Genes and associated peptides involved with aestivation in a land snail

Adamson, K J; Wang, Tianfang; Rotgans, Bronwyn; Kruangkum, Thanapong; Kuballa, Anna; Storey, Kenneth B.; Cummins, Scott F.

doi:10.1016/j.ygcen.2015.10.013

Cited by 15 publications

(8 citation statements)

References 59 publications

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“…Our molecular analysis demonstrated that the helicid LDA is released from a buccalin-like precursor, a peptide-rich precursor that is also found in other mollusks. BLASTp analysis provided strong evidence that the C. aspersum LDA precursor is a homolog of buccalin precursors that have previously been identified in several mollusks, including the sea slug (Aplysia californica), the freshwater pond snail (Lymnaea stagnalis), and the land snail T. pisana (27,28,33). It is striking that two of the helicids clearly differ from the other two land snails in this comparison (Cernuella virgata and Cochlicella acuta).…”

Section: Discussionsupporting

confidence: 61%

“…This function is supported by the presence of the C-terminal GLamide, which is a feature also found in insect allotostatin A (37) and in the class of DLamides identified in the annelid Platyneiris demurilii (38). The buccalin gene of T. pisana has widespread expression outside the mucous gland, including the CNS of aestivated (dormant in warm conditions) snails, where the buccalin-2 isoform is distributed within regions that control several physiological roles (33).…”

Section: Discussionmentioning

confidence: 90%

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A “Love” Dart Allohormone Identified in the Mucous Glands of Hermaphroditic Land Snails

Stewart

Wang

Koene

et al. 2016

Journal of Biological Chemistry

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Animals have evolved many ways to enhance their own reproductive success. One bizarre sexual ritual is the "love" dart shooting of helicid snails, which has courted many theories regarding its precise function. Acting as a hypodermic needle, the dart transfers an allohormone that increases paternity success. Its precise physiological mechanism of action within the recipient snail is to close off the entrance to the sperm digestion organ via a contraction of the copulatory canal, thereby delaying the digestion of most donated sperm. In this study, we used the common garden snail Cornu aspersum to identify the allohormone that is responsible for this physiological change in the female system of this simultaneous hermaphrodite. The love dart allohormone (LDA) was isolated from extracts derived from mucous glands that coat the dart before it is stabbed through the partner's body wall. We isolated LDA from extracts using bioassay-guided contractility measurement of the copulatory canal. LDA is encoded within a 235-amino acid precursor protein containing multiple cleavage sites that, when cleaved, releases multiple bioactive peptides. Synthetic LDA also stimulated copulatory canal contractility. Combined with our finding that the protein amino acid sequence resembles previously described molluscan buccalin precursors, this indicates that LDA is partially conserved in helicid snails and less in other molluscan species. In summary, our study provides the full identification of an allohormone that is hypodermically injected via a love dart. More importantly, our findings have important consequences for understanding reproductive biology and the evolution of alternative reproductive strategies.

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Section: Discussionsupporting

confidence: 61%

Section: Discussionmentioning

confidence: 90%

A “Love” Dart Allohormone Identified in the Mucous Glands of Hermaphroditic Land Snails

Stewart

Wang

Koene

et al. 2016

Journal of Biological Chemistry

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“…This was followed by a nested PCR using 1 µl of primary PCR and 1 µl of sense OL4, 5′‐TGYGAYTGYGARGTNATHACNGAYG‐3′ (CDCEVITD) and antisense OL2 (10 µmol each) using the same cycling parameters as the primary PCR. Reaction products were cloned and sequenced as previously described . To identify target sequences, peptides of interest were imported into the CLC Genomics Workbench (v6.0; Finlandsgade, Dk).…”

Section: Methodsmentioning

confidence: 99%

Identification of a female spawn‐associated Kazal‐type inhibitor from the tropical abalone Haliotis asinina

et al. 2016

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Abalone (Haliotis) undergoes a period of reproductive maturation, followed by the synchronous release of gametes, called broadcast spawning. Field and laboratory studies have shown that the tropical species Haliotis asinina undergoes a two-week spawning cycle, thus providing an excellent opportunity to investigate the presence of endogenous spawning-associated peptides. In female H. asinina, we have isolated a peptide (5145 Da) whose relative abundance in hemolymph increases substantially just prior to spawning and is still detected using reverse-phase high-performance liquid chromatography chromatograms up to 1-day post-spawn. We have isolated this peptide from female hemolymph as well as samples prepared from the gravid female gonad, and demonstrated through comparative sequence analysis that it contains features characteristic of Kazal-type proteinase inhibitors (KPIs). Has-KPI is expressed specifically within the gonad of adult females. A recombinant Has-KPI was generated using a yeast expression system. The recombinant Has-KPI does not induce premature spawning of female H. asinina when administered intramuscularly. However it displays homomeric aggregations and interaction with at least one mollusc-type neuropeptide (LRDFVamide), suggesting a role for it in regulating neuropeptide endocrine communication. This research provides new understanding of a peptide that can regulate reproductive processes in female abalone, which has the potential to lead to the development of greater control over abalone spawning. The findings also highlight the need to further explore abalone reproduction to clearly define a role for novel spawning-associated peptide in sexual maturation and spawning. Copyright © 2016 European Peptide Society and John Wiley & Sons, Ltd.

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“…While it may be hypothesized that Turing's reaction-diffusion model plays a role in the formation of shell patterns in molluscs, identification of the genes is a first step before testing whether the interacting substances are necessary in defining the patterns. We envisage two converging routes by which this may be made possible, either taking a gene mapping and pattern-led approach (Cossins et al, 2006;Harper et al, 2011;Peichel & Marques, 2017), or else by comparing spatial gene expression (Adamson et al, 2017;Landgrebe et al, 2002;Ståhl et al, 2016).…”

Section: Reaction Diffusion Mechanismmentioning

confidence: 99%

Quantitative measures and 3D shell models reveal interactions between bands and their position on growing snail shells

Jackson

Larsson

Davison

2021

Ecology and Evolution

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The nature of shell growth in gastropods is useful because it preserves the ontogeny of shape, colour, and banding patterns, making them an ideal system for understanding how inherited variation develops, is established and maintained within a population. However, qualitative scoring of inherited shell characters means there is a lack of knowledge regarding the mechanisms that control fine variation. Here, we combine empirical measures of quantitative variation and 3D modeling of shells to understand how bands are placed and interact. By comparing five‐banded Cepaea individuals to shells lacking individual bands, we show that individual band absence has minor but significant impacts upon the position of remaining bands, implying that the locus controlling band presence/absence mainly acts after position is established. Then, we show that the shell grows at a similar rate, except for the region below the lowermost band. This demonstrates that wider bands of Cepaea are not an artifact of greater shell growth on the lower shell; they begin wider and grow at the same rate as other bands. Finally, we show that 3D models of shell shape and banding pattern, inferred from 2D photos using ShellShaper software, are congruent with empirical measures. This work therefore establishes a method that may be used for comparative studies of quantitative banding variation in snail shells, extraction of growth parameters, and morphometrics. In the future, studies that link the banding phenotype to the network of shell matrix proteins involved in biomineralization and patterning may ultimately aid in understanding the diversity of shell forms found in molluscs.

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Genes and associated peptides involved with aestivation in a land snail

Cited by 15 publications

References 59 publications

A “Love” Dart Allohormone Identified in the Mucous Glands of Hermaphroditic Land Snails

A “Love” Dart Allohormone Identified in the Mucous Glands of Hermaphroditic Land Snails

Identification of a female spawn‐associated Kazal‐type inhibitor from the tropical abalone Haliotis asinina

Quantitative measures and 3D shell models reveal interactions between bands and their position on growing snail shells

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