Genome-Wide Transcriptional Analysis of Genes Associated with Acute Desiccation Stress in Anopheles gambiae

Abstract

Malaria transmission in sub-Saharan Africa varies seasonally in intensity. Outbreaks of malaria occur after the beginning of the rainy season, whereas, during the dry season, reports of the disease are less frequent. Anopheles gambiae mosquitoes, the main malaria vector, are observed all year long but their densities are low during the dry season that generally lasts several months. Aestivation, seasonal migration, and local adaptation have been suggested as mechanisms that enable mosquito populations to persist through the dry season. Studies of chromosomal inversions have shown that inversions 2La, 2Rb, 2Rc, 2Rd, and 2Ru are associated with various physiological changes that confer aridity resistance. However, little is known about how phenotypic plasticity responds to seasonally dry conditions. This study examined the effects of desiccation stress on transcriptional regulation in An. gambiae. We exposed female An. gambiae G3 mosquitoes to acute desiccation and conducted a genome-wide analysis of their transcriptomes using the Affymetrix Plasmodium/Anopheles Genome Array. The transcription of 248 genes (1.7% of all transcripts) was significantly affected in all experimental conditions, including 96 with increased expression and 152 with decreased expression. In general, the data indicate a reduction in the metabolic rate of mosquitoes exposed to desiccation. Transcripts accumulated at higher levels during desiccation are associated with oxygen radical detoxification, DNA repair and stress responses. The proportion of transcripts within 2La and 2Rs (2Rb, 2Rc, 2Rd, and 2Ru) (67/248, or 27%) is similar to the percentage of transcripts located within these inversions (31%). These data may be useful in efforts to elucidate the role of chromosomal inversions in aridity tolerance. The scope of application of the anopheline genome demonstrates that examining transcriptional activity in relation to genotypic adaptations greatly expands the number of candidate regions involved in the desiccation response in this important malaria vector.

Gene expression changes governing extreme dehydration tolerance in an Antarctic insect

“…In contrast, comparing our expression data with A. gambiae revealed little overlap between our dataset and the mosquito response to desiccation. Nonetheless, similar to our results, Wang et al (16) observed down-regulation of numerous metabolic genes, particularly genes related to chitin metabolism.…”

“…The transcriptomic response to dehydration has been studied in three other insects, the African sleeping midge P. vanderplanki (15), the mosquito A. gambiae (16), and the cactophilic fruit fly, D. mojavensis (17), as well as two closely related arthropods, the Arctic collembolan M. arctica (18) and the collembolan F. candida (19), thus facilitating cross-species comparisons of dehydration-induced gene expression. We observed several general similarities between our dataset and the transcriptome of P. vanderplanki, which inhabits temporary pools in tropical Africa.…”

“…To date, only three studies have examined large-scale transcriptional changes in response to dehydration in insects, all of which were conducted on tropical species. Cornette et al (15) identified genes associated with anhydrobiosis in the African sleeping midge, Polypedilum vanderplanki, using a semiquantitative EST approach, whereas Wang et al (16) and Matzkin et al (17) used microarrays to examine genome-wide transcriptional changes following dehydration in Anopheles gambiae and Drosophila mojavensis, respectively. In addition to the insect studies, transcriptional responses to desiccation have been reported for an Arctic arthropod closely related to insects, the springtail (Collembola) Megaphorura arctica (18), as well as a widely distributed collembolan, Folsomia candida (19).…”

Mechanistic underpinnings of dehydration stress in the American dog tick revealed through RNA-Seq and metabolomics

“…Dehydration can lead to changes in the regulation of transcription/translation (Rajpurohit et al, 2013;Wang et al, 2011), with some insects showing a general decrease in protein synthesis through a down-regulation of transcription-related genes (Rajpurohit et al, 2013). However, dehydrated D. variabilis showed an up-regulation of pathways associated with transcription and translation initiation (Table 2; Table S4).…”

Ecophysiology of Anopheles gambiae s.l.: Persistence in the Sahel

“…gambiae (a mix of M and S molecular forms), age-related changes in gene expression, separate from gonotrophic-cycle effects, were measured across ages up to 28 days (Wang et al, 2010). Genes which increased in expression throughout the aging process included two detoxification genes (cytochrome P450 and glutathione S-transferases) and Hsp70, a key stress-response gene (Wang et al, 2010); importantly, these classes of genes have been found in previous studies on aestivation, as mentioned above, and may implicate these genes as part of the “aestivation toolkit.” In a similar study using the G3 colony, changes in gene expression due to desiccation stress were measured, and overall, more genes showed decreased expression during desiccation than those which increased (Wang et al, 2011). Genes which were down-regulated during desiccation stress included chitin metabolism genes, oxidative-stress response genes, and binding function genes, while those which were up-regulated during desiccation stress included amino-acid biosynthesis and Hsp40 (Wang et al, 2011).…”