Abstract
SummaryThe transmission of malaria parasites to mosquitoes relies on the rapid induction of sexual reproduction upon their ingestion into a blood meal. Haploid female and male gametocytes become activated and emerge from their host cells, and the males enter the cell cycle to produce eight microgametes. The synchronized nature of gametogenesis allowed us to investigate phosphorylation signaling during its first minute in Plasmodium berghei via a high-resolution time course of the phosphoproteome. This revealed an unexpectedly broad response, with proteins related to distinct cell cycle events undergoing simultaneous phosphoregulation. We implicate several protein kinases in the process, and we validate our analyses on the plant-like calcium-dependent protein kinase 4 (CDPK4) and a homolog of serine/arginine-rich protein kinases (SRPK1). Mutants in these kinases displayed distinct phosphoproteomic disruptions, consistent with differences in their phenotypes. The results reveal the central role of protein phosphorylation in the atypical cell cycle regulation of a divergent eukaryote.
Highlights
Malaria represents a major global health concern, causing an estimated 212 million cases resulting in approximately 429,000 deaths in 2015 (World Health Organization, 2016)
Micro- and macrogametocytes respond to a small mosquito molecule, xanthurenic acid (XA), which must coincide with a drop in temperature to trigger the emergence of intraerythrocytic gametocytes and their differentiation into male microgametes and female macrogametes (Billker et al, 1997)
The time course finishes after the first minute, since this period should be sufficient to capture the key events associated with the induction of major cell cycle events in the microgametocyte
Summary
Malaria represents a major global health concern, causing an estimated 212 million cases resulting in approximately 429,000 deaths in 2015 (World Health Organization, 2016). It is caused by intracellular parasites of the genus Plasmodium, whose complex life cycles involve mosquito vectors of the genus Anopheles transmitting the parasites between vertebrate hosts. As soon as 60 s after activation, they have assembled the first mitotic spindle and four axonemes start to grow on the templates of kinetosomes at each spindle pole (Billker et al, 2002). Fertilization of the macrogametes results in the development of motile ookinetes, which escape the mosquito midgut
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