Hidden fairy rings and males—Genetic patterns of natural Burgundy truffle (Tuber aestivum Vittad.) populations reveal new insights into its life cycle
Burgundy truffles are heterothallic ascomycetes that grow in symbiosis with trees. Despite their esteemed belowground fruitbodies, the species' complex lifecycle is still not fully understood. Here, we present the genetic patterns in three natural Burgundy truffle populations based on genotyped...
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Veröffentlicht in: | Environmental microbiology 2022-12, Vol.24 (12), p.6376-6391 |
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creator | Staubli, Florian Imola, Lea Dauphin, Benjamin Molinier, Virginie Pfister, Stephanie Piñuela, Yasmine Schürz, Laura Sproll, Ludger Steidinger, Brian S. Stobbe, Uli Tegel, Willy Büntgen, Ulf Egli, Simon Peter, Martina |
description | Burgundy truffles are heterothallic ascomycetes that grow in symbiosis with trees. Despite their esteemed belowground fruitbodies, the species' complex lifecycle is still not fully understood. Here, we present the genetic patterns in three natural Burgundy truffle populations based on genotyped fruitbodies, ascospore extracts and ectomycorrhizal root tips using microsatellites and the mating‐type locus. Distinct genetic structures with high relatedness in close vicinity were found for females (forming the fruitbodies) and males (fertilizing partner as inferred from ascospore extracts), with high genotypic diversity and annual turnover of males, suggesting that ephemeral male mating partners are germinating ascospores from decaying fruitbodies. The presence of hermaphrodites and the interannual persistence of a few males suggest that persistent mycelia may sporadically also act as males. Only female or hermaphroditic individuals were detected on root tips. At one site, fruitbodies grew in a fairy ring formed by a large female individual that showed an outward growth rate of 30 cm per year, with the mycelium decaying within the ring and being fertilized by over 50 male individuals. While fairy ring structures have never been shown for truffles, the genetics of Burgundy truffle populations support a similar reproductive biology as those of other highly prized truffles. |
doi_str_mv | 10.1111/1462-2920.16131 |
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Despite their esteemed belowground fruitbodies, the species' complex lifecycle is still not fully understood. Here, we present the genetic patterns in three natural Burgundy truffle populations based on genotyped fruitbodies, ascospore extracts and ectomycorrhizal root tips using microsatellites and the mating‐type locus. Distinct genetic structures with high relatedness in close vicinity were found for females (forming the fruitbodies) and males (fertilizing partner as inferred from ascospore extracts), with high genotypic diversity and annual turnover of males, suggesting that ephemeral male mating partners are germinating ascospores from decaying fruitbodies. The presence of hermaphrodites and the interannual persistence of a few males suggest that persistent mycelia may sporadically also act as males. Only female or hermaphroditic individuals were detected on root tips. At one site, fruitbodies grew in a fairy ring formed by a large female individual that showed an outward growth rate of 30 cm per year, with the mycelium decaying within the ring and being fertilized by over 50 male individuals. While fairy ring structures have never been shown for truffles, the genetics of Burgundy truffle populations support a similar reproductive biology as those of other highly prized truffles.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.16131</identifier><identifier>PMID: 35837848</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Animals ; Ascomycota - genetics ; Ascospores ; Biology ; Ectomycorrhizas ; Fairy rings ; Females ; Fruit bodies ; Genetics ; Growth rate ; Hermaphrodites ; Hermaphroditism ; Humans ; Life cycle ; Life cycle analysis ; Life Cycle Stages ; Life cycles ; Male ; Males ; Mating ; Microsatellites ; Mycorrhizae - genetics ; Populations ; Reproductive behaviour ; Ring structures ; Symbiosis ; Tips</subject><ispartof>Environmental microbiology, 2022-12, Vol.24 (12), p.6376-6391</ispartof><rights>2022 The Authors. published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2022 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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Despite their esteemed belowground fruitbodies, the species' complex lifecycle is still not fully understood. Here, we present the genetic patterns in three natural Burgundy truffle populations based on genotyped fruitbodies, ascospore extracts and ectomycorrhizal root tips using microsatellites and the mating‐type locus. Distinct genetic structures with high relatedness in close vicinity were found for females (forming the fruitbodies) and males (fertilizing partner as inferred from ascospore extracts), with high genotypic diversity and annual turnover of males, suggesting that ephemeral male mating partners are germinating ascospores from decaying fruitbodies. The presence of hermaphrodites and the interannual persistence of a few males suggest that persistent mycelia may sporadically also act as males. Only female or hermaphroditic individuals were detected on root tips. At one site, fruitbodies grew in a fairy ring formed by a large female individual that showed an outward growth rate of 30 cm per year, with the mycelium decaying within the ring and being fertilized by over 50 male individuals. While fairy ring structures have never been shown for truffles, the genetics of Burgundy truffle populations support a similar reproductive biology as those of other highly prized truffles.</description><subject>Animals</subject><subject>Ascomycota - genetics</subject><subject>Ascospores</subject><subject>Biology</subject><subject>Ectomycorrhizas</subject><subject>Fairy rings</subject><subject>Females</subject><subject>Fruit bodies</subject><subject>Genetics</subject><subject>Growth rate</subject><subject>Hermaphrodites</subject><subject>Hermaphroditism</subject><subject>Humans</subject><subject>Life cycle</subject><subject>Life cycle analysis</subject><subject>Life Cycle Stages</subject><subject>Life cycles</subject><subject>Male</subject><subject>Males</subject><subject>Mating</subject><subject>Microsatellites</subject><subject>Mycorrhizae - genetics</subject><subject>Populations</subject><subject>Reproductive behaviour</subject><subject>Ring structures</subject><subject>Symbiosis</subject><subject>Tips</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNqFkbtuFDEUhkcIRC5Q0yFLNKHYxLfxzFQoRCGJFEQTaC3vzPHGkccefNloOh6CIs_Hk-BlwwpocONj-zv_8a-_ql4RfEzKOiFc0AXtaDkKwsiTan9383RXE7pXHcR4hzFpWIOfV3usblnT8na_erg0wwAOaWXCjIJxq4iUG9CoLMQf375fgINkejSplCC4iLxGTqUclEXvc1hlN8wohay1BXR0k5cQkIKYzDqP6ItJSQ3Hb9Hkp2xVMr4IBFhDaXZwj4yLZnWbYimSR6YU1mhA_dxbeFE908pGePm4H1afP5zfnF0urj9dXJ2dXi96Llqy0A3BuMYDUxx4K4D3bOBLClzoRi-5ghYz0VNOByIwxxjqjnFei64TnGKq2WH1bqs75eUIQw8uFW9yCmZUYZZeGfn3izO3cuXXssxtOee0KBw9KgT_NRfvcjSxB2uVA5-jpKIjuIxtNuibf9A7n4Mr_iRt6prjtsa8UCdbqg8-xgB69xuC5SZ2uQlWbkKWv2IvHa__NLHjf-dcgHoL3BsL8__05PnHq63wT1cBubY</recordid><startdate>202212</startdate><enddate>202212</enddate><creator>Staubli, Florian</creator><creator>Imola, Lea</creator><creator>Dauphin, Benjamin</creator><creator>Molinier, Virginie</creator><creator>Pfister, Stephanie</creator><creator>Piñuela, Yasmine</creator><creator>Schürz, Laura</creator><creator>Sproll, Ludger</creator><creator>Steidinger, Brian S.</creator><creator>Stobbe, Uli</creator><creator>Tegel, Willy</creator><creator>Büntgen, Ulf</creator><creator>Egli, Simon</creator><creator>Peter, Martina</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</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>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0982-4252</orcidid><orcidid>https://orcid.org/0000-0003-1001-7642</orcidid><orcidid>https://orcid.org/0000-0002-6365-6889</orcidid><orcidid>https://orcid.org/0000-0002-3821-0818</orcidid><orcidid>https://orcid.org/0000-0003-4707-2848</orcidid><orcidid>https://orcid.org/0000-0002-6674-4323</orcidid></search><sort><creationdate>202212</creationdate><title>Hidden fairy rings and males—Genetic patterns of natural Burgundy truffle (Tuber aestivum Vittad.) populations reveal new insights into its life cycle</title><author>Staubli, Florian ; 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At one site, fruitbodies grew in a fairy ring formed by a large female individual that showed an outward growth rate of 30 cm per year, with the mycelium decaying within the ring and being fertilized by over 50 male individuals. While fairy ring structures have never been shown for truffles, the genetics of Burgundy truffle populations support a similar reproductive biology as those of other highly prized truffles.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>35837848</pmid><doi>10.1111/1462-2920.16131</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-0982-4252</orcidid><orcidid>https://orcid.org/0000-0003-1001-7642</orcidid><orcidid>https://orcid.org/0000-0002-6365-6889</orcidid><orcidid>https://orcid.org/0000-0002-3821-0818</orcidid><orcidid>https://orcid.org/0000-0003-4707-2848</orcidid><orcidid>https://orcid.org/0000-0002-6674-4323</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Ascomycota - genetics Ascospores Biology Ectomycorrhizas Fairy rings Females Fruit bodies Genetics Growth rate Hermaphrodites Hermaphroditism Humans Life cycle Life cycle analysis Life Cycle Stages Life cycles Male Males Mating Microsatellites Mycorrhizae - genetics Populations Reproductive behaviour Ring structures Symbiosis Tips |
title | Hidden fairy rings and males—Genetic patterns of natural Burgundy truffle (Tuber aestivum Vittad.) populations reveal new insights into its life cycle |
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