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Autophagy-mediated degradation of integumentary tapetum is critical for embryo pattern formation
Autophagy modulates the degradation and recycling of intracellular materials and contributes to male gametophyte development and male fertility in plants. However, whether autophagy participates in seed development remains largely unknown. Here, we demonstrate that autophagy is crucial for timely pr...
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Published in: | Nature communications 2024-03, Vol.15 (1), p.2676-2676, Article 2676 |
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description | Autophagy modulates the degradation and recycling of intracellular materials and contributes to male gametophyte development and male fertility in plants. However, whether autophagy participates in seed development remains largely unknown. Here, we demonstrate that autophagy is crucial for timely programmed cell death (PCD) in the integumentary tapetum, the counterpart of anther tapetum, influencing embryo pattern formation and seed viability. Inhibition of autophagy resulted in delayed PCD of the integumentary tapetum and defects in embryo patterning. Cell-type-specific restoration of autophagic activities revealed that the integumentary tapetum plays a non-autonomous role in embryo patterning. Furthermore, high-throughput, comprehensive lipidomic analyzes uncovered an unexpected seed-developmental-stage-dependent role of autophagy in seed lipid metabolism: it contributes to triacylglycerol degradation before fertilization and to triacylglycerol biosynthesis after fertilization. This study highlights the critical role of autophagy in regulating timely integumentary tapetum PCD and reveals its significance in seed lipid metabolism and viability.
A seed consists of an embryo, endosperm, and seed coat. Here the authors show that autophagy plays a crucial role in regulating timely programmed cell death in the innermost seed coat, thereby influencing embryo pattern formation and seed viability. |
doi_str_mv | 10.1038/s41467-024-46902-8 |
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A seed consists of an embryo, endosperm, and seed coat. Here the authors show that autophagy plays a crucial role in regulating timely programmed cell death in the innermost seed coat, thereby influencing embryo pattern formation and seed viability.</description><identifier>ISSN: 2041-1723</identifier><identifier>EISSN: 2041-1723</identifier><identifier>DOI: 10.1038/s41467-024-46902-8</identifier><identifier>PMID: 38538581</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14/19 ; 14/28 ; 14/34 ; 14/63 ; 38/91 ; 631/449/2653 ; 631/449/2679/2682 ; 631/449/448 ; 631/80/39 ; Apoptosis ; Apoptosis - physiology ; Autophagy ; Autophagy - genetics ; Biosynthesis ; Cell death ; Degradation ; Developmental stages ; Embryos ; Endosperm ; Fertility ; Fertilization ; Flowers ; Gene Expression Regulation, Plant ; Humanities and Social Sciences ; Lipid metabolism ; Lipids ; Males ; Metabolism ; multidisciplinary ; Pattern formation ; Patterning ; Pollen - metabolism ; Science ; Science (multidisciplinary) ; Seed coats ; Seeds ; Skin ; Triglycerides ; Triglycerides - metabolism ; Viability</subject><ispartof>Nature communications, 2024-03, Vol.15 (1), p.2676-2676, Article 2676</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>The Author(s) 2024. This work is published 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><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c492t-de567a4e49a3e3b2209c75d8ab908b60dd60a7a4dd4ebe97faf23186a41b72273</cites><orcidid>0009-0006-2729-9024 ; 0009-0003-4829-2671 ; 0009-0000-4049-8876 ; 0000-0003-1904-8955 ; 0009-0007-6638-9564 ; 0009-0002-0766-3651 ; 0000-0002-6959-8405</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/3003349718/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3003349718?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38538581$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhao, Lin-lin</creatorcontrib><creatorcontrib>Chen, Ru</creatorcontrib><creatorcontrib>Bai, Ziyu</creatorcontrib><creatorcontrib>Liu, Junyi</creatorcontrib><creatorcontrib>Zhang, Yuhao</creatorcontrib><creatorcontrib>Zhong, Yicheng</creatorcontrib><creatorcontrib>Sun, Meng-xiang</creatorcontrib><creatorcontrib>Zhao, Peng</creatorcontrib><title>Autophagy-mediated degradation of integumentary tapetum is critical for embryo pattern formation</title><title>Nature communications</title><addtitle>Nat Commun</addtitle><addtitle>Nat Commun</addtitle><description>Autophagy modulates the degradation and recycling of intracellular materials and contributes to male gametophyte development and male fertility in plants. However, whether autophagy participates in seed development remains largely unknown. Here, we demonstrate that autophagy is crucial for timely programmed cell death (PCD) in the integumentary tapetum, the counterpart of anther tapetum, influencing embryo pattern formation and seed viability. Inhibition of autophagy resulted in delayed PCD of the integumentary tapetum and defects in embryo patterning. Cell-type-specific restoration of autophagic activities revealed that the integumentary tapetum plays a non-autonomous role in embryo patterning. Furthermore, high-throughput, comprehensive lipidomic analyzes uncovered an unexpected seed-developmental-stage-dependent role of autophagy in seed lipid metabolism: it contributes to triacylglycerol degradation before fertilization and to triacylglycerol biosynthesis after fertilization. This study highlights the critical role of autophagy in regulating timely integumentary tapetum PCD and reveals its significance in seed lipid metabolism and viability.
A seed consists of an embryo, endosperm, and seed coat. Here the authors show that autophagy plays a crucial role in regulating timely programmed cell death in the innermost seed coat, thereby influencing embryo pattern formation and seed viability.</description><subject>14/19</subject><subject>14/28</subject><subject>14/34</subject><subject>14/63</subject><subject>38/91</subject><subject>631/449/2653</subject><subject>631/449/2679/2682</subject><subject>631/449/448</subject><subject>631/80/39</subject><subject>Apoptosis</subject><subject>Apoptosis - physiology</subject><subject>Autophagy</subject><subject>Autophagy - genetics</subject><subject>Biosynthesis</subject><subject>Cell death</subject><subject>Degradation</subject><subject>Developmental stages</subject><subject>Embryos</subject><subject>Endosperm</subject><subject>Fertility</subject><subject>Fertilization</subject><subject>Flowers</subject><subject>Gene Expression Regulation, Plant</subject><subject>Humanities and Social Sciences</subject><subject>Lipid metabolism</subject><subject>Lipids</subject><subject>Males</subject><subject>Metabolism</subject><subject>multidisciplinary</subject><subject>Pattern formation</subject><subject>Patterning</subject><subject>Pollen - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Nature communications</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhao, Lin-lin</au><au>Chen, Ru</au><au>Bai, Ziyu</au><au>Liu, Junyi</au><au>Zhang, Yuhao</au><au>Zhong, Yicheng</au><au>Sun, Meng-xiang</au><au>Zhao, Peng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Autophagy-mediated degradation of integumentary tapetum is critical for embryo pattern formation</atitle><jtitle>Nature communications</jtitle><stitle>Nat Commun</stitle><addtitle>Nat Commun</addtitle><date>2024-03-27</date><risdate>2024</risdate><volume>15</volume><issue>1</issue><spage>2676</spage><epage>2676</epage><pages>2676-2676</pages><artnum>2676</artnum><issn>2041-1723</issn><eissn>2041-1723</eissn><abstract>Autophagy modulates the degradation and recycling of intracellular materials and contributes to male gametophyte development and male fertility in plants. However, whether autophagy participates in seed development remains largely unknown. Here, we demonstrate that autophagy is crucial for timely programmed cell death (PCD) in the integumentary tapetum, the counterpart of anther tapetum, influencing embryo pattern formation and seed viability. Inhibition of autophagy resulted in delayed PCD of the integumentary tapetum and defects in embryo patterning. Cell-type-specific restoration of autophagic activities revealed that the integumentary tapetum plays a non-autonomous role in embryo patterning. Furthermore, high-throughput, comprehensive lipidomic analyzes uncovered an unexpected seed-developmental-stage-dependent role of autophagy in seed lipid metabolism: it contributes to triacylglycerol degradation before fertilization and to triacylglycerol biosynthesis after fertilization. This study highlights the critical role of autophagy in regulating timely integumentary tapetum PCD and reveals its significance in seed lipid metabolism and viability.
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subjects | 14/19 14/28 14/34 14/63 38/91 631/449/2653 631/449/2679/2682 631/449/448 631/80/39 Apoptosis Apoptosis - physiology Autophagy Autophagy - genetics Biosynthesis Cell death Degradation Developmental stages Embryos Endosperm Fertility Fertilization Flowers Gene Expression Regulation, Plant Humanities and Social Sciences Lipid metabolism Lipids Males Metabolism multidisciplinary Pattern formation Patterning Pollen - metabolism Science Science (multidisciplinary) Seed coats Seeds Skin Triglycerides Triglycerides - metabolism Viability |
title | Autophagy-mediated degradation of integumentary tapetum is critical for embryo pattern formation |
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