Heterogeneous ribosome populations are present in Plasmodium berghei during development in its vector

Abstract

SummaryThe genome of the rodent malaria parasite, Plasmodium berghei, contains two sets of variant ribosomal RNA (rRNA) genes, termed the A and S types, that are expressed predominantly during the vertebrate and mosquito stages of the parasite's development respectively. Using in situ hybridization, we have examined the transcriptional activity of the A-and S-type rRNA genes, and the switch in expression of the ribosome populations that occurs after parasite transmission to the mosquito. By detection of precursor rRNA molecules, we show that A-type rRNA transcription is downregulated throughout development in the mosquito, whereas the initiation of S-type rRNA transcription is linked to the proliferative phase of the oocyst. Mature A-type rRNA persists during development of the zygote into the ookinete/young oocyst. In contrast, mature S-type rRNA is first detectable in young oocysts and is subsequently present at high levels during further development of oocysts and sporozoites. These results demonstrate that the switch in transcription between the A-and S-type rRNA genes is developmentally regulated, taking place only as the parasite begins to proliferate in the mosquito. Atype ribosomes are therefore not only translationally active in the early stages of development in the mosquito, but are also crucial at this phase.

Functional Equivalence of Structurally Distinct Ribosomes in the Malaria Parasite, Plasmodium berghei

“…Based on the structural differences in the core regions of the rRNA molecules, the existence of three different ribosome types in Plasmodium has been suggested: A-type ribosomes present during development in the liver and the blood of the host and O-and S-type ribosomes present during development in the mosquito vector. It has been suggested that the maintenance of functionally different ribosome types provides Plasmodium with a unique post-transcriptional control mechanism to regulate gene expression (15,19,24). The expression of different ribosome forms could be a major step in the commitment of the parasite to a change in life cycle stage by influencing the population of messenger rRNAs (mRNAs) that are translated.…”

“…2, A and E). S-type transcription in wt parasites starts in the developing ookinete and is up-regulated during oocyst formation (14,19) (Fig. 2A).…”

“…The A-type ribosomes are present in the liver and blood stages of the parasite, and the O-and S-type ribosomes are the predominant types produced during development in the mosquito (20). The presence of structural differences among the rRNA molecules has led to the hypothesis that the different ribosome types are also functionally different (15,18,19). Two observations support this hypothesis.…”

“…parasites that are responsible for malaria. In Plasmodium, and in contrast to other apicomplexans that possess dispersed genes, these rRNA gene units are transcribed stage-specifically, thereby reducing the total number of gene units that are simultaneously active (15)(16)(17)(18)(19). Based on the differences in expression pattern and nucleotide sequence of the rRNA gene units the existence of three types of structurally different ribosomes in Plasmodium has been postulated.…”

The differential expression of ribosomal 18S RNA paralog genes from the chaetognath Spadella cephaloptera

“…Although this has yet to be experimentally verified, there is little data to evidence that the rRNA paralogs are functional genes. To date, the sole strongest and most conclusive evidence of the functionality of the rRNA paralogs has been shown in some species of the protist Plasmodium, where at least two different types of 18S rDNA exist, with their expression linked to different stages of the parasitic life cycle of these organisms [19,20]. These last results provide support for the idea that some of the variants are not pseudogenes and are important for proper cellular function.…”