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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| creator | Rios, Kelly T McGee, James P Sebastian, Aswathy Gedara, Sanjaya Aththawala Moritz, Robert L Feric, Marina Absalon, Sabrina Swearingen, Kristian E Lindner, Scott E |
| 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. |
| doi_str_mv | 10.1371/journal.ppat.1012823 |
| format | Article |
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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.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1012823</identifier><identifier>PMID: 39777415</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Anopheles - parasitology ; Biology and Life Sciences ; Disease transmission ; Embryonic development ; Female ; Genetic aspects ; Health aspects ; Host-Parasite Interactions - physiology ; Malaria ; Malaria - parasitology ; Malaria - transmission ; Messenger RNA ; Mice ; Microbiological research ; Mosquito Vectors - parasitology ; Mosquitoes ; Physiological aspects ; Plasmodium falciparum ; Plasmodium yoelii - metabolism ; Protein Biosynthesis ; Proteins ; Proteomics - methods ; Protozoan Proteins - genetics ; Protozoan Proteins - metabolism ; Research and Analysis Methods</subject><ispartof>PLoS pathogens, 2025-01, Vol.21 (1), p.e1012823</ispartof><rights>Copyright: © 2025 Rios et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2025 Public Library of Science</rights><rights>2025 Rios et al 2025 Rios et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c416t-4d08d69c1669a73508e519e2d9795aeda2f622493a1e6ef46d290f1f8072dfaf3</cites><orcidid>0000-0003-1799-3726</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11750109/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11750109/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39777415$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rios, Kelly T</creatorcontrib><creatorcontrib>McGee, James P</creatorcontrib><creatorcontrib>Sebastian, Aswathy</creatorcontrib><creatorcontrib>Gedara, Sanjaya Aththawala</creatorcontrib><creatorcontrib>Moritz, Robert L</creatorcontrib><creatorcontrib>Feric, Marina</creatorcontrib><creatorcontrib>Absalon, Sabrina</creatorcontrib><creatorcontrib>Swearingen, Kristian E</creatorcontrib><creatorcontrib>Lindner, Scott E</creatorcontrib><title>Widespread release of translational repression across Plasmodium's host-to-vector transmission event</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><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.</description><subject>Animals</subject><subject>Anopheles - parasitology</subject><subject>Biology and Life Sciences</subject><subject>Disease transmission</subject><subject>Embryonic development</subject><subject>Female</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Host-Parasite Interactions - physiology</subject><subject>Malaria</subject><subject>Malaria - parasitology</subject><subject>Malaria - transmission</subject><subject>Messenger RNA</subject><subject>Mice</subject><subject>Microbiological research</subject><subject>Mosquito Vectors - parasitology</subject><subject>Mosquitoes</subject><subject>Physiological aspects</subject><subject>Plasmodium falciparum</subject><subject>Plasmodium yoelii - metabolism</subject><subject>Protein Biosynthesis</subject><subject>Proteins</subject><subject>Proteomics - methods</subject><subject>Protozoan Proteins - genetics</subject><subject>Protozoan Proteins - metabolism</subject><subject>Research and Analysis Methods</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNpVkttu1DAQhiMEoqXwBghF4gK4yOKJT8kVqioOK1UCcRCX1mw83maVjbe2s4K3x9ssVffKh_nmnxn7L4qXwBbANbzf-CmMOCx2O0wLYFA3NX9UnIOUvNJci8cP9mfFsxg3jAngoJ4WZ7zVWguQ54X93VuKu0Boy0ADYaTSuzIFHOOAqfe5RA5kIMZ8KLELPsby24Bx620_bd_E8sbHVCVf7alLPsy5237maU9jel48cThEenFcL4pfnz7-vPpSXX_9vLy6vK46ASpVwrLGqrYDpVrUXLKGJLRU21a3Esli7VRdi5YjkCInlK1b5sA1TNfWoeMXxXLWtR43Zhf6LYa_xmNv7i58WBsMqe8GMlmdicZJ7CQIWOlVawWhY3wlwKoVZa0Ps9ZuWm3JdnmMgMOJ6Glk7G_M2u8NgJYMWJsV3h4Vgr-dKCaTH6WjYcCR_BQNB8mbJlcXGX09o2vMvfWj81myO-DmsqkV6FpLlal3J1Tnx0R_0hqnGM3yx_dTVszs3X8FcvedAzMH_5ijf8zBP-bon5z26uHU90n_DcP_AcAWxg8</recordid><startdate>20250108</startdate><enddate>20250108</enddate><creator>Rios, Kelly T</creator><creator>McGee, James P</creator><creator>Sebastian, Aswathy</creator><creator>Gedara, Sanjaya Aththawala</creator><creator>Moritz, Robert L</creator><creator>Feric, Marina</creator><creator>Absalon, Sabrina</creator><creator>Swearingen, Kristian E</creator><creator>Lindner, Scott E</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-1799-3726</orcidid></search><sort><creationdate>20250108</creationdate><title>Widespread release of translational repression across Plasmodium's host-to-vector transmission event</title><author>Rios, Kelly T ; McGee, James P ; Sebastian, Aswathy ; Gedara, Sanjaya Aththawala ; Moritz, Robert L ; Feric, Marina ; Absalon, Sabrina ; Swearingen, Kristian E ; Lindner, Scott E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c416t-4d08d69c1669a73508e519e2d9795aeda2f622493a1e6ef46d290f1f8072dfaf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>Animals</topic><topic>Anopheles - parasitology</topic><topic>Biology and Life Sciences</topic><topic>Disease transmission</topic><topic>Embryonic development</topic><topic>Female</topic><topic>Genetic aspects</topic><topic>Health aspects</topic><topic>Host-Parasite Interactions - physiology</topic><topic>Malaria</topic><topic>Malaria - parasitology</topic><topic>Malaria - transmission</topic><topic>Messenger RNA</topic><topic>Mice</topic><topic>Microbiological research</topic><topic>Mosquito Vectors - parasitology</topic><topic>Mosquitoes</topic><topic>Physiological aspects</topic><topic>Plasmodium falciparum</topic><topic>Plasmodium yoelii - metabolism</topic><topic>Protein Biosynthesis</topic><topic>Proteins</topic><topic>Proteomics - methods</topic><topic>Protozoan Proteins - genetics</topic><topic>Protozoan Proteins - metabolism</topic><topic>Research and Analysis Methods</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rios, Kelly T</creatorcontrib><creatorcontrib>McGee, James P</creatorcontrib><creatorcontrib>Sebastian, Aswathy</creatorcontrib><creatorcontrib>Gedara, Sanjaya Aththawala</creatorcontrib><creatorcontrib>Moritz, Robert L</creatorcontrib><creatorcontrib>Feric, Marina</creatorcontrib><creatorcontrib>Absalon, Sabrina</creatorcontrib><creatorcontrib>Swearingen, Kristian E</creatorcontrib><creatorcontrib>Lindner, Scott E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rios, Kelly T</au><au>McGee, James P</au><au>Sebastian, Aswathy</au><au>Gedara, Sanjaya Aththawala</au><au>Moritz, Robert L</au><au>Feric, Marina</au><au>Absalon, Sabrina</au><au>Swearingen, Kristian E</au><au>Lindner, Scott E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Widespread release of translational repression across Plasmodium's host-to-vector transmission event</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2025-01-08</date><risdate>2025</risdate><volume>21</volume><issue>1</issue><spage>e1012823</spage><pages>e1012823-</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39777415</pmid><doi>10.1371/journal.ppat.1012823</doi><tpages>e1012823</tpages><orcidid>https://orcid.org/0000-0003-1799-3726</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Anopheles - parasitology Biology and Life Sciences Disease transmission Embryonic development Female Genetic aspects Health aspects Host-Parasite Interactions - physiology Malaria Malaria - parasitology Malaria - transmission Messenger RNA Mice Microbiological research Mosquito Vectors - parasitology Mosquitoes Physiological aspects Plasmodium falciparum Plasmodium yoelii - metabolism Protein Biosynthesis Proteins Proteomics - methods Protozoan Proteins - genetics Protozoan Proteins - metabolism Research and Analysis Methods |
| title | Widespread release of translational repression across Plasmodium's host-to-vector transmission event |
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