Modulation of Immune Responses of <I>Rhynchophorus</I>
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Archivio istituzionale della ricerca - Università di Palermo Insect Science (2015) 22, 748–760, DOI 10.1111/1744-7917.12141 ORIGINAL ARTICLE Modulation of immune responses of Rhynchophorus ferrugineus (Insecta: Coleoptera) induced by the entomopathogenic nematode Steinernema carpocapsae (Nematoda: Rhabditida) Maristella Mastore1, Vincenzo Arizza2, Barbara Manachini2 and Maurizio F. Brivio1 1Department of Theoretical and Applied Sciences, University of Insubria, Varese, Italy and 2Department of Sciences and Biological, Chemical and Pharmaceutical Technologies, University of Palermo, Palermo, Italy Abstract Aim of this study was to investigate relationships between the red palm weevil (RPW) Rhynchophorus ferrugineus (Olivier) and the entomopathogenic nematode Stein- ernema carpocapsae (EPN); particularly, the work was focused on the immune response of the insect host in naive larvae and after infection with the EPN. Two main immunological processes have been addressed: the activity and modulation of host prophenoloxidase- phenoloxidase (proPO) system, involved in melanization of not-self and hemocytes recog- nition processes responsible for not-self encapsulation. Moreover, immune depressive and immune evasive strategies of the parasite have been investigated. Our results suggest that RPW possess an efficient immune system, however in the early phase of infection, S. carpocapsae induces a strong inhibition of the host proPO system. In addition, host cell- mediated mechanisms of encapsulation, are completely avoided by the parasite, the elusive strategies of S. carpocapsae seem to be related to the structure of its body-surface, since induced alterations of the parasite cuticle resulted in the loss of its mimetic properties. S. carpocapsae before the release of its symbiotic bacteria, depress and elude RPW immune defenses, with the aim to arrange a favorable environment for its bacteria responsible of the septicemic death of the insect target. Key words encapsulation; immune depression; immune evasion; proPO system; Rhyn- chophorus ferrugineus; Steinernema carpocapsae Introduction Japan (Roda et al., 2011; Huang, 2013). As reported, the RPW is one of the most serious pests affecting at least 19 The international trade of plants and goods around the palm species (EPPO, 2008; Dembilio et al., 2009; Wang world may cause the unintentional diffusion of various et al., 2013), including ornamental palms and species of alien insect pests in new areas, this is the case of Rhyn- economic interest such as coconut, date, and oil palms. chophorus ferrugineus (Coleoptera: Curculionidae), also RPWs is wood-boring insect, often attack healthy palms named red palm weevil (RPW). RPW is native to South- and larvae feed on the soft fibers and on apical meristem east Asia but today it is distributed in almost all Mediter- of the palms creating massive damage to palm tissues, ranean areas, China, the United States, Middle East, and weakening the structure of the palm trunk and leading to the death of infested palms. The resulting cutting down Correspondence: Maurizio Francesco Brivio, Department of of infested trees is very significant in countries where Theoretical and Applied Sciences, University of Insubria, via palm trees are ornamental, changing the landscape; also, JH Dunant 3, Varese 21100, Italy. Tel: +390332421403; email: the damage is economically considerable where palms are [email protected] grown as crops. 748 C 2014 Institute of Zoology, Chinese Academy of Sciences Rhynchophorus ferrugineus immune responses 749 In order to limit the uncontrolled diffusion of this et al., 1997; Bowen et al., 1998, ffrench-Constant et al., insect pest, chemical, biological, and physical methods 2007a,b). Beyond the action of bacteria, physiological are being tested (Gitau et al., 2009). The efficacy of interactions between the parasite and its host must be chemical treatments has been evaluated when applied carefully considered; the life-cycle of an endoparasite to the soil, when injected into palm trunks or sprayed is strongly related to its ability to evade and/or to sup- on the foliage, procedures currently used to control RPW press host immune responses in the early phase of infec- are largely based on dispersal of large quantities of chem- tion. A successful infection is subjected to interactions ical pesticides, although these treatments cause great con- with the host, which can culminate in the undisturbed cern for the environment and health which is not advisable growth and reproduction of the parasite inside the host in the urban areas (Faleiro, 2006). However, the cryptic body (Toubarro et al., 2010, 2013; Castillo et al., 2011). habitat of RPW during its life-cycle makes these treat- Insects are able to maintain self-integrity discriminating ments ineffective unless they are extensive and protracted self from not self by means of a powerful immune sys- over long periods (Ferry & Gomez, 2002). tem (Schmid-Hempel, 2005); consequently, endoparasites An alternative to chemical treatments could be the use have to overcome the host immune defenses to complete of biocontrol agents such as bacteria, fungi, or ento- their life-cycles (Loker, 1994, Loker et al., 2004; Carton mopathogenic nematodes. Biological control with Bacil- et al., 2008; Schmid-Hempel, 2012). lus thuringiensis (Bt) is now common in many agricultural Invertebrates (i.e., insects) lack finely tuned im- systems, besides the troubles related to the concealed habi- munorecognition receptors (antibodies and B and T cells tat of the RPW, a major weakness in the use of Bt is the are absent) but they possess a pool of cellular and hu- onset of resistance to the bacterial toxin in the host target moral Pattern-Recognition Receptors (PRRs) able to in- populations (Pardo-Lopez et al., 2013). The use of fungi teract specifically with a broad range of foreign antigenic as biopesticides is now well established (Pedrini et al., surface compounds, commonly named PAMPs (pathogen- 2007), to date, few studies about pathogenic fungi with associated molecular patterns). PAMPs-PRRs interaction specific effects versus RPW have been carried out is a key process of the discriminatory steps of innate im- (Dembilio et al., 2010a; Guerri-Agullo,` 2010). At present, munity that usually lead to effectors mechanisms respon- the most promising biological agents against RPW seem sible for the elimination of not self (Medzhitov, 2001; to be entomopathogenic nematodes (EPNs). Several stud- Janeway & Medzhitov, 2002; Kanost et al., 2004). Insect ies have been performed with EPNs, these parasites spend immune responses involve both humoral and cellular de- most of the life-cycle within insects body and through- fenses mechanisms (Hoffmann et al., 1996; Janeway & out this endoparasitic phase, they kill the host and repro- Medzhitov, 2002; Hoffmann, 2003); humoral defenses in- duce (Llacer´ et al., 2009; Dembilio, 2010b; Triggiani & clude processes such as, antimicrobial peptides synthesis, Tarasco, 2011). EPNs are safe for both the environment lectin-mediated recognition and melanization (also called and vertebrates and the operating cost is now reduced by humoral encapsulation), the latter is consequent to the ac- mass production in liquid media (Ehlers, 2003). With re- tivation of the prophenoloxidase-phenoloxidase (proPO) gard to RPW, the cryptic habitat inside the palm seem system (Cerenius & Soderhall,¨ 2004; Wang & Jiang, 2004; could be favorable to EPNs action, since this dark and wet Xue et al., 2006; Cytrynska´ et al., 2007). Moreover, main environment minimize nematode damage due to ultravio- cellular processes such as phagocytosis and encapsulation let light and dehydration (Mracek, 2003). Temperature is are carried out by immunocompetent cells called hemo- also an important factor sometimes limiting the efficacy cytes (Ribeiro et al., 1999; Ribeiro & Brehelin, 2006; Tojo of the parasite, for instance, warm habitats of Mediter- et al., 2000; Lavine & Strand, 2002). ranean areas suggest the use of EPNs as Steinernema car- Though, both proPO system activity and cellular encap- pocapsae, which seems to be more effective under these sulation are the more effective defenses processes against conditions (Kaya & Stock, 1997; Llacer´ et al., 2009). foreign multicellular organisms, in previous works we The EPNs are mutualistically associated to bacteria, described how the entomoparasite Steinernema feltiae particularly, S. carpocapsae is symbiotic with the bac- is able to escape from immunological detection of the terium Xenorhabdus nematophila and the infective 3rd host Galleria mellonella (Lepidoptera: Pyralidae), avoid- juvenile stage of the nematocomplex (stage IJ3) reaches ing hemocytes encapsulation and inhibiting the activity the hemocoel cavity of its host in a range from 1 to 2 h. of the host proPO system (Brivio et al., 2002, 2004; Ma- When parasites are inside the hemocoel, symbiotic bac- store & Brivio, 2008). The majority of studies regard- teria are released and the subsequent death of the in- ing the interaction between EPNs and immune host sys- sect is mainly due to bacteria-induced septicaemia in the tem, are focused on lepidopteran and dipteran species (Li late phase of infection (Akhurst & Dunphy, 1993; Ehlers et al., 2007; Castillo et al., 2013), few data are available C 2014 Institute of Zoology, Chinese Academy of Sciences, 22, 748–760 750 M. Mastore et al. regarding the huge order of Coleoptera.