{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T02:42:23Z","timestamp":1780368143915,"version":"3.54.1"},"reference-count":82,"publisher":"Wiley","issue":"1","license":[{"start":{"date-parts":[[2020,11,23]],"date-time":"2020-11-23T00:00:00Z","timestamp":1606089600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Biology of the Cell"],"published-print":{"date-parts":[[2021,1]]},"abstract":"<jats:sec>\n                    <jats:title>Background Information<\/jats:title>\n                    <jats:p>\n                      Like other apicomplexan parasites,\n                      <jats:italic>Toxoplasma gondii<\/jats:italic>\n                      harbours a four\u2010membraned endosymbiotic organelle\u00a0\u2013 the apicoplast. Apicoplast proteins are nuclear encoded and trafficked to the organelle through the endoplasmic reticulum (ER). From the ER to the apicoplast, two distinct protein trafficking pathways can be used. One such pathway is the cell's secretory pathway involving the Golgi, whereas the other is a unique Golgi\u2010independent pathway. Using different experimental approaches, many apicoplast proteins have been shown to utilize the Golgi\u2010independent pathway, whereas a handful of reports show that a few proteins use the Golgi\u2010dependent pathway. This has led to an emphasis towards the unique Golgi\u2010independent pathway when apicoplast protein trafficking is discussed in the literature. Additionally, the molecular features that drive proteins to each pathway are not known.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      In this report, we systematically test eight apicoplast proteins, using a C\u2010terminal HDEL sequence to assess the role of the Golgi in their transport. We demonstrate that dually localised proteins of the apicoplast and mitochondrion (\n                      <jats:italic>Tg<\/jats:italic>\n                      SOD2,\n                      <jats:italic>Tg<\/jats:italic>\n                      TPx1\/2 and\n                      <jats:italic>Tg<\/jats:italic>\n                      ACN\/IRP) are trafficked through the Golgi, whereas proteins localised exclusively to the apicoplast are trafficked independent of the Golgi. Mutants of the dually localised proteins that localised exclusively to the apicoplast also showed trafficking through the Golgi. Phylogenetic analysis of\n                      <jats:italic>Tg<\/jats:italic>\n                      SOD2,\n                      <jats:italic>Tg<\/jats:italic>\n                      TPx1\/2 and\n                      <jats:italic>Tg<\/jats:italic>\n                      ACN\/IRP suggested that the evolutionary origins of\n                      <jats:italic>Tg<\/jats:italic>\n                      SOD2 and\n                      <jats:italic>Tg<\/jats:italic>\n                      TPx1\/2 lie in the mitochondrion, whereas\n                      <jats:italic>Tg<\/jats:italic>\n                      ACN\/IRP appears to have originated from the apicoplast.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions and Significance<\/jats:title>\n                    <jats:p>Collectively, with these results, for the first time, we establish that the driver of the Golgi\u2010dependent trafficking route to the apicoplast is the dual localisation of the protein to the apicoplast and the mitochondrion.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1111\/boc.202000050","type":"journal-article","created":{"date-parts":[[2020,10,28]],"date-time":"2020-10-28T12:06:43Z","timestamp":1603886803000},"page":"58-78","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Dually localised proteins found in both the apicoplast and mitochondrion utilize the Golgi\u2010dependent pathway for apicoplast targeting in\n                    <i>Toxoplasma gondii<\/i>"],"prefix":"10.1111","volume":"113","author":[{"given":"Aparna","family":"Prasad","sequence":"first","affiliation":[{"name":"Department of Biosciences &amp; Bioengineering Indian Institute of Technology Bombay, Powai  Mumbai 400076 India"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pragati","family":"Mastud","sequence":"additional","affiliation":[{"name":"Department of Biosciences &amp; Bioengineering Indian Institute of Technology Bombay, Powai  Mumbai 400076 India"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7633-657X","authenticated-orcid":false,"given":"Swati","family":"Patankar","sequence":"additional","affiliation":[{"name":"Department of Biosciences &amp; Bioengineering Indian Institute of Technology Bombay, Powai  Mumbai 400076 India"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2020,11,23]]},"reference":[{"key":"e_1_2_10_2_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00425-007-0647-3"},{"key":"e_1_2_10_3_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M109.044024"},{"key":"e_1_2_10_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-2836(05)80360-2"},{"key":"e_1_2_10_5_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2002.1193"},{"key":"e_1_2_10_6_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(94)90138-4"},{"key":"e_1_2_10_7_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2004.05.028"},{"key":"e_1_2_10_8_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00267462"},{"key":"e_1_2_10_9_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1006836"},{"key":"e_1_2_10_10_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1550-7408.1999.tb04615.x"},{"key":"e_1_2_10_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2009.12.002"},{"key":"e_1_2_10_12_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.00750"},{"key":"e_1_2_10_13_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkl124"},{"key":"e_1_2_10_14_1","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.3128"},{"key":"e_1_2_10_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1742-4658.2012.08746.x"},{"key":"e_1_2_10_16_1","doi-asserted-by":"publisher","DOI":"10.1023\/B:PLAN.0000006939.87660.4f"},{"key":"e_1_2_10_17_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2014.00473"},{"key":"e_1_2_10_18_1","doi-asserted-by":"publisher","DOI":"10.1128\/EC.00081-08"},{"key":"e_1_2_10_19_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.01627"},{"issue":"22","key":"e_1_2_10_20_1","doi-asserted-by":"crossref","first-page":"3969","DOI":"10.1242\/jcs.113.22.3969","article-title":"Analysis of targeting sequences demonstrates that trafficking to the Toxoplasma gondii plastid branches off the secretory system","volume":"113","author":"DeRocher A.","year":"2000","journal-title":"J. Cell Sci."},{"key":"e_1_2_10_21_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0803862105"},{"key":"e_1_2_10_22_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M116.725069"},{"key":"e_1_2_10_23_1","doi-asserted-by":"publisher","DOI":"10.1128\/MR.50.2.166-178.1986"},{"key":"e_1_2_10_24_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6941.2006.00060.x"},{"key":"e_1_2_10_25_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a003818"},{"key":"e_1_2_10_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.1985.tb00420.x"},{"key":"e_1_2_10_27_1","doi-asserted-by":"publisher","DOI":"10.1128\/EC.4.4.814-826.2005"},{"key":"e_1_2_10_28_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1076003"},{"key":"e_1_2_10_29_1","doi-asserted-by":"publisher","DOI":"10.1091\/mbc.e03-02-0101"},{"key":"e_1_2_10_30_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M112.405100"},{"key":"e_1_2_10_31_1","first-page":"1","article-title":"Has the endosymbiont hypothesis been proven?","volume":"46","author":"Gray M.W.","year":"1982","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"e_1_2_10_32_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.112.16.2631"},{"key":"e_1_2_10_33_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msg195"},{"key":"e_1_2_10_34_1","doi-asserted-by":"publisher","DOI":"10.1016\/0304-4157(84)90004-2"},{"key":"e_1_2_10_35_1","doi-asserted-by":"publisher","DOI":"10.1111\/tra.12226"},{"key":"e_1_2_10_36_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-642-60885-8_7"},{"key":"e_1_2_10_37_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/8.3.275"},{"key":"e_1_2_10_38_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.272.50.31801"},{"key":"e_1_2_10_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0854.2007.00637.x"},{"key":"e_1_2_10_40_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2007.05619.x"},{"key":"e_1_2_10_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molbiopara.2009.03.004"},{"key":"e_1_2_10_42_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.275.5305.1485"},{"key":"e_1_2_10_43_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.139.7.1677"},{"key":"e_1_2_10_44_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msy096"},{"key":"e_1_2_10_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/0166-6851(92)90187-O"},{"key":"e_1_2_10_46_1","doi-asserted-by":"publisher","DOI":"10.1186\/1475-2875-12-25"},{"key":"e_1_2_10_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(90)90699-F"},{"key":"e_1_2_10_48_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-arplant-042809-112222"},{"key":"e_1_2_10_49_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.134.2.315"},{"key":"e_1_2_10_50_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2009.0252"},{"key":"e_1_2_10_51_1","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.7215"},{"key":"e_1_2_10_52_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1550-7408.1999.tb04613.x"},{"key":"e_1_2_10_53_1","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2000-1-4-reviews1026"},{"key":"e_1_2_10_54_1","doi-asserted-by":"publisher","DOI":"10.1038\/381482a0"},{"key":"e_1_2_10_55_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(87)90086-9"},{"key":"e_1_2_10_56_1","doi-asserted-by":"publisher","DOI":"10.1002\/2211-5463.12527"},{"key":"e_1_2_10_57_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.277.5325.556"},{"key":"e_1_2_10_58_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(86)90734-8"},{"key":"e_1_2_10_59_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.6.1.93"},{"key":"e_1_2_10_60_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1467-7652.2006.00200.x"},{"key":"e_1_2_10_61_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0030115"},{"key":"e_1_2_10_62_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.genet.41.110306.130134"},{"key":"e_1_2_10_63_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0168-9525(03)00137-9"},{"key":"e_1_2_10_64_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.gene.2004.01.008"},{"key":"e_1_2_10_65_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.2006128"},{"key":"e_1_2_10_66_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.273.4.2467"},{"key":"e_1_2_10_67_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(90)90698-E"},{"key":"e_1_2_10_68_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1002392"},{"key":"e_1_2_10_69_1","doi-asserted-by":"publisher","DOI":"10.1111\/tra.12333"},{"key":"e_1_2_10_70_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molbiopara.2004.05.005"},{"key":"e_1_2_10_71_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.81.2.493"},{"key":"e_1_2_10_72_1","doi-asserted-by":"publisher","DOI":"10.1016\/B978-012369542-0\/50017-9"},{"key":"e_1_2_10_73_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0854.2009.00954.x"},{"key":"e_1_2_10_74_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0707827105"},{"key":"e_1_2_10_75_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molbiopara.2006.08.001"},{"key":"e_1_2_10_76_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2006.05244.x"},{"key":"e_1_2_10_77_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-6851(00)00324-8"},{"key":"e_1_2_10_78_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-9822(03)00239-2"},{"key":"e_1_2_10_79_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gky1049"},{"key":"e_1_2_10_80_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.21.12352"},{"key":"e_1_2_10_81_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.21.12352"},{"key":"e_1_2_10_82_1","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/19.8.1794"},{"key":"e_1_2_10_83_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.82.13.4443"}],"container-title":["Biology of the Cell"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/boc.202000050","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/boc.202000050","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/boc.202000050","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,3]],"date-time":"2023-09-03T05:33:49Z","timestamp":1693719229000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/boc.202000050"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,11,23]]},"references-count":82,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,1]]}},"alternative-id":["10.1111\/boc.202000050"],"URL":"https:\/\/doi.org\/10.1111\/boc.202000050","archive":["Portico"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.03.25.007476","asserted-by":"object"}]},"ISSN":["0248-4900","1768-322X"],"issn-type":[{"value":"0248-4900","type":"print"},{"value":"1768-322X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,23]]},"assertion":[{"value":"2020-04-13","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-10-07","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-11-23","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}