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Small RNA sequencing provides candidate miRNA-target pairs for revealing the mechanism of apomixis in Zanthoxylum bungeanum
Apomixis is a form of asexual reproduction that produces offspring without the need for combining male and female gametes, and the offspring have the same genetic makeup as the mother. Therefore, apomixis technology has great application potential in plant breeding. To identify the apomixis types an...
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Published in: | BMC plant biology 2021-04, Vol.21 (1), p.178-178, Article 178 |
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description | Apomixis is a form of asexual reproduction that produces offspring without the need for combining male and female gametes, and the offspring have the same genetic makeup as the mother. Therefore, apomixis technology has great application potential in plant breeding. To identify the apomixis types and critical period, embryonic development at different flower development stages of Zanthoxylum bungeanum was observed by cytology.
The results show that the S3 stage is the critical period of apomixis, during which the nucellar cells develop into an adventitious primordial embryo. Cytological observations showed that the type of apomixis in Z. bungeanum is sporophytic apomixis. Furthermore, miRNA sequencing, miRNA-target gene interaction, dual luciferase reporter assay, and RT-qPCR verification were used to reveal the dynamic regulation of miRNA-target pairs in Z. bungeanum apomixis. The miRNA sequencing identified 96 mature miRNAs, of which 40 were known and 56 were novel. Additionally, 29 differentially expressed miRNAs were screened according to the miRNAs expression levels at the different developmental stages. Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) enrichment analyses showed that the target genes of the differentially expressed miRNAs were mainly enriched in plant hormone signal transduction, RNA biosynthetic process, and response to hormone pathways.
During the critical period of apomictic embryonic development, miR172c significantly reduces the expression levels of TOE3 and APETALA 2 (AP2) genes, thereby upregulating the expression of the AGAMOUS gene. A molecular regulation model of miRNA-target pairs was constructed based on their interactions and expression patterns to further understand the role of miRNA-target pairs in apomixis. Our data suggest that miR172c may regulates AGAMOUS expression by inhibiting TOE3 in the critical period of apomixis. |
doi_str_mv | 10.1186/s12870-021-02935-5 |
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The results show that the S3 stage is the critical period of apomixis, during which the nucellar cells develop into an adventitious primordial embryo. Cytological observations showed that the type of apomixis in Z. bungeanum is sporophytic apomixis. Furthermore, miRNA sequencing, miRNA-target gene interaction, dual luciferase reporter assay, and RT-qPCR verification were used to reveal the dynamic regulation of miRNA-target pairs in Z. bungeanum apomixis. The miRNA sequencing identified 96 mature miRNAs, of which 40 were known and 56 were novel. Additionally, 29 differentially expressed miRNAs were screened according to the miRNAs expression levels at the different developmental stages. Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) enrichment analyses showed that the target genes of the differentially expressed miRNAs were mainly enriched in plant hormone signal transduction, RNA biosynthetic process, and response to hormone pathways.
During the critical period of apomictic embryonic development, miR172c significantly reduces the expression levels of TOE3 and APETALA 2 (AP2) genes, thereby upregulating the expression of the AGAMOUS gene. A molecular regulation model of miRNA-target pairs was constructed based on their interactions and expression patterns to further understand the role of miRNA-target pairs in apomixis. Our data suggest that miR172c may regulates AGAMOUS expression by inhibiting TOE3 in the critical period of apomixis.</description><identifier>ISSN: 1471-2229</identifier><identifier>EISSN: 1471-2229</identifier><identifier>DOI: 10.1186/s12870-021-02935-5</identifier><identifier>PMID: 33849456</identifier><language>eng</language><publisher>England: BioMed Central</publisher><subject>AGAMOUS ; AGAMOUS gene ; Apomixis ; Apomixis - genetics ; Asexual reproduction ; Critical period ; Cytology ; Developmental stages ; Embryogenesis ; Embryonic growth stage ; Embryos ; Encyclopedias ; Flowers - growth & development ; Gametes ; Gene expression ; Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Gene sequencing ; Genes ; Genomes ; MicroRNAs - genetics ; miR172 ; miRNA ; miRNA-target pairs ; Offspring ; Plant Breeding ; Plant hormones ; Principal components analysis ; Ribonucleic acid ; RNA ; RNA, Plant - genetics ; Seeds - embryology ; Sequence Analysis, RNA ; Signal processing ; Signal transduction ; TOE3 ; Zanthoxylum - embryology ; Zanthoxylum - genetics ; Zanthoxylum - physiology ; Zanthoxylum bungeanum</subject><ispartof>BMC plant biology, 2021-04, Vol.21 (1), p.178-178, Article 178</ispartof><rights>2021. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c496t-cafd9f073c8db27cde314794442885a46b099c670e24ef9b8c895fc2e573a2b33</citedby><cites>FETCH-LOGICAL-c496t-cafd9f073c8db27cde314794442885a46b099c670e24ef9b8c895fc2e573a2b33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042946/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2514800843?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33849456$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fei, Xitong</creatorcontrib><creatorcontrib>Lei, Yu</creatorcontrib><creatorcontrib>Qi, Yichen</creatorcontrib><creatorcontrib>Wang, Shujie</creatorcontrib><creatorcontrib>Hu, Haichao</creatorcontrib><creatorcontrib>Wei, Anzhi</creatorcontrib><title>Small RNA sequencing provides candidate miRNA-target pairs for revealing the mechanism of apomixis in Zanthoxylum bungeanum</title><title>BMC plant biology</title><addtitle>BMC Plant Biol</addtitle><description>Apomixis is a form of asexual reproduction that produces offspring without the need for combining male and female gametes, and the offspring have the same genetic makeup as the mother. Therefore, apomixis technology has great application potential in plant breeding. To identify the apomixis types and critical period, embryonic development at different flower development stages of Zanthoxylum bungeanum was observed by cytology.
The results show that the S3 stage is the critical period of apomixis, during which the nucellar cells develop into an adventitious primordial embryo. Cytological observations showed that the type of apomixis in Z. bungeanum is sporophytic apomixis. Furthermore, miRNA sequencing, miRNA-target gene interaction, dual luciferase reporter assay, and RT-qPCR verification were used to reveal the dynamic regulation of miRNA-target pairs in Z. bungeanum apomixis. The miRNA sequencing identified 96 mature miRNAs, of which 40 were known and 56 were novel. Additionally, 29 differentially expressed miRNAs were screened according to the miRNAs expression levels at the different developmental stages. Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) enrichment analyses showed that the target genes of the differentially expressed miRNAs were mainly enriched in plant hormone signal transduction, RNA biosynthetic process, and response to hormone pathways.
During the critical period of apomictic embryonic development, miR172c significantly reduces the expression levels of TOE3 and APETALA 2 (AP2) genes, thereby upregulating the expression of the AGAMOUS gene. A molecular regulation model of miRNA-target pairs was constructed based on their interactions and expression patterns to further understand the role of miRNA-target pairs in apomixis. Our data suggest that miR172c may regulates AGAMOUS expression by inhibiting TOE3 in the critical period of apomixis.</description><subject>AGAMOUS</subject><subject>AGAMOUS gene</subject><subject>Apomixis</subject><subject>Apomixis - genetics</subject><subject>Asexual reproduction</subject><subject>Critical period</subject><subject>Cytology</subject><subject>Developmental stages</subject><subject>Embryogenesis</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>Encyclopedias</subject><subject>Flowers - growth & development</subject><subject>Gametes</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genomes</subject><subject>MicroRNAs - genetics</subject><subject>miR172</subject><subject>miRNA</subject><subject>miRNA-target pairs</subject><subject>Offspring</subject><subject>Plant Breeding</subject><subject>Plant hormones</subject><subject>Principal components analysis</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Plant - genetics</subject><subject>Seeds - embryology</subject><subject>Sequence Analysis, RNA</subject><subject>Signal processing</subject><subject>Signal transduction</subject><subject>TOE3</subject><subject>Zanthoxylum - embryology</subject><subject>Zanthoxylum - genetics</subject><subject>Zanthoxylum - physiology</subject><subject>Zanthoxylum bungeanum</subject><issn>1471-2229</issn><issn>1471-2229</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpdkk1v1DAQhiMEoqXwBzggS1y4BPyVxL4gVRWUShVIfFy4WBNnvOtVYi92smrFn6-3W6qWgzWW_cyreUdvVb1m9D1jqv2QGVcdrSln5WjR1M2T6pjJjtWcc_30wf2oepHzhlLWKamfV0dClCqb9rj6-2OCcSTfv56SjH8WDNaHFdmmuPMDZmIhDH6AGcnkC1PPkFY4ky34lImLiSTcIYz7nnldILRrCD5PJDoC2zj5K5-JD-Q3hHkdr67HZSL9ElYIYZleVs8cjBlf3dWT6tfnTz_PvtSX384vzk4vayt1O9cW3KAd7YRVQ887O6AoxrSUkivVgGx7qrVtO4pcotO9sko3znJsOgG8F-KkujjoDhE2Zpv8BOnaRPDm9iGmlYE0ezuiAYl9i-gkU73s0IFQTFvkCK2VbeOK1seD1nbpJxwshjnB-Ej08U_wa7OKO6Oo5Fq2ReDdnUCKZd95NpPPFscRAsYlG94w3kkmNC_o2__QTVxSKKvaU1JRquTeHT9QNsWcE7r7YRg1-5yYQ05MyYm5zYlpStObhzbuW_4FQ9wAO3G7jg</recordid><startdate>20210413</startdate><enddate>20210413</enddate><creator>Fei, Xitong</creator><creator>Lei, Yu</creator><creator>Qi, Yichen</creator><creator>Wang, Shujie</creator><creator>Hu, Haichao</creator><creator>Wei, Anzhi</creator><general>BioMed Central</general><general>BMC</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>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</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>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20210413</creationdate><title>Small RNA sequencing provides candidate miRNA-target pairs for revealing the mechanism of apomixis in Zanthoxylum bungeanum</title><author>Fei, Xitong ; Lei, Yu ; Qi, Yichen ; Wang, Shujie ; Hu, Haichao ; Wei, Anzhi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c496t-cafd9f073c8db27cde314794442885a46b099c670e24ef9b8c895fc2e573a2b33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>AGAMOUS</topic><topic>AGAMOUS gene</topic><topic>Apomixis</topic><topic>Apomixis - genetics</topic><topic>Asexual reproduction</topic><topic>Critical period</topic><topic>Cytology</topic><topic>Developmental stages</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Embryos</topic><topic>Encyclopedias</topic><topic>Flowers - growth & development</topic><topic>Gametes</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Genomes</topic><topic>MicroRNAs - genetics</topic><topic>miR172</topic><topic>miRNA</topic><topic>miRNA-target pairs</topic><topic>Offspring</topic><topic>Plant Breeding</topic><topic>Plant hormones</topic><topic>Principal components analysis</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA, Plant - genetics</topic><topic>Seeds - embryology</topic><topic>Sequence Analysis, RNA</topic><topic>Signal processing</topic><topic>Signal transduction</topic><topic>TOE3</topic><topic>Zanthoxylum - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>BMC plant biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fei, Xitong</au><au>Lei, Yu</au><au>Qi, Yichen</au><au>Wang, Shujie</au><au>Hu, Haichao</au><au>Wei, Anzhi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Small RNA sequencing provides candidate miRNA-target pairs for revealing the mechanism of apomixis in Zanthoxylum bungeanum</atitle><jtitle>BMC plant biology</jtitle><addtitle>BMC Plant Biol</addtitle><date>2021-04-13</date><risdate>2021</risdate><volume>21</volume><issue>1</issue><spage>178</spage><epage>178</epage><pages>178-178</pages><artnum>178</artnum><issn>1471-2229</issn><eissn>1471-2229</eissn><abstract>Apomixis is a form of asexual reproduction that produces offspring without the need for combining male and female gametes, and the offspring have the same genetic makeup as the mother. Therefore, apomixis technology has great application potential in plant breeding. To identify the apomixis types and critical period, embryonic development at different flower development stages of Zanthoxylum bungeanum was observed by cytology.
The results show that the S3 stage is the critical period of apomixis, during which the nucellar cells develop into an adventitious primordial embryo. Cytological observations showed that the type of apomixis in Z. bungeanum is sporophytic apomixis. Furthermore, miRNA sequencing, miRNA-target gene interaction, dual luciferase reporter assay, and RT-qPCR verification were used to reveal the dynamic regulation of miRNA-target pairs in Z. bungeanum apomixis. The miRNA sequencing identified 96 mature miRNAs, of which 40 were known and 56 were novel. Additionally, 29 differentially expressed miRNAs were screened according to the miRNAs expression levels at the different developmental stages. Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) enrichment analyses showed that the target genes of the differentially expressed miRNAs were mainly enriched in plant hormone signal transduction, RNA biosynthetic process, and response to hormone pathways.
During the critical period of apomictic embryonic development, miR172c significantly reduces the expression levels of TOE3 and APETALA 2 (AP2) genes, thereby upregulating the expression of the AGAMOUS gene. A molecular regulation model of miRNA-target pairs was constructed based on their interactions and expression patterns to further understand the role of miRNA-target pairs in apomixis. Our data suggest that miR172c may regulates AGAMOUS expression by inhibiting TOE3 in the critical period of apomixis.</abstract><cop>England</cop><pub>BioMed Central</pub><pmid>33849456</pmid><doi>10.1186/s12870-021-02935-5</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | AGAMOUS AGAMOUS gene Apomixis Apomixis - genetics Asexual reproduction Critical period Cytology Developmental stages Embryogenesis Embryonic growth stage Embryos Encyclopedias Flowers - growth & development Gametes Gene expression Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Gene sequencing Genes Genomes MicroRNAs - genetics miR172 miRNA miRNA-target pairs Offspring Plant Breeding Plant hormones Principal components analysis Ribonucleic acid RNA RNA, Plant - genetics Seeds - embryology Sequence Analysis, RNA Signal processing Signal transduction TOE3 Zanthoxylum - embryology Zanthoxylum - genetics Zanthoxylum - physiology Zanthoxylum bungeanum |
title | Small RNA sequencing provides candidate miRNA-target pairs for revealing the mechanism of apomixis in Zanthoxylum bungeanum |
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