Abstract
Stage-specific transcription is a fundamental biological process in the life cycle of the Plasmodium parasite. Proteins containing the AP2 DNA-binding domain are responsible for stage-specific transcriptional regulation and belong to the only known family of transcription factors in Plasmodium parasites. Comprehensive identification of their target genes will advance our understanding of the molecular basis of stage-specific transcriptional regulation and stage-specific parasite development. AP2-O is an AP2 family transcription factor that is expressed in the mosquito midgut-invading stage, called the ookinete, and is essential for normal morphogenesis of this stage. In this study, we identified the genome-wide target genes of AP2-O by chromatin immunoprecipitation-sequencing and elucidate how this AP2 family transcription factor contributes to the formation of this motile stage. The analysis revealed that AP2-O binds specifically to the upstream genomic regions of more than 500 genes, suggesting that approximately 10% of the parasite genome is directly regulated by AP2-O. These genes are involved in distinct biological processes such as morphogenesis, locomotion, midgut penetration, protection against mosquito immunity and preparation for subsequent oocyst development. This direct and global regulation by AP2-O provides a model for gene regulation in Plasmodium parasites and may explain how these parasites manage to control their complex life cycle using a small number of sequence-specific AP2 transcription factors.
Highlights
Malarial parasites require two host animals during their life cycle and undergo multiple developmental changes in each host
Our previous study suggested that stage-specific AP2 family transcription factors have critical roles in maintaining the Plasmodium parasite life cycle
AP2-O is an AP2 family transcription factor that is expressed during the mosquito midgut-invading stage, the ookinete, and is essential for normal development of this stage
Summary
Malarial parasites require two host animals during their life cycle and undergo multiple developmental changes in each host. According to these changes in the life cycle, parasites remarkably alter their repertoire of gene expression [1]. The total number of sequence-specific transcription factors is exceptionally small compared with that in other eukaryotic organisms [4,5,6], suggesting that malaria parasites have a unique gene regulation system. Previous studies by us and other groups suggest that AP2-family transcription factors are involved in stage-specific gene regulation and are essential for normal development of the stages in which they are expressed [7,8,9,10,11]. Only partial information has been obtained about their target genes; it remains elusive how these transcription factors contribute to the development of each stage
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