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Title: Search for hidden messenger molecules: capa-gene expression in ants

Author
item Choi, Man-Yeon
item KOHLER, RENE - University Of Cologne
item Vander Meer, Robert - Bob
item Valles, Steven
item NEUPERT, SUSANNE - University Of Cologne
item PREDEL, REINHARD - University Of Cologne

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/19/2014
Publication Date: 4/9/2014
Citation: Choi, M.Y., Kohler, R., Vander Meer, R.K., Valles, S.M., Neupert, S., Predel, R. 2014. Search for hidden messenger molecules: capa-gene expression in ants. PLoS One. 9(4):1-10.

Interpretive Summary: Insect neuropeptides play many critical roles in insect development and metamorphosis. One of insect neuropeptides is derived from the capa-gene that is well conserved. The peptide(s) function to stimulate visceral muscle contraction and regulate the activity of Malpighian tubules in many insects. Identifying and understanding the mode of action for this neuropeptide could lead to new non-insecticidal control methods. Recently, insect genomes including ants have been reported; however, capa-genes have not been reported from ant genomes. The capa-gene may have been overlooked from ants, including the red imported fire ant, Solenopsis invicta. The fire ant is among the world’s 100 worst invasive alien species. In the United States this ant species infests more than 320 million acres in 13 southern tier states and Puerto Rico and are spreading northward. Scientists at the Center for Medical, Agricultural and Veterinary Entomology, USDA, ARS, Gainesville, FL, and the Zoological Institute, Biocenter University of Cologne, Cologne, Germany have identified and characterized the capa-gene from the fire ant. Scientists found that ants possess and express a capa-gene, and the gene occurs with alternative transcripts in the central nervous system. The S. invicta capa-gene includes all predicted CAPA-periviscerokinins (PVKs) and CAPA-pyrokinin (PK) peptides as identified from cloning of the capa-gene and MALDI-TOF mass spectrometry. As in other holometabolous insects, only two capa-neurons are present in unfused abdominal ganglia. Our results demonstrate that non-detection of genes by bioinformatic analyses of genome data does not necessarily mean that the genes are absent. The entire CAPA-precursor sequence of S. invicta shows a surprisingly low homology with those of other holometabolous insects.

Technical Abstract: Recent genome analyses suggested the absence of a number of neuropeptide genes and corresponding receptor genes in ants. That absence raised questions about compensation of functions of these peptides in hymenopteran insects. One of the missing genes is the capa-gene. CAPA-peptides are known to regulate diuresis and visceral muscle contraction and are typically associated with the abdominal ventral nerve cord of the insect neuroendocrine systems. To search for a potentially unrecognized capa-gene in the fire ant, S. invicta, we employed a traditional PCR-based strategy using degenerate primers designed from conserved amino acid sequences of insect capa-genes. Our findings demonstrate that ants possess and express a capa-gene, and the gene occurs with alternative transcripts in the CNS. Processed products of the S. invicta capa-gene included all predicted CAPA-periviscerokinins (PVKs) and CAPA-pyrokinin (PK) peptides as identified by MALDI-TOF mass spectrometry. As in other holometabolous insects, only two capa-neurons are present in unfused abdominal ganglia and project into abdominal perisympathetic organs (PSOs), which are major hormone release sites of the abdominal ganglia. The ventral position of the abdominal PSOs is unique for insects and was also found in another ant, Atta sexdens. These results demonstrate that non-detection of genes by bioinformatic analyses of genome data does not necessarily mean that the genes are absent. The entire CAPA-precursor sequence of S. invicta shows a surprisingly low homology with those of other holometabolous insects.