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The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X–Y Gene Conversion, and Feeding Strategy
Among extant cetaceans, mysticetes are filter feeders that do not possess teeth and use their baleen for feeding, while most odontocetes are considered suction feeders, which capture prey by suction without biting or chewing with teeth. In the present study, we address the functionality of amelogeni...
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Published in: | Journal of molecular evolution 2020-03, Vol.88 (2), p.122-135 |
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creator | Kawasaki, Kazuhiko Mikami, Masato Goto, Mutsuo Shindo, Junji Amano, Masao Ishiyama, Mikio |
description | Among extant cetaceans, mysticetes are filter feeders that do not possess teeth and use their baleen for feeding, while most odontocetes are considered suction feeders, which capture prey by suction without biting or chewing with teeth. In the present study, we address the functionality of amelogenin (
AMEL
) genes in cetaceans.
AMEL
encodes a protein that is specifically involved in dental enamel formation and is located on the sex chromosomes in eutherians. The X-copy
AMELX
is functional in enamel-bearing eutherians, whereas the Y-copy
AMELY
appears to have undergone decay and was completely lost in some species. Consistent with these premises, we detected various deleterious mutations and/or non-canonical splice junctions in
AMELX
of mysticetes and four suction feeding odontocetes,
Delphinapterus leucas
,
Monodon monoceros
,
Kogia breviceps
, and
Physeter macrocephalus
, and in
AMELY
of mysticetes and odontocetes. Regardless of the functionality, both
AMELX
and
AMELY
are equally and unusually small in cetaceans, and even their functional
AMELX
genes presumably encode a degenerate core region, which is thought to be essential for enamel matrix assembly and enamel crystal growth. Furthermore, our results suggest that the most recent common ancestors of extant cetaceans had functional
AMELX
and
AMELY
, both of which are similar to
AMELX
of
Platanista minor
. Similar small
AMELX
and
AMELY
in archaic cetaceans can be explained by gene conversion between
AMELX
and
AMELY
. We speculate that common ancestors of modern cetaceans employed a degenerate
AMELX
, transferred from a decaying
AMELY
by gene conversion, at an early stage of their transition to suction feeders. |
doi_str_mv | 10.1007/s00239-019-09917-0 |
format | article |
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AMEL
) genes in cetaceans.
AMEL
encodes a protein that is specifically involved in dental enamel formation and is located on the sex chromosomes in eutherians. The X-copy
AMELX
is functional in enamel-bearing eutherians, whereas the Y-copy
AMELY
appears to have undergone decay and was completely lost in some species. Consistent with these premises, we detected various deleterious mutations and/or non-canonical splice junctions in
AMELX
of mysticetes and four suction feeding odontocetes,
Delphinapterus leucas
,
Monodon monoceros
,
Kogia breviceps
, and
Physeter macrocephalus
, and in
AMELY
of mysticetes and odontocetes. Regardless of the functionality, both
AMELX
and
AMELY
are equally and unusually small in cetaceans, and even their functional
AMELX
genes presumably encode a degenerate core region, which is thought to be essential for enamel matrix assembly and enamel crystal growth. Furthermore, our results suggest that the most recent common ancestors of extant cetaceans had functional
AMELX
and
AMELY
, both of which are similar to
AMELX
of
Platanista minor
. Similar small
AMELX
and
AMELY
in archaic cetaceans can be explained by gene conversion between
AMELX
and
AMELY
. We speculate that common ancestors of modern cetaceans employed a degenerate
AMELX
, transferred from a decaying
AMELY
by gene conversion, at an early stage of their transition to suction feeders.</description><identifier>ISSN: 0022-2844</identifier><identifier>EISSN: 1432-1432</identifier><identifier>DOI: 10.1007/s00239-019-09917-0</identifier><identifier>PMID: 31754761</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Amelogenin ; Amelogenin - genetics ; Animal Genetics and Genomics ; Animals ; Base Sequence ; Biological evolution ; Biomedical and Life Sciences ; Biting ; Cell Biology ; Cetacea ; Cetacea - genetics ; Chewing ; Chromosomes ; Conversion ; Crystal growth ; Dental enamel ; Dental Enamel Proteins - genetics ; Enamel ; Evolution, Molecular ; Evolutionary Biology ; Evolutionary genetics ; Exons ; Feeders ; Feeding ; Feeding Behavior ; Filter feeders ; Gene Conversion ; Genes ; Introns ; Life Sciences ; Microbiology ; Mutation ; Original Article ; Plant Genetics and Genomics ; Plant Sciences ; Prey ; Sex chromosomes ; Splice junctions ; Suction ; Teeth ; X Chromosome - genetics ; Y Chromosome - genetics ; Y gene</subject><ispartof>Journal of molecular evolution, 2020-03, Vol.88 (2), p.122-135</ispartof><rights>Springer Science+Business Media, LLC, part of Springer Nature 2019</rights><rights>Journal of Molecular Evolution is a copyright of Springer, (2019). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-73a792dc1fb69e29f75a1b08e72e714888660d4a25090bddffe8804810fddd4b3</citedby><cites>FETCH-LOGICAL-c474t-73a792dc1fb69e29f75a1b08e72e714888660d4a25090bddffe8804810fddd4b3</cites><orcidid>0000-0003-1090-5340</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31754761$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kawasaki, Kazuhiko</creatorcontrib><creatorcontrib>Mikami, Masato</creatorcontrib><creatorcontrib>Goto, Mutsuo</creatorcontrib><creatorcontrib>Shindo, Junji</creatorcontrib><creatorcontrib>Amano, Masao</creatorcontrib><creatorcontrib>Ishiyama, Mikio</creatorcontrib><title>The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X–Y Gene Conversion, and Feeding Strategy</title><title>Journal of molecular evolution</title><addtitle>J Mol Evol</addtitle><addtitle>J Mol Evol</addtitle><description>Among extant cetaceans, mysticetes are filter feeders that do not possess teeth and use their baleen for feeding, while most odontocetes are considered suction feeders, which capture prey by suction without biting or chewing with teeth. In the present study, we address the functionality of amelogenin (
AMEL
) genes in cetaceans.
AMEL
encodes a protein that is specifically involved in dental enamel formation and is located on the sex chromosomes in eutherians. The X-copy
AMELX
is functional in enamel-bearing eutherians, whereas the Y-copy
AMELY
appears to have undergone decay and was completely lost in some species. Consistent with these premises, we detected various deleterious mutations and/or non-canonical splice junctions in
AMELX
of mysticetes and four suction feeding odontocetes,
Delphinapterus leucas
,
Monodon monoceros
,
Kogia breviceps
, and
Physeter macrocephalus
, and in
AMELY
of mysticetes and odontocetes. Regardless of the functionality, both
AMELX
and
AMELY
are equally and unusually small in cetaceans, and even their functional
AMELX
genes presumably encode a degenerate core region, which is thought to be essential for enamel matrix assembly and enamel crystal growth. Furthermore, our results suggest that the most recent common ancestors of extant cetaceans had functional
AMELX
and
AMELY
, both of which are similar to
AMELX
of
Platanista minor
. Similar small
AMELX
and
AMELY
in archaic cetaceans can be explained by gene conversion between
AMELX
and
AMELY
. We speculate that common ancestors of modern cetaceans employed a degenerate
AMELX
, transferred from a decaying
AMELY
by gene conversion, at an early stage of their transition to suction feeders.</description><subject>Amelogenin</subject><subject>Amelogenin - genetics</subject><subject>Animal Genetics and Genomics</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Biological evolution</subject><subject>Biomedical and Life Sciences</subject><subject>Biting</subject><subject>Cell Biology</subject><subject>Cetacea</subject><subject>Cetacea - genetics</subject><subject>Chewing</subject><subject>Chromosomes</subject><subject>Conversion</subject><subject>Crystal growth</subject><subject>Dental enamel</subject><subject>Dental Enamel Proteins - genetics</subject><subject>Enamel</subject><subject>Evolution, Molecular</subject><subject>Evolutionary Biology</subject><subject>Evolutionary genetics</subject><subject>Exons</subject><subject>Feeders</subject><subject>Feeding</subject><subject>Feeding Behavior</subject><subject>Filter feeders</subject><subject>Gene Conversion</subject><subject>Genes</subject><subject>Introns</subject><subject>Life Sciences</subject><subject>Microbiology</subject><subject>Mutation</subject><subject>Original Article</subject><subject>Plant Genetics and Genomics</subject><subject>Plant Sciences</subject><subject>Prey</subject><subject>Sex chromosomes</subject><subject>Splice junctions</subject><subject>Suction</subject><subject>Teeth</subject><subject>X Chromosome - genetics</subject><subject>Y Chromosome - genetics</subject><subject>Y gene</subject><issn>0022-2844</issn><issn>1432-1432</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp9Udtq3DAQFaWl2aT9gT4UQV_6UDeSLFsShUJYkrQQSCEJtE9CtsaOgy0lkr2whUD_oX-YL4nWm6aXhyKkGXTOHM3oIPSKkveUELEfCWG5yghNWykqMvIELSjPWbY5nqJFwlnGJOc7aDfGK0KoKFT-HO3kKeGipAt0e34J-HDl-2nsvMO-wRduipPp-zU-G1LABwP0vgXXOXwMDiJOyRJGU4Nx8QP-EmGyM_7dbCTe4a93P35-m7l46d0KQpyvjbP4CMB2rsVnYzAjtOsX6Flj-ggvH-Ieujg6PF9-yk5Ojz8vD06ymgs-ZiI3QjFb06YqFTDViMLQikgQDATlUsqyJJYbVhBFKmubBqQkXFLSWGt5le-hj1vd66kawNbgUgO9vg7dYMJae9PpvxHXXerWr7RiBZVEJIG3DwLB30wQRz10sYa-Nw78FDXL568taJmob_6hXvkpuDReYqWeRFpFYrEtqw4-xgDNYzOU6I27euuuTu7q2V1NUtHrP8d4LPllZyLkW0JMkGsh_H77P7L30vKyMQ</recordid><startdate>20200301</startdate><enddate>20200301</enddate><creator>Kawasaki, Kazuhiko</creator><creator>Mikami, Masato</creator><creator>Goto, Mutsuo</creator><creator>Shindo, Junji</creator><creator>Amano, Masao</creator><creator>Ishiyama, Mikio</creator><general>Springer US</general><general>Springer Nature B.V</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>3V.</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7T7</scope><scope>7TK</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1090-5340</orcidid></search><sort><creationdate>20200301</creationdate><title>The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X–Y Gene Conversion, and Feeding Strategy</title><author>Kawasaki, Kazuhiko ; Mikami, Masato ; Goto, Mutsuo ; Shindo, Junji ; Amano, Masao ; Ishiyama, Mikio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-73a792dc1fb69e29f75a1b08e72e714888660d4a25090bddffe8804810fddd4b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Amelogenin</topic><topic>Amelogenin - genetics</topic><topic>Animal Genetics and Genomics</topic><topic>Animals</topic><topic>Base Sequence</topic><topic>Biological evolution</topic><topic>Biomedical and Life Sciences</topic><topic>Biting</topic><topic>Cell Biology</topic><topic>Cetacea</topic><topic>Cetacea - genetics</topic><topic>Chewing</topic><topic>Chromosomes</topic><topic>Conversion</topic><topic>Crystal growth</topic><topic>Dental enamel</topic><topic>Dental Enamel Proteins - genetics</topic><topic>Enamel</topic><topic>Evolution, Molecular</topic><topic>Evolutionary Biology</topic><topic>Evolutionary genetics</topic><topic>Exons</topic><topic>Feeders</topic><topic>Feeding</topic><topic>Feeding Behavior</topic><topic>Filter feeders</topic><topic>Gene Conversion</topic><topic>Genes</topic><topic>Introns</topic><topic>Life Sciences</topic><topic>Microbiology</topic><topic>Mutation</topic><topic>Original Article</topic><topic>Plant Genetics and Genomics</topic><topic>Plant Sciences</topic><topic>Prey</topic><topic>Sex chromosomes</topic><topic>Splice junctions</topic><topic>Suction</topic><topic>Teeth</topic><topic>X Chromosome - genetics</topic><topic>Y Chromosome - genetics</topic><topic>Y gene</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kawasaki, Kazuhiko</creatorcontrib><creatorcontrib>Mikami, Masato</creatorcontrib><creatorcontrib>Goto, Mutsuo</creatorcontrib><creatorcontrib>Shindo, Junji</creatorcontrib><creatorcontrib>Amano, Masao</creatorcontrib><creatorcontrib>Ishiyama, Mikio</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of molecular evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kawasaki, Kazuhiko</au><au>Mikami, Masato</au><au>Goto, Mutsuo</au><au>Shindo, Junji</au><au>Amano, Masao</au><au>Ishiyama, Mikio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X–Y Gene Conversion, and Feeding Strategy</atitle><jtitle>Journal of molecular evolution</jtitle><stitle>J Mol Evol</stitle><addtitle>J Mol Evol</addtitle><date>2020-03-01</date><risdate>2020</risdate><volume>88</volume><issue>2</issue><spage>122</spage><epage>135</epage><pages>122-135</pages><issn>0022-2844</issn><eissn>1432-1432</eissn><abstract>Among extant cetaceans, mysticetes are filter feeders that do not possess teeth and use their baleen for feeding, while most odontocetes are considered suction feeders, which capture prey by suction without biting or chewing with teeth. In the present study, we address the functionality of amelogenin (
AMEL
) genes in cetaceans.
AMEL
encodes a protein that is specifically involved in dental enamel formation and is located on the sex chromosomes in eutherians. The X-copy
AMELX
is functional in enamel-bearing eutherians, whereas the Y-copy
AMELY
appears to have undergone decay and was completely lost in some species. Consistent with these premises, we detected various deleterious mutations and/or non-canonical splice junctions in
AMELX
of mysticetes and four suction feeding odontocetes,
Delphinapterus leucas
,
Monodon monoceros
,
Kogia breviceps
, and
Physeter macrocephalus
, and in
AMELY
of mysticetes and odontocetes. Regardless of the functionality, both
AMELX
and
AMELY
are equally and unusually small in cetaceans, and even their functional
AMELX
genes presumably encode a degenerate core region, which is thought to be essential for enamel matrix assembly and enamel crystal growth. Furthermore, our results suggest that the most recent common ancestors of extant cetaceans had functional
AMELX
and
AMELY
, both of which are similar to
AMELX
of
Platanista minor
. Similar small
AMELX
and
AMELY
in archaic cetaceans can be explained by gene conversion between
AMELX
and
AMELY
. We speculate that common ancestors of modern cetaceans employed a degenerate
AMELX
, transferred from a decaying
AMELY
by gene conversion, at an early stage of their transition to suction feeders.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>31754761</pmid><doi>10.1007/s00239-019-09917-0</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-1090-5340</orcidid><oa>free_for_read</oa></addata></record> |
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language | eng |
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source | Springer Nature |
subjects | Amelogenin Amelogenin - genetics Animal Genetics and Genomics Animals Base Sequence Biological evolution Biomedical and Life Sciences Biting Cell Biology Cetacea Cetacea - genetics Chewing Chromosomes Conversion Crystal growth Dental enamel Dental Enamel Proteins - genetics Enamel Evolution, Molecular Evolutionary Biology Evolutionary genetics Exons Feeders Feeding Feeding Behavior Filter feeders Gene Conversion Genes Introns Life Sciences Microbiology Mutation Original Article Plant Genetics and Genomics Plant Sciences Prey Sex chromosomes Splice junctions Suction Teeth X Chromosome - genetics Y Chromosome - genetics Y gene |
title | The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X–Y Gene Conversion, and Feeding Strategy |
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