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

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.

[1]  M. Dong,et al.  Possible role of pectin-containing mucilage and dew in repairing embryo DNA of seeds adapted to desert conditions. , 2007, Annals of botany.

[2]  Y. Touré,et al.  The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. , 1998, Parassitologia.

[3]  A. Panek,et al.  Oxidative stress and its effects during dehydration. , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[4]  L. Lyne,et al.  The requirement for DNA repair in desiccation tolerance of germinating embryos , 1997, Seed Science Research.

[5]  K. Paaijmans,et al.  Understanding the link between malaria risk and climate , 2009, Proceedings of the National Academy of Sciences.

[6]  M. Coluzzi,et al.  Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. , 1979, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[7]  Masahiko Watanabe Anhydrobiosis in invertebrates , 2006 .

[8]  K. Dietz,et al.  Age and seasonal variation in the transition rates and detectability of Plasmodium falciparum malaria , 2005, Parasitology.

[9]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[10]  W. Hawley,et al.  The effective population size of Anopheles gambiae in Kenya: implications for population structure. , 1998, Molecular biology and evolution.

[11]  A. della Torre,et al.  A Polytene Chromosome Analysis of the Anopheles gambiae Species Complex , 2002, Science.

[12]  A. James,et al.  Genome‐wide analysis of gene expression in adult Anopheles gambiae , 2006, Insect molecular biology.

[13]  J. Venn,et al.  . On the diagrammatic and mechanical representation of propositions and reasonings , 2022 .

[14]  D. Chevalier,et al.  DAWDLE, a Forkhead-Associated Domain Gene, Regulates Multiple Aspects of Plant Development1[W] , 2006, Plant Physiology.

[15]  B. Cassone,et al.  Localization of Candidate Regions Maintaining a Common Polymorphic Inversion (2La) in Anopheles gambiae , 2007, PLoS genetics.

[16]  A. James,et al.  Genome-Wide Patterns of Gene Expression during Aging in the African Malaria Vector Anopheles gambiae , 2010, PloS one.

[17]  C. Dye,et al.  World Malaria Report, 2008. , 2008 .

[18]  S. McCready,et al.  Adaptation and impairment of DNA repair function in pollen of Betula verrucosa and seeds of Oenothera biennis from differently radionuclide-contaminated sites of Chernobyl. , 2007, Annals of botany.

[19]  N. F. Hadley Wax Secretion and Color Phases of the Desert Tenebrionid Beetle Cryptoglossa verrucosa (LeConte) , 1979, Science.

[20]  A. Weeks,et al.  Chromosomal inversion polymorphisms and adaptation. , 2004, Trends in ecology & evolution.

[21]  A. Hoffmann,et al.  Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster , 2010, The FEBS journal.

[22]  N. Besansky,et al.  Inversion 2La is associated with enhanced desiccation resistance in Anopheles gambiae , 2009, Malaria Journal.

[23]  T. Theander,et al.  Chronic Plasmodium falciparum infections in an area of low intensity malaria transmission in the Sudan , 2000, Parasitology.

[24]  E. Nevo,et al.  DNA repair efficiency and thermotolerance in Drosophila melanogaster from "Evolution Canyon". , 2004, Mutagenesis.

[25]  N. Besansky,et al.  The Population Genomics of Trans-Specific Inversion Polymorphisms in Anopheles gambiae , 2009, Genetics.

[26]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[27]  H. Mwambi,et al.  Estimating Dispersal and Survival of Anopheles gambiae and Anopheles funestus Along the Kenyan Coast by Using Mark–Release–Recapture Methods , 2007, Journal of medical entomology.

[28]  Ira Vaughan Hiscock,et al.  Genetics of the Evolutionary Process , 1971, The Yale Journal of Biology and Medicine.

[29]  Pei-Yu Wu,et al.  Structure and Function of the Phosphothreonine-Specific FHA Domain , 2008, Science Signaling.

[30]  D. Denlinger,et al.  Heat shock proteins contribute to mosquito dehydration tolerance. , 2010, Journal of insect physiology.

[31]  J. Ribeiro,et al.  Population Size and Migration of Anopheles gambiae in the Bancoumana Region of Mali and Their Significance for Efficient Vector Control , 2010, PloS one.

[32]  B. Johansson,et al.  The impact of translocations and gene fusions on cancer causation , 2007, Nature Reviews Cancer.

[33]  G. Yan,et al.  A network population model of the dynamics and control of African malaria vectors. , 2010, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[34]  F. Collins,et al.  Association of two esterase genes, a chromosomal inversion, and susceptibility to Plasmodium cynomolgi in the African malaria vector Anopheles gambiae. , 1993, The American journal of tropical medicine and hygiene.

[35]  Abdelilah Arredouani,et al.  Contribution of the endoplasmic reticulum to the glucose-induced [Ca(2+)](c) response in mouse pancreatic islets. , 2002, American journal of physiology. Endocrinology and metabolism.

[36]  Peter Philippsen,et al.  Contribution of the Endoplasmic Reticulum to Peroxisome Formation , 2005, Cell.

[37]  Thomas A. Smith,et al.  The rise and fall of Anopheles arabiensis (Diptera: Culicidae) in a Tanzanian village. , 1995 .

[38]  A. James,et al.  The impact of aging on genome-wide patterns of gene expression in the African malaria vector Anopheles gambiae , 2010 .

[39]  J. Lighton Discontinuous gas exchange in insects. , 1996, Annual review of entomology.

[40]  A. Dao,et al.  Aestivation of the African Malaria Mosquito, Anopheles gambiae in the Sahel , 2010, The American journal of tropical medicine and hygiene.

[41]  M. Cáceres,et al.  Silencing of a gene adjacent to the breakpoint of a widespread Drosophila inversion by a transposon-induced antisense RNA , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  E. De Pauw,et al.  Transcriptomic and proteomic analyses of seasonal photoperiodism in the pea aphid , 2009, BMC Genomics.

[43]  I. Glazer,et al.  Expression of different desiccation-tolerance related genes in various species of entomopathogenic nematodes. , 2008, Molecular and biochemical parasitology.

[44]  J. Cloudsley-Thompson,et al.  Dry Season Biology of Anopheles gambiae Giles in the Sudan , 1968 .

[45]  H. Yoshida ER stress response, peroxisome proliferation, mitochondrial unfolded protein response and Golgi stress response , 2009, IUBMB life.

[46]  S. Goto,et al.  Peripheral circadian clock for the cuticle deposition rhythm in Drosophila melanogaster , 2008, Proceedings of the National Academy of Sciences.

[47]  D. Denlinger,et al.  Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens , 2007, Journal of Experimental Biology.

[48]  G. A. Leng ON POPULATION. , 1963, Singapore medical journal.

[49]  J. Willis,et al.  5 – Cuticular Proteins , 2012 .

[50]  A. Githeko,et al.  Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. , 2006, The American journal of tropical medicine and hygiene.

[51]  Dean P. Jones,et al.  Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. , 2006, Annual review of pharmacology and toxicology.

[52]  A. Moya,et al.  Sex versus parthenogenesis: a transcriptomic approach of photoperiod response in the model aphid Acyrthosiphon pisum (Hemiptera: Aphididae). , 2008, Gene.

[53]  Jeffrey A. Bailey,et al.  Genome Landscape and Evolutionary Plasticity of Chromosomes in Malaria Mosquitoes , 2010, PloS one.

[54]  M. Ohmori,et al.  Gene Expression in the Cyanobacterium Anabaena sp. PCC7120 under Desiccation , 2004, Microbial Ecology.

[55]  Amparo Querol,et al.  Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. , 2002, Genome research.

[56]  Paul E. Parham,et al.  Modelling climate change and malaria transmission. , 2010, Advances in experimental medicine and biology.

[57]  D. Conway,et al.  Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia , 2008, Malaria Journal.

[58]  M. Sharakhova,et al.  Arm-specific dynamics of chromosome evolution in malaria mosquitoes , 2011, BMC Evolutionary Biology.

[59]  J. Charlwood,et al.  Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. , 2000, The American journal of tropical medicine and hygiene.

[60]  B. Sabater-Muñoz,et al.  Seasonal photoperiodism regulates the expression of cuticular and signalling protein genes in the pea aphid. , 2007, Insect biochemistry and molecular biology.

[61]  T. Bradley,et al.  Physiology of desiccation resistance in Anopheles gambiae and Anopheles arabiensis. , 2005, The American journal of tropical medicine and hygiene.

[62]  L. Riddiford,et al.  Structure and expression of a Manduca sexta larval cuticle gene homologous to Drosophila cuticle genes. , 1988, Journal of molecular biology.

[63]  J. Ribeiro,et al.  AnoXcel: an Anopheles gambiae protein database , 2004, Insect molecular biology.

[64]  M. Rose,et al.  Metabolic Reserves and Evolved Stress Resistance in Drosophila melanogaster , 1998, Physiological Zoology.

[65]  J. Cloudsley-Thompson,et al.  Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. , 1970, Bulletin of the World Health Organization.

[66]  K. Paaijmans,et al.  Influence of climate on malaria transmission depends on daily temperature variation , 2010, Proceedings of the National Academy of Sciences.