{"id":"https://openalex.org/W2160290482","doi":"https://doi.org/10.1098/rstb.2009.0253","title":"Indirect development, transdifferentiation and the macroregulatory evolution of metazoans","display_name":"Indirect development, transdifferentiation and the macroregulatory evolution of metazoans","publication_year":2010,"publication_date":"2010-01-18","ids":{"openalex":"https://openalex.org/W2160290482","doi":"https://doi.org/10.1098/rstb.2009.0253","mag":"2160290482","pmid":"https://pubmed.ncbi.nlm.nih.gov/20083640","pmcid":"https://www.ncbi.nlm.nih.gov/pmc/articles/2817142"},"language":"en","primary_location":{"id":"doi:10.1098/rstb.2009.0253","doi":"https://doi.org/10.1098/rstb.2009.0253","is_oa":false,"landing_page_url":"https://doi.org/10.1098/rstb.2009.0253","pdf_url":null,"source":{"id":"https://openalex.org/S91660768","display_name":"Philosophical Transactions of the Royal Society B Biological Sciences","issn_l":"0962-8436","issn":["0962-8436","1471-2970"],"is_oa":false,"is_in_doaj":false,"is_core":true,"listed_in":["anvur-class-a","anvur-scientific","cwts-core","dongbi-d","jufo-2","ki-jl-2","medline","norway-2","poland-140","russia-white-list-1","vabb-shw"],"host_organization":"https://openalex.org/P4310319787","host_organization_name":"Royal Society","host_organization_lineage":["https://openalex.org/P4310319787"],"host_organization_lineage_names":["Royal Society"],"type":"journal"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Philosophical Transactions of the Royal Society B: Biological Sciences","raw_type":"journal-article"},"volume":null,"type":"review","indexed_in":["crossref","pubmed"],"open_access":{"is_oa":true,"oa_status":"green","oa_url":"https://www.ncbi.nlm.nih.gov/pmc/articles/2817142","any_repository_has_fulltext":true},"authorships":[{"author_position":"first","author":{"id":"https://openalex.org/A5082379936","display_name":"C\u00e9sar Arenas\u2010Mena","orcid":"https://orcid.org/0009-0005-6617-2563","observed_orcids":["https://orcid.org/0009-0005-6617-2563"]},"institutions":[{"id":"https://openalex.org/I26538001","display_name":"San Diego State University","ror":"https://ror.org/0264fdx42","country_code":"US","type":"education","lineage":["https://openalex.org/I26538001"]}],"countries":["US"],"is_corresponding":true,"raw_author_name":"Cesar Arenas-Mena","raw_affiliation_strings":["Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182-4614, USA"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182-4614, USA","institution_ids":["https://openalex.org/I26538001"]}]}],"institutions":[],"countries_distinct_count":1,"institutions_distinct_count":1,"corresponding_author_ids":["https://openalex.org/A5082379936"],"corresponding_institution_ids":["https://openalex.org/I26538001"],"apc_list":null,"apc_paid":null,"fwci":0.2543,"has_fulltext":false,"cited_by_count":56,"citation_normalized_percentile":{"value":0.21082761,"is_in_top_1_percent":false,"is_in_top_10_percent":false},"cited_by_percentile_year":{"min":89,"max":99},"biblio":{"volume":"365","issue":"1540","first_page":"653","last_page":"669"},"is_retracted":false,"is_paratext":false,"is_xpac":false,"primary_topic":{"id":"https://openalex.org/T10268","display_name":"Developmental Biology and Gene Regulation","score":0.8862000107765198,"subfield":{"id":"https://openalex.org/subfields/1312","display_name":"Molecular Biology"},"field":{"id":"https://openalex.org/fields/13","display_name":"Biochemistry, Genetics and Molecular Biology"},"domain":{"id":"https://openalex.org/domains/1","display_name":"Life Sciences"}},"topics":[{"id":"https://openalex.org/T10268","display_name":"Developmental Biology and Gene Regulation","score":0.8862000107765198,"subfield":{"id":"https://openalex.org/subfields/1312","display_name":"Molecular Biology"},"field":{"id":"https://openalex.org/fields/13","display_name":"Biochemistry, Genetics and Molecular Biology"},"domain":{"id":"https://openalex.org/domains/1","display_name":"Life Sciences"}},{"id":"https://openalex.org/T12142","display_name":"Marine Invertebrate Physiology and Ecology","score":0.10840000212192535,"subfield":{"id":"https://openalex.org/subfields/1911","display_name":"Paleontology"},"field":{"id":"https://openalex.org/fields/19","display_name":"Earth and Planetary Sciences"},"domain":{"id":"https://openalex.org/domains/3","display_name":"Physical Sciences"}},{"id":"https://openalex.org/T12789","display_name":"Planarian Biology and Electrostimulation","score":0.0015999999595806003,"subfield":{"id":"https://openalex.org/subfields/1312","display_name":"Molecular Biology"},"field":{"id":"https://openalex.org/fields/13","display_name":"Biochemistry, Genetics and Molecular Biology"},"domain":{"id":"https://openalex.org/domains/1","display_name":"Life Sciences"}}],"keywords":[{"id":"https://openalex.org/keywords/indirect-development","display_name":"indirect development","score":1.0},{"id":"https://openalex.org/keywords/transdifferentiation","display_name":"transdifferentiation","score":0.9509999752044678},{"id":"https://openalex.org/keywords/dedifferentiation","display_name":"dedifferentiation","score":0.8019999861717224},{"id":"https://openalex.org/keywords/developmental-plasticity","display_name":"developmental plasticity","score":0.8799999952316284},{"id":"https://openalex.org/keywords/animal-evolution","display_name":"animal evolution","score":0.7990000247955322},{"id":"https://openalex.org/keywords/polyphenism","display_name":"polyphenism","score":0.7519999742507935},{"id":"https://openalex.org/keywords/histone-h2a-z","display_name":"histone H2A.Z","score":0.8740000128746033},{"id":"https://openalex.org/keywords/hox-genes","display_name":"Hox genes","score":0.7429999709129333},{"id":"https://openalex.org/keywords/gonad-formation","display_name":"gonad formation","score":0.8029999732971191},{"id":"https://openalex.org/keywords/serial-homology","display_name":"serial homology","score":0.5540000200271606}],"concepts":[{"id":"https://openalex.org/C60870556","wikidata":"https://www.wikidata.org/wiki/Q2300675","display_name":"Transdifferentiation","level":3,"score":0.6392587423324585},{"id":"https://openalex.org/C86803240","wikidata":"https://www.wikidata.org/wiki/Q420","display_name":"Biology","level":0,"score":0.5716834664344788},{"id":"https://openalex.org/C78458016","wikidata":"https://www.wikidata.org/wiki/Q840400","display_name":"Evolutionary biology","level":1,"score":0.5664127469062805},{"id":"https://openalex.org/C2988562018","wikidata":"https://www.wikidata.org/wiki/Q1063","display_name":"Biological evolution","level":2,"score":0.48548558354377747},{"id":"https://openalex.org/C151730666","wikidata":"https://www.wikidata.org/wiki/Q7205","display_name":"Paleontology","level":1,"score":0.3622676432132721},{"id":"https://openalex.org/C18903297","wikidata":"https://www.wikidata.org/wiki/Q7150","display_name":"Ecology","level":1,"score":0.34699106216430664},{"id":"https://openalex.org/C54355233","wikidata":"https://www.wikidata.org/wiki/Q7162","display_name":"Genetics","level":1,"score":0.20403704047203064},{"id":"https://openalex.org/C28328180","wikidata":"https://www.wikidata.org/wiki/Q48196","display_name":"Stem cell","level":2,"score":0.09020811319351196}],"mesh":[{"descriptor_ui":"D000818","descriptor_name":"Animals","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D000845","descriptor_name":"Annelida","qualifier_ui":"Q000166","qualifier_name":"cytology","is_major_topic":false},{"descriptor_ui":"D000845","descriptor_name":"Annelida","qualifier_ui":"Q000235","qualifier_name":"genetics","is_major_topic":false},{"descriptor_ui":"D000845","descriptor_name":"Annelida","qualifier_ui":"Q000254","qualifier_name":"growth & development","is_major_topic":false},{"descriptor_ui":"D002454","descriptor_name":"Cell Differentiation","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D005075","descriptor_name":"Biological Evolution","qualifier_ui":null,"qualifier_name":null,"is_major_topic":true},{"descriptor_ui":"D005801","descriptor_name":"Genes, Homeobox","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D005835","descriptor_name":"Genitalia","qualifier_ui":"Q000254","qualifier_name":"growth & development","is_major_topic":false},{"descriptor_ui":"D007814","descriptor_name":"Larva","qualifier_ui":"Q000254","qualifier_name":"growth & development","is_major_topic":false},{"descriptor_ui":"D008018","descriptor_name":"Life Cycle Stages","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D008954","descriptor_name":"Models, Biological","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D010802","descriptor_name":"Phylogeny","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D013234","descriptor_name":"Stem Cells","qualifier_ui":"Q000166","qualifier_name":"cytology","is_major_topic":false},{"descriptor_ui":"D013234","descriptor_name":"Stem Cells","qualifier_ui":"Q000378","qualifier_name":"metabolism","is_major_topic":false},{"descriptor_ui":"D018507","descriptor_name":"Gene Expression Regulation, Developmental","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D048788","descriptor_name":"Growth and Development","qualifier_ui":null,"qualifier_name":null,"is_major_topic":true},{"descriptor_ui":"D053263","descriptor_name":"Gene Regulatory Networks","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D054262","descriptor_name":"Gastrulation","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false},{"descriptor_ui":"D054338","descriptor_name":"Cell Transdifferentiation","qualifier_ui":null,"qualifier_name":null,"is_major_topic":false}],"locations_count":4,"locations":[{"id":"doi:10.1098/rstb.2009.0253","doi":"https://doi.org/10.1098/rstb.2009.0253","is_oa":false,"landing_page_url":"https://doi.org/10.1098/rstb.2009.0253","pdf_url":null,"source":{"id":"https://openalex.org/S91660768","display_name":"Philosophical Transactions of the Royal Society B Biological Sciences","issn_l":"0962-8436","issn":["0962-8436","1471-2970"],"is_oa":false,"is_in_doaj":false,"is_core":true,"listed_in":["anvur-class-a","anvur-scientific","cwts-core","dongbi-d","jufo-2","ki-jl-2","medline","norway-2","poland-140","russia-white-list-1","vabb-shw"],"host_organization":"https://openalex.org/P4310319787","host_organization_name":"Royal Society","host_organization_lineage":["https://openalex.org/P4310319787"],"host_organization_lineage_names":["Royal Society"],"type":"journal"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Philosophical Transactions of the Royal Society B: Biological Sciences","raw_type":"journal-article"},{"id":"pmh:oai:europepmc.org:2048565","doi":null,"is_oa":true,"landing_page_url":"https://www.ncbi.nlm.nih.gov/pmc/articles/2817142","pdf_url":null,"source":{"id":"https://openalex.org/S4306400806","display_name":"Europe PMC (PubMed Central)","issn_l":null,"issn":null,"is_oa":false,"is_in_doaj":false,"is_core":false,"listed_in":[],"host_organization":"https://openalex.org/I1303153112","host_organization_name":"European Bioinformatics Institute","host_organization_lineage":["https://openalex.org/I1303153112"],"host_organization_lineage_names":[],"type":"repository"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":null,"raw_type":"Text"},{"id":"pmh:oai:pubmedcentral.nih.gov:2817142","doi":null,"is_oa":true,"landing_page_url":"https://www.ncbi.nlm.nih.gov/pmc/articles/2817142","pdf_url":null,"source":{"id":"https://openalex.org/S2764455111","display_name":"PubMed Central","issn_l":null,"issn":null,"is_oa":true,"is_in_doaj":false,"is_core":false,"listed_in":[],"host_organization":"https://openalex.org/I1299303238","host_organization_name":"National Institutes of Health","host_organization_lineage":["https://openalex.org/I1299303238"],"host_organization_lineage_names":[],"type":"repository"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Philos Trans R Soc Lond B Biol Sci","raw_type":"Text"},{"id":"pmid:20083640","doi":null,"is_oa":false,"landing_page_url":"https://pubmed.ncbi.nlm.nih.gov/20083640","pdf_url":null,"source":{"id":"https://openalex.org/S4306525036","display_name":"PubMed","issn_l":null,"issn":null,"is_oa":false,"is_in_doaj":false,"is_core":false,"listed_in":[],"host_organization":"https://openalex.org/I1299303238","host_organization_name":"National Institutes of Health","host_organization_lineage":["https://openalex.org/I1299303238"],"host_organization_lineage_names":[],"type":"repository"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"Philosophical transactions of the Royal Society of London. Series B, Biological sciences","raw_type":"Journal Article"}],"best_oa_location":{"id":"pmh:oai:europepmc.org:2048565","doi":null,"is_oa":true,"landing_page_url":"https://www.ncbi.nlm.nih.gov/pmc/articles/2817142","pdf_url":null,"source":{"id":"https://openalex.org/S4306400806","display_name":"Europe PMC (PubMed Central)","issn_l":null,"issn":null,"is_oa":false,"is_in_doaj":false,"is_core":false,"listed_in":[],"host_organization":"https://openalex.org/I1303153112","host_organization_name":"European Bioinformatics Institute","host_organization_lineage":["https://openalex.org/I1303153112"],"host_organization_lineage_names":[],"type":"repository"},"license":null,"license_id":null,"version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":null,"raw_type":"Text"},"sustainable_development_goals":[],"study_designs":[],"awards":[{"id":"https://openalex.org/G780497929","display_name":"Spiralian developmental system for the study of multipotency","funder_award_id":"1R21RR024195","funder_id":"https://openalex.org/F4320337375","funder_display_name":"National Center for Research Resources"}],"funders":[{"id":"https://openalex.org/F4320337375","display_name":"National Center for Research Resources","ror":"https://ror.org/04pw6fb54"}],"has_content":{"pdf":false,"grobid_xml":false},"content_urls":null,"referenced_works_count":136,"referenced_works":["https://openalex.org/W173310403","https://openalex.org/W1509835094","https://openalex.org/W1511656840","https://openalex.org/W1526370110","https://openalex.org/W1536901845","https://openalex.org/W1565489073","https://openalex.org/W1581739371","https://openalex.org/W1592299811","https://openalex.org/W1594616195","https://openalex.org/W1596064049","https://openalex.org/W1607382116","https://openalex.org/W1615515432","https://openalex.org/W1938960599","https://openalex.org/W1965178844","https://openalex.org/W1968505138","https://openalex.org/W1969025265","https://openalex.org/W1972643909","https://openalex.org/W1972759541","https://openalex.org/W1974164983","https://openalex.org/W1974484497","https://openalex.org/W1976798874","https://openalex.org/W1977966381","https://openalex.org/W1980347984","https://openalex.org/W1982344295","https://openalex.org/W1986306345","https://openalex.org/W1989641503","https://openalex.org/W1989717344","https://openalex.org/W1991201077","https://openalex.org/W1993838585","https://openalex.org/W1995349078","https://openalex.org/W1995418425","https://openalex.org/W1998140558","https://openalex.org/W1998607539","https://openalex.org/W1999269547","https://openalex.org/W1999586167","https://openalex.org/W2001728721","https://openalex.org/W2006205550","https://openalex.org/W2008494541","https://openalex.org/W2009851083","https://openalex.org/W2011033963","https://openalex.org/W2016597274","https://openalex.org/W2017838223","https://openalex.org/W2022586823","https://openalex.org/W2023198782","https://openalex.org/W2024713711","https://openalex.org/W2029609524","https://openalex.org/W2030545022","https://openalex.org/W2031305337","https://openalex.org/W2033087961","https://openalex.org/W2033352040","https://openalex.org/W2039007955","https://openalex.org/W2041739600","https://openalex.org/W2043656979","https://openalex.org/W2045220362","https://openalex.org/W2045663135","https://openalex.org/W2046256742","https://openalex.org/W2050944577","https://openalex.org/W2052393548","https://openalex.org/W2054216558","https://openalex.org/W2056187821","https://openalex.org/W2057195804","https://openalex.org/W2058855891","https://openalex.org/W2060399360","https://openalex.org/W2063679723","https://openalex.org/W2064217705","https://openalex.org/W2069674573","https://openalex.org/W2073514647","https://openalex.org/W2073641185","https://openalex.org/W2075033992","https://openalex.org/W2075118649","https://openalex.org/W2075585528","https://openalex.org/W2075613902","https://openalex.org/W2076004673","https://openalex.org/W2078854027","https://openalex.org/W2078952624","https://openalex.org/W2080948129","https://openalex.org/W2081696843","https://openalex.org/W2083438848","https://openalex.org/W2084448229","https://openalex.org/W2086025948","https://openalex.org/W2086124124","https://openalex.org/W2086833256","https://openalex.org/W2088317834","https://openalex.org/W2088656564","https://openalex.org/W2090445280","https://openalex.org/W2091255780","https://openalex.org/W2091430768","https://openalex.org/W2091685617","https://openalex.org/W2091734168","https://openalex.org/W2096334391","https://openalex.org/W2096641211","https://openalex.org/W2099355889","https://openalex.org/W2099958663","https://openalex.org/W2102109312","https://openalex.org/W2102241613","https://openalex.org/W2102631576","https://openalex.org/W2103105169","https://openalex.org/W2103841961","https://openalex.org/W2107449113","https://openalex.org/W2110697328","https://openalex.org/W2111677103","https://openalex.org/W2112037903","https://openalex.org/W2113449459","https://openalex.org/W2113478190","https://openalex.org/W2116544762","https://openalex.org/W2123350521","https://openalex.org/W2123447967","https://openalex.org/W2126414770","https://openalex.org/W2126796287","https://openalex.org/W2127207904","https://openalex.org/W2129622728","https://openalex.org/W2135271831","https://openalex.org/W2136096754","https://openalex.org/W2138131045","https://openalex.org/W2139542661","https://openalex.org/W2142571210","https://openalex.org/W2143837955","https://openalex.org/W2147212824","https://openalex.org/W2149086579","https://openalex.org/W2153590739","https://openalex.org/W2153646569","https://openalex.org/W2154216495","https://openalex.org/W2154833122","https://openalex.org/W2157044516","https://openalex.org/W2157523980","https://openalex.org/W2158657731","https://openalex.org/W2158901355","https://openalex.org/W2162137086","https://openalex.org/W2165909183","https://openalex.org/W2165937624","https://openalex.org/W2166039615","https://openalex.org/W2287375854","https://openalex.org/W2591760982","https://openalex.org/W2617181777","https://openalex.org/W3161381604","https://openalex.org/W4212989115"],"related_works":["https://openalex.org/W2116847257","https://openalex.org/W2287375854","https://openalex.org/W7095563377","https://openalex.org/W2122337391","https://openalex.org/W4317952817","https://openalex.org/W2025066435","https://openalex.org/W2921644417","https://openalex.org/W2560836588","https://openalex.org/W2172674994","https://openalex.org/W2097736793"],"abstract_inverted_index":{"It":[0,203],"is":[1,30,187,204],"proposed":[2,206],"here":[3],"that":[4,207],"a":[5,107],"biphasic":[6],"life":[7],"cycle":[8],"with":[9,189],"partial":[10],"dedifferentiation":[11],"of":[12,23,27,35,43,53,67,84,91,102,118,125,132,149,165,192,196,211],"intermediate":[13],"juvenile":[14],"or":[15,109,157],"larval":[16,51],"stages":[17],"represents":[18],"the":[19,32,40,44,89,97,115,150,166,175,184,190,193,197,208,212],"mainstream":[20],"developmental":[21],"mode":[22],"metazoans.":[24],"Developmental":[25,82],"plasticity":[26,83],"differentiated":[28,50,68,85],"cells":[29,52],"considered":[31],"essential":[33],"characteristic":[34],"indirect":[36,54,111],"development,":[37],"rather":[38,219],"than":[39,220],"exclusive":[41],"development":[42],"adult":[45,63],"from":[46],"'set-aside'":[47],"cells.":[48],"Many":[49],"developers":[55,171],"resume":[56],"proliferation,":[57],"partially":[58],"dedifferentiate":[59],"and":[60,73,104,113,127,159,168],"contribute":[61],"to":[62,75,122,144,178],"tissues.":[64],"Transcriptional":[65],"pluripotency":[66],"states":[69,86],"has":[70],"premetazoan":[71],"origins":[72],"seems":[74,142],"be":[76],"facilitated":[77],"by":[78,139,155],"histone":[79],"variant":[80],"H2A.Z.":[81],"also":[87],"facilitates":[88],"evolution":[90],"polyphenism.":[92],"Uncertainty":[93],"remains":[94],"about":[95],"whether":[96],"most":[98],"recent":[99],"common":[100],"ancestor":[101],"protostomes":[103],"deuterostomes":[105],"was":[106,215],"direct":[108],"an":[110],"developer,":[112],"how":[114],"feeding":[116],"larvae":[117,124,131],"bilaterians":[119,133],"are":[120],"related":[121,143],"non-feeding":[123],"sponges":[126],"cnidarians.":[128,147],"Feeding":[129],"ciliated":[130,181],"form":[134],"their":[135,180],"primary":[136],"gut":[137,152],"opening":[138,153],"invagination,":[140],"which":[141],"invagination":[145],"in":[146,216,221],"Formation":[148],"secondary":[151],"proceeds":[154],"protostomy":[156],"deuterostomy,":[158],"gene":[160],"usage":[161],"suggests":[162],"serial":[163],"homology":[164],"mouth":[167],"anus.":[169],"Indirect":[170],"do":[172],"not":[173],"use":[174],"Hox":[176,185,213],"vector":[177,186],"build":[179],"larvae,":[182],"but":[183],"associated":[188],"construction":[191],"reproductive":[194],"portion":[195],"animal":[198],"during":[199],"feeding-dependent":[200],"posterior":[201],"growth.":[202],"further":[205],"original":[209],"function":[210],"cluster":[214],"gonad":[217],"formation":[218],"anteroposterior":[222],"diversification.":[223]},"counts_by_year":[{"year":2026,"cited_by_count":1},{"year":2025,"cited_by_count":6},{"year":2024,"cited_by_count":5},{"year":2023,"cited_by_count":4},{"year":2022,"cited_by_count":8},{"year":2020,"cited_by_count":5},{"year":2019,"cited_by_count":1},{"year":2018,"cited_by_count":3},{"year":2017,"cited_by_count":1},{"year":2016,"cited_by_count":4},{"year":2015,"cited_by_count":7},{"year":2014,"cited_by_count":2},{"year":2013,"cited_by_count":3},{"year":2012,"cited_by_count":2}],"updated_date":"2026-11-04T10:54:05.112534","created_date":"2016-06-24T00:00:00"}