Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs
Key message In this manuscript, we show that Oryza sativa indica Argonaute protein AGO18 is required for male gametophyte development likely to through a small RNA-mediated mechanism. Monocots have evolved unique gene silencing pathways due to the presence of unique members of Dicer-like and Argonau...
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| Veröffentlicht in: | Plant reproduction 2020-03, Vol.33 (1), p.59-73 |
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| creator | Das, Soumita Swetha, Chenna Pachamuthu, Kannan Nair, Ashwin Shivaprasad, P. V. |
| description | Key message
In this manuscript, we show that
Oryza sativa
indica Argonaute protein AGO18 is required for male gametophyte development likely to through a small RNA-mediated mechanism.
Monocots have evolved unique gene silencing pathways due to the presence of unique members of Dicer-like and Argonaute (AGO) family members. Among the monocot AGO homologs, AGO18 occupies a unique position. Previous reports have implicated this protein in viral resistance as well as in gametogenesis, likely through its competition with AGO1 clade members for micro(mi)RNAs and other small (s)RNAs. Although expression of rice AGO18 in specific stages of male gametogenesis has been documented, its major functions in plant development remain poorly understood. Here, we show that
Oryza sativa indica
AGO18 is involved in male gametophyte development. Knockdown (KD) of AGO18 in transgenic rice lines resulted in stunted plants that are male sterile, whereas their carpels were functional. Transcriptome analysis revealed downregulation of several pollen development-associated genes in KD lines. sRNA sequencing in vegetative and reproductive tissues of KD lines indicated reduction of miRNAs and phased secondary sRNAs implicated in male gametophyte development. Our results indicate a distinct role for rice AGO18 in male fertility. |
| doi_str_mv | 10.1007/s00497-020-00386-w |
| format | Article |
| fullrecord | <record><control><sourceid>gale_webof</sourceid><recordid>TN_cdi_webofscience_primary_000519442600007</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A617417478</galeid><sourcerecordid>A617417478</sourcerecordid><originalsourceid>FETCH-LOGICAL-c448t-e87ddade3c7e3a66c5f99fa5e4be1d6655946e1a7b3cc538e41c264daa5471da3</originalsourceid><addsrcrecordid>eNqNkl1rFDEUhgdRbKn9A15IwBtFpiaTr5nLZfGjsFioeh2yyZk1ZTZZk0zX7a9vdqeu1AuRBHJInvdwTt5TVS8JviAYy_cJY9bJGje4xpi2ot4-qU4b0rFadoI8PcacnlTnKd1gjAmmhGP2vDqhDeGSCXJarRYhJRR61I_eZBf8Pr6KuzuNks7uVqNZXAWvxwyItMh5OxpIaK0HQClDdIPLO6S9RRHK0yGD82jzQyewKBVuQNdfZulF9azXQ4Lzh_Os-v7xw7f553px9elyPlvUhrE219BKa7UFaiRQLYThfdf1mgNbArFCcN4xAUTLJTWG0xYYMY1gVmvOJLGanlVvprybGH6OkLJau2RgGLSHMCbVUCkaymnDC_r6L_QmjNGX6g5U23HeikJdTNSqtKyc70OO2pRlYe1M8NC7cj8TRLKyZVsEbx8JCpPhV17pMSV1-fX6MdtMrInFhgi92kS31nGnCFZ7m9Vksyo2q4PNaltErx7qHpdrsEfJb1ML0E7AFpahT8aBN3DEyiDwMhqsESXCcu6y3rs2D6PPRfru_6WFphOdCuFXEP_84D_qvwc3A9Jj</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2376895586</pqid></control><display><type>article</type><title>Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs</title><source>MEDLINE</source><source>SpringerNature Journals</source><source>Web of Science - Science Citation Index Expanded - 2020<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" /></source><creator>Das, Soumita ; Swetha, Chenna ; Pachamuthu, Kannan ; Nair, Ashwin ; Shivaprasad, P. V.</creator><creatorcontrib>Das, Soumita ; Swetha, Chenna ; Pachamuthu, Kannan ; Nair, Ashwin ; Shivaprasad, P. V.</creatorcontrib><description>Key message
In this manuscript, we show that
Oryza sativa
indica Argonaute protein AGO18 is required for male gametophyte development likely to through a small RNA-mediated mechanism.
Monocots have evolved unique gene silencing pathways due to the presence of unique members of Dicer-like and Argonaute (AGO) family members. Among the monocot AGO homologs, AGO18 occupies a unique position. Previous reports have implicated this protein in viral resistance as well as in gametogenesis, likely through its competition with AGO1 clade members for micro(mi)RNAs and other small (s)RNAs. Although expression of rice AGO18 in specific stages of male gametogenesis has been documented, its major functions in plant development remain poorly understood. Here, we show that
Oryza sativa indica
AGO18 is involved in male gametophyte development. Knockdown (KD) of AGO18 in transgenic rice lines resulted in stunted plants that are male sterile, whereas their carpels were functional. Transcriptome analysis revealed downregulation of several pollen development-associated genes in KD lines. sRNA sequencing in vegetative and reproductive tissues of KD lines indicated reduction of miRNAs and phased secondary sRNAs implicated in male gametophyte development. Our results indicate a distinct role for rice AGO18 in male fertility.</description><identifier>ISSN: 2194-7953</identifier><identifier>EISSN: 2194-7961</identifier><identifier>DOI: 10.1007/s00497-020-00386-w</identifier><identifier>PMID: 32157461</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Agriculture ; Analysis ; Argonaute Proteins - genetics ; Argonaute Proteins - metabolism ; Biological evolution ; Biomedical and Life Sciences ; Carpels ; Cell Biology ; Fertility ; Gametogenesis ; Gene Expression Regulation, Plant ; Gene Knockdown Techniques ; Gene silencing ; Genetic engineering ; Homology ; Life Sciences ; Life Sciences & Biomedicine ; Male sterility ; MicroRNA ; MicroRNAs - genetics ; Original Article ; Oryza - genetics ; Oryza sativa indica ; Plant Sciences ; Pollen ; Proteins ; Reduction ; Reproduction ; Reproductive Biology ; Ribonucleic acid ; Rice ; RNA ; Science & Technology ; Transgenic plants</subject><ispartof>Plant reproduction, 2020-03, Vol.33 (1), p.59-73</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2020</rights><rights>COPYRIGHT 2020 Springer</rights><rights>Plant Reproduction is a copyright of Springer, (2020). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>19</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000519442600007</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c448t-e87ddade3c7e3a66c5f99fa5e4be1d6655946e1a7b3cc538e41c264daa5471da3</citedby><cites>FETCH-LOGICAL-c448t-e87ddade3c7e3a66c5f99fa5e4be1d6655946e1a7b3cc538e41c264daa5471da3</cites><orcidid>0000-0002-9823-044X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00497-020-00386-w$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00497-020-00386-w$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>315,781,785,27929,27930,28253,41493,42562,51324</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32157461$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Das, Soumita</creatorcontrib><creatorcontrib>Swetha, Chenna</creatorcontrib><creatorcontrib>Pachamuthu, Kannan</creatorcontrib><creatorcontrib>Nair, Ashwin</creatorcontrib><creatorcontrib>Shivaprasad, P. V.</creatorcontrib><title>Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs</title><title>Plant reproduction</title><addtitle>Plant Reprod</addtitle><addtitle>PLANT REPROD</addtitle><addtitle>Plant Reprod</addtitle><description>Key message
In this manuscript, we show that
Oryza sativa
indica Argonaute protein AGO18 is required for male gametophyte development likely to through a small RNA-mediated mechanism.
Monocots have evolved unique gene silencing pathways due to the presence of unique members of Dicer-like and Argonaute (AGO) family members. Among the monocot AGO homologs, AGO18 occupies a unique position. Previous reports have implicated this protein in viral resistance as well as in gametogenesis, likely through its competition with AGO1 clade members for micro(mi)RNAs and other small (s)RNAs. Although expression of rice AGO18 in specific stages of male gametogenesis has been documented, its major functions in plant development remain poorly understood. Here, we show that
Oryza sativa indica
AGO18 is involved in male gametophyte development. Knockdown (KD) of AGO18 in transgenic rice lines resulted in stunted plants that are male sterile, whereas their carpels were functional. Transcriptome analysis revealed downregulation of several pollen development-associated genes in KD lines. sRNA sequencing in vegetative and reproductive tissues of KD lines indicated reduction of miRNAs and phased secondary sRNAs implicated in male gametophyte development. Our results indicate a distinct role for rice AGO18 in male fertility.</description><subject>Agriculture</subject><subject>Analysis</subject><subject>Argonaute Proteins - genetics</subject><subject>Argonaute Proteins - metabolism</subject><subject>Biological evolution</subject><subject>Biomedical and Life Sciences</subject><subject>Carpels</subject><subject>Cell Biology</subject><subject>Fertility</subject><subject>Gametogenesis</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Knockdown Techniques</subject><subject>Gene silencing</subject><subject>Genetic engineering</subject><subject>Homology</subject><subject>Life Sciences</subject><subject>Life Sciences & Biomedicine</subject><subject>Male sterility</subject><subject>MicroRNA</subject><subject>MicroRNAs - genetics</subject><subject>Original Article</subject><subject>Oryza - genetics</subject><subject>Oryza sativa indica</subject><subject>Plant Sciences</subject><subject>Pollen</subject><subject>Proteins</subject><subject>Reduction</subject><subject>Reproduction</subject><subject>Reproductive Biology</subject><subject>Ribonucleic acid</subject><subject>Rice</subject><subject>RNA</subject><subject>Science & Technology</subject><subject>Transgenic plants</subject><issn>2194-7953</issn><issn>2194-7961</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkl1rFDEUhgdRbKn9A15IwBtFpiaTr5nLZfGjsFioeh2yyZk1ZTZZk0zX7a9vdqeu1AuRBHJInvdwTt5TVS8JviAYy_cJY9bJGje4xpi2ot4-qU4b0rFadoI8PcacnlTnKd1gjAmmhGP2vDqhDeGSCXJarRYhJRR61I_eZBf8Pr6KuzuNks7uVqNZXAWvxwyItMh5OxpIaK0HQClDdIPLO6S9RRHK0yGD82jzQyewKBVuQNdfZulF9azXQ4Lzh_Os-v7xw7f553px9elyPlvUhrE219BKa7UFaiRQLYThfdf1mgNbArFCcN4xAUTLJTWG0xYYMY1gVmvOJLGanlVvprybGH6OkLJau2RgGLSHMCbVUCkaymnDC_r6L_QmjNGX6g5U23HeikJdTNSqtKyc70OO2pRlYe1M8NC7cj8TRLKyZVsEbx8JCpPhV17pMSV1-fX6MdtMrInFhgi92kS31nGnCFZ7m9Vksyo2q4PNaltErx7qHpdrsEfJb1ML0E7AFpahT8aBN3DEyiDwMhqsESXCcu6y3rs2D6PPRfru_6WFphOdCuFXEP_84D_qvwc3A9Jj</recordid><startdate>20200301</startdate><enddate>20200301</enddate><creator>Das, Soumita</creator><creator>Swetha, Chenna</creator><creator>Pachamuthu, Kannan</creator><creator>Nair, Ashwin</creator><creator>Shivaprasad, P. V.</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature</general><general>Springer</general><general>Springer Nature B.V</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</scope><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>3V.</scope><scope>7X2</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M0K</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-9823-044X</orcidid></search><sort><creationdate>20200301</creationdate><title>Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs</title><author>Das, Soumita ; Swetha, Chenna ; Pachamuthu, Kannan ; Nair, Ashwin ; Shivaprasad, P. V.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c448t-e87ddade3c7e3a66c5f99fa5e4be1d6655946e1a7b3cc538e41c264daa5471da3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Agriculture</topic><topic>Analysis</topic><topic>Argonaute Proteins - genetics</topic><topic>Argonaute Proteins - metabolism</topic><topic>Biological evolution</topic><topic>Biomedical and Life Sciences</topic><topic>Carpels</topic><topic>Cell Biology</topic><topic>Fertility</topic><topic>Gametogenesis</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Knockdown Techniques</topic><topic>Gene silencing</topic><topic>Genetic engineering</topic><topic>Homology</topic><topic>Life Sciences</topic><topic>Life Sciences & Biomedicine</topic><topic>Male sterility</topic><topic>MicroRNA</topic><topic>MicroRNAs - genetics</topic><topic>Original Article</topic><topic>Oryza - genetics</topic><topic>Oryza sativa indica</topic><topic>Plant Sciences</topic><topic>Pollen</topic><topic>Proteins</topic><topic>Reduction</topic><topic>Reproduction</topic><topic>Reproductive Biology</topic><topic>Ribonucleic acid</topic><topic>Rice</topic><topic>RNA</topic><topic>Science & Technology</topic><topic>Transgenic plants</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Das, Soumita</creatorcontrib><creatorcontrib>Swetha, Chenna</creatorcontrib><creatorcontrib>Pachamuthu, Kannan</creatorcontrib><creatorcontrib>Nair, Ashwin</creatorcontrib><creatorcontrib>Shivaprasad, P. V.</creatorcontrib><collection>Web of Science - Science Citation Index Expanded - 2020</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><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>ProQuest Central (Corporate)</collection><collection>Agricultural Science Collection</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><jtitle>Plant reproduction</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Das, Soumita</au><au>Swetha, Chenna</au><au>Pachamuthu, Kannan</au><au>Nair, Ashwin</au><au>Shivaprasad, P. V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs</atitle><jtitle>Plant reproduction</jtitle><stitle>Plant Reprod</stitle><stitle>PLANT REPROD</stitle><addtitle>Plant Reprod</addtitle><date>2020-03-01</date><risdate>2020</risdate><volume>33</volume><issue>1</issue><spage>59</spage><epage>73</epage><pages>59-73</pages><issn>2194-7953</issn><eissn>2194-7961</eissn><abstract>Key message
In this manuscript, we show that
Oryza sativa
indica Argonaute protein AGO18 is required for male gametophyte development likely to through a small RNA-mediated mechanism.
Monocots have evolved unique gene silencing pathways due to the presence of unique members of Dicer-like and Argonaute (AGO) family members. Among the monocot AGO homologs, AGO18 occupies a unique position. Previous reports have implicated this protein in viral resistance as well as in gametogenesis, likely through its competition with AGO1 clade members for micro(mi)RNAs and other small (s)RNAs. Although expression of rice AGO18 in specific stages of male gametogenesis has been documented, its major functions in plant development remain poorly understood. Here, we show that
Oryza sativa indica
AGO18 is involved in male gametophyte development. Knockdown (KD) of AGO18 in transgenic rice lines resulted in stunted plants that are male sterile, whereas their carpels were functional. Transcriptome analysis revealed downregulation of several pollen development-associated genes in KD lines. sRNA sequencing in vegetative and reproductive tissues of KD lines indicated reduction of miRNAs and phased secondary sRNAs implicated in male gametophyte development. Our results indicate a distinct role for rice AGO18 in male fertility.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>32157461</pmid><doi>10.1007/s00497-020-00386-w</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-9823-044X</orcidid></addata></record> |
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| ispartof | Plant reproduction, 2020-03, Vol.33 (1), p.59-73 |
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| subjects | Agriculture Analysis Argonaute Proteins - genetics Argonaute Proteins - metabolism Biological evolution Biomedical and Life Sciences Carpels Cell Biology Fertility Gametogenesis Gene Expression Regulation, Plant Gene Knockdown Techniques Gene silencing Genetic engineering Homology Life Sciences Life Sciences & Biomedicine Male sterility MicroRNA MicroRNAs - genetics Original Article Oryza - genetics Oryza sativa indica Plant Sciences Pollen Proteins Reduction Reproduction Reproductive Biology Ribonucleic acid Rice RNA Science & Technology Transgenic plants |
| title | Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs |
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