Diversity, abundance, and sex-specific expression of chemosensory proteins in the reproductive organs of the locust Locusta migratoria manilensis

Abstract

Chemosensory proteins (CSPs) are small soluble proteins often associated with chemosensory organs in insects but include members involved in other functions, such as pheromone delivery and development. Although the CSPs of the sensory organs have been extensively studied, little is known on their functions in other parts of the body. A first screening of the available databases has identified 70 sequences encoding CSPs in the oriental locust Locusta migratoria manilensis. Applying proteomic analysis, we have identified 17 of them abundantly expressed in the female reproductive organs, but only one (CSP91) in male organs. Bacterially expressed CSP91 binds fatty acids with a specificity for oleic and linoleic acid, as well as medium-length alcohols and esters. The same acids have been detected as the main gas chromatographic peaks in the dichloromethane extracts of reproductive organs of both sexes. The abundance and the number of CSPs in female reproductive organs indicates important roles for these proteins. We cannot exclude that different functions can be associated with each of the 17 CSPs, including delivery of semiochemicals, solubilization of hormones, direct control of development, or other unknown tasks.

Soluble proteins of chemical communication: an overview across arthropods

“…With respect to OBPs, CSPs are in general more widely expressed in different parts of the body, suggestive often of nonspecific functions. As already observed for OBPs, also the number of CSP genes in different species of insects is highly variable, from as few as four in D. melanogaster (Vieira and Rozas, 2011) to at least 70 in L. migratoria (Zhou et al, 2013). Although proteins of both classes, owing to their successful folding and stability, are utilized for different tasks besides chemical communication, it is true that most of the studies on OBPs have been associated with chemoreception, while often CSPs have been reported in connection with other physiological events.…”

“…Both OBPs and CSPs have been detected in pheromone glands or in reproductive organs, where they might assist releasing of semiochemicals into the environment. Typical examples are the CSPs found in the pheromone glands of Mamestra brassicae (Jacquin-Joly et al, 2001), Bombyx mori (Dani et al, 2011) and Agrotis ipsilon (Gu et al, 2013), as well as the OBP10 of Helicoverpa armigera and H. assulta (Sun et al, 2012b), the OBP22 of Aedes aegypti (Li et al, 2008) and the CSP91 of Locusta migratoria , produced in the male seminal fluid and transferred to the female, likely with a bound pheromone, during mating (Ban et al, 2013; Zhou et al, 2013). Several OBPs and CSPs are also expressed in the mandibular glands of the honey bee (Iovinella et al, 2011).…”

“…Moreover, members of both classes have been reported in other tissues and shown to be involved in functions unrelated to chemical communication. (1) Finlayson et al, 1965; Bacchini et al, 1992; (2) Dinh et al, 1965; (3) Singer et al, 1986; (4) D'Innocenzo et al, 2006; (5) Mastrogiacomo et al, 2014; (6) Marchese et al, 1998; (7) Zeng et al, 1996; (8) Nomura et al, 1992; Kitabayashi et al, 1998; (9) Zhou et al, 2013; (10) Jacquin-Joly et al, 2001; (11) Gu et al, 2013; (12) Dani et al, 2011; (13) Sun et al, 2012b; Liu et al, 2014a; (14) Iovinella et al, 2011; Maleszka et al, 2007; (15) Ishida et al, 2013; (16) Calvo et al, 2009; Costa-da-Silva et al, 2013; Marinotti et al, 2014; Li et al, 2008.…”

Discovery of Chemosensory Genes in the Oriental Fruit Fly, Bactrocera dorsalis

“…Most olfaction-related OBPs and CSPs are abundant in the sensillum lymph of olfactory organs (antennae and maxillary palp), and play a critical role as solubilizers and/or carriers of odorants and pheromones[63,64,77–82]. However, non-olfaction-related OBPs and CSPs have been found in the pheromone gland secretions involved in the delivery of semiochemicals (example, pheromones)[83–89], and secretions of the reproductive organs involved in egg and embryo development[90,91]. The expression patterns of both olfaction and non-olfaction related B .…”

Unique function of a chemosensory protein in the proboscis of two Helicoverpa species

“…Apart from those expressed in chemosensilla, the family of CSPs includes members present in pheromone glands or reproductive organs, where they could act as carriers for semiochemicals, assisting their release into the environment (Dyanov and Dzitoeva, 1995;Jacquin-Joly et al, 2001;Dani et al, 2011;Iovinella et al, 2011;Iovinella et al, 2013;Sun et al, 2012;Zhou et al, 2013). Most interestingly, other functions, completely unrelated to chemical communication, have been reported to be associated with some CSPs.…”