Polyamines Involved in Regulating Self-Incompatibility in Apple
Apple exhibits typical gametophytic self-incompatibility, in which self-S-RNase can arrest pollen tube growth, leading to failure of fertilization. To date, there have been few studies on how to resist the toxicity of self-S-RNase. In this study, pollen tube polyamines were found to respond to self-...
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Veröffentlicht in: | Genes 2021-11, Vol.12 (11), p.1797, Article 1797 |
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description | Apple exhibits typical gametophytic self-incompatibility, in which self-S-RNase can arrest pollen tube growth, leading to failure of fertilization. To date, there have been few studies on how to resist the toxicity of self-S-RNase. In this study, pollen tube polyamines were found to respond to self-S-RNase and help pollen tubes defend against self-S-RNase. In particular, the contents of putrescine, spermidine, and spermine in the pollen tube treated with self-S-RNase were substantially lower than those treated with non-self-S-RNase. Further analysis of gene expression of key enzymes in the synthesis and degradation pathways of polyamines found that the expression of DIAMINE OXIDASE 4 (MdDAO4) as well as several polyamine oxidases such as POLYAMINE OXIDASES 3 (MdPAO3), POLYAMINE OXIDASES 4 (MdPAO4), and POLYAMINE OXIDASES 6 (MdPAO6) were significantly up-regulated under self-S-RNase treatment, resulting in the reduction of polyamines. Silencing MdPAO6 in pollen tubes alleviates the inhibitory effect of self-S-RNase on pollen tube growth. In addition, exogenous polyamines also enhance pollen tube resistance to self-S-RNase. Transcriptome sequencing data found that polyamines may communicate with S-RNase through the calcium signal pathway, thereby regulating the growth of the pollen tubes. To summarize, our results suggested that polyamines responded to the self-incompatibility reaction and could enhance pollen tube tolerance to S-RNase, thus providing a potential way to break self-incompatibility in apple. |
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To date, there have been few studies on how to resist the toxicity of self-S-RNase. In this study, pollen tube polyamines were found to respond to self-S-RNase and help pollen tubes defend against self-S-RNase. In particular, the contents of putrescine, spermidine, and spermine in the pollen tube treated with self-S-RNase were substantially lower than those treated with non-self-S-RNase. Further analysis of gene expression of key enzymes in the synthesis and degradation pathways of polyamines found that the expression of DIAMINE OXIDASE 4 (MdDAO4) as well as several polyamine oxidases such as POLYAMINE OXIDASES 3 (MdPAO3), POLYAMINE OXIDASES 4 (MdPAO4), and POLYAMINE OXIDASES 6 (MdPAO6) were significantly up-regulated under self-S-RNase treatment, resulting in the reduction of polyamines. Silencing MdPAO6 in pollen tubes alleviates the inhibitory effect of self-S-RNase on pollen tube growth. In addition, exogenous polyamines also enhance pollen tube resistance to self-S-RNase. Transcriptome sequencing data found that polyamines may communicate with S-RNase through the calcium signal pathway, thereby regulating the growth of the pollen tubes. To summarize, our results suggested that polyamines responded to the self-incompatibility reaction and could enhance pollen tube tolerance to S-RNase, thus providing a potential way to break self-incompatibility in apple.</description><identifier>ISSN: 2073-4425</identifier><identifier>EISSN: 2073-4425</identifier><identifier>DOI: 10.3390/genes12111797</identifier><identifier>PMID: 34828403</identifier><language>eng</language><publisher>BASEL: Mdpi</publisher><subject>Calcium signalling ; Catalysis ; Caustic soda ; Cell division ; Dehydrogenases ; Fertility ; Fertilization ; Gene expression ; Genetics & Heredity ; Life Sciences & Biomedicine ; Malus - genetics ; Malus - metabolism ; Malus - physiology ; Metabolism ; Oxidoreductases Acting on CH-NH Group Donors - genetics ; Oxidoreductases Acting on CH-NH Group Donors - metabolism ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant reproduction ; Pollen - genetics ; Pollen - metabolism ; Pollen - physiology ; Pollen tubes ; Polyamine Oxidase ; Polyamines ; Polyamines - metabolism ; Proteins ; Putrescine ; Science & Technology ; Seeds ; Self-incompatibility ; Self-Incompatibility in Flowering Plants ; Spermidine ; Spermine ; Toxicity ; Transcriptomes</subject><ispartof>Genes, 2021-11, Vol.12 (11), p.1797, Article 1797</ispartof><rights>2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 by the authors. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>7</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000723416100001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c415t-244cc00b485164afe43cc8d2ec3dd27835128e69ca2507f876b3da75c5a409fd3</citedby><cites>FETCH-LOGICAL-c415t-244cc00b485164afe43cc8d2ec3dd27835128e69ca2507f876b3da75c5a409fd3</cites><orcidid>0000-0002-9805-8707</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8620888/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8620888/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,886,27928,27929,53795,53797</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34828403$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Jie</creatorcontrib><creatorcontrib>Wang, Baoan</creatorcontrib><creatorcontrib>Fan, Wenqi</creatorcontrib><creatorcontrib>Fan, Songbo</creatorcontrib><creatorcontrib>Xu, Ya</creatorcontrib><creatorcontrib>Liu, Chunsheng</creatorcontrib><creatorcontrib>Lv, Tianxing</creatorcontrib><creatorcontrib>Liu, Wanda</creatorcontrib><creatorcontrib>Wu, Ling</creatorcontrib><creatorcontrib>Xian, Linfeng</creatorcontrib><creatorcontrib>Li, Tianzhong</creatorcontrib><title>Polyamines Involved in Regulating Self-Incompatibility in Apple</title><title>Genes</title><addtitle>GENES-BASEL</addtitle><addtitle>Genes (Basel)</addtitle><description>Apple exhibits typical gametophytic self-incompatibility, in which self-S-RNase can arrest pollen tube growth, leading to failure of fertilization. To date, there have been few studies on how to resist the toxicity of self-S-RNase. In this study, pollen tube polyamines were found to respond to self-S-RNase and help pollen tubes defend against self-S-RNase. In particular, the contents of putrescine, spermidine, and spermine in the pollen tube treated with self-S-RNase were substantially lower than those treated with non-self-S-RNase. Further analysis of gene expression of key enzymes in the synthesis and degradation pathways of polyamines found that the expression of DIAMINE OXIDASE 4 (MdDAO4) as well as several polyamine oxidases such as POLYAMINE OXIDASES 3 (MdPAO3), POLYAMINE OXIDASES 4 (MdPAO4), and POLYAMINE OXIDASES 6 (MdPAO6) were significantly up-regulated under self-S-RNase treatment, resulting in the reduction of polyamines. Silencing MdPAO6 in pollen tubes alleviates the inhibitory effect of self-S-RNase on pollen tube growth. In addition, exogenous polyamines also enhance pollen tube resistance to self-S-RNase. Transcriptome sequencing data found that polyamines may communicate with S-RNase through the calcium signal pathway, thereby regulating the growth of the pollen tubes. To summarize, our results suggested that polyamines responded to the self-incompatibility reaction and could enhance pollen tube tolerance to S-RNase, thus providing a potential way to break self-incompatibility in apple.</description><subject>Calcium signalling</subject><subject>Catalysis</subject><subject>Caustic soda</subject><subject>Cell division</subject><subject>Dehydrogenases</subject><subject>Fertility</subject><subject>Fertilization</subject><subject>Gene expression</subject><subject>Genetics & Heredity</subject><subject>Life Sciences & Biomedicine</subject><subject>Malus - genetics</subject><subject>Malus - metabolism</subject><subject>Malus - physiology</subject><subject>Metabolism</subject><subject>Oxidoreductases Acting on CH-NH Group Donors - genetics</subject><subject>Oxidoreductases Acting on CH-NH Group Donors - metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant reproduction</subject><subject>Pollen - genetics</subject><subject>Pollen - metabolism</subject><subject>Pollen - physiology</subject><subject>Pollen tubes</subject><subject>Polyamine Oxidase</subject><subject>Polyamines</subject><subject>Polyamines - metabolism</subject><subject>Proteins</subject><subject>Putrescine</subject><subject>Science & Technology</subject><subject>Seeds</subject><subject>Self-incompatibility</subject><subject>Self-Incompatibility in Flowering Plants</subject><subject>Spermidine</subject><subject>Spermine</subject><subject>Toxicity</subject><subject>Transcriptomes</subject><issn>2073-4425</issn><issn>2073-4425</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>HGBXW</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkdtLwzAUh4Mobsw9-ioDH6WaW9vsRRnFy2CgeHkOaXpaM7qk9jLZf2_m5tjezEtC8p1fDt9B6Jzga8bG-KYACw2hhJB4HB-hPsUxCzin4fHeuYeGTTPHfnFMMQ5PUY9xQQXHrI_uXly5Ugvjc0ZTu3TlErKRsaNXKLpStcYWozco82BqtVtU_iI1pWlXa2RSVSWcoZNclQ0Mt_sAfTzcvydPwez5cZpMZoHmJGwDyrnWGKdchCTiKgfOtBYZBc2yjMaChYQKiMZa0RDHuYijlGUqDnWoOB7nGRug201u1aULyDTYtlalrGqzUPVKOmXk4Ys1n7JwSykiioUQPuByG1C7rw6aVs5dV1vfs6SR98IF_qWCDaVr1zQ15LsfCJZr5fJAuecv9tva0X-CPSA2wDekLm-0Aathh_mZxJRxEpH1eEhiWm_Y2cR1tvWlV_8vZT-yjp3Q</recordid><startdate>20211115</startdate><enddate>20211115</enddate><creator>Yu, Jie</creator><creator>Wang, Baoan</creator><creator>Fan, Wenqi</creator><creator>Fan, Songbo</creator><creator>Xu, Ya</creator><creator>Liu, Chunsheng</creator><creator>Lv, Tianxing</creator><creator>Liu, Wanda</creator><creator>Wu, Ling</creator><creator>Xian, Linfeng</creator><creator>Li, Tianzhong</creator><general>Mdpi</general><general>MDPI AG</general><general>MDPI</general><scope>BLEPL</scope><scope>DTL</scope><scope>HGBXW</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>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9805-8707</orcidid></search><sort><creationdate>20211115</creationdate><title>Polyamines Involved in Regulating Self-Incompatibility in Apple</title><author>Yu, Jie ; Wang, Baoan ; Fan, Wenqi ; Fan, Songbo ; Xu, Ya ; Liu, Chunsheng ; Lv, Tianxing ; Liu, Wanda ; Wu, Ling ; Xian, Linfeng ; Li, Tianzhong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c415t-244cc00b485164afe43cc8d2ec3dd27835128e69ca2507f876b3da75c5a409fd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Calcium signalling</topic><topic>Catalysis</topic><topic>Caustic soda</topic><topic>Cell division</topic><topic>Dehydrogenases</topic><topic>Fertility</topic><topic>Fertilization</topic><topic>Gene expression</topic><topic>Genetics & Heredity</topic><topic>Life Sciences & Biomedicine</topic><topic>Malus - genetics</topic><topic>Malus - metabolism</topic><topic>Malus - physiology</topic><topic>Metabolism</topic><topic>Oxidoreductases Acting on CH-NH Group Donors - genetics</topic><topic>Oxidoreductases Acting on CH-NH Group Donors - metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant reproduction</topic><topic>Pollen - genetics</topic><topic>Pollen - metabolism</topic><topic>Pollen - physiology</topic><topic>Pollen tubes</topic><topic>Polyamine Oxidase</topic><topic>Polyamines</topic><topic>Polyamines - metabolism</topic><topic>Proteins</topic><topic>Putrescine</topic><topic>Science & Technology</topic><topic>Seeds</topic><topic>Self-incompatibility</topic><topic>Self-Incompatibility in Flowering Plants</topic><topic>Spermidine</topic><topic>Spermine</topic><topic>Toxicity</topic><topic>Transcriptomes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yu, Jie</creatorcontrib><creatorcontrib>Wang, Baoan</creatorcontrib><creatorcontrib>Fan, Wenqi</creatorcontrib><creatorcontrib>Fan, Songbo</creatorcontrib><creatorcontrib>Xu, Ya</creatorcontrib><creatorcontrib>Liu, Chunsheng</creatorcontrib><creatorcontrib>Lv, Tianxing</creatorcontrib><creatorcontrib>Liu, Wanda</creatorcontrib><creatorcontrib>Wu, Ling</creatorcontrib><creatorcontrib>Xian, Linfeng</creatorcontrib><creatorcontrib>Li, Tianzhong</creatorcontrib><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Web of Science - Science Citation Index Expanded - 2021</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</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>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Access via ProQuest (Open Access)</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 China</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genes</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yu, Jie</au><au>Wang, Baoan</au><au>Fan, Wenqi</au><au>Fan, Songbo</au><au>Xu, Ya</au><au>Liu, Chunsheng</au><au>Lv, Tianxing</au><au>Liu, Wanda</au><au>Wu, Ling</au><au>Xian, Linfeng</au><au>Li, Tianzhong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Polyamines Involved in Regulating Self-Incompatibility in Apple</atitle><jtitle>Genes</jtitle><stitle>GENES-BASEL</stitle><addtitle>Genes (Basel)</addtitle><date>2021-11-15</date><risdate>2021</risdate><volume>12</volume><issue>11</issue><spage>1797</spage><pages>1797-</pages><artnum>1797</artnum><issn>2073-4425</issn><eissn>2073-4425</eissn><abstract>Apple exhibits typical gametophytic self-incompatibility, in which self-S-RNase can arrest pollen tube growth, leading to failure of fertilization. To date, there have been few studies on how to resist the toxicity of self-S-RNase. In this study, pollen tube polyamines were found to respond to self-S-RNase and help pollen tubes defend against self-S-RNase. In particular, the contents of putrescine, spermidine, and spermine in the pollen tube treated with self-S-RNase were substantially lower than those treated with non-self-S-RNase. Further analysis of gene expression of key enzymes in the synthesis and degradation pathways of polyamines found that the expression of DIAMINE OXIDASE 4 (MdDAO4) as well as several polyamine oxidases such as POLYAMINE OXIDASES 3 (MdPAO3), POLYAMINE OXIDASES 4 (MdPAO4), and POLYAMINE OXIDASES 6 (MdPAO6) were significantly up-regulated under self-S-RNase treatment, resulting in the reduction of polyamines. Silencing MdPAO6 in pollen tubes alleviates the inhibitory effect of self-S-RNase on pollen tube growth. In addition, exogenous polyamines also enhance pollen tube resistance to self-S-RNase. Transcriptome sequencing data found that polyamines may communicate with S-RNase through the calcium signal pathway, thereby regulating the growth of the pollen tubes. To summarize, our results suggested that polyamines responded to the self-incompatibility reaction and could enhance pollen tube tolerance to S-RNase, thus providing a potential way to break self-incompatibility in apple.</abstract><cop>BASEL</cop><pub>Mdpi</pub><pmid>34828403</pmid><doi>10.3390/genes12111797</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-9805-8707</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Calcium signalling Catalysis Caustic soda Cell division Dehydrogenases Fertility Fertilization Gene expression Genetics & Heredity Life Sciences & Biomedicine Malus - genetics Malus - metabolism Malus - physiology Metabolism Oxidoreductases Acting on CH-NH Group Donors - genetics Oxidoreductases Acting on CH-NH Group Donors - metabolism Plant Proteins - genetics Plant Proteins - metabolism Plant reproduction Pollen - genetics Pollen - metabolism Pollen - physiology Pollen tubes Polyamine Oxidase Polyamines Polyamines - metabolism Proteins Putrescine Science & Technology Seeds Self-incompatibility Self-Incompatibility in Flowering Plants Spermidine Spermine Toxicity Transcriptomes |
title | Polyamines Involved in Regulating Self-Incompatibility in Apple |
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