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Title: Genes encoding proteins with peritrophin A-type chitin-binding domains in Tribolium castaneum are grouped into three distinct families based on phylogeny, expression and function

Author
item JASRAPURIA, SINU - Kansas State University
item ARAKANE, YASUYUKI - Kansas State University
item OSMAN, GAMAL - Kansas State University
item KRAMER, KARL - Collaborator
item Beeman, Richard
item MUTHUKRISHNAN, SUBBARATNAM - Kansas State University

Submitted to: Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/29/2010
Publication Date: 3/15/2010
Citation: Jasrapuria, S., Arakane, Y., Osman, G., Kramer, K.J., Beeman, R.W., Muthukrishnan, S. 2010. Genes encoding proteins with peritrophin A-type chitin-binding domains in Tribolium castaneum are grouped into three distinct families based on phylogeny, expression and function. Insect Biochemistry and Molecular Biology. 40(3):214-227. doi:doi:10.1016/j.ibmb.2010.01.011.

Interpretive Summary: Digestion and exoskeleton are unique and sensitive aspects of insect physiology that could be exploited by appropriately-targeted biopesticides. Peritrophins are a poorly-understood class of proteins that are believed to be the major structural proteins of the insect midgut digestive sac. We identified 29 peritrophin-like proteins in the red flour beetle, and showed that 11 of these appear to have unique and specific functions in digestion in the midgut. Surprisingly, the remaining 18 do not appear to have a digestive function. Instead, at least some of them are required for development of the exoskeleton or other tissues of similar composition. Studying the detailed functions of insect genes continues to reveal new weaknesses that may be exploited for insect control.

Technical Abstract: This study is focused on the characterization and expression of genes in the red flour beetle, Tribolium castaneum, encoding proteins that possess six-cysteine-containing chitin-binding domains (CBDs) related to the peritrophin A domain (ChtBD2). An exhaustive bioinformatics search of the genome of T. castaneum queried with ChtBD2 sequences yielded 13 previously characterized chitin metabolic enzymes and 29 additional proteins with signal peptides as well as ChtBD2s. Using phylogenetic analyses, these 29 proteins were classified into two large groups. The first group includes 11 proteins closely related to the peritrophins, each containing 1-14 ChtBD2s. The expression of these genes is restricted to the midgut and to feeding stages. The second group includes 18 proteins, eight of which are closely related to gasp/obstructor-like proteins with three ChtBD2s each and the remaining ten being of diverse sizes and sequences that contain only one ChtBD2 each. The eight gasp/obstructor-like proteins are encoded by seven genes (two of the proteins result from alternative splicing of a single gene) and are expressed in non-midgut tissues throughout all stages of development. We propose the names “Peritrophic Matrix Proteins” (PMPs) and “Cuticular Proteins Analogous to Peritophins” (CPAPs) for the first and second groups, respectively. We determined the exon-intron organization of these genes, as well as the domain organization of the encoded proteins. All 29 proteins have predicted cleavable signal peptides and ChtBD2s, suggesting that they interact with extracellular chitin. Comparison of ChtBD2s-containing proteins in different insect species belonging to different orders suggests that ChtBD2s are ancient protein domains whose affinity for chitin has been exploited many times for achieving a wide range of biological functions.