Regulation of Gene Expression Patterns in Mosquito Reproduction.
In multicellular organisms, development, growth and reproduction require coordinated expression of numerous functional and regulatory genes. Insects, in addition to being the most speciose animal group with enormous biological and economical significance, represent outstanding model organisms for studying regulation of synchronized gene expression due to their rapid development and reproduction. Disease-transmitting female mosquitoes have adapted uniquely for ingestion and utilization of the huge blood meal required for swift reproductive events to complete egg development within a 72-h period. We investigated the network of regulatory factors mediating sequential gene expression in the fat body, a multifunctional organ analogous to the vertebrate liver and adipose tissue, of the female Aedes aegypti mosquito. Transcriptomic and bioinformatics analyses revealed that ~7500 transcripts are differentially expressed in four sequential waves during the 72-h reproductive period. A combination of RNA-interference gene-silencing and in-vitro organ culture identified the major regulators for each of these waves. Amino acids (AAs) regulate the first wave of gene activation between 3 h and 12 h post-blood meal (PBM). During the second wave, between 12 h and 36 h, most genes are highly upregulated by a synergistic action of AAs, 20-hydroxyecdysone (20E) and the Ecdysone-Receptor (EcR). Between 36 h and 48 h, the third wave of gene activation-regulated mainly by HR3-occurs. Juvenile Hormone (JH) and its receptor Methoprene-Tolerant (Met) are major regulators for the final wave between 48 h and 72 h. Each of these key regulators also has repressive effects on one or more gene sets. Our study provides a better understanding of the complexity of the regulatory mechanisms related to temporal coordination of gene expression during reproduction. We have detected the novel function of 20E/EcR responsible for transcriptional repression. This study also reveals the previously unidentified large-scale effects of HR3 and JH/Met on transcriptional regulation during the termination of vitellogenesis and remodeling of the fat body.
Department of Entomology, University of California, Riverside, Riverside, California, United States of America; Institute of Integrative Genome Biology, University of California, Riverside, Riverside, California, United States of America.
Sourav
S
Roy
Department of Entomology, University of California, Riverside, Riverside, California, United States of America; Institute of Integrative Genome Biology, University of California, Riverside, Riverside, California, United States of America.
Tusar T
TT
Saha
Department of Entomology, University of California, Riverside, Riverside, California, United States of America; Institute of Integrative Genome Biology, University of California, Riverside, Riverside, California, United States of America; Graduate Program in Cell, Molecular and Developmental Biology, University of California, Riverside, Riverside, California, United States of America.
Lisa
L
Johnson
Department of Entomology, University of California, Riverside, Riverside, California, United States of America; Institute of Integrative Genome Biology, University of California, Riverside, Riverside, California, United States of America.
Bo
B
Zhao
Department of Entomology, University of California, Riverside, Riverside, California, United States of America; Institute of Integrative Genome Biology, University of California, Riverside, Riverside, California, United States of America; Graduate Program in Genetics, Genomics and Bioinformatics, University of California, Riverside, Riverside, California, United States of America.
Jisu
J
Ha
Institute for Genomics and Systems Biology, University of Chicago, Chicago, Illinois, United States of America.
Kevin P
KP
White
Institute of Integrative Genome Biology, University of California, Riverside, Riverside, California, United States of America; Department of Botany and Plant Sciences, University of California, Riverside, Riverside, California, United States of America.
Thomas
T
Girke
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
Zhen
Z
Zou
Department of Entomology, University of California, Riverside, Riverside, California, United States of America; Institute of Integrative Genome Biology, University of California, Riverside, Riverside, California, United States of America.
Alexander S
AS
Raikhel
D000330:Aedes / Q000235:genetics* / Q000378:metabolism; D000596:Amino Acids / Q000502:physiology; D000818:Animals; D004441:Ecdysterone / Q000502:physiology; D005216:Fat Body / Q000378:metabolism; D005260:Female; D005786:Gene Expression Regulation; D017344:Genes, Insect; D019476:Insect Proteins / Q000235:genetics / Q000378:metabolism; D007605:Juvenile Hormones / Q000502:physiology; D019518:Postprandial Period; D011987:Receptors, Steroid / Q000502:physiology; D012098:Reproduction; D059467:Transcriptome
D000596:Amino Acids; D019476:Insect Proteins; D007605:Juvenile Hormones; D011987:Receptors, Steroid; C055469:ecdysone receptor; D004441:Ecdysterone