352 lines
46 KiB
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352 lines
46 KiB
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<document id="86C51178E9A5316913FE3489E04C578D" ID-CLB-Dataset="6312" ID-DOI="10.11646/phytotaxa.9.1.13" ID-GBIF-Dataset="21a2a91a-28ae-40c8-911e-13d0c279e095" ID-ISSN="1179-3163" ID-Zenodo-Dep="4895360" IM.metadata_approvedBy="felipe" IM.taxonomicNames_approvedBy="felipe" checkinTime="1621604093317" checkinUser="felipe" docAuthor="Pressel, Silvia, Bidartondo, Martin I., Ligrone, Roberto & Duckett, Jeffrey G." docDate="2010" docId="03F587D3FFD4B945B5974CB4FD26FCA8" docLanguage="en" docName="Phytotaxa.9.238-253.pdf" docOrigin="Phytotaxa 9" docStyle="DocumentStyle:E765CC7F3D29AC31B7D5F874DD99C2DD.4:Phytotaxa.2009-2010.journal_article" docStyleId="E765CC7F3D29AC31B7D5F874DD99C2DD" docStyleName="Phytotaxa.2009-2010.journal_article" docStyleVersion="4" docTitle="Jungermanniales" docType="treatment" docVersion="9" lastPageNumber="249" masterDocId="FFCCFFABFFDDB94EB500481FFFC0FFEB" masterDocTitle="Fungal symbioses in bryophytes: New insights in the Twenty First Century" masterLastPageNumber="253" masterPageNumber="238" pageNumber="247" updateTime="1698941776982" updateUser="ExternalLinkService" zenodo-license-document="CLOSED">
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<mods:mods id="392DA90F92756B04B690A08C12F9F0FE" xmlns:mods="http://www.loc.gov/mods/v3">
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<mods:titleInfo id="A6CBEECFA24E6DB110364A05B40B047C">
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<mods:title id="EE8EE63F38C6A729FCFB99083C847B36">Fungal symbioses in bryophytes: New insights in the Twenty First Century</mods:title>
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</mods:titleInfo>
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<mods:name id="221F6258188E08BB7F6F8EAC84BE0B2D" type="personal">
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<mods:role id="F17DD82759CA19B7A395553BC0D856BE">
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<mods:roleTerm id="05345FFD5DE57583769154DD0FB674EF">Author</mods:roleTerm>
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</mods:role>
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<mods:namePart id="DA6C57A99252C0A29117A56F657810F5">Pressel, Silvia</mods:namePart>
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</mods:name>
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<mods:name id="535A267C20B7783EC5B7685CFFBCEB9E" type="personal">
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<mods:roleTerm id="817B71735EA83AB6C05C5933F66725C1">Author</mods:roleTerm>
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</mods:role>
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<mods:namePart id="DC79D114AAC328BB3AE991045E4F82FD">Bidartondo, Martin I.</mods:namePart>
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<mods:affiliation id="588B8B17A7CE82FAB4857C74DF8BD52E">Imperial College London and Royal Botanic Gardens, Kew TW 9 3 DS, UK; email: m. bidartondo @ imperial. ac. uk</mods:affiliation>
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</mods:name>
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<mods:name id="74F31A3522A7C51B3A73AE6D951CA55C" type="personal">
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<mods:roleTerm id="15AFF04ECB4E465B96D0F37A01A3EA14">Author</mods:roleTerm>
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</mods:role>
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<mods:namePart id="D6036BBF29410A3AA1ABCD744EE1F51C">Ligrone, Roberto</mods:namePart>
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<mods:affiliation id="3A31CE7A95BD2A0324D8C2958BC14BF3">Dipartimento di Scienze ambientali, Seconda Università di Napoli, via Vivaldi 43, 81100 Caserta, Italy;</mods:affiliation>
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</mods:name>
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<mods:name id="B850FE4AAA43624381014BD55FE22CAD" type="personal">
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<mods:role id="81E6F674234CF175B8659630C220B98B">
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<mods:roleTerm id="261EC76F9413DF5FAD8528A47661E686">Author</mods:roleTerm>
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</mods:role>
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<mods:namePart id="ED260B088F710423D499146543DE9685">Duckett, Jeffrey G.</mods:namePart>
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</mods:name>
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<mods:typeOfResource id="3CC3DD227DDA0E135E6E41B7438FC681">text</mods:typeOfResource>
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<mods:titleInfo id="5605DE89DDB826AF8262E23323123060">
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<mods:title id="DD69FE4645ECC81C6800C20AD21E2BB8">Phytotaxa</mods:title>
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</mods:titleInfo>
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<mods:part id="0C757F2F6DC9EFD10B42D88960FC440E">
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<mods:date id="373EE3F6E476857025151E525A163ED3">2010</mods:date>
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<mods:detail id="4F8179D409EE8B2B10F24A5B31DCA461" type="pubDate">
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<mods:number id="1BA3B62E7CDFC5E3E55CB6ECFFB3AED7">2010-09-30</mods:number>
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</mods:detail>
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<mods:detail id="DC351BE2E37745977013874509DFB15B" type="volume">
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<mods:number id="413710D55A8ABF8081F43CA78B606C49">9</mods:number>
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</mods:detail>
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<mods:extent id="AFBBDA862799C35EC9AD5B8440021EF8" unit="page">
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<mods:start id="9FA14E8E839EB5D477A63C10D00ECC0C">238</mods:start>
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<mods:end id="487EA27375BB21D608D4A3872A62117C">253</mods:end>
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<mods:classification id="EBF62C2DBE18638BE1604DD238E729D1">journal article</mods:classification>
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<mods:identifier id="CB11D33EC299E731D33C21632097283F" type="CLB-Dataset">6312</mods:identifier>
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<mods:identifier id="3B576847483B36C6482A617B6B99458D" type="DOI">10.11646/phytotaxa.9.1.13</mods:identifier>
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<mods:identifier id="5FBF17698537D9A289C2D52811252009" type="GBIF-Dataset">21a2a91a-28ae-40c8-911e-13d0c279e095</mods:identifier>
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<mods:identifier id="C0B9AFF0C149993C8D8183AA4C2C24EB" type="ISSN">1179-3163</mods:identifier>
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<treatment id="03F587D3FFD4B945B5974CB4FD26FCA8" ID-DOI="http://doi.org/10.5281/zenodo.5076293" ID-GBIF-Taxon="182486524" ID-Zenodo-Dep="5076293" LSID="urn:lsid:plazi:treatment:03F587D3FFD4B945B5974CB4FD26FCA8" httpUri="http://treatment.plazi.org/id/03F587D3FFD4B945B5974CB4FD26FCA8" lastPageId="11" lastPageNumber="249" pageId="9" pageNumber="247">
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<subSubSection id="C346654EFFD4B947B5974CB4FE4AFB2E" box="[151,394,1195,1221]" pageId="9" pageNumber="247" type="nomenclature">
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<paragraph id="8BE336C5FFD4B947B5974CB4FE4AFB2E" blockId="9.[151,394,1195,1221]" box="[151,394,1195,1221]" pageId="9" pageNumber="247">
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<heading id="D0AB81A9FFD4B947B5974CB4FE4AFB2E" bold="true" box="[151,394,1195,1221]" fontSize="10" level="2" pageId="9" pageNumber="247" reason="2">
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<emphasis id="B928EAD7FFD4B947B5974CB4FE4AFB2E" bold="true" box="[151,394,1195,1221]" pageId="9" pageNumber="247">
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b)
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<taxonomicName id="4C5C4D46FFD4B947B5B74CB4FE4AFB2E" authority="H. Klinggr, 1858" box="[183,394,1195,1221]" class="Jungermanniopsida" higherTaxonomySource="GBIF" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="order">Jungermanniales</taxonomicName>
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</emphasis>
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</heading>
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</paragraph>
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</subSubSection>
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<subSubSection id="C346654EFFD4B945B5974CE6FD26FCA8" lastPageId="11" lastPageNumber="249" pageId="9" pageNumber="247" type="description">
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<paragraph id="8BE336C5FFD4B947B5974CE6FDEFF819" blockId="9.[151,1436,1273,2034]" pageId="9" pageNumber="247">
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Electron microscopy and molecular studies (
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<bibRefCitation id="EFCD4B34FFD4B947B79D4CE6FCA0FAF8" author="Read, D. J. & Duckett, J. G. & Francis, R. & Ligrone, R. & Russell, A." box="[669,864,1273,1299]" pageId="9" pageNumber="247" pagination="815 - 832" refId="ref9946" refString="Read, D. J., Duckett, J. G., Francis, R., Ligrone, R. & Russell, A. (2000) Symbiotic fungal associations in ' lower' land plants. Philosophical Transactions of the Royal Society B. 355: 815 - 832." type="journal article" year="2000">
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Read
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<emphasis id="B928EAD7FFD4B947B7E24CE6FCDCFAF9" box="[738,796,1273,1298]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
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2000
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</bibRefCitation>
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;
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<bibRefCitation id="EFCD4B34FFD4B947B66C4CE6FB81FAF8" author="Kottke, I. & Beiter, A. & Weiss, M. & Haug, I. & Oberwinkler, F. & Nebel, M." box="[876,1089,1273,1299]" pageId="9" pageNumber="247" pagination="957 - 968" refId="ref8862" refString="Kottke, I., Beiter, A., Weiss, M., Haug, I., Oberwinkler, F. & Nebel, M. (2003) Heterobasidiomycetes from symbiotic associations with hepatics: Jungermanniales have sebacinoid mycobionts while Aneura pinguis (Metzgeriales) is associated with a Tulasnella species. Mycological Research 107: 957 - 968." type="journal article" year="2003">
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Kottke
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<emphasis id="B928EAD7FFD4B947B6C24CE6FC3CFAF9" box="[962,1020,1273,1298]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
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2003
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</bibRefCitation>
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;
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<bibRefCitation id="EFCD4B34FFD4B947B14C4CE6FA8AFAF8" author="Kottke, I. & Nebel, M." box="[1100,1354,1273,1299]" pageId="9" pageNumber="247" pagination="330 - 334" refId="ref8926" refString="Kottke, I. & Nebel, M. (2005) The evolution of mycorrhiza-like associations in liverworts: an update. New Phytologist 167: 330 - 334." type="journal article" year="2005">Kottke & Nebel 2005</bibRefCitation>
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;
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<bibRefCitation id="EFCD4B34FFD4B947B0564CE6FEDBFAD1" author="Nebel, M. & Kreier, H. - P. & Preussing, M. & Weiss, M. A." pageId="9" pageNumber="247" pagination="339 - 360" refId="ref9433" refString="Nebel, M., Kreier, H. - P., Preussing, M. & Weiss, M. A. (2004) Symbiotic fungal associations with liverworts are the possible ancestors of mycorrhizae. In: Agerer, R., Piepenbring, H. & Blanz, P. (Eds.), Frontiers in Basidiomycote Mycology, HIW-Verlag, Ecking, Germany, pp. 339 - 360." type="book chapter" year="2004">
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Nebel
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<emphasis id="B928EAD7FFD4B947B5974D3FFF13FAD2" box="[151,211,1312,1337]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
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2004
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</bibRefCitation>
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;
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<bibRefCitation id="EFCD4B34FFD4B947B4294D3FFDE3FAD1" author="Duckett, J. G. & Russell, J. & Ligrone, R." box="[297,547,1312,1338]" pageId="9" pageNumber="247" pagination="1075 - 1093" refId="ref7648" refString="Duckett, J. G., Russell, J. & Ligrone, R. (2006 b) Basidiomycetous endophytes in jungermannialean (leafy) liverworts have novel cytology and species-specific host-ranges: a cytological and experimental study. Canadian Journal of Botany 84: 1075 - 1093." type="journal article" year="2006">
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Duckett
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<emphasis id="B928EAD7FFD4B947B48F4D3FFE0CFAD2" box="[399,460,1312,1337]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
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2006b
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</bibRefCitation>
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;
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||
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<bibRefCitation id="EFCD4B34FFD4B947B7304D3FFC44FAD1" author="Bidartondo, M. I. & Duckett, J. G." box="[560,900,1312,1338]" pageId="9" pageNumber="247" pagination="485 - 492" refId="ref7007" refString="Bidartondo, M. I. & Duckett, J. G. (2010) Conservative ecological and evolutionary patterns in liverwort-fungal symbioses. Proceedings of the Royal Society B. 277: 485 - 492." type="journal article" year="2010">Bidartondo & Duckett 2010</bibRefCitation>
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;
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<bibRefCitation id="EFCD4B34FFD4B947B6924D3FFB07FAD1" author="Newsham, K. K. & Bridge, P. D." box="[914,1223,1312,1338]" pageId="9" pageNumber="247" pagination="307 - 313" refId="ref9534" refString="Newsham, K. K. & Bridge, P. D. (2010) Sebacinales are associates of the leafy liverwort Lophozia excisa in the southern maritime Antarctic. Mycorrhiza 20: 307 - 313." type="journal article" year="2010">Newsham & Bridge 2010</bibRefCitation>
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) have shown that eight or nine leafy liverwort genera;
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<taxonomicName id="4C5C4D46FFD4B947B75F4D58FCADFA8B" authority="Loeske" authorityName="Loeske" authorityYear="1907" box="[607,877,1350,1376]" class="Jungermanniopsida" family="Anastrophyllaceae" genus="Barbilophozia" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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<emphasis id="B928EAD7FFD4B947B75F4D58FCCEFA8B" box="[607,782,1351,1376]" italics="true" pageId="9" pageNumber="247">Barbilophozia</emphasis>
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Loeske
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</taxonomicName>
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,
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<taxonomicName id="4C5C4D46FFD4B947B67F4D58FADAFA8B" authority="(Dumort.) Dumort." authorityName="Dumort." baseAuthorityName="Dumort." box="[895,1306,1350,1376]" class="Jungermanniopsida" family="Scapaniaceae" genus="Diplophyllum" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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<emphasis id="B928EAD7FFD4B947B67F4D58FBE6FA8B" box="[895,1062,1351,1376]" italics="true" pageId="9" pageNumber="247">Diplophyllum</emphasis>
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(Dumort.) Dumort.
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</taxonomicName>
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,
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<taxonomicName id="4C5C4D46FFD4B947B02B4D58FEBEFA6C" authority="(Dumort.) Dumort." authorityName="Dumort." baseAuthorityName="Dumort." class="Jungermanniopsida" family="Scapaniaceae" genus="Lophozia" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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<emphasis id="B928EAD7FFD4B947B02B4D58FA5CFA8B" box="[1323,1436,1351,1376]" italics="true" pageId="9" pageNumber="247">Lophozia</emphasis>
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(Dumort.) Dumort.
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</taxonomicName>
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,
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<taxonomicName id="4C5C4D46FFD4B947B48E4D72FD2FFA6C" authority="(Dumort.) Dumort." authorityName="Dumort." baseAuthorityName="Dumort." box="[398,751,1389,1415]" class="Jungermanniopsida" family="Scapaniaceae" genus="Scapania" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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<emphasis id="B928EAD7FFD4B947B48E4D72FE3EFA6D" box="[398,510,1389,1414]" italics="true" pageId="9" pageNumber="247">Scapania</emphasis>
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(Dumort.) Dumort.
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</taxonomicName>
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and
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<taxonomicName id="4C5C4D46FFD4B947B62B4D72FB5CFA6C" authority="Schiffn. ex Loeske" authorityName="Loeske" box="[811,1180,1389,1415]" class="Jungermanniopsida" family="Scapaniaceae" genus="Tritomaria" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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<emphasis id="B928EAD7FFD4B947B62B4D72FC6EFA6D" box="[811,942,1389,1414]" italics="true" pageId="9" pageNumber="247">Tritomaria</emphasis>
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Schiffn. ex Loeske
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</taxonomicName>
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in the
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<taxonomicName id="4C5C4D46FFD4B947B1F24D72FA57FA6C" box="[1266,1431,1389,1415]" class="Jungermanniopsida" family="Scapaniaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Scapaniaceae</taxonomicName>
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,
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<taxonomicName id="4C5C4D46FFD4B947B5974D8BFEEDFA45" authority="Gray" authorityName="Gray" box="[151,301,1428,1454]" class="Jungermanniopsida" family="Solenostomataceae" genus="Nardia" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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<emphasis id="B928EAD7FFD4B947B5974D8BFF2AFA46" box="[151,234,1428,1453]" italics="true" pageId="9" pageNumber="247">Nardia</emphasis>
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Gray
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</taxonomicName>
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in the
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<taxonomicName id="4C5C4D46FFD4B947B4814D8BFD9FFA45" box="[385,607,1428,1454]" class="Jungermanniopsida" family="Jungermanniaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Jungermanniaceae</taxonomicName>
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,
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<taxonomicName id="4C5C4D46FFD4B947B76C4D8BFC98FA45" authority="Dumort." authorityName="Dumort." box="[620,856,1428,1454]" class="Jungermanniopsida" family="Geocalycaceae" genus="Saccogyna" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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<emphasis id="B928EAD7FFD4B947B76C4D8BFD2CFA46" box="[620,748,1428,1453]" italics="true" pageId="9" pageNumber="247">Saccogyna</emphasis>
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Dumort.
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</taxonomicName>
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in the
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<taxonomicName id="4C5C4D46FFD4B947B6AB4D8BFB9CFA45" box="[939,1116,1428,1454]" class="Jungermanniopsida" family="Geocalycaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Geocalycaceae</taxonomicName>
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and
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<taxonomicName id="4C5C4D46FFD4B947B1994D8BFAA4FA45" authority="Spruce" authorityName="Spruce" authorityYear="1849" box="[1177,1380,1428,1454]" class="Jungermanniopsida" family="Arnelliaceae" genus="Southbya" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
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|
<emphasis id="B928EAD7FFD4B947B1994D8BFAC7FA46" box="[1177,1287,1428,1453]" italics="true" pageId="9" pageNumber="247">Southbya</emphasis>
|
||
|
|
Spruce
|
||
|
|
</taxonomicName>
|
||
|
|
, and almost certainly
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B4664DA4FD96FA3F" authority="Nees" authorityName="Nees" box="[358,598,1466,1492]" class="Jungermanniopsida" family="Arnelliaceae" genus="Gongylanthus" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
|
||
|
|
<emphasis id="B928EAD7FFD4B947B4664DA4FDD1FA3F" box="[358,529,1467,1492]" italics="true" pageId="9" pageNumber="247">Gongylanthus</emphasis>
|
||
|
|
Nees
|
||
|
|
</taxonomicName>
|
||
|
|
, in the
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B7B64DA5FC94FA3F" authorityName="Nakai" authorityYear="1943" box="[694,852,1466,1492]" class="Jungermanniopsida" family="Arnelliaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Arnelliaceae</taxonomicName>
|
||
|
|
, consistently and predominantly associate with members of the
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B4654DFEFD7FFA10" authority="Oberw." authorityName="Oberw." box="[357,703,1505,1531]" class="Agaricomycetes" family="Sebacinaceae" genus="Sebacina" kingdom="Fungi" order="Sebacinales" pageId="9" pageNumber="247" phylum="Basidiomycota" rank="species" species="vermifera">
|
||
|
|
<emphasis id="B928EAD7FFD4B947B4654DFEFD9BFA11" box="[357,603,1505,1530]" italics="true" pageId="9" pageNumber="247">Sebacina vermifera</emphasis>
|
||
|
|
Oberw.
|
||
|
|
</taxonomicName>
|
||
|
|
species complex, in striking contrast to
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B1C64DFEFA89FA11" box="[1222,1353,1505,1530]" class="Agaricomycetes" family="Tulasnellaceae" genus="Tulasnella" kingdom="Fungi" order="Cantharellales" pageId="9" pageNumber="247" phylum="Basidiomycota" rank="genus">
|
||
|
|
<emphasis id="B928EAD7FFD4B947B1C64DFEFA89FA11" box="[1222,1353,1505,1530]" italics="true" pageId="9" pageNumber="247">Tulasnella</emphasis>
|
||
|
|
</taxonomicName>
|
||
|
|
as the predominant endophyte in the
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B7014E17FD50F9C9" box="[513,656,1544,1570]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
|
||
|
|
. As in most liverwort-fungus associations, these endophytes enter the hosts via the rhizoids. However colonization by these basidiomycetes causes the rhizoids to become highly branched (
|
||
|
|
<figureCitation id="13672A40FFD4B947B46D4E4AFE0DF984" box="[365,461,1621,1647]" captionStart="FIGURE 5" captionStartId="10.[151,257,1664,1688]" captionTargetBox="[151,1436,197,1639]" captionTargetId="figure-140@10.[151,1436,197,1639]" captionTargetPageId="10" captionText="FIGURE 5. Basidiomycetes in Jungermanniales. A. Scanning electron micrograph. B-F. Transmission electron micrographs. A. Saccogyna viticulosa (L.) Dumort.; branched rhizoid tip associated with numerous hyphae. B. Scapania cuspiduligera (Nees) Müll. Frib.; infected and uninfected cells. Note the outgrowths of host wall (arrowed) preventing the ingress of hyphae into the uninfected cell. C. Dolipore septum (d) with imperforate parenthosome (p), typical of the genera Sebacina and Tulasnella. D-F. Southbya nigrella (De Not.) Henriq.. D. Infected cells packed with hyphae lying next to an uninfected cell containing numerous oil bodies (ob). E. Newly infected cell showing degenerating oil bodies (dob). F. Older infected cell. Note that the hyphae outlive the host. Scale bars = (A) 50 µm; (B, D-F) 5 µm; (C) 1m." figureDoi="http://doi.org/10.5281/zenodo.4895372" httpUri="https://zenodo.org/record/4895372/files/figure.png" pageId="9" pageNumber="247">Fig. 5A</figureCitation>
|
||
|
|
) rather than eliciting the terminal swellings typical of ascomycetous infections. Within the liverwort stems two kinds of association have been described. In the
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B14D4E63FB21F97D" authorityName="Nakai" authorityYear="1943" box="[1101,1249,1660,1686]" class="Jungermanniopsida" family="Arnelliaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Arnelliaceae</taxonomicName>
|
||
|
|
the endophytes colonize a cluster of cells in the centre of the stems (
|
||
|
|
<figureCitation id="13672A40FFD4B947B7F94EBDFC94F957" box="[761,852,1698,1724]" captionStart="FIGURE 5" captionStartId="10.[151,257,1664,1688]" captionTargetBox="[151,1436,197,1639]" captionTargetId="figure-140@10.[151,1436,197,1639]" captionTargetPageId="10" captionText="FIGURE 5. Basidiomycetes in Jungermanniales. A. Scanning electron micrograph. B-F. Transmission electron micrographs. A. Saccogyna viticulosa (L.) Dumort.; branched rhizoid tip associated with numerous hyphae. B. Scapania cuspiduligera (Nees) Müll. Frib.; infected and uninfected cells. Note the outgrowths of host wall (arrowed) preventing the ingress of hyphae into the uninfected cell. C. Dolipore septum (d) with imperforate parenthosome (p), typical of the genera Sebacina and Tulasnella. D-F. Southbya nigrella (De Not.) Henriq.. D. Infected cells packed with hyphae lying next to an uninfected cell containing numerous oil bodies (ob). E. Newly infected cell showing degenerating oil bodies (dob). F. Older infected cell. Note that the hyphae outlive the host. Scale bars = (A) 50 µm; (B, D-F) 5 µm; (C) 1m." figureDoi="http://doi.org/10.5281/zenodo.4895372" httpUri="https://zenodo.org/record/4895372/files/figure.png" pageId="9" pageNumber="247">Fig. 5D</figureCitation>
|
||
|
|
) and there are no visible features in the host walls indicating why the fungus is so restricted. In the
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B7E94ED6FC4DF908" box="[745,909,1737,1763]" class="Jungermanniopsida" family="Scapaniaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Scapaniaceae</taxonomicName>
|
||
|
|
,
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B69A4ED6FBB7F908" box="[922,1143,1737,1763]" class="Jungermanniopsida" family="Jungermanniaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Jungermanniaceae</taxonomicName>
|
||
|
|
and
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B1B44ED6FAABF908" box="[1204,1387,1737,1763]" class="Jungermanniopsida" family="Geocalycaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Geocalycaceae</taxonomicName>
|
||
|
|
, the central region of the stems contains a mosaic of infected and fungus-free cells. Growth of hyphae into the latter is prevented by overgrowths of host wall material (
|
||
|
|
<figureCitation id="13672A40FFD4B947B65B4F09FC7DF8DB" box="[859,957,1814,1840]" captionStart="FIGURE 5" captionStartId="10.[151,257,1664,1688]" captionTargetBox="[151,1436,197,1639]" captionTargetId="figure-140@10.[151,1436,197,1639]" captionTargetPageId="10" captionText="FIGURE 5. Basidiomycetes in Jungermanniales. A. Scanning electron micrograph. B-F. Transmission electron micrographs. A. Saccogyna viticulosa (L.) Dumort.; branched rhizoid tip associated with numerous hyphae. B. Scapania cuspiduligera (Nees) Müll. Frib.; infected and uninfected cells. Note the outgrowths of host wall (arrowed) preventing the ingress of hyphae into the uninfected cell. C. Dolipore septum (d) with imperforate parenthosome (p), typical of the genera Sebacina and Tulasnella. D-F. Southbya nigrella (De Not.) Henriq.. D. Infected cells packed with hyphae lying next to an uninfected cell containing numerous oil bodies (ob). E. Newly infected cell showing degenerating oil bodies (dob). F. Older infected cell. Note that the hyphae outlive the host. Scale bars = (A) 50 µm; (B, D-F) 5 µm; (C) 1m." figureDoi="http://doi.org/10.5281/zenodo.4895372" httpUri="https://zenodo.org/record/4895372/files/figure.png" pageId="9" pageNumber="247">Fig. 5B</figureCitation>
|
||
|
|
). In both kinds of infection there is no evidence of fungus digestion by the host and healthy hyphae persist long after the death of the host cells in older stems (
|
||
|
|
<figureCitation id="13672A40FFD4B947B4354F7BFE53F895" box="[309,403,1892,1918]" captionStart="FIGURE 5" captionStartId="10.[151,257,1664,1688]" captionTargetBox="[151,1436,197,1639]" captionTargetId="figure-140@10.[151,1436,197,1639]" captionTargetPageId="10" captionText="FIGURE 5. Basidiomycetes in Jungermanniales. A. Scanning electron micrograph. B-F. Transmission electron micrographs. A. Saccogyna viticulosa (L.) Dumort.; branched rhizoid tip associated with numerous hyphae. B. Scapania cuspiduligera (Nees) Müll. Frib.; infected and uninfected cells. Note the outgrowths of host wall (arrowed) preventing the ingress of hyphae into the uninfected cell. C. Dolipore septum (d) with imperforate parenthosome (p), typical of the genera Sebacina and Tulasnella. D-F. Southbya nigrella (De Not.) Henriq.. D. Infected cells packed with hyphae lying next to an uninfected cell containing numerous oil bodies (ob). E. Newly infected cell showing degenerating oil bodies (dob). F. Older infected cell. Note that the hyphae outlive the host. Scale bars = (A) 50 µm; (B, D-F) 5 µm; (C) 1m." figureDoi="http://doi.org/10.5281/zenodo.4895372" httpUri="https://zenodo.org/record/4895372/files/figure.png" pageId="9" pageNumber="247">Fig. 5F</figureCitation>
|
||
|
|
). In fact, host cell death occurs very rapidly in the mosaic infections (
|
||
|
|
<bibRefCitation id="EFCD4B34FFD4B947B1F34F7BFF28F84F" author="Duckett, J. G. & Russell, J. & Ligrone, R." pageId="9" pageNumber="247" pagination="1075 - 1093" refId="ref7648" refString="Duckett, J. G., Russell, J. & Ligrone, R. (2006 b) Basidiomycetous endophytes in jungermannialean (leafy) liverworts have novel cytology and species-specific host-ranges: a cytological and experimental study. Canadian Journal of Botany 84: 1075 - 1093." type="journal article" year="2006">
|
||
|
|
Duckett
|
||
|
|
<emphasis id="B928EAD7FFD4B947B05E4F7BFA5CF896" box="[1374,1436,1892,1917]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
|
||
|
|
2006b
|
||
|
|
</bibRefCitation>
|
||
|
|
). One previously overlooked effect of fungal colonization in the
|
||
|
|
<taxonomicName id="4C5C4D46FFD4B947B10B4F95FB65F84F" authorityName="Nakai" authorityYear="1943" box="[1035,1189,1930,1956]" class="Jungermanniopsida" family="Arnelliaceae" kingdom="Plantae" order="Jungermanniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Arnelliaceae</taxonomicName>
|
||
|
|
is that oil bodies in infected cells rapidly break down (
|
||
|
|
<figureCitation id="13672A40FFD4B947B7434FAEFD5FF820" box="[579,671,1969,1995]" captionStart="FIGURE 5" captionStartId="10.[151,257,1664,1688]" captionTargetBox="[151,1436,197,1639]" captionTargetId="figure-140@10.[151,1436,197,1639]" captionTargetPageId="10" captionText="FIGURE 5. Basidiomycetes in Jungermanniales. A. Scanning electron micrograph. B-F. Transmission electron micrographs. A. Saccogyna viticulosa (L.) Dumort.; branched rhizoid tip associated with numerous hyphae. B. Scapania cuspiduligera (Nees) Müll. Frib.; infected and uninfected cells. Note the outgrowths of host wall (arrowed) preventing the ingress of hyphae into the uninfected cell. C. Dolipore septum (d) with imperforate parenthosome (p), typical of the genera Sebacina and Tulasnella. D-F. Southbya nigrella (De Not.) Henriq.. D. Infected cells packed with hyphae lying next to an uninfected cell containing numerous oil bodies (ob). E. Newly infected cell showing degenerating oil bodies (dob). F. Older infected cell. Note that the hyphae outlive the host. Scale bars = (A) 50 µm; (B, D-F) 5 µm; (C) 1m." figureDoi="http://doi.org/10.5281/zenodo.4895372" httpUri="https://zenodo.org/record/4895372/files/figure.png" pageId="9" pageNumber="247">Fig. 5E</figureCitation>
|
||
|
|
) as hyphae proliferate suggesting that their contents may be a nutrient source for the endophytes.
|
||
|
|
</paragraph>
|
||
|
|
<caption id="DF23664DFFD7B944B5974E9FFEAAF861" ID-DOI="http://doi.org/10.5281/zenodo.4895372" ID-Zenodo-Dep="4895372" httpUri="https://zenodo.org/record/4895372/files/figure.png" pageId="10" pageNumber="248" startId="10.[151,257,1664,1688]" targetBox="[151,1436,197,1639]" targetPageId="10">
|
||
|
|
<paragraph id="8BE336C5FFD7B944B5974E9FFEAAF861" blockId="10.[151,1436,1664,1930]" pageId="10" pageNumber="248">
|
||
|
|
<emphasis id="B928EAD7FFD7B944B5974E9FFEDFF973" bold="true" box="[151,287,1664,1688]" pageId="10" pageNumber="248">FIGURE 5.</emphasis>
|
||
|
|
Basidiomycetes in
|
||
|
|
<taxonomicName id="4C5C4D46FFD7B944B7054E9FFD04F97C" box="[517,708,1664,1687]" class="Jungermanniopsida" higherTaxonomySource="GBIF" kingdom="Plantae" order="Jungermanniales" pageId="10" pageNumber="248" phylum="Bryophyta" rank="order">Jungermanniales</taxonomicName>
|
||
|
|
.
|
||
|
|
<emphasis id="B928EAD7FFD7B944B7D74E9FFD32F973" bold="true" box="[727,754,1664,1688]" pageId="10" pageNumber="248">A.</emphasis>
|
||
|
|
Scanning electron micrograph.
|
||
|
|
<emphasis id="B928EAD7FFD7B944B1644E9FFB55F973" bold="true" box="[1124,1173,1664,1688]" pageId="10" pageNumber="248">B-F.</emphasis>
|
||
|
|
Transmission electron micrographs.
|
||
|
|
<emphasis id="B928EAD7FFD7B944B4344EBDFE8EF951" bold="true" box="[308,334,1698,1722]" pageId="10" pageNumber="248">A.</emphasis>
|
||
|
|
<taxonomicName id="4C5C4D46FFD7B944B45F4EBCFD91F951" box="[351,593,1699,1722]" class="Jungermanniopsida" family="Geocalycaceae" genus="Saccogyna" kingdom="Plantae" order="Jungermanniales" pageId="10" pageNumber="248" phylum="Bryophyta" rank="species" species="viticulosa">
|
||
|
|
<emphasis id="B928EAD7FFD7B944B45F4EBCFD91F951" box="[351,593,1699,1722]" italics="true" pageId="10" pageNumber="248">Saccogyna viticulosa</emphasis>
|
||
|
|
</taxonomicName>
|
||
|
|
(L.) Dumort.; branched rhizoid tip associated with numerous hyphae.
|
||
|
|
<emphasis id="B928EAD7FFD7B944B0834EBDFA5CF951" bold="true" box="[1411,1436,1698,1722]" pageId="10" pageNumber="248">B.</emphasis>
|
||
|
|
<taxonomicName id="4C5C4D46FFD7B944B5974EDAFDA9F937" authority="(Nees) Mull. Frib." authorityName="Mull. Frib." baseAuthorityName="Nees" box="[151,617,1733,1756]" class="Jungermanniopsida" family="Scapaniaceae" genus="Scapania" kingdom="Plantae" order="Jungermanniales" pageId="10" pageNumber="248" phylum="Bryophyta" rank="species" species="cuspiduligera">
|
||
|
|
<emphasis id="B928EAD7FFD7B944B5974EDAFE58F937" box="[151,408,1733,1756]" italics="true" pageId="10" pageNumber="248">Scapania cuspiduligera</emphasis>
|
||
|
|
(Nees) Müll. Frib.
|
||
|
|
</taxonomicName>
|
||
|
|
; infected and uninfected cells. Note the outgrowths of host wall (arrowed) preventing the ingress of hyphae into the uninfected cell.
|
||
|
|
<emphasis id="B928EAD7FFD7B944B6134EF7FCEDF8EB" bold="true" box="[787,813,1768,1792]" pageId="10" pageNumber="248">C.</emphasis>
|
||
|
|
Dolipore septum (d) with imperforate parenthosome (p), typical of the genera
|
||
|
|
<taxonomicName id="4C5C4D46FFD7B944B4774F14FE18F8C9" box="[375,472,1803,1826]" class="Agaricomycetes" family="Sebacinaceae" genus="Sebacina" kingdom="Fungi" order="Sebacinales" pageId="10" pageNumber="248" phylum="Basidiomycota" rank="genus">
|
||
|
|
<emphasis id="B928EAD7FFD7B944B4774F14FE18F8C9" box="[375,472,1803,1826]" italics="true" pageId="10" pageNumber="248">Sebacina</emphasis>
|
||
|
|
</taxonomicName>
|
||
|
|
and
|
||
|
|
<taxonomicName id="4C5C4D46FFD7B944B70C4F14FDBBF8C9" box="[524,635,1803,1826]" class="Agaricomycetes" family="Tulasnellaceae" genus="Tulasnella" kingdom="Fungi" order="Cantharellales" pageId="10" pageNumber="248" phylum="Basidiomycota" rank="genus">
|
||
|
|
<emphasis id="B928EAD7FFD7B944B70C4F14FDBBF8C9" box="[524,635,1803,1826]" italics="true" pageId="10" pageNumber="248">Tulasnella</emphasis>
|
||
|
|
</taxonomicName>
|
||
|
|
.
|
||
|
|
<emphasis id="B928EAD7FFD7B944B78E4F15FD7FF8C9" bold="true" box="[654,703,1802,1826]" pageId="10" pageNumber="248">D-F.</emphasis>
|
||
|
|
<taxonomicName id="4C5C4D46FFD7B944B7CB4F14FB88F8C9" authority="(De Not.) Henriq" authorityName="Henriq" baseAuthorityName="De Not." box="[715,1096,1803,1826]" class="Jungermanniopsida" family="Arnelliaceae" genus="Southbya" kingdom="Plantae" order="Jungermanniales" pageId="10" pageNumber="248" phylum="Bryophyta" rank="species" species="nigrella">
|
||
|
|
<emphasis id="B928EAD7FFD7B944B7CB4F14FC48F8C9" box="[715,904,1803,1826]" italics="true" pageId="10" pageNumber="248">Southbya nigrella</emphasis>
|
||
|
|
(De Not.) Henriq
|
||
|
|
</taxonomicName>
|
||
|
|
..
|
||
|
|
<emphasis id="B928EAD7FFD7B944B15F4F15FBB9F8C9" bold="true" box="[1119,1145,1802,1826]" pageId="10" pageNumber="248">D.</emphasis>
|
||
|
|
Infected cells packed with hyphae lying next to an uninfected cell containing numerous oil bodies (ob).
|
||
|
|
<emphasis id="B928EAD7FFD7B944B1254F32FBFEF8AE" bold="true" box="[1061,1086,1837,1861]" pageId="10" pageNumber="248">E.</emphasis>
|
||
|
|
Newly infected cell showing degenerating oil bodies (dob).
|
||
|
|
<emphasis id="B928EAD7FFD7B944B4E34F4FFE38F883" bold="true" box="[483,504,1872,1896]" pageId="10" pageNumber="248">F.</emphasis>
|
||
|
|
Older infected cell. Note that the hyphae outlive the host. Scale bars = (A) 50 µm; (B, D-F) 5 µm; (C) 1m.
|
||
|
|
</paragraph>
|
||
|
|
</caption>
|
||
|
|
<paragraph id="8BE336C5FFD6B945B5C64887FDA0FE71" blockId="11.[151,1436,152,835]" pageId="11" pageNumber="249">
|
||
|
|
In striking contrast to the vast host range of the rhizoidal ascomycetes, cross-infection experiments on the leafy liverwort basidiomycetes strongly suggested these to be highly host specific (
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B16048A1FA94FF33" author="Duckett, J. G. & Russell, J. & Ligrone, R." box="[1120,1364,190,216]" pageId="11" pageNumber="249" pagination="1075 - 1093" refId="ref7648" refString="Duckett, J. G., Russell, J. & Ligrone, R. (2006 b) Basidiomycetous endophytes in jungermannialean (leafy) liverworts have novel cytology and species-specific host-ranges: a cytological and experimental study. Canadian Journal of Botany 84: 1075 - 1093." type="journal article" year="2006">
|
||
|
|
Duckett
|
||
|
|
<emphasis id="B928EAD7FFD6B945B1C548A0FB3FFF33" box="[1221,1279,191,216]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
|
|
2006b
|
||
|
|
</bibRefCitation>
|
||
|
|
). This situation has now been confirmed by a molecular study (
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B62848FAFBB2FF14" author="Bidartondo, M. I. & Duckett, J. G." box="[808,1138,229,255]" pageId="11" pageNumber="249" pagination="485 - 492" refId="ref7007" refString="Bidartondo, M. I. & Duckett, J. G. (2010) Conservative ecological and evolutionary patterns in liverwort-fungal symbioses. Proceedings of the Royal Society B. 277: 485 - 492." type="journal article" year="2010">Bidartondo & Duckett 2010</bibRefCitation>
|
||
|
|
) revealing a high level of fungal specificity to the extent that where multiple liverworts co-occur they almost never share the same endophyte. This remarkable symbiotic conservatism differs fundamentally from the generalist pattern of mycorrhizas in seed plants that repeatedly evolved to form ectomycorrhizas simultaneously with a range of distantly related basidiomycete genera.
|
||
|
|
</paragraph>
|
||
|
|
<paragraph id="8BE336C5FFD6B945B5C649B9FD26FCA8" blockId="11.[151,1436,152,835]" pageId="11" pageNumber="249">
|
||
|
|
The phylogenetic position of these basidiomycete-associated leafy liverworts (
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B16A49B9FB36FE2B" author="Davis, E. C." box="[1130,1270,422,448]" pageId="11" pageNumber="249" pagination="61 - 86" refId="ref7272" refString="Davis, E. C. (2004) Molecular phylogeny of leafy liverworts according to analysis of twelve genes. In: Goffinet, B., Hollowell, V. & Magill, R. (Eds.), Molecular Systematics of Bryophytes, Missouri Botanical Gardens Press, St. Louis, pp. 61 - 86." type="book chapter" year="2004">Davis 2004</bibRefCitation>
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;
|
||
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<bibRefCitation id="EFCD4B34FFD6B945B00449B9FF16FE0C" author="Forrest, L. L. & Davis, E. C. & Long, D. G. & Crandall-Stotler, B. J. & Clark, A. & Hollingsworth, M. L." pageId="11" pageNumber="249" pagination="303 - 334" refId="ref7864" refString="Forrest, L. L., Davis, E. C., Long, D. G., Crandall-Stotler, B. J., Clark, A. & Hollingsworth, M. L. (2006) Unraveling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses. Bryologist 109: 303 - 334." type="journal article" year="2006">
|
||
|
|
Forrest
|
||
|
|
<emphasis id="B928EAD7FFD6B945B06049B8FA5CFE2B" box="[1376,1436,423,448]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
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|
2006
|
||
|
|
</bibRefCitation>
|
||
|
|
;
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B5E349D2FE22FE0C" author="Heinrichs, J. & Gradstein, S. R. & Wilson, R. & Schneider, H." box="[227,482,461,487]" pageId="11" pageNumber="249" pagination="131 - 150" refId="ref8209" refString="Heinrichs, J., Gradstein, S. R., Wilson, R. & Schneider, H. (2005) Towards a natural classification of liverworts (Marchantiophyta) based on the chloroplast gene (rbc L). Cryptogamie Bryology 26: 131 - 150." type="journal article" year="2005">
|
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Heinrichs
|
||
|
|
<emphasis id="B928EAD7FFD6B945B45F49D2FE5CFE0D" box="[351,412,461,486]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
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|
2005
|
||
|
|
</bibRefCitation>
|
||
|
|
,
|
||
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|
<bibRefCitation id="EFCD4B34FFD6B945B4F049D2FDEFFE0C" author="Heinrichs, J. & Hentschel, J. & Wilson, R. & Feldberg, K. & Schneider, H." box="[496,559,461,487]" pageId="11" pageNumber="249" pagination="31 - 44" refId="ref8260" refString="Heinrichs, J., Hentschel, J., Wilson, R., Feldberg, K. & Schneider, H. (2007) Evolution of leafy liverworts (Jungermanniidae, Marchantiophyta): estimating divergence times from chloroplast DNA sequences using penalized likelihood. Taxon 56: 31 - 44." type="journal article" year="2007">2007</bibRefCitation>
|
||
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;
|
||
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|
<bibRefCitation id="EFCD4B34FFD6B945B73C49D2FCFEFE0C" author="Hentschel, J. & Wilson, R. & Burghards, M. & Zundorf, H-J. & Schneider, H. & Heinrichs, J." box="[572,830,461,487]" pageId="11" pageNumber="249" pagination="211 - 226" refId="ref8315" refString="Hentschel, J., Wilson, R., Burghards, M., Zundorf, H-J., Schneider, H. & Heinrichs, J. (2006) Reinstatement of Lophocoleaceae (Jungermanniopsida) based on chloroplast gene rbc L data: exploring the importance of female involucres for the systematics of Jungermanniales. Plant Systematics and Evolution 258: 211 - 226." type="journal article" year="2006">
|
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|
Hentschel
|
||
|
|
<emphasis id="B928EAD7FFD6B945B7BC49D2FD39FE0D" box="[700,761,461,486]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
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2006
|
||
|
|
</bibRefCitation>
|
||
|
|
) and the fact that they are far more restricted than those with ascomycetes suggest that the basidiomycetes were a secondary acquisition following the loss of ascomycetes. However, the position of the
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B7AD4A05FCFDFDDF" box="[685,829,538,564]" class="Agaricomycetes" kingdom="Fungi" order="Sebacinales" pageId="11" pageNumber="249" phylum="Basidiomycota" rank="order">Sebacinales</taxonomicName>
|
||
|
|
in fungal phylogenies suggests that they may be considerably more ancient than the
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B7404A5EFD7BFDB1" box="[576,699,577,602]" class="Agaricomycetes" family="Tulasnellaceae" genus="Tulasnella" kingdom="Fungi" order="Cantharellales" pageId="11" pageNumber="249" phylum="Basidiomycota" rank="genus">
|
||
|
|
<emphasis id="B928EAD7FFD6B945B7404A5EFD7BFDB1" box="[576,699,577,602]" italics="true" pageId="11" pageNumber="249">Tulasnella</emphasis>
|
||
|
|
</taxonomicName>
|
||
|
|
associations in the
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B6A64A5EFBF1FDB0" box="[934,1073,577,603]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
|
||
|
|
(
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B1424A5EFADFFDB0" author="Kottke, I. & Beiter, A. & Weiss, M. & Haug, I. & Oberwinkler, F. & Nebel, M." box="[1090,1311,577,603]" pageId="11" pageNumber="249" pagination="957 - 968" refId="ref8862" refString="Kottke, I., Beiter, A., Weiss, M., Haug, I., Oberwinkler, F. & Nebel, M. (2003) Heterobasidiomycetes from symbiotic associations with hepatics: Jungermanniales have sebacinoid mycobionts while Aneura pinguis (Metzgeriales) is associated with a Tulasnella species. Mycological Research 107: 957 - 968." type="journal article" year="2003">
|
||
|
|
Kottke
|
||
|
|
<emphasis id="B928EAD7FFD6B945B19C4A5EFB18FDB1" box="[1180,1240,577,602]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
|
|
2003
|
||
|
|
</bibRefCitation>
|
||
|
|
;
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B02C4A5EFEE6FD69" author="Kottke, I. & Nebel, M." pageId="11" pageNumber="249" pagination="330 - 334" refId="ref8926" refString="Kottke, I. & Nebel, M. (2005) The evolution of mycorrhiza-like associations in liverworts: an update. New Phytologist 167: 330 - 334." type="journal article" year="2005">Kottke & Nebel 2005</bibRefCitation>
|
||
|
|
). The discovery that basidiomycetes are widespread in
|
||
|
|
<emphasis id="B928EAD7FFD6B945B6BF4A77FA5CFD6A" box="[959,1436,616,641]" italics="true" pageId="11" pageNumber="249">
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B6BF4A77FBF1FD6A" box="[959,1073,616,641]" class="Jungermanniopsida" family="Scapaniaceae" genus="Scapania" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="genus">Scapania</taxonomicName>
|
||
|
|
,
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B13E4A77FB25FD6A" box="[1086,1253,616,641]" class="Jungermanniopsida" family="Scapaniaceae" genus="Diplophyllum" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="genus">Diplophyllum</taxonomicName>
|
||
|
|
,
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B1F24A77FA5CFD6A" authorityName="Loeske" authorityYear="1907" box="[1266,1436,616,641]" class="Jungermanniopsida" family="Anastrophyllaceae" genus="Barbilophozia" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="genus">Barbilophozia</taxonomicName>
|
||
|
|
</emphasis>
|
||
|
|
and
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B5CB4A90FEFBFD43" box="[203,315,655,680]" class="Jungermanniopsida" family="Scapaniaceae" genus="Lophozia" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="genus">
|
||
|
|
<emphasis id="B928EAD7FFD6B945B5CB4A90FEFBFD43" box="[203,315,655,680]" italics="true" pageId="11" pageNumber="249">Lophozia</emphasis>
|
||
|
|
</taxonomicName>
|
||
|
|
is congruent with their close evolutionary relationship (
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B6EA4A91FB02FD43" author="Schill, D. & Long, D. G. & Moeller, M. & Squirrell, J." box="[1002,1218,654,680]" pageId="11" pageNumber="249" pagination="141 - 149" refId="ref10081" refString="Schill, D., Long, D. G., Moeller, M. & Squirrell, J. (2004) Phyolgenetic relationships between Lophoziaceae and Scapaniaceae based on chloroplast sequences. Monographs in Systematics of the Missouri Botanical Garden 98: 141 - 149." type="journal article" year="2004">
|
||
|
|
Schill
|
||
|
|
<emphasis id="B928EAD7FFD6B945B13B4A90FBB9FD43" box="[1083,1145,655,680]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
|
|
2004
|
||
|
|
</bibRefCitation>
|
||
|
|
;
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B1CF4A91FF15FD24" author="Yatsentyuk, S. P. & Konstantinova, N. A. & Ignatov, M. S. & Hyvonen, J. & Troiysky, A. V." pageId="11" pageNumber="249" pagination="243 - 260" refId="ref10828" refString="Yatsentyuk, S. P., Konstantinova, N. A., Ignatov, M. S., Hyvonen, J. & Troiysky, A. V. (2004) On the phylogeny of Lophoziaceae and related families (Hepaticae, Jungermanniales), based on trnL-trnF intron-spacer sequences of chloroplast DNA. Monographs in Systematics of the Missouri Botanical Garden 98: 243 - 260." type="journal article" year="2004">
|
||
|
|
Yatsentyuk
|
||
|
|
<emphasis id="B928EAD7FFD6B945B05E4A90FA5CFD43" box="[1374,1436,655,680]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
|
|
2004
|
||
|
|
</bibRefCitation>
|
||
|
|
;
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B5E04AAAFE27FD24" author="He-Nygren, X. & Ahonen, I. & Juslen, A. & Glenny, D. & Piippo, S." box="[224,487,693,719]" pageId="11" pageNumber="249" pagination="1 - 31" refId="ref8383" refString="He-Nygren, X., Ahonen, I., Juslen, A., Glenny, D. & Piippo, S. (2006) Illuminating the evolutionary history of liverworts (Marchantiophyta) - Towards a natural classification. Cladistics 22: 1 - 31." type="journal article" year="2006">
|
||
|
|
He-Nygrén
|
||
|
|
<emphasis id="B928EAD7FFD6B945B46B4AAAFE65FD25" box="[363,421,693,718]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
|
|
2006
|
||
|
|
</bibRefCitation>
|
||
|
|
) whilst the placement of basidiomycete-associated liverworts (
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B1C64AAAFE11FD1D" authority="(Nees & Huebener) Grolle" authorityName="Grolle" baseAuthorityName="Nees & Huebener" class="Jungermanniopsida" family="Scapaniaceae" genus="Lophozia" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="species" species="sudetica">
|
||
|
|
<emphasis id="B928EAD7FFD6B945B1C64AAAFA5BFD25" box="[1222,1435,693,718]" italics="true" pageId="11" pageNumber="249">Lophozia sudetica</emphasis>
|
||
|
|
(Nees & Huebener) Grolle
|
||
|
|
</taxonomicName>
|
||
|
|
,
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B4E04AC3FBA9FD1D" authority="(Schmieder ex Schreb.) Loeske" authorityName="Loeske" baseAuthorityName="Schreb." box="[480,1129,732,758]" class="Jungermanniopsida" family="Anastrophyllaceae" genus="Barbilophozia" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="species" species="barbata">
|
||
|
|
<emphasis id="B928EAD7FFD6B945B4E04AC3FD2DFD1E" box="[480,749,732,757]" italics="true" pageId="11" pageNumber="249">Barbilophozia barbata</emphasis>
|
||
|
|
(Schmieder ex Schreb.) Loeske
|
||
|
|
</taxonomicName>
|
||
|
|
,
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B1764AC3FF2CFCF7" authority="(Wallr.) Loeske" authorityName="Loeske" baseAuthorityName="Wallr." class="Jungermanniopsida" family="Anastrophyllaceae" genus="Barbilophozia" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="species" species="lycopodioides">
|
||
|
|
<emphasis id="B928EAD7FFD6B945B1764AC3FAFAFD1E" box="[1142,1338,732,757]" italics="true" pageId="11" pageNumber="249">B. lycopodioides</emphasis>
|
||
|
|
(Wallr.) Loeske
|
||
|
|
</taxonomicName>
|
||
|
|
and
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B4254B1DFD4BFCF7" authority="(A. Evans) Loeske" authorityName="Loeske" baseAuthorityName="A. Evans" box="[293,651,770,796]" class="Jungermanniopsida" family="Anastrophyllaceae" genus="Barbilophozia" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="species" species="hatchery">
|
||
|
|
<emphasis id="B928EAD7FFD6B945B4254B1DFE6CFCF0" box="[293,428,770,795]" italics="true" pageId="11" pageNumber="249">B. hatchery</emphasis>
|
||
|
|
(A.Evans) Loeske
|
||
|
|
</taxonomicName>
|
||
|
|
) sister to other members of the
|
||
|
|
<taxonomicName id="4C5C4D46FFD6B945B1034B1DFA5CFCF7" authority="(de Roo et al. 2007)" baseAuthorityName="de Roo" baseAuthorityYear="2007" box="[1027,1436,770,796]" class="Jungermanniopsida" family="Lophoziaceae" kingdom="Plantae" order="Jungermanniales" pageId="11" pageNumber="249" phylum="Bryophyta" rank="family">
|
||
|
|
Lophoziaceae (
|
||
|
|
<bibRefCitation id="EFCD4B34FFD6B945B1B64B1DFA53FCF7" author="De Roo, R. T. & Hedderson, T. A. & Soderstrom, L." box="[1206,1427,770,796]" pageId="11" pageNumber="249" pagination="301 - 314" refId="ref7334" refString="De Roo, R. T., Hedderson, T. A. & Soderstrom, L. (2007) Molecular insights into the phylogeny of the leafy liverwort family Lophoziaceae Cavers. Taxon 56: 301 - 314." type="journal article" year="2007">
|
||
|
|
de Roo
|
||
|
|
<emphasis id="B928EAD7FFD6B945B0144B1DFA90FCF0" box="[1300,1360,770,795]" italics="true" pageId="11" pageNumber="249">et al.</emphasis>
|
||
|
|
2007
|
||
|
|
</bibRefCitation>
|
||
|
|
)
|
||
|
|
</taxonomicName>
|
||
|
|
suggests ancestral presence of fungi in this family.
|
||
|
|
</paragraph>
|
||
|
|
</subSubSection>
|
||
|
|
</treatment>
|
||
|
|
</document>
|