Widespread release of translational repression across Plasmodium's host-to-vector transmission event.

Malaria parasites must respond quickly to environmental changes, including during their transmission between mammalian and mosquito hosts. Therefore, female gametocytes proactively produce and translationally repress mRNAs that encode essential proteins that the zygote requires to establish a new in...

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Main Authors: Kelly T Rios, James P McGee, Aswathy Sebastian, Sanjaya Aththawala Gedara, Robert L Moritz, Marina Feric, Sabrina Absalon, Kristian E Swearingen, Scott E Lindner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1012823
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author Kelly T Rios
James P McGee
Aswathy Sebastian
Sanjaya Aththawala Gedara
Robert L Moritz
Marina Feric
Sabrina Absalon
Kristian E Swearingen
Scott E Lindner
author_facet Kelly T Rios
James P McGee
Aswathy Sebastian
Sanjaya Aththawala Gedara
Robert L Moritz
Marina Feric
Sabrina Absalon
Kristian E Swearingen
Scott E Lindner
author_sort Kelly T Rios
collection DOAJ
description Malaria parasites must respond quickly to environmental changes, including during their transmission between mammalian and mosquito hosts. Therefore, female gametocytes proactively produce and translationally repress mRNAs that encode essential proteins that the zygote requires to establish a new infection. While the release of translational repression of individual mRNAs has been documented, the details of the global release of translational repression have not. Moreover, changes in the spatial arrangement and composition of the DOZI/CITH/ALBA complex that contribute to translational control are also not known. Therefore, we have conducted the first quantitative, comparative transcriptomics and DIA-MS proteomics of Plasmodium parasites across the host-to-vector transmission event to document the global release of translational repression. Using female gametocytes and zygotes of P. yoelii, we found that ~200 transcripts are released for translation soon after fertilization, including those encoding essential functions. Moreover, we identified that many transcripts remain repressed beyond this point. TurboID-based proximity proteomics of the DOZI/CITH/ALBA regulatory complex revealed substantial spatial and/or compositional changes across this transmission event, which are consistent with recent, paradigm-shifting models of translational control. Together, these data provide a model for the essential translational control mechanisms that promote Plasmodium's efficient transmission from mammalian host to mosquito vector.
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spelling doaj-art-350048f5ac5141b7b9d4eaf03b41d6be2025-02-05T05:30:50ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-01-01211e101282310.1371/journal.ppat.1012823Widespread release of translational repression across Plasmodium's host-to-vector transmission event.Kelly T RiosJames P McGeeAswathy SebastianSanjaya Aththawala GedaraRobert L MoritzMarina FericSabrina AbsalonKristian E SwearingenScott E LindnerMalaria parasites must respond quickly to environmental changes, including during their transmission between mammalian and mosquito hosts. Therefore, female gametocytes proactively produce and translationally repress mRNAs that encode essential proteins that the zygote requires to establish a new infection. While the release of translational repression of individual mRNAs has been documented, the details of the global release of translational repression have not. Moreover, changes in the spatial arrangement and composition of the DOZI/CITH/ALBA complex that contribute to translational control are also not known. Therefore, we have conducted the first quantitative, comparative transcriptomics and DIA-MS proteomics of Plasmodium parasites across the host-to-vector transmission event to document the global release of translational repression. Using female gametocytes and zygotes of P. yoelii, we found that ~200 transcripts are released for translation soon after fertilization, including those encoding essential functions. Moreover, we identified that many transcripts remain repressed beyond this point. TurboID-based proximity proteomics of the DOZI/CITH/ALBA regulatory complex revealed substantial spatial and/or compositional changes across this transmission event, which are consistent with recent, paradigm-shifting models of translational control. Together, these data provide a model for the essential translational control mechanisms that promote Plasmodium's efficient transmission from mammalian host to mosquito vector.https://doi.org/10.1371/journal.ppat.1012823
spellingShingle Kelly T Rios
James P McGee
Aswathy Sebastian
Sanjaya Aththawala Gedara
Robert L Moritz
Marina Feric
Sabrina Absalon
Kristian E Swearingen
Scott E Lindner
Widespread release of translational repression across Plasmodium's host-to-vector transmission event.
PLoS Pathogens
title Widespread release of translational repression across Plasmodium's host-to-vector transmission event.
title_full Widespread release of translational repression across Plasmodium's host-to-vector transmission event.
title_fullStr Widespread release of translational repression across Plasmodium's host-to-vector transmission event.
title_full_unstemmed Widespread release of translational repression across Plasmodium's host-to-vector transmission event.
title_short Widespread release of translational repression across Plasmodium's host-to-vector transmission event.
title_sort widespread release of translational repression across plasmodium s host to vector transmission event
url https://doi.org/10.1371/journal.ppat.1012823
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