{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T17:49:56Z","timestamp":1791308996680,"version":"4.3.1"},"reference-count":30,"publisher":"National Academy of Sciences","issue":"19","content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2002,9,17]]},"abstract":"<jats:p>\n                    The view that parasites can develop cooperative symbiotic relationships with their hosts is both appealing and widely held; however, there is no molecular genetic evidence of such a transition. Here we demonstrate that a mutualistic bacterial endosymbiont of grain weevils maintains and expresses\n                    <jats:italic>inv<\/jats:italic>\n                    \/\n                    <jats:italic>spa<\/jats:italic>\n                    genes encoding a type III secretion system homologous to that used for invasion by bacterial pathogens. Phylogenetic analyses indicate that\n                    <jats:italic>inv<\/jats:italic>\n                    \/\n                    <jats:italic>spa<\/jats:italic>\n                    genes were present in presymbiotic ancestors of the weevil endosymbionts, occurring at least 50 million years ago. The function of\n                    <jats:italic>inv\/spa<\/jats:italic>\n                    genes in maintaining symbiosis is demonstrated by the up-regulation of their expression under both\n                    <jats:italic>in vivo<\/jats:italic>\n                    and\n                    <jats:italic>in vitro<\/jats:italic>\n                    conditions that coincide with host cell invasion.\n                  <\/jats:p>","DOI":"10.1073\/pnas.182213299","type":"journal-article","created":{"date-parts":[[2002,9,17]],"date-time":"2002-09-17T12:40:55Z","timestamp":1032266455000},"page":"12397-12402","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":172,"title":["Type III secretion systems and the evolution of mutualistic endosymbiosis"],"prefix":"10.1073","volume":"99","author":[{"given":"Colin","family":"Dale","sequence":"first","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, Center for Insect Science, and Department of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, AZ 85721"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gordon R.","family":"Plague","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, Center for Insect Science, and Department of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, AZ 85721"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ben","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, Center for Insect Science, and Department of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, AZ 85721"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Howard","family":"Ochman","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, Center for Insect Science, and Department of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, AZ 85721"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nancy A.","family":"Moran","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, Center for Insect Science, and Department of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, AZ 85721"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2002,9,4]]},"reference":[{"key":"e_1_3_3_1_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.284.5418.1322"},{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1128\/MMBR.62.2.379-433.1998"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.98.4.1883"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1099\/00207713-49-1-267"},{"key":"e_1_3_3_5_2","unstructured":"Buchner P. 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