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Venom-related transcripts from Bothrops jararaca tissues provide novel molecular insights into the production and evolution of snake venom.
Mol Biol Evol. 2015 Mar; 32(3):754-66.MB

Abstract

Attempts to reconstruct the evolutionary history of snake toxins in the context of their co-option to the venom gland rarely account for nonvenom snake genes that are paralogous to toxins, and which therefore represent important connectors to ancestral genes. In order to reevaluate this process, we conducted a comparative transcriptomic survey on body tissues from a venomous snake. A nonredundant set of 33,000 unigenes (assembled transcripts of reference genes) was independently assembled from six organs of the medically important viperid snake Bothrops jararaca, providing a reference list of 82 full-length toxins from the venom gland and specific products from other tissues, such as pancreatic digestive enzymes. Unigenes were then screened for nontoxin transcripts paralogous to toxins revealing 1) low level coexpression of approximately 20% of toxin genes (e.g., bradykinin-potentiating peptide, C-type lectin, snake venom metalloproteinase, snake venom nerve growth factor) in body tissues, 2) the identity of the closest paralogs to toxin genes in eight classes of toxins, 3) the location and level of paralog expression, indicating that, in general, co-expression occurs in a higher number of tissues and at lower levels than observed for toxin genes, and 4) strong evidence of a toxin gene reverting back to selective expression in a body tissue. In addition, our differential gene expression analyses identify specific cellular processes that make the venom gland a highly specialized secretory tissue. Our results demonstrate that the evolution and production of venom in snakes is a complex process that can only be understood in the context of comparative data from other snake tissues, including the identification of genes paralogous to venom toxins.

Authors+Show Affiliations

Laboratório Especial de Toxinologia Aplicada, Center of Toxins, Immune-Response and Cell Signaling (CeTICS), Instituto Butantan, São Paulo, Brazil Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil inacio.azevedo@butantan.gov.br.Laboratório Especial de Toxinologia Aplicada, Center of Toxins, Immune-Response and Cell Signaling (CeTICS), Instituto Butantan, São Paulo, Brazil Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil.Centro de Biotecnologia, Instituto Butantan, São Paulo, Brazil.Laboratório de Farmacologia, Instituto Butantan, São Paulo-SP, Brazil.Laboratório de Farmacologia, Instituto Butantan, São Paulo-SP, Brazil.Alistair Reid Venom Research Unit, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

25502939

Citation

Junqueira-de-Azevedo, Inácio L M., et al. "Venom-related Transcripts From Bothrops Jararaca Tissues Provide Novel Molecular Insights Into the Production and Evolution of Snake Venom." Molecular Biology and Evolution, vol. 32, no. 3, 2015, pp. 754-66.
Junqueira-de-Azevedo IL, Bastos CM, Ho PL, et al. Venom-related transcripts from Bothrops jararaca tissues provide novel molecular insights into the production and evolution of snake venom. Mol Biol Evol. 2015;32(3):754-66.
Junqueira-de-Azevedo, I. L., Bastos, C. M., Ho, P. L., Luna, M. S., Yamanouye, N., & Casewell, N. R. (2015). Venom-related transcripts from Bothrops jararaca tissues provide novel molecular insights into the production and evolution of snake venom. Molecular Biology and Evolution, 32(3), 754-66. https://doi.org/10.1093/molbev/msu337
Junqueira-de-Azevedo IL, et al. Venom-related Transcripts From Bothrops Jararaca Tissues Provide Novel Molecular Insights Into the Production and Evolution of Snake Venom. Mol Biol Evol. 2015;32(3):754-66. PubMed PMID: 25502939.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Venom-related transcripts from Bothrops jararaca tissues provide novel molecular insights into the production and evolution of snake venom. AU - Junqueira-de-Azevedo,Inácio L M, AU - Bastos,Carolina Mancini Val, AU - Ho,Paulo Lee, AU - Luna,Milene Schmidt, AU - Yamanouye,Norma, AU - Casewell,Nicholas R, Y1 - 2014/12/09/ PY - 2014/12/16/entrez PY - 2014/12/17/pubmed PY - 2016/3/10/medline KW - Bothrops jararaca KW - Serpentes KW - differential expression KW - snake toxin KW - transcriptome KW - venom gland SP - 754 EP - 66 JF - Molecular biology and evolution JO - Mol. Biol. Evol. VL - 32 IS - 3 N2 - Attempts to reconstruct the evolutionary history of snake toxins in the context of their co-option to the venom gland rarely account for nonvenom snake genes that are paralogous to toxins, and which therefore represent important connectors to ancestral genes. In order to reevaluate this process, we conducted a comparative transcriptomic survey on body tissues from a venomous snake. A nonredundant set of 33,000 unigenes (assembled transcripts of reference genes) was independently assembled from six organs of the medically important viperid snake Bothrops jararaca, providing a reference list of 82 full-length toxins from the venom gland and specific products from other tissues, such as pancreatic digestive enzymes. Unigenes were then screened for nontoxin transcripts paralogous to toxins revealing 1) low level coexpression of approximately 20% of toxin genes (e.g., bradykinin-potentiating peptide, C-type lectin, snake venom metalloproteinase, snake venom nerve growth factor) in body tissues, 2) the identity of the closest paralogs to toxin genes in eight classes of toxins, 3) the location and level of paralog expression, indicating that, in general, co-expression occurs in a higher number of tissues and at lower levels than observed for toxin genes, and 4) strong evidence of a toxin gene reverting back to selective expression in a body tissue. In addition, our differential gene expression analyses identify specific cellular processes that make the venom gland a highly specialized secretory tissue. Our results demonstrate that the evolution and production of venom in snakes is a complex process that can only be understood in the context of comparative data from other snake tissues, including the identification of genes paralogous to venom toxins. SN - 1537-1719 UR - https://www.unboundmedicine.com/medline/citation/25502939/Venom_related_transcripts_from_Bothrops_jararaca_tissues_provide_novel_molecular_insights_into_the_production_and_evolution_of_snake_venom_ L2 - https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msu337 DB - PRIME DP - Unbound Medicine ER -