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Open Access Research article

Differential impacts of juvenile hormone, soldier head extract and alternate caste phenotypes on host and symbiont transcriptome composition in the gut of the termite Reticulitermes flavipes

Ruchira Sen1, Rhitoban Raychoudhury1, Yunpeng Cai24, Yijun Sun25, Verena-Ulrike Lietze3, Drion G Boucias3 and Michael E Scharf1*

Author Affiliations

1 Department of Entomology, Purdue University, West Lafayette, IN, USA

2 Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, USA

3 Entomology and Nematology Department, University of Florida, Gainesville, FL, USA

4 Current Address: Research Center for Biomedical Information Technology, Shenzhen Institutes of Advance Technology, Chinese Academy of Sciences, Shenzhen, China

5 Current Address: Department of Microbiology and Immunology & New York State Center of Excellence in Bioinformatics and Life Sciences, The State University of New York at Buffalo, Buffalo, NY 14203, USA

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BMC Genomics 2013, 14:491  doi:10.1186/1471-2164-14-491

Published: 19 July 2013

Abstract

Background

Termites are highly eusocial insects and show a division of labor whereby morphologically distinct individuals specialize in distinct tasks. In the lower termite Reticulitermes flavipes (Rhinotermitidae), non-reproducing individuals form the worker and soldier castes, which specialize in helping (e.g., brood care, cleaning, foraging) and defense behaviors, respectively. Workers are totipotent juveniles that can either undergo status quo molts or develop into soldiers or neotenic reproductives. This caste differentiation can be regulated by juvenile hormone (JH) and primer pheromones contained in soldier head extracts (SHE). Here we offered worker termites a cellulose diet treated with JH or SHE for 24-hr, or held them with live soldiers (LS) or live neotenic reproductives (LR). We then determined gene expression profiles of the host termite gut and protozoan symbionts concurrently using custom cDNA oligo-microarrays containing 10,990 individual ESTs.

Results

JH was the most influential treatment (501 total ESTs affected), followed by LS (24 ESTs), LR (12 ESTs) and SHE treatments (6 ESTs). The majority of JH up- and downregulated ESTs were of host and symbiont origin, respectively; in contrast, SHE, LR and LS treatments had more uniform impacts on host and symbiont gene expression. Repeat “follow-up” bioassays investigating combined JH + SHE impacts in relation to individual JH and SHE treatments on a subset of array-positive genes revealed (i) JH and SHE treatments had opposite impacts on gene expression and (ii) JH + SHE impacts on gene expression were generally intermediate between JH and SHE.

Conclusions

Our results show that JH impacts hundreds of termite and symbiont genes within 24-hr, strongly suggesting a role for the termite gut in JH-dependent caste determination. Additionally, differential impacts of SHE and LS treatments were observed that are in strong agreement with previous studies that specifically investigated soldier caste regulation. However, it is likely that gene expression outside the gut may be of equal or greater importance than gut gene expression.

Keywords:
Metagenomics; Soldier head extract; Microarray; Caste differentiation; Live soldier; Live reproductive