Evolution of Soldier-Specific Venomous Protease in Social Aphids

Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan.
Molecular Biology and Evolution (Impact Factor: 9.11). 10/2008; 25(12):2627-41. DOI: 10.1093/molbev/msn203
Source: PubMed

ABSTRACT In social aphids of the genus Tuberaphis a cysteine protease gene of the family cathepsin B exhibits soldier-specific expression and intestinal protease production. The product is orally excreted and injected by soldier nymphs into natural enemies, thereby exerting an insecticidal activity. In an attempt to gain insights into when and how the novel venomous protease for the altruistic caste has evolved, we investigated the soldier-specific type (S-type) and nonspecific type (N-type) cathepsin B genes from social and nonsocial aphids. All the social aphids examined, representing the genera Tuberaphis, Astegopteryx, and Cerataphis, possessed both the S-type and N-type genes. Phylogenetically distant nonsocial aphids also possessed cathepsin B genes allied to the S-type and the N-type, indicating the evolutionary origin of these genes in the common ancestor of extant aphids. In Tuberaphis species the S-type genes exhibited significant soldier-specific expression and accelerated molecular evolution whereas the N-type genes did not. In Astegopteryx and Cerataphis species, meanwhile, both the S-type and N-type genes exhibited neither remarkable soldier-specific expression nor accelerated molecular evolution. These results suggest that the S-type gene acquired the soldier-specific expression and the venom function after divergence of the genus Tuberaphis. On the structural model of the S-type protease of Tuberaphis styraci the accelerated molecular evolution was associated with the molecular surface rather than the catalytic cleft, suggesting that the venom activity was probably acquired by relatively minor modifications on the molecular surface rather than by generation of a novel active site. In Cerataphis jamuritsu the S-type gene was, although containing a stop codon, structurally almost intact and still transcribed, suggesting recent pseudogenization of the gene copy and possible relevance to relaxed functional constraint in the highly multiplied protease gene family. On the basis of these results we suggest that the massive amplification in aphid cathepsin B genes might have predisposed the evolution of venomous protease in the social aphid lineage and argue that gene duplication, accelerated molecular evolution, and acquisition of novel gene function must have played considerable roles in the evolution of complex biological systems including insect sociality.

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Available from: Claude Rispe, Sep 29, 2015
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    • "These results indicate that functional divergence occurs during the evolutionary process of cathepsin genes, which could be attributed to chromosome replication or gene duplication (Fig. 2). Kutsukake et al. (2008) showed that gene duplication and accelerated molecular evolution comprise a general and important evolutionary process that enables the acquisition of novel functions [45]. In the present study, cathepsin L in zebrafish, cathepsins S and K in xenopus, and cathepsin L1 in mice and rats underwent severe tandem duplications (Figs. 2 and 3), which was in accordance with Kutsukake's notion [45]. "
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    ABSTRACT: Cathepsin L family, an important cysteine protease found in lysosomes, is categorized into cathepsins B, F, H, K, L, S, and W in vertebrates. This categorization is based on their sequence alignment and traditional functional classification, but the evolutionary relationship of family members is unclear. This study determined the evolutionary relationship of cathepsin L family genes in vertebrates through phylogenetic construction. Results showed that cathepsins F, H, S and K, and L and V were chronologically diverged. Tandem-repeat duplication was found to occur in the evolutionary history of cathepsin L family. Cathepsin L in zebrafish, cathepsins S and K in xenopus, and cathepsin L in mice and rats underwent evident tandem-repeat events. Positive selection was detected in cathepsin L-like members in mice and rats, and amino acid sites under positive selection pressure were calculated. Most of these sites appeared at the connection of secondary structures, suggesting that the sites may slightly change spatial structure. Severe positive selection was also observed in cathepsin V (L2) of primates, indicating that this enzyme had some special functions. Our work provided a brief evolutionary history of cathepsin L family and differentiated cathepsins S and K from cathepsin L based on vertebrate appearance. Positive selection was the specific cause of differentiation of cathepsin L family genes, confirming that gene function variation after expansion events was related to interactions with the environment and adaptability.
    International journal of biological sciences 07/2015; 11(9):1016-25. DOI:10.7150/ijbs.11751 · 4.51 Impact Factor
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    • "Fantastic examples of aphid polyphenisms , beyond dispersal and reproduction, come from eusocial aphids where a soldier caste may be produced. Members of the genus Tuberaphis produce a soldier caste that kills invaders by injecting them with a soldier-specific venom, and soldiers from the genus Pseudoregma have modified front legs and well-developed horns for ripping invaders apart (Shingleton & Foster, 2000; Kutsukake et al., 2008). This diversity in morphology and behaviour exists among genetically identical individuals and is best explained as an epigenetic phenomenon. "
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    ABSTRACT: Aphids display extraordinary developmental plasticity in response to environmental cues. These differential responses to environmental changes may be due in part to changes in gene expression patterns. To understand the molecular basis for aphid developmental plasticity, we attempted to identify the chromatin-remodelling machinery in the recently sequenced pea aphid genome. We find that the pea aphid possesses a complement of metazoan histone modifying enzymes with greater gene family diversity than that seen in a number of other arthropods. Several genes appear to have undergone recent duplication and divergence, potentially enabling greater combinatorial diversity among the chromatin-remodelling complexes. The abundant aphid chromatin modifying enzymes may facilitate the phenotypic plasticity necessary to maintain the complex life cycle of the aphid.
    Insect Molecular Biology 03/2010; 19 Suppl 2:201-14. DOI:10.1111/j.1365-2583.2009.00972.x · 2.59 Impact Factor
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    ABSTRACT: For evolution and maintenance of the social systems of insect colonies, caste production should be controlled in response to external cues so that caste ratio in the colony is kept at an optimal range. Recent developments using artificial diet rearing techniques have revealed an underlying mechanism for adaptive control of caste production in a social aphid, Tuberaphis styraci, which has a sterile soldier caste in the 2(nd) instar. Aphid density was the proximate cue that acts on 1(st) instar nymphs and embryos to induce soldier differentiation. The final determination of soldier differentiation occurred postnatally, probably at a late 1(st) instar stage. Direct contact stimuli from live non-soldier aphids mediated the density effect. While coexisting non-soldiers facilitated soldier differentiation in 1(st) instar nymphs, coexisting soldiers acted to suppress such differentiation. These results suggest that caste production in aphid colonies is controlled by positive and negative feedback mechanisms consisting of density-dependent induction and suppression of soldier differentiation. Here, we demonstrate the mechanisms that coordinate aphid society, and provide a striking case of clonal superorganism system where simple responses of colony members to local extrinsic stimuli are integrated into a highly organized regulation of the whole colony.
    Communicative & integrative biology 01/2010; 3(1):1-5. DOI:10.4161/cib.3.1.9694
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