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
Hauptverfasser: Yu, Jie, Wang, Baoan, Fan, Wenqi, Fan, Songbo, Xu, Ya, Liu, Chunsheng, Lv, Tianxing, Liu, Wanda, Wu, Ling, Xian, Linfeng, Li, Tianzhong
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container_end_page
container_issue 11
container_start_page 1797
container_title Genes
container_volume 12
creator Yu, Jie
Wang, Baoan
Fan, Wenqi
Fan, Songbo
Xu, Ya
Liu, Chunsheng
Lv, Tianxing
Liu, Wanda
Wu, Ling
Xian, Linfeng
Li, Tianzhong
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.
doi_str_mv 10.3390/genes12111797
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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. 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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/). 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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. 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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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