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<document id="241EA4D36179403E903044A0D40D7A94" 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 &amp; Duckett, Jeffrey G." docDate="2010" docId="03F587D3FFDAB947B5974D8CFEE9FBB9" 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="Aneuraceae" docType="treatment" docVersion="9" lastPageNumber="247" masterDocId="FFCCFFABFFDDB94EB500481FFFC0FFEB" masterDocTitle="Fungal symbioses in bryophytes: New insights in the Twenty First Century" masterLastPageNumber="253" masterPageNumber="238" pageNumber="245" updateTime="1698941776982" updateUser="ExternalLinkService" zenodo-license-document="CLOSED">
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<mods:title id="A869C9E053984D351B5915291C95F7DF">Fungal symbioses in bryophytes: New insights in the Twenty First Century</mods:title>
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<treatment id="03F587D3FFDAB947B5974D8CFEE9FBB9" ID-DOI="http://doi.org/10.5281/zenodo.5076291" ID-GBIF-Taxon="182486523" ID-Zenodo-Dep="5076291" LSID="urn:lsid:plazi:treatment:03F587D3FFDAB947B5974D8CFEE9FBB9" httpUri="http://treatment.plazi.org/id/03F587D3FFDAB947B5974D8CFEE9FBB9" lastPageId="9" lastPageNumber="247" pageId="7" pageNumber="245">
<subSubSection id="C346654EFFDAB949B5974D8CFE88FA46" box="[151,328,1427,1453]" pageId="7" pageNumber="245" type="nomenclature">
<paragraph id="8BE336C5FFDAB949B5974D8CFE88FA46" blockId="7.[151,1436,1427,2033]" box="[151,328,1427,1453]" pageId="7" pageNumber="245">
<heading id="D0AB81A9FFDAB949B5974D8CFE88FA46" bold="true" box="[151,328,1427,1453]" fontSize="10" level="2" pageId="7" pageNumber="245" reason="2">
<emphasis id="B928EAD7FFDAB949B5974D8CFE88FA46" bold="true" box="[151,328,1427,1453]" pageId="7" pageNumber="245">
a)
<taxonomicName id="4C5C4D46FFDAB949B5B64D8CFE88FA46" authority="Klinggr., 1858" box="[182,328,1427,1453]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
</emphasis>
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<paragraph id="8BE336C5FFDAB949B5974DA5FE80F909" blockId="7.[151,1436,1427,2033]" pageId="7" pageNumber="245">
The
<taxonomicName id="4C5C4D46FFDAB949B5CC4DA5FE96FA3F" authority="Klinggr., 1858" box="[204,342,1466,1492]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
are the only thalloid liverworts found to date to contain basidiomycetous endophytes clearly identified as such by the presence of dolipore septa (
<figureCitation id="13672A40FFDAB949B6074DFEFC45FA10" box="[775,901,1505,1531]" captionStart="FIGURE 4" captionStartId="8.[150,255,1825,1849]" captionTargetBox="[151,1436,306,1801]" captionTargetId="figure-162@8.[151,1436,306,1801]" captionTargetPageId="8" captionText="FIGURE 4. Basidiomycetes in the Aneuraceae. A-D. Scanning electron micrographs. E, F. Transmission electron micrographs. A, B. Riccardia cochleata. A. Rhizomes extending into the substratum from the lower surface of a thallus (arrowed). B. Hyphal coils in an epidermal cell of a rhizome. C, D. Riccardia pennata. C. Lower epidermal cells almost completely filled by hyphae (h) showing no sign of degeneration. D. Detail of septum with dolipore (d). E, F. Verdoornia succulenta R.M.Schust.. E. Infected cell with healthy (h) and degenerating (dh) hyphae. F. Detail of a typical dolipore septum (d). Scale bars = (A) 500 µm; (B, C, E) 10 µm; (D, F) 2 µm." figureDoi="http://doi.org/10.5281/zenodo.4895370" httpUri="https://zenodo.org/record/4895370/files/figure.png" pageId="7" pageNumber="245">Fig. 4D, F</figureCitation>
) (
<bibRefCitation id="EFCD4B34FFDAB949B69D4DFEFB6DFA10" author="Bidartondo, M. I. &amp; Bruns, T. D. &amp; Weiss, M. &amp; Sergio, C. &amp; Read, D. J." box="[925,1197,1505,1531]" pageId="7" pageNumber="245" pagination="835 - 842" refId="ref6950" refString="Bidartondo, M. I., Bruns, T. D., Weiss, M., Sergio, C. &amp; Read, D. J. (2003) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proceedings of the Royal Society B. 270: 835 - 842." type="journal article" year="2003">
Bidartondo
<emphasis id="B928EAD7FFDAB949B12C4DFEFBA7FA11" box="[1068,1127,1505,1530]" italics="true" pageId="7" pageNumber="245">et al.</emphasis>
2003
</bibRefCitation>
;
<bibRefCitation id="EFCD4B34FFDAB949B1BB4DFEFF23F9CA" author="Duckett, J. G. &amp; Ligrone, R." pageId="7" pageNumber="245" pagination="346 - 358" refId="ref7699" refString="Duckett, J. G. &amp; Ligrone, R. (2008 a) A cytological analysis of basidiomycetous endophytes in New Zealand Aneuraceae (simple thalloid liverworts, Metzgeriidae); confirmation of the derived status of Verdoornia. Canadian Journal of Botany 86: 346 - 358." type="journal article" year="2008">Duckett &amp; Ligrone 2008a</bibRefCitation>
, b;
<bibRefCitation id="EFCD4B34FFDAB949B4114E18FDC0F9CA" author="Ligrone, R. &amp; Pocock, K. &amp; Duckett, J. G." box="[273,512,1543,1569]" pageId="7" pageNumber="245" pagination="666 - 679" refId="ref9149" refString="Ligrone, R., Pocock, K. &amp; Duckett, J. G. (1993) A comparative ultrastructural study of the endophytic basidiomycetes in the parasitic hepatic Cryptothallus mirabilis and the closely allied photosynthetic species Aneura pinguis (Metzgeriales). Canadian Journal of Botany 71: 666 - 679." type="journal article" year="1993">
Ligrone
<emphasis id="B928EAD7FFDAB949B47A4E18FE77F9CB" box="[378,439,1543,1568]" italics="true" pageId="7" pageNumber="245">et al.</emphasis>
1993
</bibRefCitation>
;
<bibRefCitation id="EFCD4B34FFDAB949B70E4E18FD25F9CA" author="Nebel, M. &amp; Kreier, H. - P. &amp; Preussing, M. &amp; Weiss, M. A." box="[526,741,1543,1569]" pageId="7" pageNumber="245" pagination="339 - 360" refId="ref9433" refString="Nebel, M., Kreier, H. - P., Preussing, M. &amp; Weiss, M. A. (2004) Symbiotic fungal associations with liverworts are the possible ancestors of mycorrhizae. In: Agerer, R., Piepenbring, H. &amp; Blanz, P. (Eds.), Frontiers in Basidiomycote Mycology, HIW-Verlag, Ecking, Germany, pp. 339 - 360." type="book chapter" year="2004">
Nebel
<emphasis id="B928EAD7FFDAB949B75E4E18FD5CF9CB" box="[606,668,1543,1568]" italics="true" pageId="7" pageNumber="245">et al.</emphasis>
2004
</bibRefCitation>
;
<bibRefCitation id="EFCD4B34FFDAB949B7F34E18FC31F9CA" author="Preussing, M. &amp; Nebel, M. &amp; Oberwinkler, M. &amp; Weiss, M." box="[755,1009,1543,1569]" pageId="7" pageNumber="245" pagination="147 - 159" refId="ref9893" refString="Preussing, M., Nebel, M., Oberwinkler, M. &amp; Weiss, M. (2010) Diverging diversity patterns in Tulasnella (Basidiomycota, Tulasnellales) mycobionts of Aneura pinguis (Marchantiophyta, Metzgeriales) from Europe and Ecuador. Mycorrhiza 20: 147 - 159." type="journal article" year="2010">
Preussing
<emphasis id="B928EAD7FFDAB949B6684E18FC5EF9CB" box="[872,926,1543,1568]" italics="true" pageId="7" pageNumber="245">et al</emphasis>
. 2010
</bibRefCitation>
). The endophyte-host relationships recall those in orchids with the formation of hyphal coils in the colonised cells. These are then digested by the host to be followed by one or more reinfection cycles. As in the Marchantiophyta, the number of cell layers colonized by the fungus varies among taxa: from two to five in Chilean and
<collectingCountry id="F34B7655FFDAB949B10B4E64FB67F97E" box="[1035,1191,1659,1685]" name="New Zealand" pageId="7" pageNumber="245">New Zealand</collectingCountry>
species of
<taxonomicName id="4C5C4D46FFDAB949B0284E64FABEF97F" ID-CoL="9G2DJ" authority="Dumort." authorityName="Dumort." box="[1320,1406,1659,1684]" class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="7" pageNumber="245" phylum="Arthropoda" rank="genus">
<emphasis id="B928EAD7FFDAB949B0284E64FABEF97F" box="[1320,1406,1659,1684]" italics="true" pageId="7" pageNumber="245">Aneura</emphasis>
</taxonomicName>
to approximately half the thallus in northern hemisphere
<taxonomicName id="4C5C4D46FFDAB949B63E4EBDFC34F957" authority="L." box="[830,1012,1698,1724]" class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="7" pageNumber="245" phylum="Arthropoda" rank="species" species="pinguis">
<emphasis id="B928EAD7FFDAB949B63E4EBDFC7CF950" box="[830,956,1698,1723]" italics="true" pageId="7" pageNumber="245">A. pinguis</emphasis>
(L.)
</taxonomicName>
Dumort. to virtually every cell in
<emphasis id="B928EAD7FFDAB949B5974ED6FE80F909" box="[151,320,1737,1762]" italics="true" pageId="7" pageNumber="245">
<taxonomicName id="4C5C4D46FFDAB949B5974ED6FEFCF909" box="[151,316,1737,1762]" class="Jungermanniopsida" family="Aneuraceae" genus="Cryptothallus" higherTaxonomySource="CoL" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Marchantiophyta" rank="genus">Cryptothallus</taxonomicName>
.
</emphasis>
</paragraph>
<paragraph id="8BE336C5FFDAB947B5C64EF0FF28FECD" blockId="7.[151,1436,1427,2033]" lastBlockId="9.[151,1436,152,1106]" lastPageId="9" lastPageNumber="247" pageId="7" pageNumber="245">
Whilst this kind of association is also found in
<taxonomicName id="4C5C4D46FFDAB949B7EA4EF0FBC6F8E2" authority="R. M. Schust." authorityName="R. M. Schust." box="[746,1030,1775,1801]" class="Jungermanniopsida" family="Aneuraceae" genus="Verdoornia" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Bryophyta" rank="genus">
<emphasis id="B928EAD7FFDAB949B7EA4EF0FCADF8E3" box="[746,877,1775,1800]" italics="true" pageId="7" pageNumber="245">Verdoornia</emphasis>
R.M.Schust.
</taxonomicName>
(
<bibRefCitation id="EFCD4B34FFDAB949B1144EF0FA85F8E2" author="Duckett, J. G. &amp; Ligrone, R." box="[1044,1349,1775,1801]" pageId="7" pageNumber="245" pagination="346 - 358" refId="ref7699" refString="Duckett, J. G. &amp; Ligrone, R. (2008 a) A cytological analysis of basidiomycetous endophytes in New Zealand Aneuraceae (simple thalloid liverworts, Metzgeriidae); confirmation of the derived status of Verdoornia. Canadian Journal of Botany 86: 346 - 358." type="journal article" year="2008">Duckett &amp; Ligrone 2008a</bibRefCitation>
) and in nearly all collections of
<taxonomicName id="4C5C4D46FFDAB949B4B44F09FDB5F8DB" ID-CoL="9G2DJ" authority="Dumort." authorityName="Dumort." box="[436,629,1814,1840]" class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="7" pageNumber="245" phylum="Arthropoda" rank="genus">
<emphasis id="B928EAD7FFDAB949B4B44F09FDCAF8C4" box="[436,522,1814,1839]" italics="true" pageId="7" pageNumber="245">Aneura</emphasis>
Dumort.
</taxonomicName>
examined to date with the exception of
<taxonomicName id="4C5C4D46FFDAB949B14F4F09FA88F8DB" authority="(Horik.)" baseAuthorityName="Horik." box="[1103,1352,1814,1840]" class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="7" pageNumber="245" phylum="Arthropoda" rank="species" species="pellioides">
<emphasis id="B928EAD7FFDAB949B14F4F09FB22F8C4" box="[1103,1250,1814,1839]" italics="true" pageId="7" pageNumber="245">A. pellioides</emphasis>
(Horik.)
</taxonomicName>
and
<taxonomicName id="4C5C4D46FFDAB949B0834F09FF2DF8BD" authority="L." class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="7" pageNumber="245" phylum="Arthropoda" rank="species" species="pinguis">
<emphasis id="B928EAD7FFDAB949B0834F09FF2DF8BD" italics="true" pageId="7" pageNumber="245">A. pinguis</emphasis>
</taxonomicName>
from California (
<bibRefCitation id="EFCD4B34FFDAB949B4BC4F23FCCDF8BD" author="Bidartondo, M. I. &amp; Duckett, J. G." box="[444,781,1852,1878]" pageId="7" pageNumber="245" pagination="485 - 492" refId="ref7007" refString="Bidartondo, M. I. &amp; 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 &amp; Duckett 2010</bibRefCitation>
), the sister genus
<taxonomicName id="4C5C4D46FFDAB949B6DF4F22FB54F8BD" authority="Gray" authorityName="Gray" box="[991,1172,1852,1878]" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Bryophyta" rank="genus">
<emphasis id="B928EAD7FFDAB949B6DF4F22FB91F8BD" box="[991,1105,1853,1878]" italics="true" pageId="7" pageNumber="245">Riccardia</emphasis>
Gray
</taxonomicName>
is almost fungus-free. In three
<taxonomicName id="4C5C4D46FFDAB949B5FD4F7CFEB2F897" authority="Gray" authorityName="Gray" box="[253,370,1891,1916]" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Bryophyta" rank="genus">
<emphasis id="B928EAD7FFDAB949B5FD4F7CFEB2F897" box="[253,370,1891,1916]" italics="true" pageId="7" pageNumber="245">Riccardia</emphasis>
</taxonomicName>
taxa, all
<collectingCountry id="F34B7655FFDAB949B4E34F7CFD44F896" box="[483,644,1891,1917]" name="New Zealand" pageId="7" pageNumber="245">New Zealand</collectingCountry>
endemics, where an endophyte is present the associations appear distinctively different from those in
<taxonomicName id="4C5C4D46FFDAB949B73F4F95FD55F848" ID-CoL="9G2DJ" box="[575,661,1930,1955]" class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="7" pageNumber="245" phylum="Arthropoda" rank="genus">
<emphasis id="B928EAD7FFDAB949B73F4F95FD55F848" box="[575,661,1930,1955]" italics="true" pageId="7" pageNumber="245">Aneura</emphasis>
</taxonomicName>
. Two of these we describe here for the first time (
<figureCitation id="13672A40FFDAB949B1DF4F95FAA2F84F" box="[1247,1378,1930,1956]" captionStart="FIGURE 4" captionStartId="8.[150,255,1825,1849]" captionTargetBox="[151,1436,306,1801]" captionTargetId="figure-162@8.[151,1436,306,1801]" captionTargetPageId="8" captionText="FIGURE 4. Basidiomycetes in the Aneuraceae. A-D. Scanning electron micrographs. E, F. Transmission electron micrographs. A, B. Riccardia cochleata. A. Rhizomes extending into the substratum from the lower surface of a thallus (arrowed). B. Hyphal coils in an epidermal cell of a rhizome. C, D. Riccardia pennata. C. Lower epidermal cells almost completely filled by hyphae (h) showing no sign of degeneration. D. Detail of septum with dolipore (d). E, F. Verdoornia succulenta R.M.Schust.. E. Infected cell with healthy (h) and degenerating (dh) hyphae. F. Detail of a typical dolipore septum (d). Scale bars = (A) 500 µm; (B, C, E) 10 µm; (D, F) 2 µm." figureDoi="http://doi.org/10.5281/zenodo.4895370" httpUri="https://zenodo.org/record/4895370/files/figure.png" pageId="7" pageNumber="245">Fig. 4AD</figureCitation>
), but a third species
<taxonomicName id="4C5C4D46FFDAB949B4464FAEFDB9F820" authority="A. E. Brown" authorityName="A. E. Brown" box="[326,633,1969,1995]" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Bryophyta" rank="species" species="intercellula">
<emphasis id="B928EAD7FFDAB949B4464FAEFE2CF821" box="[326,492,1969,1994]" italics="true" pageId="7" pageNumber="245">R. intercellula</emphasis>
A.E.Brown
</taxonomicName>
is known from but a single collection and has never been refound in nature (
<bibRefCitation id="EFCD4B34FFDAB949B5F04FC8FDD9F81A" author="Brown, E. A. &amp; Braggins, J. E." box="[240,537,2007,2033]" pageId="7" pageNumber="245" pagination="1 - 132" refId="ref7117" refString="Brown, E. A. &amp; Braggins, J. E. (1989) A revision of the genus Riccardia S. F. Gray in New Zealand with notes on the genus Aneura Dum. Journal of the Hattori Botanical Laboratory 66: 1 - 132." type="journal article" year="1989">Brown &amp; Braggins 1989</bibRefCitation>
). In
<taxonomicName id="4C5C4D46FFDAB949B74D4FC8FC9AF81A" authority="A. E. Brown" authorityName="A. E. Brown" box="[589,858,2007,2033]" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="7" pageNumber="245" phylum="Bryophyta" rank="species" species="pennata">
<emphasis id="B928EAD7FFDAB949B74D4FC8FD0CF81B" box="[589,716,2007,2032]" italics="true" pageId="7" pageNumber="245">R. pennata</emphasis>
A.E.Brown
</taxonomicName>
, prominent basidiomycetous hyphal coils, which show no signs of digestion by the host, fill the ventral epidermal cells (
<figureCitation id="13672A40FFD5B946B6E04887FBFEFF59" box="[992,1086,152,178]" captionStart="FIGURE 4" captionStartId="8.[150,255,1825,1849]" captionTargetBox="[151,1436,306,1801]" captionTargetId="figure-162@8.[151,1436,306,1801]" captionTargetPageId="8" captionText="FIGURE 4. Basidiomycetes in the Aneuraceae. A-D. Scanning electron micrographs. E, F. Transmission electron micrographs. A, B. Riccardia cochleata. A. Rhizomes extending into the substratum from the lower surface of a thallus (arrowed). B. Hyphal coils in an epidermal cell of a rhizome. C, D. Riccardia pennata. C. Lower epidermal cells almost completely filled by hyphae (h) showing no sign of degeneration. D. Detail of septum with dolipore (d). E, F. Verdoornia succulenta R.M.Schust.. E. Infected cell with healthy (h) and degenerating (dh) hyphae. F. Detail of a typical dolipore septum (d). Scale bars = (A) 500 µm; (B, C, E) 10 µm; (D, F) 2 µm." figureDoi="http://doi.org/10.5281/zenodo.4895370" httpUri="https://zenodo.org/record/4895370/files/figure.png" pageId="8" pageNumber="246">Fig. 4C</figureCitation>
). Even more remarkable is
<taxonomicName id="4C5C4D46FFD5B946B0834887FEC9FF33" authorityName="Kuntze" authorityYear="1891" baseAuthorityName="Hook.f. &amp; Taylor" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="8" pageNumber="246" phylum="Bryophyta" rank="species" species="cochleata">
<emphasis id="B928EAD7FFD5B946B0834887FEC9FF33" italics="true" pageId="8" pageNumber="246">R. cochleata</emphasis>
</taxonomicName>
(Hook.f. &amp; Taylor) Kuntze. This species produces achlorophyllous radially symmetrical rhizomes (
<bibRefCitation id="EFCD4B34FFD4B947B59F4887FE0AFF59" author="Brown, E. A. &amp; Braggins, J. E." box="[159,458,152,178]" pageId="9" pageNumber="247" pagination="1 - 132" refId="ref7117" refString="Brown, E. A. &amp; Braggins, J. E. (1989) A revision of the genus Riccardia S. F. Gray in New Zealand with notes on the genus Aneura Dum. Journal of the Hattori Botanical Laboratory 66: 1 - 132." type="journal article" year="1989">Brown &amp; Braggins 1989</bibRefCitation>
) recalling the roots of
<taxonomicName id="4C5C4D46FFD4B947B7F04887FC58FF5A" box="[752,920,152,177]" class="Haplomitriopsida" family="Haplomitriaceae" genus="Haplomitrium" kingdom="Plantae" order="Calobryales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
<emphasis id="B928EAD7FFD4B947B7F04887FC58FF5A" box="[752,920,152,177]" italics="true" pageId="9" pageNumber="247">Haplomitrium</emphasis>
</taxonomicName>
but lacking the mucilage investiture of the latter (
<figureCitation id="13672A40FFD4B947B5E348A1FE81FF33" box="[227,321,190,216]" captionStart="FIGURE 4" captionStartId="8.[150,255,1825,1849]" captionTargetBox="[151,1436,306,1801]" captionTargetId="figure-162@8.[151,1436,306,1801]" captionTargetPageId="8" captionText="FIGURE 4. Basidiomycetes in the Aneuraceae. A-D. Scanning electron micrographs. E, F. Transmission electron micrographs. A, B. Riccardia cochleata. A. Rhizomes extending into the substratum from the lower surface of a thallus (arrowed). B. Hyphal coils in an epidermal cell of a rhizome. C, D. Riccardia pennata. C. Lower epidermal cells almost completely filled by hyphae (h) showing no sign of degeneration. D. Detail of septum with dolipore (d). E, F. Verdoornia succulenta R.M.Schust.. E. Infected cell with healthy (h) and degenerating (dh) hyphae. F. Detail of a typical dolipore septum (d). Scale bars = (A) 500 µm; (B, C, E) 10 µm; (D, F) 2 µm." figureDoi="http://doi.org/10.5281/zenodo.4895370" httpUri="https://zenodo.org/record/4895370/files/figure.png" pageId="9" pageNumber="247">Fig. 4A</figureCitation>
). While the fleshy surface-growing thalli are fungus-free, the first investigation of the anatomy of the rhizomes revealed that the epidermal cells are packed with hyphal coils (
<figureCitation id="13672A40FFD4B947B12E48FAFB48FF14" box="[1070,1160,229,255]" captionStart="FIGURE 4" captionStartId="8.[150,255,1825,1849]" captionTargetBox="[151,1436,306,1801]" captionTargetId="figure-162@8.[151,1436,306,1801]" captionTargetPageId="8" captionText="FIGURE 4. Basidiomycetes in the Aneuraceae. A-D. Scanning electron micrographs. E, F. Transmission electron micrographs. A, B. Riccardia cochleata. A. Rhizomes extending into the substratum from the lower surface of a thallus (arrowed). B. Hyphal coils in an epidermal cell of a rhizome. C, D. Riccardia pennata. C. Lower epidermal cells almost completely filled by hyphae (h) showing no sign of degeneration. D. Detail of septum with dolipore (d). E, F. Verdoornia succulenta R.M.Schust.. E. Infected cell with healthy (h) and degenerating (dh) hyphae. F. Detail of a typical dolipore septum (d). Scale bars = (A) 500 µm; (B, C, E) 10 µm; (D, F) 2 µm." figureDoi="http://doi.org/10.5281/zenodo.4895370" httpUri="https://zenodo.org/record/4895370/files/figure.png" pageId="9" pageNumber="247">Fig. 4B</figureCitation>
) that undergo digestion cycles.
</paragraph>
</subSubSection>
<caption id="DF23664DFFD5B946B5964F3EFBE3F80D" ID-DOI="http://doi.org/10.5281/zenodo.4895370" ID-Zenodo-Dep="4895370" httpUri="https://zenodo.org/record/4895370/files/figure.png" pageId="8" pageNumber="246" startId="8.[150,255,1825,1849]" targetBox="[151,1436,306,1801]" targetPageId="8">
<paragraph id="8BE336C5FFD5B946B5964F3EFBE3F80D" blockId="8.[150,1436,1825,2023]" pageId="8" pageNumber="246">
<emphasis id="B928EAD7FFD5B946B5964F3EFEDBF8D2" bold="true" box="[150,283,1825,1849]" pageId="8" pageNumber="246">FIGURE 4.</emphasis>
Basidiomycetes in the
<taxonomicName id="4C5C4D46FFD5B946B7234F3DFD66F8D2" box="[547,678,1826,1849]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="8" pageNumber="246" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
.
<emphasis id="B928EAD7FFD5B946B7B94F3EFD30F8D2" bold="true" box="[697,752,1825,1849]" pageId="8" pageNumber="246">A-D.</emphasis>
Scanning electron micrographs.
<emphasis id="B928EAD7FFD5B946B1684F3EFB5DF8D2" bold="true" box="[1128,1181,1825,1849]" pageId="8" pageNumber="246">E, F.</emphasis>
Transmission electron micrographs.
<emphasis id="B928EAD7FFD5B946B4294F5BFEA2F8B7" bold="true" box="[297,354,1860,1884]" pageId="8" pageNumber="246">A, B.</emphasis>
<taxonomicName id="4C5C4D46FFD5B946B46F4F5BFD85F8B0" authorityName="Kuntze" authorityYear="1891" baseAuthorityName="Hook.f. &amp; Taylor" box="[367,581,1860,1883]" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="8" pageNumber="246" phylum="Bryophyta" rank="species" species="cochleata">
<emphasis id="B928EAD7FFD5B946B46F4F5BFD85F8B0" box="[367,581,1860,1883]" italics="true" pageId="8" pageNumber="246">Riccardia cochleata</emphasis>
</taxonomicName>
.
<emphasis id="B928EAD7FFD5B946B7594F5BFDB3F8B7" bold="true" box="[601,627,1860,1884]" pageId="8" pageNumber="246">A.</emphasis>
Rhizomes extending into the substratum from the lower surface of a thallus (arrowed).
<emphasis id="B928EAD7FFD5B946B4184F78FEF0F894" bold="true" box="[280,304,1895,1919]" pageId="8" pageNumber="246">B.</emphasis>
Hyphal coils in an epidermal cell of a rhizome.
<emphasis id="B928EAD7FFD5B946B6544F78FC50F894" bold="true" box="[852,912,1895,1919]" pageId="8" pageNumber="246">C, D.</emphasis>
<taxonomicName id="4C5C4D46FFD5B946B69F4F78FBA8F895" box="[927,1128,1895,1918]" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="8" pageNumber="246" phylum="Bryophyta" rank="species" species="pennata">
<emphasis id="B928EAD7FFD5B946B69F4F78FBA8F895" box="[927,1128,1895,1918]" italics="true" pageId="8" pageNumber="246">Riccardia pennata</emphasis>
</taxonomicName>
.
<emphasis id="B928EAD7FFD5B946B17E4F78FB58F894" bold="true" box="[1150,1176,1895,1919]" pageId="8" pageNumber="246">C.</emphasis>
Lower epidermal cells almost completely filled by hyphae (h) showing no sign of degeneration.
<emphasis id="B928EAD7FFD5B946B6B74F96FC11F84A" bold="true" box="[951,977,1929,1953]" pageId="8" pageNumber="246">D.</emphasis>
Detail of septum with dolipore (d).
<emphasis id="B928EAD7FFD5B946B0674F96FA5CF84A" bold="true" box="[1383,1436,1929,1953]" pageId="8" pageNumber="246">E, F.</emphasis>
<taxonomicName id="4C5C4D46FFD5B946B5974FB3FDDDF828" authority="R. M. Schust" authorityName="R. M. Schust" box="[151,541,1964,1987]" class="Jungermanniopsida" family="Aneuraceae" genus="Verdoornia" kingdom="Plantae" order="Metzgeriales" pageId="8" pageNumber="246" phylum="Bryophyta" rank="species" species="succulenta">
<emphasis id="B928EAD7FFD5B946B5974FB3FE50F828" box="[151,400,1964,1987]" italics="true" pageId="8" pageNumber="246">Verdoornia succulenta</emphasis>
R.M.Schust
</taxonomicName>
..
<emphasis id="B928EAD7FFD5B946B7304FB3FD89F82F" bold="true" box="[560,585,1964,1988]" pageId="8" pageNumber="246">E.</emphasis>
Infected cell with healthy (h) and degenerating (dh) hyphae.
<emphasis id="B928EAD7FFD5B946B0014FB3FAD6F82F" bold="true" box="[1281,1302,1964,1988]" pageId="8" pageNumber="246">F.</emphasis>
Detail of a typical dolipore septum (d). Scale bars = (A) 500 µm; (B, C, E) 10 µm; (D, F) 2 µm.
</paragraph>
</caption>
<subSubSection id="C346654EFFD4B947B5C6492DFEE9FBB9" pageId="9" pageNumber="247" type="description">
<paragraph id="8BE336C5FFD4B947B5C6492DFEE9FBB9" blockId="9.[151,1436,152,1106]" pageId="9" pageNumber="247">
The fact that the
<taxonomicName id="4C5C4D46FFD4B947B49F492DFDE9FEA7" box="[415,553,306,332]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
forms the crown group of an otherwise fungus-free lineage comprising
<taxonomicName id="4C5C4D46FFD4B947B5974946FEBFFE98" authority="Dumort." authorityName="Dumort." box="[151,383,345,371]" class="Jungermanniopsida" family="Pleuroziaceae" genus="Pleurozia" kingdom="Plantae" order="Pleuroziales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
<emphasis id="B928EAD7FFD4B947B5974946FECEFE99" box="[151,270,345,370]" italics="true" pageId="9" pageNumber="247">Pleurozia</emphasis>
Dumort.
</taxonomicName>
,
<taxonomicName id="4C5C4D46FFD4B947B4904946FD0DFE98" authority="E. A. Hodgs." authorityName="E. A. Hodgs." box="[400,717,345,371]" class="Jungermanniopsida" family="Phyllothalliaceae" genus="Phyllothallia" kingdom="Plantae" order="Pallaviciniales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="genus">
<emphasis id="B928EAD7FFD4B947B4904946FDF2FE99" box="[400,562,345,370]" italics="true" pageId="9" pageNumber="247">Phyllothallia</emphasis>
E.A.Hodgs.
</taxonomicName>
and the
<taxonomicName id="4C5C4D46FFD4B947B63B4946FC2FFE98" box="[827,1007,345,371]" class="Jungermanniopsida" family="Metzgeriaceae" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Metzgeriaceae</taxonomicName>
and the discovery from the initial molecular studies that the fungus from both
<taxonomicName id="4C5C4D46FFD4B947B799499FFD2FFE72" box="[665,751,384,409]" class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="9" pageNumber="247" phylum="Arthropoda" rank="genus">
<emphasis id="B928EAD7FFD4B947B799499FFD2FFE72" box="[665,751,384,409]" italics="true" pageId="9" pageNumber="247">Aneura</emphasis>
</taxonomicName>
and
<taxonomicName id="4C5C4D46FFD4B947B626499FFC07FE72" box="[806,967,384,409]" class="Jungermanniopsida" family="Aneuraceae" genus="Cryptothallus" higherTaxonomySource="CoL" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Marchantiophyta" rank="genus">
<emphasis id="B928EAD7FFD4B947B626499FFC07FE72" box="[806,967,384,409]" italics="true" pageId="9" pageNumber="247">Cryptothallus</emphasis>
</taxonomicName>
belongs to the derived genus
<taxonomicName id="4C5C4D46FFD4B947B022499FFF3FFE2B" authority="J. Schrot." authorityName="J. Schrot." class="Agaricomycetes" family="Tulasnellaceae" genus="Tulasnella" kingdom="Fungi" order="Cantharellales" pageId="9" pageNumber="247" phylum="Basidiomycota" rank="genus">
<emphasis id="B928EAD7FFD4B947B022499FFA5CFE72" box="[1314,1436,384,409]" italics="true" pageId="9" pageNumber="247">Tulasnella</emphasis>
J.Schröt.
</taxonomicName>
(
<bibRefCitation id="EFCD4B34FFD4B947B40F49B9FDE2FE2B" author="Bidartondo, M. I. &amp; Bruns, T. D. &amp; Weiss, M. &amp; Sergio, C. &amp; Read, D. J." box="[271,546,422,448]" pageId="9" pageNumber="247" pagination="835 - 842" refId="ref6950" refString="Bidartondo, M. I., Bruns, T. D., Weiss, M., Sergio, C. &amp; Read, D. J. (2003) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proceedings of the Royal Society B. 270: 835 - 842." type="journal article" year="2003">
Bidartondo
<emphasis id="B928EAD7FFD4B947B49E49B8FE1BFE2B" box="[414,475,423,448]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
2003
</bibRefCitation>
;
<bibRefCitation id="EFCD4B34FFD4B947B72E49B9FCC9FE2B" author="Kottke, I. &amp; Beiter, A. &amp; Weiss, M. &amp; Haug, I. &amp; Oberwinkler, F. &amp; Nebel, M." box="[558,777,422,448]" pageId="9" pageNumber="247" pagination="957 - 968" refId="ref8862" refString="Kottke, I., Beiter, A., Weiss, M., Haug, I., Oberwinkler, F. &amp; 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="B928EAD7FFD4B947B78849B8FD04FE2B" box="[648,708,423,448]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
2003
</bibRefCitation>
) indicate that the aneuracean associations are of recent origin. Much more extensive sequencing investigations (
<bibRefCitation id="EFCD4B34FFD4B947B63949D2FB4CFE0C" author="Bidartondo, M. I. &amp; Duckett, J. G." box="[825,1164,461,487]" pageId="9" pageNumber="247" pagination="485 - 492" refId="ref7007" refString="Bidartondo, M. I. &amp; 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 &amp; Duckett 2010</bibRefCitation>
;
<bibRefCitation id="EFCD4B34FFD4B947B19849D2FA4FFE0C" author="Preussing, M. &amp; Nebel, M. &amp; Oberwinkler, M. &amp; Weiss, M." box="[1176,1423,461,487]" pageId="9" pageNumber="247" pagination="147 - 159" refId="ref9893" refString="Preussing, M., Nebel, M., Oberwinkler, M. &amp; Weiss, M. (2010) Diverging diversity patterns in Tulasnella (Basidiomycota, Tulasnellales) mycobionts of Aneura pinguis (Marchantiophyta, Metzgeriales) from Europe and Ecuador. Mycorrhiza 20: 147 - 159." type="journal article" year="2010">
Preussing
<emphasis id="B928EAD7FFD4B947B00B49D2FA80FE0D" box="[1291,1344,461,486]" italics="true" pageId="9" pageNumber="247">et al</emphasis>
. 2010
</bibRefCitation>
), embracing over one hundred collections of the
<taxonomicName id="4C5C4D46FFD4B947B7E049EBFCB3FDE5" box="[736,883,500,526]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
, revealed that whilst in the vast majority the fungus is
<emphasis id="B928EAD7FFD4B947B4074A05FE48FDD8" box="[263,392,538,563]" italics="true" pageId="9" pageNumber="247">
<taxonomicName id="4C5C4D46FFD4B947B4074A05FE44FDD8" box="[263,388,538,563]" class="Agaricomycetes" family="Tulasnellaceae" genus="Tulasnella" kingdom="Fungi" order="Cantharellales" pageId="9" pageNumber="247" phylum="Basidiomycota" rank="genus">Tulasnella</taxonomicName>
,
</emphasis>
two gatherings (from
<collectingCountry id="F34B7655FFD4B947B78D4A05FD0DFDDF" box="[653,717,538,564]" name="Chile" pageId="9" pageNumber="247">Chile</collectingCountry>
and
<collectingCountry id="F34B7655FFD4B947B6044A05FC52FDDF" box="[772,914,538,564]" name="Switzerland" pageId="9" pageNumber="247">Switzerland</collectingCountry>
) contained
<taxonomicName id="4C5C4D46FFD4B947B1194A05FB7CFDDF" authority="Tul." authorityName="Tul." box="[1049,1212,538,564]" class="Agaricomycetes" family="Sebacinaceae" genus="Sebacina" kingdom="Fungi" order="Sebacinales" pageId="9" pageNumber="247" phylum="Basidiomycota" rank="genus">
<emphasis id="B928EAD7FFD4B947B1194A05FB44FDD8" box="[1049,1156,538,563]" italics="true" pageId="9" pageNumber="247">Sebacina</emphasis>
Tul.
</taxonomicName>
, the basidiomycete genus characteristic of leafy liverworts (
<bibRefCitation id="EFCD4B34FFD4B947B77B4A5EFC9DFDB0" author="Kottke, I. &amp; Beiter, A. &amp; Weiss, M. &amp; Haug, I. &amp; Oberwinkler, F. &amp; Nebel, M." box="[635,861,577,603]" pageId="9" pageNumber="247" pagination="957 - 968" refId="ref8862" refString="Kottke, I., Beiter, A., Weiss, M., Haug, I., Oberwinkler, F. &amp; 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="B928EAD7FFD4B947B7D74A5EFCD4FDB1" box="[727,788,577,602]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
2003
</bibRefCitation>
). The molecular diversity discovered within the
<taxonomicName id="4C5C4D46FFD4B947B5974A77FED9FD6A" box="[151,281,616,641]" class="Agaricomycetes" family="Tulasnellaceae" genus="Tulasnella" kingdom="Fungi" order="Cantharellales" pageId="9" pageNumber="247" phylum="Basidiomycota" rank="genus">
<emphasis id="B928EAD7FFD4B947B5974A77FED9FD6A" box="[151,281,616,641]" italics="true" pageId="9" pageNumber="247">Tulasnella</emphasis>
</taxonomicName>
symbionts (
<bibRefCitation id="EFCD4B34FFD4B947B4B54A77FCDCFD69" author="Bidartondo, M. I. &amp; Duckett, J. G." box="[437,796,616,642]" pageId="9" pageNumber="247" pagination="485 - 492" refId="ref7007" refString="Bidartondo, M. I. &amp; 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 &amp; Duckett 2010</bibRefCitation>
;
<bibRefCitation id="EFCD4B34FFD4B947B62A4A77FBF1FD69" author="Preussing, M. &amp; Nebel, M. &amp; Oberwinkler, M. &amp; Weiss, M." box="[810,1073,616,642]" pageId="9" pageNumber="247" pagination="147 - 159" refId="ref9893" refString="Preussing, M., Nebel, M., Oberwinkler, M. &amp; Weiss, M. (2010) Diverging diversity patterns in Tulasnella (Basidiomycota, Tulasnellales) mycobionts of Aneura pinguis (Marchantiophyta, Metzgeriales) from Europe and Ecuador. Mycorrhiza 20: 147 - 159." type="journal article" year="2010">
Preussing
<emphasis id="B928EAD7FFD4B947B6A54A77FC1CFD6A" box="[933,988,616,641]" italics="true" pageId="9" pageNumber="247">et al</emphasis>
. 2010
</bibRefCitation>
), plus the rare occurrence of sebacinoids, in seemingly closely allied aneuracean taxa was at first sight most surprising. However recent molecular studies on the liverworts (Wackowiak
<emphasis id="B928EAD7FFD4B947B7E94AAAFCE6FD25" box="[745,806,693,718]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
2007;
<bibRefCitation id="EFCD4B34FFD4B947B67C4AAAFB63FD24" author="Baczkiewicz, A. &amp; Sawicki, J. &amp; Buczkowska, K. &amp; Polok, K. &amp; Zielinski, R." box="[892,1187,693,719]" pageId="9" pageNumber="247" pagination="3 - 21" refId="ref6796" refString="Baczkiewicz, A., Sawicki, J., Buczkowska, K., Polok, K. &amp; Zielinski, R. (2008) Application of different DNA markers in studies on cryptic species of Aneura pinguis (Jungermanniopsida, Metzgeriales). Cryptogamie Bryologie 29: 3 - 21." type="journal article" year="2008">
Baczkiewicz
<emphasis id="B928EAD7FFD4B947B11E4AAAFB9BFD25" box="[1054,1115,693,718]" italics="true" pageId="9" pageNumber="247">et al.</emphasis>
2008
</bibRefCitation>
;
<bibRefCitation id="EFCD4B34FFD4B947B1B04AAAFF13FD1D" author="Wickett, N. J. &amp; Goffinet, B." pageId="9" pageNumber="247" pagination="1 - 12" refId="ref10738" refString="Wickett, N. J. &amp; Goffinet, B. (2008) Origin and relationships of the myco-heterotrophic liverwort Cryptothallus mirabilis Malmb. (Metzgeriales, Marchantiophyta). Botanical Journal of the Linnean Society 156: 1 - 12." type="journal article" year="2008">Wickett &amp; Goffinet 2008</bibRefCitation>
) have revealed that conservative thallus morphology within the
<taxonomicName id="4C5C4D46FFD4B947B6C04AC3FB8AFD1D" box="[960,1098,732,758]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
conceals remarkable genetic diversity. In fact, the diversity in the endophytes closely mirrors that in the hosts and includes noteworthy congruence between the fungal and liverwort phylogenies. Indeed the nesting of
<taxonomicName id="4C5C4D46FFD4B947B1494B36FB2AFCA9" box="[1097,1258,809,834]" class="Jungermanniopsida" family="Aneuraceae" genus="Cryptothallus" higherTaxonomySource="CoL" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Marchantiophyta" rank="genus">
<emphasis id="B928EAD7FFD4B947B1494B36FB2AFCA9" box="[1097,1258,809,834]" italics="true" pageId="9" pageNumber="247">Cryptothallus</emphasis>
</taxonomicName>
within a single clade of
<taxonomicName id="4C5C4D46FFD4B947B4054B4FFD7EFC81" authority="(Wickett &amp; Goffinet 2008)" baseAuthorityName="Wickett &amp; Goffinet" baseAuthorityYear="2008" box="[261,702,848,874]" class="Insecta" family="Mycetophilidae" genus="Aneura" kingdom="Animalia" order="Diptera" pageId="9" pageNumber="247" phylum="Arthropoda" rank="genus">
<emphasis id="B928EAD7FFD4B947B4054B4FFEA0FC82" box="[261,352,848,873]" italics="true" pageId="9" pageNumber="247">Aneura</emphasis>
(
<bibRefCitation id="EFCD4B34FFD4B947B4724B4FFD76FC81" author="Wickett, N. J. &amp; Goffinet, B." box="[370,694,848,874]" pageId="9" pageNumber="247" pagination="1 - 12" refId="ref10738" refString="Wickett, N. J. &amp; Goffinet, B. (2008) Origin and relationships of the myco-heterotrophic liverwort Cryptothallus mirabilis Malmb. (Metzgeriales, Marchantiophyta). Botanical Journal of the Linnean Society 156: 1 - 12." type="journal article" year="2008">Wickett &amp; Goffinet 2008</bibRefCitation>
)
</taxonomicName>
, leading to the subsuming of the former into this genus is reinforced by the fungal data. Systematic considerations aside, with wholesale fungal digestion a standard feature of the aneuracean associations compared to those with basidiomycetes in leafy liverworts, it is perhaps not surprising that in this group we find the only achlorophyllose liverworts. Although on the one hand the fungus in the achlorophyllose rhizomes in
<taxonomicName id="4C5C4D46FFD4B947B7924BF5FC40FBE8" authorityName="Kuntze" authorityYear="1891" baseAuthorityName="Hook.f. &amp; Taylor" box="[658,896,1002,1027]" class="Jungermanniopsida" family="Aneuraceae" genus="Riccardia" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="species" species="cochleata">
<emphasis id="B928EAD7FFD4B947B7924BF5FC40FBE8" box="[658,896,1002,1027]" italics="true" pageId="9" pageNumber="247">Riccardia cochleata</emphasis>
</taxonomicName>
is most likely an independent acquisition, on the other the rhizomes perhaps provide an example as to how mycoheterotrophy may have evolved in the
<taxonomicName id="4C5C4D46FFD4B947B5974C27FEE5FBB9" box="[151,293,1080,1106]" class="Jungermanniopsida" family="Aneuraceae" kingdom="Plantae" order="Metzgeriales" pageId="9" pageNumber="247" phylum="Bryophyta" rank="family">Aneuraceae</taxonomicName>
.
</paragraph>
</subSubSection>
</treatment>
</document>