elicitors from herbivores and initiate 2000). the defensive process by activating kinase networks and phytohormones (Maffei et al. 2012; Pieterse et al. 2012). The important plant signalling phytohormones are JA, How do insects adapt to plant defence? SA and ET. Jasmonic acid and SA mediated signalling Insect pests can be generalist or specialist herbivores. pathways against chewing insects (Howe and Jander The generalist herbivores feed on a number of host 2008) and phloem-feeding insects (Pieterse et al. 2012), plants and have a complex defensive system since they respectively. However, in rice plants, resistance to leaf encounter a wide variety of plant defensive chemicals, folder Cnaphalocrocis medinalis is mediated by SA and while specialist insect pests have a restricted host range ET signalling pathways (Wang et al. 2011). When plants and cannot adapt easily to the variety of toxic plant are infested by sucking insect pests, activation of iso- compounds. This makes induced resistance more suc- chorismate pathway and the phenylalanine ammonium cessful against specialist herbivores than the general- lyase pathways lead to the synthesis of SA (Dempsey ists under field conditions (Karban and Agrawal 2002; et al. 2011). Accumulation of SA in plant tissues trig- Després et al. 2007). Insects have developed counter- gers translocation of the non-expressor protein of the adaptations to plant defensive traits through alter- pathogenesis-related genes 1 (NPR1) to the nucleus. ation in morphological, behavioural and biochemical The SA-responsive genes are regulated downstream traits (War and Sharma 2014; Fig. 2). Such adaptations of NPR1. The NPR1 targets the WRKY transcription fac- enable the herbivores to withstand plant defence pres- tor genes, interacts with TGA-type transcription factors sure and therefore, challenges the insect pest manage- and leads to up-regulation of pathogenesis-related (PR) ment programmes (Karban and Agrawal 2002; Després proteins (Durrant and Dong 2004). Salicylic acid signal- et al. 2007). For instance, mirid bug, Pameridea roridulae; ling pathway has also been reported to be activated by cotton bollworm, Helicoverpa armigera; H. zea and S. exi- insect eggs (Reymond 2013). gua feed successfully on Roridula gorgonais, Arabidopsis Jasmonoyl-isoleucine conjugate synthase 1 (JAR1) thaliana and Nicotiana tabacum, respectively (Musser conjugates JA to the amino acid isoleucine (Ile) to form et al. 2002; Shroff et al. 2008). JA-Ile (Staswick and Tiryaki 2004). When JA-Ile binds One important factor for insects being successful to the F-box protein coronatine-insensitive 1 (COI1), organism is the strong olfactory system and its rapid evo- the jasmonate ZIM domain (JAZ) repressor proteins lution in short time spans (Hansson and Stensmyr 2011). are degraded, which bind to the transcriptional activa- Antennae, proboscis and/or maxillary palps are the tors such as MYC2 and in turn repress the JA signalling important insect chemosensory organs through which

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Figure 2. Counter-adaptations of insects to plant defensive systems (source: War and Sharma 2014). the insects perceive plant compounds (by olfaction and Insects respond to plant defensive traits by up- and/ taste) for selecting the suitable plants for oviposition and or down-regulation of a number of genes encoding vari- feeding (Bruce and Pickett 2011; Hansson and Stensmyr ous enzymes. Callosobruchus maculatus responds to 2011). Recognition of the chemicals depends on the acti- soybean cystatin (a cysteine protease inhibitor, scN) by vation of specific proteins, including odorant-binding the up-regulation of genes encoding proteins and car- proteins (OBPs), olfactory receptors (ORs) and gustatory bohydrates (Zhu-Salzman et al. 2003; Ahn et al. 2007). receptors (GRs). These chemosensory chemicals are solu- The turnip sawfly, Athalia rosae not only avoids plant bilized and transported by the OBPs, which cause activa- defences, but also utilizes the plant tissues as a photo- tion of chemosensory neurons (Leal 2013). For the insects synthesis reservoir to draw the nutrients (Opitz et al. with short contact and fast response time, ORs are highly 2010; Abdalsamee and Müller 2012). It also reduces important as they detect the diversity of chemicals and and/or modifies the toxic phenols in the gall and utilizes also perceive the airborne orders (Hansson and Stensmyr them for larval development (Nyman and Julkunen- 2011; Getahun et al. 2012; Missbach et al. 2014). The Tiitto 2000). The larvae also sequester glucosinolates evolution of OBPs and ORs/GRs has been attributed to to avoid the formation of toxic isothiocyanates by con- the regulation of genes in insects in response to vari- verting them into desulfoGS sulfates (Opitz et al. 2010). ous stresses (Guo and Kim 2007; Vieira et al. 2007). In Manduca sexta while feeding on tobacco plants accu- D. sechellia and Drosophila erecta, the evolution of OBP mulates the toxic nicotine in its body and uses it as a occurs rapidly (Vieira et al. 2007). Drosophila sechellia has defence against parasitoids (Thorpe and Barbosa 1986; developed physiological and behavioural adaptations to Harvey et al. 2007). In O. nubilalis, GOX in saliva induces M. citrifolia due to the regulation of OBPs and related che- or suppresses the plant defensive response by increas- mosensory genes (Matsuo et al. 2007; Kopp et al. 2008). ing the expression of l