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Insect Heat Shock Proteins During Stress and Diapause Allison M. King and Thomas H. MacRae∗ Department of Biology, Dalhousie University, Halifax, NS, B3H 4R2, Canada; email: [email protected], [email protected]

Annu. Rev. Entomol. 2015. 60:59–75

Keywords

First published online as a Review in Advance on October 8, 2014

molecular chaperones, cochaperones, stress tolerance, dormancy

The Annual Review of Entomology is online at ento.annualreviews.org

Abstract

This article’s doi: 10.1146/annurev-ento-011613-162107 c 2015 by Annual Reviews. Copyright  All rights reserved ∗

Corresponding author

Insect heat shock proteins include ATP-independent small heat shock proteins and the larger ATP-dependent proteins, Hsp70, Hsp90, and Hsp60. In concert with cochaperones and accessory proteins, heat shock proteins mediate essential activities such as protein folding, localization, and degradation. Heat shock proteins are synthesized constitutively in insects and induced by stressors such as heat, cold, crowding, and anoxia. Synthesis depends on the physiological state of the insect, but the common function of heat shock proteins, often working in networks, is to maintain cell homeostasis through interaction with substrate proteins. Stress-induced expression of heat shock protein genes occurs in a background of protein synthesis inhibition, but in the course of diapause, a state of dormancy and increased stress tolerance, these genes undergo differential regulation without the general disruption of protein production. During diapause, when ATP concentrations are low, heat shock proteins may sequester rather than fold proteins.

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INTRODUCTION Diapause: a physiological process characterized by behavioral modification, metabolic suppression, and increased stress tolerance that enhances organismal survival in adverse environments Hsp: heat shock protein, sometimes called a molecular chaperone or stress protein; directs the folding, oligomerization, secretion, and degradation of proteins and protects against their denaturation Cochaperone: a protein that interacts with and influences the activity of heat shock proteins

During normal growth, upon exposure to stress, and when entering diapause—a physiological state of reduced metabolism, developmental delay, and enhanced stress tolerance—insects regulate the synthesis of heat shock proteins (HSPs), also known as stress proteins and molecular chaperones. HSPs are divided into families on the basis of molecular mass, amino acid sequence, and function. In insects, four major families of HSPs, along with several cochaperones, are recognized, including the small heat shock proteins (sHsps), Hsp60, Hsp70, and Hsp90. The sHsps, acting independently of ATP, are the first line of cell defense, preventing irreversible denaturation of substrate proteins, especially when cells are stressed (1, 5). The remaining HSPs interact with proteins and promote, in an ATP-dependent manner that involves structural rearrangement of the HSPs, protein folding, degradation, disaggregation, and cell localization, thereby influencing essential processes such as protein synthesis, cell signaling, transcription, and metabolism (14, 78). Upon exposure of insects and other animals to stressors such as heat, cold, anoxia, and crowding, the synthesis of most proteins declines, but HSPs increase, binding aberrant proteins and aiding refolding. HSPs function in networks associated with cochaperones like the J-domain protein, Hsp40, ensuring intracellular protein homeostasis (14, 84). The synthesis and function of insect HSPs during stress and diapause are considered herein (Figure 1).

LIMITATIONS OF HSP ANALYSES IN INSECTS It is prudent to think about limitations encountered in the analysis of HSPs before considering their production and activity in insects. Multigene methodologies such as microarray analysis, which rely on genome sequences for maximum information retrieval, reveal the expression of insect HSP genes under changing conditions but say little about protein synthesis and function. The probing of Northern blots and analysis by quantitative reverse transcriptase polymerase chain

Desiccation Cold

Heat

Embryos

Larvae

Starvation

HSPs—stress

Anoxia

HSPs—diapause

Adults

Pupae

Figure 1 The expression of insect heat shock protein (HSP) genes is induced by several insults, among which heat, cold, desiccation, starvation, and anoxia are common (top). The HSPs contribute to insect survival throughout normal growth and under stress conditions by promoting protein integrity and cell homeostasis. Many insects undergo diapause, a physiological state of dormancy and enhanced stress tolerance generally restricted to one life history stage in each species (bottom). During diapause the expression of HSP genes and the accumulation of their products may increase, decrease, or remain unchanged, thereby facilitating insect survival under adverse circumstances. It is likely that HSPs function in similar ways during stress and diapause. 60

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reaction (qRT-PCR) demonstrate HSP mRNA quantities at particular times in the life of an insect but disclose neither when the transcripts are produced nor when they are translated. Proteomics and immunological methods detect proteins but do not tell us anything about activity, the latter being influenced by posttranslational modifications including phosphorylation and acetylation. If loss of an HSP is nonlethal, function can be determined by gene knockout or protein knockdown by RNA interference (RNAi), but even here HSP influence on physiological processes is uncertain. For example, Hsp90 interacts with signaling molecules that regulate molecular events potentially upstream of processes under consideration. Or, decreasing an HSP may permit cell activity that is normally suppressed but not divulge with which protein(s) the HSP interacts; substrate identification is essential if the role of HSPs is to be understood. HSPs act within networks, potentially undertaking different roles based on their relative abundance and ATP availability. The functions of individual proteins within an HSP family often differ with developmental stage, subcellular location, and environmental conditions. Incomplete knowledge of insect HSPs may enhance the perceived importance of those HSPs that are more easily studied, such as Hsp70, while downplaying others. Despite these limitations it is apparent that HSPs have important roles in insects, diverging from one species to another and within the same species under different physiological, developmental, and environmental states.

INSECT HSPS AND STRESS Temperature Extremes and Insect HSPs An important determinant of insect abundance and distribution is temperature, with extremes of heat and cold eliciting adaptive induction of HSP gene expression required for survival. Nondiapausing larvae of the apple maggot, Rhagoletis pomonella, respond to heat in the laboratory by strong and weak upregulation, respectively, of Hsp90 and Hsp70 mRNAs (57). Increasing HSPs is ecologically relevant because apples within orchards experience high temperature as the day progresses, and the accumulation of Hsp70 and Hsp90 protects R. pomonella. The sHsp genes shsp19.9, shsp20.1, shsp20.4, shsp20.8, shsp21.4, and shsp23.7 from the silkworm, Bombyx mori, are constitutively expressed very weakly in nine tissues of fifth instar larvae (79). All of these sHsp genes, with the exception of shsp21.4, which is two times larger than the other sHsp genes and is the only gene in the group with an intron, are induced in the larval fat body, testis, and ovary by heat stress, whereas Hsp70 and shsp21.4 are downregulated (52, 79). The absence of introns is thought to favor the expression of stress-responsive genes because no mRNA processing, which could slow transcript accumulation and/or be disrupted by stress, is required. In these analyses changes in protein and mRNA generally coincide, and the degree of HSP induction depends on sex, intensity of treatment, and strain, with thermotolerant insect strains synthesizing less HSP mRNA in response to high temperature than thermosensitive strains (52). Many studies of thermal tolerance in insects include the effects of heat and cold. In the leafminers Liriomyza sativa and Liriomyza huidobrensis, heat augments the transcription of genes encoding the cochaperone Hsp40 as well as those for Hsp20, Hsp70, Hsp90, and mitochondrial Hsp60, and with the exception of Hsp60, all of these genes are induced by cold (36, 37). The induction temperature for each HSP gene varies, as does the extent of the response, with Hsp70 and Hsp20 amplified most intensely. Such differences suggest functional deviation among the HSPs, but this issue remains to be addressed in Liriomyza. Stimulation of HSP gene expression in L. huidobrensis occurs at a lower temperature than in L. sativa, corresponding to the ability of the former to live farther north and to better survive cold (36). Likewise, HSP gene expression is prompted at a lower www.annualreviews.org • Insect Heat Shock Proteins

sHsp: small heat shock protein, an ATP-independent heat shock protein that possesses an α-crystallin domain and prevents the irreversible denaturation of other proteins Hsp70, Hsp90, and Hsp60: structurally different ATPdependent heat shock proteins of 70, 90, and 60 kDa, respectively, that normally fold other proteins Hsp40: J-domain-containing cochaperone that delivers proteins to Hsp70 and stimulates its ATPase activity qRT-PCR: quantitative reverse transcriptase polymerase chain reaction RNAi: RNA interference

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temperature upon heat shock in L. huidobrensis than in L. sativa, further influencing geographical distribution of these insect species. When larvae of the gall fly Eurosta solidaginis are examined before and during diapause in late fall and winter, increases in several HSPs, including sHsps, Grp75, Grp78, Hsp40, Hsp70, and Hsp110, occur, indicating they protect against cold (98). Freezing of E. solidaginis larvae acclimated to 15◦ C increases Hsp70, Hsp40, and Grp75, but Hsp110, Hsp60, and sHsps are unchanged until recovery from freezing. These studies are noteworthy because E. solidaginis is a freeze-tolerant insect whereas many studies of HSP induction by low temperature are performed on insects that are not cold tolerant. Five sHsp genes, termed Cshsp19.8, Cshsp21.4, Cshsp21.5, Cshsp21.7a, and Cshsp21.7b, have been characterized in larvae of the rice stem borer, Chilo suppressalis (59). Cshsp19.8 and Cshsp21.7b are induced by extreme high and low but not mild temperatures, whereas Cshsp21.5 responds to cold only. Cshsp21.4 and Cshsp21.7a possess introns, and they are not induced by temperature change. As stated above, intron absence favors the expression of stress-responsive genes. Hsp90 mRNA increases upon exposure to cold in nondiapausing but not diapausing larvae of C. suppressalis (86). Moreover, mitochondrial Hsp60 mRNA and protein rise in the hemocytes of heat-stressed fifth instar larvae of C. suppressalis, suggesting Hsp60 protects mitochondria, an activity possibly common to this HSP in many insects (21). The probing of Northern blots reveals that Hsp90 mRNA is upregulated in nondiapausing and diapausing pupae of the flesh fly, Sarcophaga crassipalpis, upon heat and cold shock (72). However, Hsp90 mRNA decreases during diapause of S. crassipalpis, indicating divergent control of HSP gene expression in the course of heat shock and diapause. Nondiapausing pupae of the onion maggot, Delia antiqua, exhibit low amounts of Hsp70 mRNA, which builds up on exposure to heat and cold, followed by a gradual decline if cold persists (12). Additionally, Hsp90 mRNA rises slowly with elevated temperature whereas Hsp90 mRNA increases and then wanes at low temperature (11). Hsp70 is amplified in summer and winter diapausing pupae of D. antiqua by cold shock, but only winter diapausing pupae react to heat (12). Although high and low temperatures boost Hsp90 mRNA in diapausing pupae of D. antiqua the patterns of accumulation differ, with gradual augmentation in summer diapausing pupae and a decline in winter diapausing pupae after initial escalation (11). The amount of Hsp60 mRNA in assorted tissues correlates with the cold hardiness of winter diapausing D. antiqua and cold-acclimated pupae, perhaps repressing actin depolymerization upon cold exposure, which in turn promotes membrane stability (41, 42). The regulation of HSP genes in D. antiqua obviously varies with the physiological state of the insect and the gene under consideration. Drosophila Hsp23, Hsp22, Hsp26, Hsp27, Hsp40, Hsp68, Hsp70Aa, and Hsp83 (Hsp90) are cold inducible, whereas Hsp60, Hsp67Ba, and Hsc70-1 are not (16, 18). With the possible exception of Hsp67Ba, the Drosophila genes are induced more strongly by heat than cold (18), perhaps because of differential activation of the transcription factor, heat shock factor 1 (HSF1). The knockdown of Drosophila Hsp22 and Hsp23 by RNAi using the GAL4/UAS system slows fly recovery from chill coma but does not affect mortality, indicating a role in thermal stress (17). Hsp23 influences recovery from chill coma more than Hsp22, suggesting their products play distinct roles, conceivably mandated by chaperone activity and cell location (17). Hsp23, Hsp26, and Hsp70 are upregulated upon heat shock of Drosophila triauraria adults, but Hsp83 is not (29, 30). Hsp70 mRNA accumulation due to heat shock is equivalent in D. triauraria nondiapausing and diapausing adults, but the latter are more tolerant of heat and cold (30). These results suggest that, in contrast to Hsp70 in most other insects, Hsp70 in D. triauraria is not required for thermal tolerance. Hsp70 production by Drosophila melanogaster takes place during recovery from and not in the course of cold shock, the delay possibly caused by metabolic repression (8, 18, 83, 85). Hsp70 synthesis occurs upon recovery from cold in other Drosophila species (28, 30); the adult linden bug,

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HSF1: heat shock factor 1

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Pyrrhocoris apterus (46); nondiapausing and diapausing pupae of the corn earworm, Helicoverpa zea (99); nondiapausing and diapausing pupae and pharate adults of S. crassipalpis (39, 72); diapausing Culex pipiens (74); and the diapausing adults of the Colorado potato beetle, Leptinotarsa decemlineata (96). Hsp90 in Drosophila auraria is produced during recovery from cold shock (95), as is SnoHsp83 (Hsp90) in larvae of the moth Sesamia nonagrioides (27). Two sHsp genes are induced rapidly in S. nonagrioides larvae upon recovery from cold, but accumulation of their products diverges, suggesting different roles for each sHsp (25). Knockdown by RNAi shows the importance of HSPs for insect survival in response to temperature extremes. The knockdown of two sHsps in the leaf beetle Gastrophysa atrocyanea decreases viability and lowers heat resistance, indicating HSPs are involved in thermal tolerance (2). Elimination of Pahsp70 mRNA and protein, both induced by heat and cold, hinders heat shock recovery and repair of chilling injuries in adult Pyrrhocoris apterus (46). The removal of Hsp22 and Hsp23 mRNA by RNAi in D. melanogaster disrupts recovery from chill injury (17), and the deletion of Hsp23 and Hsp70 mRNA reduces heat hardiness and cold hardiness in S. crassipalpis diapausing pupae but has no effect on entry into diapause, showing the role of these HSPs in stress tolerance during diapause (73).

Cold and Heat Hardening of Insects Many insects exhibit enhanced cold tolerance when exposed for a short time to mild cold, a process distinct from cold acclimation called rapid cold hardening (77). As determined by liquid chromatography–tandem mass spectrometry, Hsp26 increases in the brain of S. crassipalpis upon rapid cold hardening, whereas Hsp70 is unaffected. Hsp90 decreases during cold hardening; it is downregulated during diapause but accumulates in heated and chilled nondiapausing and diapausing S. crassipalpis (48, 72). These observations demonstrate that the induction of HSP genes varies with the intensity of thermal stress and the insect’s physiological state. Enhanced tolerance to heat after hardening by cold, known as cross-tolerance, is observed in adults of D. melanogaster; however, in contrast to results with Drosophila larvae (8) and P. apterus (46), hardening by heat fails to improve cold resistance (83), a finding also obtained with one-dayold L. huidobrensis adults, where Hsp70 and Hsp20 mRNAs are induced by heat hardening (35). Cold hardening of L. sativa two-day pupae stimulates expression of the sHsp genes ls-hsp19.5, ls-hsp20.8, and ls-hsp21.7, with ls-hsp20.8 activated at a lower temperature and to a larger extent, showing the greater cold sensitivity of ls-hsp20.8 (37). Cold hardening of D. melanogaster promotes Hsp70 synthesis, suggesting cross protection is due partly to this HSP (83). In nondiapausing P. apterus adults, Hsp70 but not Hsc70, as determined by measuring mRNA and protein, is upregulated by heat and cold. In this work the amount of induced mRNA did not reflect the quantity of corresponding protein (46), an observation germane to all studies where only mRNA is quantified.

HSPs and Desiccation Tolerance in Insects HSP mRNAs are upregulated in nondiapausing pupae of S. crassipalpis exposed to 0% relative humidity (89). Hsp23 and Hsp70 mRNAs accrue in lower amounts than if triggered by heat shock, as observed in other insects, and even though Hsp23 and Hsp70 mRNAs increase, resistance to heat and cold declines upon desiccation, presumably because of cell damage caused by water deficiency. On the one hand, the upregulation of Hsp23 and Hsp70 mRNAs persists in nondiapausing pupae of S. crassipalpis as long as drying continues (34). Diapausing pupae of S. crassipalpis, on the other hand, possess high levels of Hsp23 and Hsp70 transcripts and desiccation increases neither, suggesting these HSPs are sufficiently abundant to permit the insect to survive water loss without gene www.annualreviews.org • Insect Heat Shock Proteins

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activation. Constitutively expressed Hsc70 and Hsp90 are indifferent to desiccation in diapausing and nondiapausing pupae of S. crassipalpis although they are upregulated with rehydration (34). Hsp70 mRNA collects in the mosquitoes Aedes aegypti, Anopheles gambiae, and Cx. pipiens during dehydration, but only the latter expresses Hsp70 upon rehydration (6). Hsp90 transcripts, high in nonstressed mosquitos, remain elevated throughout dehydration and rehydration except in Cx. pipiens, where Hsp90 mRNA is not apparent during rehydration. RNAi knockdown of Hsp70 and Hsp90 in Ae. aegypti lowers dehydration tolerance, demonstrating these HSPs protect mosquitoes from drying. Dehydration may amplify protein denaturation and reactive oxygen species (ROS) while modifying membranes; these perturbations are offset by the chaperone activity of HSPs and indicate the importance of these proteins upon dehydration/rehydration (6). Genes encoding a sHsp, Hsp70, and Hsp90 in larvae of the Antarctic midge, Belgica antarctica, are shown by suppressive subtractive hybridization to react to changing hydration (56). The HSP genes are activated by fast dehydration, but during slow dehydration only Hsp70 is upregulated, and sHsp and Hsp90 are unaffected. Throughout rapid rehydration sHsp and Hsp70 mRNA levels remain high, but Hsp90 mRNA declines. The consequences of dehydration and rehydration reflect the variable environment experienced by B. antarctica; HSPs likely protect intracellular proteins and membranes, promoting survival under extreme conditions.

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Anoxia/Hypoxia, Oxidative Stress, and HSPs in Insects As shown by qRT-PCR, red-eye pharate adults of S. crassipalpis subject to hypoxia increase the expression of several HSP genes (64). Hsp70 responds most quickly to hypoxia and displays the greatest appreciation in expression, followed by the sHsp genes Hsp18, Hsp23, and Hsp25, then Hsp40 and Hsp60. Hsp27 mRNA is constant throughout 10 days of anoxia, and Hsp90 and HSF mRNA decrease, which is unexpected based on the induction of numerous HSP genes. The expression of all S. crassipalpis HSP genes, except those encoding Hsp60 and Hsp90, declines during recovery from hypoxia. Hsp60 mRNA goes up and then drops to levels found in control insects during recovery, whereas Hsp90 mRNA expands about fourfold. D. melanogaster adults upregulate at least four HSP genes in the course of hypoxia, including Hsp23, Hsp67Bc, Hsp68, and Hsp40, with Hsp23 most responsive to oxygen deprivation (54). Overexpression of Hsp70 by the UAS-Gal4 system in Drosophila hemocytes and heart allows the insects to survive hypoxia for several days, an effect less evident with Hsp70 overexpression in muscle and brain, and these flies are resistant to insults such as oxidation (3). The enhanced protection is related to Hsp70 that reduces ROS in flies, an effect duplicated in an unknown way by hemocyte elimination (3). Grp78 (Hsp70) and the sHsps in cold-hardy E. solidaginis increase in response to anoxia, a condition that may occur upon whole-body freezing, whereas Hsp40 does not change and Hsp60 and Hsp110 decrease (98). B. antarctica, among other insects in Antarctica, experiences oxidative stress from high ultraviolet (UV) radiation and ROS production during anoxia and freeze-thaw (58). Exposure to sunlight for six hours strongly induces the synthesis of mRNAs encoding a sHsp and Hsp70, but Hsp90 is amplified somewhat less; a role for HSPs in protection against oxidative stress in B. antarctica awaits demonstration. By comparison, AccHsp27.6 expression in worker bees of Apis cerana cerana increases only slightly upon UV exposure and more strongly in response to H2 O2 , with the latter acting more quickly than the former (55).

Starvation and Crowding Induce Insect HSP Gene Expression The sHsps Hsp20.5, Hsp20.6, and Hsp20.7, as well as Hsp40, Hsp70, and Hsp90, were examined during solitary and gregarious phases, representing low and high population densities, respectively, 64

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of the migratory locust, Locusta migratoria L. (93). HSP mRNAs are more abundant in gregarious than solitary animals, suggesting that crowding mediates HSP gene activation. Enhanced HSP gene expression potentially reflects increased energy demand resulting from competition for food and space, or it may signify desiccation and pathogen infection (93). Crowding could lead to starvation, a multifaceted stressor that modifies water and ion balance and lowers energy availability. Crowding effects on the expression of Hsp20.5, Hsp20.6, Hsp20.7, Hsp40, Hsc70, and Hsp90 in the neural tissue of fifth instar nymphs of the Australian plague locust, Chortoicetes terminifera, were examined by RT-qPCR (10). In contrast to findings in L. migratoria (93), only Hsp20.5 and Hsp20.7 are upregulated under crowding, and these sHsps may, on the basis of sequence, be found only in Orthoptera. Possibly, HSPs are sufficiently abundant prior to crowding to protect C. terminifera. Starvation induces the expression of genes encoding Hsp20, Hsp60, Hsc70, and Hsp90 in the endoparasitoid wasp, Pteromalus puparum (92); these HSPs are similar to those seen in L. migratoria upon crowding.

Hop: heat shock 90/70 organizing protein

Insect Cochaperones Other than Hsp40, a J-domain protein mentioned throughout the review, little is known about insect cochaperones. Starvin (Stv), a BAG-family member, modulates Hsp70 ATPase activity, and it appears in D. melanogaster during cold recovery (15, 16). The coordinated synthesis of D. melanogaster Stv and Hsp70 suggests cooperation to offset cold injury, perhaps through protein folding/degradation and by regulating apoptosis (15). B. mori contains a homolog of Stv termed Samui that, along with Hsp70, increases in diapausing and nondiapausing silkworms under cold stress, with expression of both genes controlled by the transcription factor HSFd (43, 65, 66). Samui binds Hsp70 and may facilitate transmission of an environmental signal, in this case reduced temperature, to downstream effectors, thus facilitating termination of diapause. A third insect cochaperone, Fohop, the heat shock 90/70 organizing protein (Hop), modulates contact of Hsp90 and Hsp70 and is described for the western flower thrips, Frankliniella occidentalis (51), and D. melanogaster, where it is named dHop (9). Fohop is constitutively expressed throughout the development of F. occidentalis, and high temperature increases its transcription in larvae and adults, with the response in larvae but not in adults varying with temperature. Fohop transcript levels are constant in adults during cold, but low temperature downregulates Fohop mRNA in larvae (51).

HSPS AND DIAPAUSE IN INSECTS Diapause is a physiological condition of developmental delay seen in many insects and characterized by metabolic decline, dormancy, and enhanced stress tolerance. Insect diapause is induced by signals such as photoperiod, temperature, and crowding, but it can occur independently of environmental change (31, 45, 61). Insects initiate diapause by increased feeding, altered gene expression, modified protein synthesis and activity, and upregulated lipid metabolism. Initiation merges with maintenance, which involves inhibition of activities such as DNA replication, metabolism, cell division, and apoptosis (70, 88). Termination of diapause is induced in many insects by changes in temperature and day length. Upon termination, either development resumes if conditions are favorable or insects enter quiescence and remain dormant until they encounter appropriate temperature, aeration, hydration, and/or day length. Stress tolerance persists during quiescence but fades as growth resumes. Because many insect pests overwinter and survive eradication when in diapause, an understanding of this process has practical implications for agriculture, forestry, and medicine. During diapause HSPs either increase or decrease in amount or remain constant, with changes occurring in anticipation of, rather than in response to, stress. Diapause-induced modifications www.annualreviews.org • Insect Heat Shock Proteins

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in HSPs tend to last longer than those caused by stress, and HSP production occurs without the general inhibition of protein manufacture seen in stressed cells (73). HSP synthesis is differently regulated during diapause, and within an insect individual HSPs may either increase or decrease in diapause versus nondiapause development. Additionally, in an insect undergoing diapause, one or more HSPs may rise in amount while others are reduced or do not change (61). The differential synthesis of HSPs and their responsibility for protein folding and storage, as influenced by ATP, predict their role in protein maintenance and stress tolerance throughout diapause.

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HSPS IN INSECTS UNDERGOING DIAPAUSE AT DIFFERENT DEVELOPMENTAL STAGES HSPs in Insect Embryos Experiencing Diapause Embryos of B. mori, in which 16 sHsps were identified by genome-wide analysis (53), undergo diapause characterized by profound reduction in metabolic activity. mRNAs for Hsp20.4, Hsp20.8, Hsp40, Hsp70, and Hsp90 were reported not to change in diapausing B. mori (80); however, it was shown previously that Hsp20.8A is upregulated in diapausing silkworm embryos (38), as are mRNAs for Hsp70, DnaJ (66, 82), and Hsc71 (81). Shotgun proteomics reveals that Hsp19.1, Hsp20.1, Hsp20.4, Hsp20.8, Hsp23.7, Hsp70, Hsc70, and Hsp90 are present in roughly equal amounts in nondiapausing and early diapausing eggs of B. mori, where they may influence embryo development, metabolism, and immune defense by ensuring proteins are properly folded and protecting against their denaturation (23, 81). The variation in results may have arisen because B. mori eggs were examined at different stages of development, and it is not until embryos display diapause characteristics such as stress tolerance that HSPs are present. By comparison, in diapausing embryos of the cricket Allonemobius socius, distinguished by 64% reduction in metabolism, mRNA transcripts encoding Hsp20.7 and Hsp90 are reduced relative to nondiapausing animals, whereas Hsp70 transcripts are unchanged (70, 71).

HSPs in Diapausing Insect Larvae Diapausing larvae of the corn stalk borer, Sesamia nonagrioides, which feed and undergo supernumerary molts, display differential regulation of sHsp genes, with SnoHsp19.5 expressed consistently and SnoHsp20.8 downregulated and then upregulated as diapause ends (25). Hsp90 and Hsc70 mRNAs increase, whereas Hsp70 decreases in the course of S. nonagrioides diapause (26, 27). Proteomic studies show uncoupling of a sHsp and Hsp90 throughout larval diapause of the parasitic solitary wasp, Nasonia vitripennis, with Hsp20 upregulated and Hsp90 downregulated (94). The bamboo borer, Omphisa fuscidentalis, undergoes diapause in the relatively constant environment of bamboo culm internodes, featuring an average temperature of 20◦ C and high humidity. Hsp70 and Hsp90 mRNA decline relative to nondiapause life stages, although Hsp90 mRNA increases transiently upon diapause termination. Hsc70 mRNA is amplified in the second half of O. fuscidentalis diapause followed by a slow decline as diapause ends (91). Larval diapause of C. suppressalis is typified by augmentation of Hsp90 mRNA, whereas Hsc70 is constant (86). Synthesis of the five sHsps identified in C. suppressalis has not yet been examined in relation to diapause (59). Hsp23, Hsp70, and Hsp90 transcripts are unchanged during diapause in the blow fly Lucilia sericata, a nonfeeding stage. However, Hsp90 rises when diapause transitions to postdiapause, a process requiring exposure to 7.5◦ C and perhaps ecdysteroid (87). By comparison, hsp23, hsp24, and hsp70 are upregulated in diapause larvae of the blow fly Calliphora vicina, a necrophagous insect, suggesting its use for determining time of death when present on human corpses (24). 66

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HSPs in Insect Prepupae and Pupae During Diapause Hsp70 mRNA is amplified strongly in diapausing prepupae of the solitary bee Megachile rotundata, which experience an 80% drop in O2 consumption, although respiration oscillates. In contrast, Hsc70 and Hsp90 mRNAs change only slightly and are prominent throughout diapause and nondiapause (97). On the one hand, sHsp, Hsp70, and Hsp60 transcripts accumulate in S. crassipalpis, an insect that undergoes approximately 90% reduction in metabolism during diapause. On the other hand, Hsc70 is unchanged and Hsp90 decreases, the latter possibly due to limiting ecdysone and with the potential to affect expression of sHsp and Hsp70 (33, 50, 69, 72, 73, 75, 76). The coordinated upturn of sHsp, Hsp70, and Hsp60 mRNAs suggests these HSPs cooperate to protect pupae from diapause-associated stress. RNAi knockdown of sHsps and Hsp70 confirms their role in cold tolerance, an important aspect of diapause in S. crassipalpis (73). As shown by the probing of Western blots, Hsp70 rises in diapausing pupae of the blueberry maggot, Rhagoletis mendax, which experience approximately 85% reduction in metabolism (90). In contrast to Hsp70 in diapausing S. crassipalpis (76), Hsp70 is responsive to heat in diapausing R. mendax. The different results may reflect environmental circumstances experienced by the insects, the experimental methods employed, and/or the level of Hsp70 in the insect when heat was first applied. Hsp70 is upregulated and Hsp90 is downregulated in diapausing pupae of R. pomonella (57). Conversely, brain Hsp70 mRNA is not boosted during diapause of H. zea, nor is brain Hsc70, although diapausing pupae are more cold tolerant than nondiapausing pupae (99). Hsp90, known to bind steroid receptors and kinases, diminishes and may reflect low ecdysteroid levels (99). Metabolomic and proteomic analyses show that the larval brain and hemolymph of the cotton bollworm, Helicoverpa armigera, upon induction of and preparation for diapause, display several regulatory proteins and biochemical changes, but no HSPs are observed at this early prediapause stage (100, 101), as is true for the Asian tiger mosquito, Aedes albopictus, as it prepares for adult reproductive diapause (68). Hsp20.7 and Hsp90 decline in the brain during diapause of H. armigera, while Hsp21.4 rises (13, 60), as does Hsp70 mRNA (4). Augmentation of HSPs indicates that stress tolerance increases even in the early stages of diapause, as H. armigera gets ready for harsh winter conditions. D. antiqua undergoes a marked reduction in metabolic activity during diapause, accompanied by upregulation of Hsp70 (12, 32), Hsp60 (41, 42), and Hsp90 (11). Hsp60 may enhance cold hardiness by stabilizing microfilaments (42). Protection of proteins essential to development, such as actin and tubulin, implicates Hsp60 in diapause; however, information on this HSP during insect diapause is limited, making conclusions difficult. Proteomics demonstrates upregulation of Hsp70 during diapause of the parasitic wasp Praon volucre (20), an insect undergoing a 27% drop in metabolism during diapause (19), somewhat less than in the pupae of most other insects for which this value is known.

HSPs During Adult/Reproductive Diapause of Insects It is advantageous for insects to maintain HSPs engaged in protein folding for the duration of adult diapause because these animals experience limited reduction in metabolism and generally encounter mild stress. Primary ovarian follicle development is blocked in adult diapause of Cx. pipiens, during which Hsp70 mRNA is not upregulated (74), one sHsp transcript increases modestly (77), and as shown by proteomics, Hsc70 decreases (49). L. decemlineata marginally elevates mRNA encoded by one of its two known Hsp70 genes, but not the other, when in diapause (96). Hsp23, Hsp26, Hsp70, and Hsp83 (Hsp90) transcripts fail to rise during adult diapause of D. triauraria even though the insect shows enhanced stress tolerance and its known HSP genes, with the exception of Hsp83, are heat sensitive (29, 30). Candidate gene microarray analysis of wholebody RNA from the northern malt fly, Drosophila montana, a species able to survive severe winters, www.annualreviews.org • Insect Heat Shock Proteins

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established downregulation of Hop, Hsc70-3, and Hsp83 in diapause whereas Hsp20 and Hsp26, unchanged in diapausing females, increase in reproducing as opposed to young females (40). The synthesis of sHsp, Hsc70, and Hsp90 mRNAs associated with adult diapause in young queens of the bumble bee, Bombus terrestris, occurs in a complex, tissue-specific, temporal pattern (44). The amounts of Hsc70 and Hsp90 mRNA are similar in the brain, thoracic muscle, gut, and ovary. mRNA encoding a brain sHsp is cut back in mid-diapause but intensifies in the ovary as diapause progresses, with no change in the gut and muscle. Hsc70 and Hsp90 mRNAs are upregulated in B. terrestris muscle during diapause but decrease in the ovary, with no modifications in the gut and brain. Differential synthesis, especially of sHsp mRNA in ovaries, suggests tissue-specific functions for HSPs in diapause (44).

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BAG protein: a cochaperone that modulates Hsp70 activity through interaction with its ATPase domain

HSP NETWORKS AND PROTEIN INTEGRITY DURING DIAPAUSE HSPs operate in networks with functions influenced by differential abundance, as described above, and ATP availability, determined by metabolism. Interaction between sHsps and Hsp70 is fundamental to the diapause HSP network. Besides folding nascent proteins in translationally active insects, Hsp70 removes substrates from sHsps and participates in refolding and degradation, either acting alone or with other HSPs (22, 47). Protein release from sHsps and folding by Hsp70 take place as diapause terminates and ATP increases. Additionally, Hsp70 potentially combines with compromised proteins when ATP is limiting, thereby augmenting protein storage by sHsps and other HSPs during diapause-dependent metabolic suppression. J-domain proteins, like the cochaperone Hsp40, may benefit diapausing organisms because they promote substrate binding to Hsp70 and enhance ATP hydrolysis, favoring protein association with ADP-Hsp70 as ATP decreases. If nucleotide exchange factors are low the exchange of ATP for ADP on Hsp70 is disrupted and substrate binding is favored. Hsp40 increases in early diapause of S. crassipalpis (69), and it is hyperphosphorylated in the fly brain (67), but the consequences of these changes are unknown. The amount of the BAG protein Samui increases when B. mori terminates diapause upon exposure to 5◦ C. Samui is proposed to transfer information from an environmental signal to promote diapause termination as well as to favor substrate release from Hsp70 should it, like other BAG proteins, facilitate nucleotide exchange (65, 66). Under normal physiological conditions Hsp90 folds nascent proteins, some of which transfer from Hsp70 in a complex with Hsp40, a process requiring the cochaperone Hop. Hsp90 binds substrate when in an open conformation, but sequestering of proteins is unlikely when ATP is not restrictive because nucleotide-induced structural rearrangements free bound substrate. Under limiting ATP, as happens in diapause, substrates may bind with apo Hsp90 until metabolism increases. Hsp90 regulates many important cell activities by interacting with kinases and steroid receptors, and it potentially sequesters these types of proteins when ATP is limiting. Hop inhibits Hsp90 ATPase activity and stabilizes substrate attachment to the open configuration of this HSP, suggesting enhanced protection of denaturing proteins by Hsp90 in diapausing insects if Hop is amplified. Hop mRNA rises early in the pupal diapause of S. crassipalpis (69), and it declines during the adult diapause of D. montana (40). The evidence suggests that Hsp90 functions with cochaperones to fold proteins, bind denaturing proteins, and preserve signaling molecules. Hsp90 works with other HSPs in a functional network where nascent and denaturing proteins associated with Hsp70 transfer to Hsp90 for refolding, the latter when diapause terminates. Understanding the role of Hsp90 in diapause depends on a more comprehensive appreciation of substrate binding and release by this HSP, especially in relation to the availability of ATP, other HSPs, and cochaperones. Hsp60 folds nascent proteins including the cytoskeletal elements tubulin and actin and regulatory molecules such as kinases, supporting readiness for cell development, growth, and division. 68

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Diapause/stress

sHsps + substrates Hsp40 + substrate

Stress relief Increasing ATP

Hsp70 + substrate

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ATP ADP + Pi

Hsp40 Hop NEF

ADP Folded protein

ATP

Hsp90 + substrate ATP

Hsp60 + substrate ATP

?

ADP + Pi

ADP + Pi Folded protein

Folded protein

Figure 2 HSP networks enable protein folding and degradation during growth and protect proteins from damage upon stress and diapause. Insects experiencing diapause adapt in several ways, including the differential synthesis of HSPs. The sHsps prevent irreversible denaturation of proteins, and when stress is relieved and ATP becomes more plentiful proteins are removed from sHsps by Hsp70 and either refolded or degraded. Alternatively, proteins are transferred from Hsp70 to Hsp90 and Hsp60 where ATP hydrolysis permits protein folding. Hsp70, Hsp90, and Hsp60 may store rather than fold proteins if ATP is limiting. The relationship between Hsp90 and Hsp60 is less well defined than for other HSPs. Abbreviations: Hop, heat shock 90/70 organizing protein; NEF, nucleotide exchange factor.

Hsp60 may prevent aggregation of denaturing proteins during diapause and participate in refolding (7, 62), with accumulation of apo Hsp60 in the open configuration offering protection for proteins when ATP is limiting. Actin associates with ADP-Hsp60 but fails to fold (63), demonstrating the availability of binding sites for this and perhaps other proteins that could function during diapause. In summary, sHsps often accumulate in the course of insect diapause, especially if metabolism is depressed significantly, thereby increasing protein binding capacity. Proteins stored in association with sHsps are saved from irreversible denaturation; this is the first line of defense for cells against stress-induced protein loss during diapause. The liberation of substrates from sHsps postdiapause, and either their folding or degradation, is proposed to occur within cooperative networks of ATPdependent HSPs, which in low ATP concentrations may store denaturing proteins for subsequent refolding (Figure 2). Refolded proteins are then used in the cell, enhancing growth by reducing the requirement for energy-expensive transcription and translation after diapause completion.

CONCLUSIONS Insect HSPs increase in response to temperature extremes, crowding, starvation, and hypoxia/ anoxia, and they are produced differently during diapause, when they likely guard against some www.annualreviews.org • Insect Heat Shock Proteins

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of the stresses just mentioned. HSPs contribute to the folding of nascent proteins and to stress tolerance by shielding proteins from irreversible denaturation and by promoting degradation if they cannot be salvaged. During diapause, a physiological process characterized in insects by disparate levels of metabolism, the sHsp/Hsp70/Hsp90/Hsp60 network has the potential to boost both protein folding and storage, with the outcome influenced by ATP availability. Substrate binding to sHsps is ATP independent, and increasing the amount of sHsps potentiates protein protection. If ATP is in short supply proteins may bind stably to Hsp70, Hsp90, and Hsp60, expanding storage during diapause, especially if one or more of these HSPs increase in amount. With nonlimiting ATP concentrations, the downregulation of Hsp70, Hsp90, and/or Hsp60, normally responsible for folding, may enhance protein storage in association with sHsps. Effective storage conserves cell resources by ensuring proteins are not repaired repeatedly. Clearly, we are just beginning to understand how the differential synthesis of HSPs and changing metabolic activity mediate protein structure and function in insects during stress and diapause.

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SUMMARY POINTS 1. Insects produce HSPs in response to stressors such as temperature extremes, crowding, desiccation, and hypoxia/anoxia. 2. HSPs protect proteins from irreversible denaturation during stress and contribute to their refolding and degradation once stress ends. 3. HSPs may increase, decrease, or remain constant in diapausing versus nondiapausing insects, and within a diapausing insect some HSPs rise, some are reduced, and others are unchanged. 4. The sHsps, Hsp70, Hsp90, and Hsp60, in association with cochaperones, are thought to form molecular networks with important roles in protein synthesis, stress tolerance, and diapause. 5. The sHsps function in protein storage independent of ATP, whereas the major activity of other HSPs is the ATP-dependent folding and/or degradation of proteins. 6. HSP activity may change from folding and degradation to storage of proteins with function dependent on the availability of each HSP and ATP.

FUTURE ISSUES 1. Identify substrates that bind to insect HSPs, with emphasis on the HSPs that change during physiological stress and diapause. This approach may lead to the identification of proteins with key regulatory and functional roles during stress tolerance and diapause in insects. 2. Determine the functions of insect HSPs in vivo using methods such as protein knockdown by RNAi. The work will identify HSPs essential for stress tolerance and diapause and reveal previously unanticipated functions of these proteins, while commenting on the identity of HSP substrates. 3. Establish if there are similarities between the upregulated and downregulated HSPs when insects are grouped by level of metabolic suppression experienced during diapause.

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4. Consider how the study of HSPs during stress and diapause can be used to control insect pests that impinge on agriculture, forestry, and the health of other animals and to understand the effects of global warming on the behavior of insects.

DISCLOSURE STATEMENT

Annu. Rev. Entomol. 2015.60:59-75. Downloaded from www.annualreviews.org Access provided by Cornell University - Weill Medical College on 10/17/16. For personal use only.

The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS The work was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to T.H.M. LITERATURE CITED 1. Arrigo A-P. 2013. Human small heat shock proteins: protein interactomes of homo- and heterooligomeric complexes; an update. FEBS Lett. 587:1959–69 2. Atungulu E, Tanaka H, Fujita K, Yamamoto K, Sakata M, et al. 2006. A double chaperone function of the sHsp genes against heat-based environmental adversity in the soil-dwelling leaf beetles. J. Insect Biotechnol. Sericol. 75:15–22 3. Azad P, Ryu J, Haddad GG. 2011. Distinct role of Hsp70 in Drosophila hemocytes during severe hypoxia. Free Rad. Biol. Med. 51:530–38 4. Bao B, Xu W-H. 2011. Identification of gene expression changes associated with the initiation of diapause in the brain of the cotton bollworm, Helicoverpa armigera. BMC Genomics 12:224 5. Basha E, O’Neill H, Vierling E. 2012. Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem. Sci. 37:106–17 6. Benoit JB, Lopez-Martinez G, Phillips ZP, Patrick KR, Denlinger DL. 2010. Heat shock proteins contribute to mosquito dehydration tolerance. J. Insect Physiol. 56:151–56 7. Brackley KI, Grantham J. 2009. Activities of the chaperonin containing TCP-1 (CCT): implications for cell cycle progression and cytoskeletal organisation. Cell Stress Chaperones 14:23–31 8. Burton V, Mitchell HK, Young P, Petersen NS. 1988. Heat shock protection against cold stress of Drosophila melanogaster. Mol. Cell. Biol. 8:3550–52 9. Carrigan PE, Riggs DL, Chinkers M, Smith DF. 2005. Functional comparison of human and Drosophila Hop reveals novel role in steroid receptor maturation. J. Biol. Chem. 280:8906–11 10. Chapuis M-P, Simpson SJ, Blondin L, Sword GA. 2011. Taxa-specific heat shock proteins are overexpressed with crowding in the Australian plague locust. J. Insect Physiol. 57:1562–67 11. Chen B, Kayukawa T, Monteiro A, Ishikawa Y. 2005. The expression of the HSP90 gene in response to winter and summer diapauses and thermal-stress in the onion maggot, Delia antiqua. Insect Mol. Biol. 14:697–702 12. Chen B, Kayukawa T, Monteiro A, Ishikawa Y. 2006. Cloning and characterization of the HSP70 gene, and its expression in response to diapauses and thermal stress in the onion maggot, Delia antiqua. J. Biochem. Mol. Biol. 39:749–58 13. Chen L, Ma W, Wang X, Niu C, Lei C. 2009. Analysis of pupal head proteome and its alteration in diapausing pupae of Helicoverpa armigera. J. Insect Physiol. 56:247–52 14. Clare DK, Saibil HR. 2013. ATP-driven molecular chaperone machines. Biopolymers 99:846–59 15. Colinet H, Hoffmann A. 2010. Gene and protein expression of Drosophila Starvin during cold stress and recovery from chill coma. Insect Biochem. Mol. Biol. 40:425–28 16. Colinet H, Hoffmann AA. 2012. Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Funct. Ecol. 26:84–93 www.annualreviews.org • Insect Heat Shock Proteins

5. Describes sHsp structure and its function in protein protection during stress.

14. Provides a description of the structure and function of ATP-dependent HSPs.

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22. Depicts sHsps as platforms that bind denaturing proteins and enable subsequent refolding.

30. Reveals that Hsp70 is not required for adult diapause in Drosophila (see also Ref. 29).

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40. Kankare M, Salminen T, Laiho A, Vesala L, Hoikkala A. 2010. Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study. BMC Ecol. 10:3 41. Kayukawa T, Chen B, Miyazaki S, Itoyama K, Shinoda T, Ishikawa Y. 2005. Expression of mRNA for the t-complex polypeptide–1, a subunit of chaperonin CCT, is upregulated in association with increased cold hardiness in Delia antiqua. Cell Stress Chaperones 10:204–10 42. Kayukawa T, Ishikawa Y. 2009. Chaperonin contributes to cold hardiness of the onion maggot Delia antiqua through repression of depolymerization of actin at low temperatures. PLOS ONE 4(12):e8277 43. Kihara F, Niimi T, Yamashita O, Yaginuma T. 2011. Heat shock factor binds to heat shock elements upstream of heat shock protein 70a and Samui genes to confer transcriptional activity in Bombyx mori diapause eggs exposed to 5◦ C. Insect Biochem. Mol. Biol. 41:843–51 44. Kim B-G, Shim J-K, Kim D-W, Kwon YJ, Lee K-Y. 2008. Tissue-specific variation of heat shock protein gene expression in relation to diapause in the bumblebee Bombus terrestris. Entomolog. Res. 38:10–16 45. Koˇstal ´ V. 2006. Eco-physiological phases of insect diapause. J. Insect Physiol. 52:113–27 46. Koˇst´al V, Tollarov´a-Borovansk´a M. 2009. The 70 kDa heat shock protein assists during the repair of chilling injury in the insect, Pyrrhocoris apterus. PLoS ONE 4(2):e4546 47. Lee GJ, Vierling E. 2000. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122:189–97 48. Li A, Denlinger DL. 2008. Rapid cold hardening elicits changes in brain protein profiles of the flesh fly, Sarcophaga crassipalpis. Insect Mol. Biol. 17:565–72 49. Li A, Denlinger DL. 2009. Pupal cuticle protein is abundant during early adult diapause in the mosquito Culex pipiens. J. Med. Entomol. 46:1382–86 50. Li AQ, Popova-Butler A, Dean DH, Denlinger DL. 2007. Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause. J. Insect Physiol. 53:385–91 51. Li H-B, Du Y-Z. 2013. Molecular cloning and characterization of an Hsp90/70 organizing protein gene from Frankliniella occidentalis (Insecta: Thysanoptera, Thripidae). Gene 520:148–55 52. Li J, Moghaddam HH, Du X, Zhong B, Chen Y-Y. 2012. Comparative analysis on the expression of inducible HSPs in the silkworm, Bombyx mori. Mol. Biol. Rep. 39:3915–23 53. Li Z-W, Li X, Yu Q-Y, Xiang Z-H, Kishino H, Zhang Z. 2009. The small heat shock protein (sHSP) genes in the silkworm, Bombyx mori, and comparative analysis with other insect sHSP genes. BMC Evol. Biol. 9:215 54. Liu G, Roy J, Johnson EA. 2006. Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiol. Genomics 25:134–41 55. Liu Z, Xi D, Kang M, Guo X, Xu B. 2012. Molecular cloning and characterization of Hsp27.6: the first reported small heat shock protein from Apis cerana cerana. Cell Stress Chaperones 17:539–51 56. Lopez-Martinez G, Benoit JB, Rinehart JP, Elnitsky MA, Lee RE Jr, Denlinger DL. 2009. Dehydration, rehydration, and overhydration alter patterns of gene expression in the Antarctic midge, Belgica antarctica. J. Comp. Physiol. B 179:481–91 57. Lopez-Martinez G, Denlinger DL. 2008. Regulation of heat shock proteins in the apple maggot Rhagoletis pomonella during hot summer days and overwintering diapause. Physiol. Entomol. 33:346–52 58. Lopez-Martinez G, Elnitsky MA, Benoit JB, Lee RE Jr, Denlinger DL. 2008. High resistance to oxidative damage in the Antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. Insect Biochem. Mol. Biol. 38:796–804 59. Lu M-X, Hua J, Cui Y-D, Du Y-Z. 2014. Five small heat shock protein genes from Chilo suppressalis: characteristics of gene, genomic organization, structural analysis, and transcription profiles. Cell Stress Chaperones 19:91–104 60. Lu Y-X, Xu W-H. 2010. Proteomic and phosphoproteomic analysis at diapause initiation in the cotton bollworm, Helicoverpa armigera. J. Proteome Res. 9:5053–64 61. MacRae TH. 2010. Gene expression, metabolic regulation and stress tolerance during diapause. Cell. Mol. Life Sci. 67:2405–24 62. Mayer MP. 2010. Gymnastics of molecular chaperones. Mol. Cell 39:321–31 www.annualreviews.org • Insect Heat Shock Proteins

45. Presents a thorough account of different phases throughout insect diapause.

50. Illustrates an early use of proteomics to examine HSPs during diapause.

61. Molecular analysis of diapause in several organisms, including insects.

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73. HSP production and function during diapause and cold tolerance in several insects.

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Contents

Annual Review of Entomology Volume 60, 2015

Breaking Good: A Chemist Wanders into Entomology John H. Law p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Multiorganismal Insects: Diversity and Function of Resident Microorganisms Angela E. Douglas p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p17 Crop Domestication and Its Impact on Naturally Selected Trophic Interactions Yolanda H. Chen, Rieta Gols, and Betty Benrey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p35 Insect Heat Shock Proteins During Stress and Diapause Allison M. King and Thomas H. MacRae p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p59 Termites as Targets and Models for Biotechnology Michael E. Scharf p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p77 Small Is Beautiful: Features of the Smallest Insects and Limits to Miniaturization Alexey A. Polilov p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 103 Insects in Fluctuating Thermal Environments Herv´e Colinet, Brent J. Sinclair, Philippe Vernon, and David Renault p p p p p p p p p p p p p p p p p 123 Developmental Mechanisms of Body Size and Wing-Body Scaling in Insects H. Frederik Nijhout and Viviane Callier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 141 Evolutionary Biology of Harvestmen (Arachnida, Opiliones) Gonzalo Giribet and Prashant P. Sharma p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157 Chorion Genes: A Landscape of Their Evolution, Structure, and Regulation Argyris Papantonis, Luc Swevers, and Kostas Iatrou p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177 Encyrtid Parasitoids of Soft Scale Insects: Biology, Behavior, and Their Use in Biological Control Apostolos Kapranas and Alejandro Tena p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 195

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Extrafloral Nectar at the Plant-Insect Interface: A Spotlight on Chemical Ecology, Phenotypic Plasticity, and Food Webs Martin Heil p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 213 Insect Response to Plant Defensive Protease Inhibitors Keyan Zhu-Salzman and Rensen Zeng p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 233 Origin, Development, and Evolution of Butterfly Eyespots Ant´onia Monteiro p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 253

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Whitefly Parasitoids: Distribution, Life History, Bionomics, and Utilization Tong-Xian Liu, Philip A. Stansly, and Dan Gerling p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 273 Recent Advances in the Integrative Nutrition of Arthropods Stephen J. Simpson, Fiona J. Clissold, Mathieu Lihoreau, Fleur Ponton, Shawn M. Wilder, and David Raubenheimer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 293 Biology, Ecology, and Control of Elaterid Beetles in Agricultural Land Michael Traugott, Carly M. Benefer, Rod P. Blackshaw, Willem G. van Herk, and Robert S. Vernon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 313 Anopheles punctulatus Group: Evolution, Distribution, and Control Nigel W. Beebe, Tanya Russell, Thomas R. Burkot, and Robert D. Cooper p p p p p p p p p p p p p p 335 Adenotrophic Viviparity in Tsetse Flies: Potential for Population Control and as an Insect Model for Lactation Joshua B. Benoit, Geoffrey M. Attardo, Aaron A. Baumann, Veronika Michalkova, and Serap Aksoy p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351 Bionomics of Temperate and Tropical Culicoides Midges: Knowledge Gaps and Consequences for Transmission of Culicoides-Borne Viruses B.V. Purse, S. Carpenter, G.J. Venter, G. Bellis, and B.A. Mullens p p p p p p p p p p p p p p p p p p p p 373 Mirid (Hemiptera: Heteroptera) Specialists of Sticky Plants: Adaptations, Interactions, and Ecological Implications Alfred G. Wheeler Jr. and Billy A. Krimmel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 393 Honey Bee Toxicology Reed M. Johnson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 415 DNA Methylation in Social Insects: How Epigenetics Can Control Behavior and Longevity Hua Yan, Roberto Bonasio, Daniel F. Simola, Jurgen ¨ Liebig, Shelley L. Berger, and Danny Reinberg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 435 Exaggerated Trait Growth in Insects Laura Lavine, Hiroki Gotoh, Colin S. Brent, Ian Dworkin, and Douglas J. Emlen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 453

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Physiology of Environmental Adaptations and Resource Acquisition in Cockroaches Donald E. Mullins p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 473 Plant Responses to Insect Egg Deposition Monika Hilker and Nina E. Fatouros p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 493

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Root-Feeding Insects and Their Interactions with Organisms in the Rhizosphere Scott N. Johnson and Sergio Rasmann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 517 Insecticide Resistance in Mosquitoes: Impact, Mechanisms, and Research Directions Nannan Liu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 537 Vector Ecology of Equine Piroplasmosis Glen A. Scoles and Massaro W. Ueti p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561 Trail Pheromones: An Integrative View of Their Role in Social Insect Colony Organization Tomer J. Czaczkes, Christoph Gruter, ¨ and Francis L.W. Ratnieks p p p p p p p p p p p p p p p p p p p p p p 581 Sirex Woodwasp: A Model for Evolving Management Paradigms of Invasive Forest Pests Bernard Slippers, Brett P. Hurley, and Michael J. Wingfield p p p p p p p p p p p p p p p p p p p p p p p p p p p p 601 Economic Value of Biological Control in Integrated Pest Management of Managed Plant Systems Steven E. Naranjo, Peter C. Ellsworth, and George B. Frisvold p p p p p p p p p p p p p p p p p p p p p p p p p 621 Indexes Cumulative Index of Contributing Authors, Volumes 51–60 p p p p p p p p p p p p p p p p p p p p p p p p p p p 647 Cumulative Index of Article Titles, Volumes 51–60 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 652 Errata An online log of corrections to Annual Review of Entomology articles may be found at http://www.annualreviews.org/errata/ento

Contents

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Insect heat shock proteins during stress and diapause.

Insect heat shock proteins include ATP-independent small heat shock proteins and the larger ATP-dependent proteins, Hsp70, Hsp90, and Hsp60. In concer...
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