Research Article |
Corresponding author: Juan Larraín ( musgoschiloe@gmail.com ) Academic editor: Endymion Cooper
© 2015 Juan Larraín, Benjamin Carter, Blanka Shaw, Joern Hentschel, Lynika Strozier, Tatsuwo Furuki, Jochen Heinrichs, Barbara Crandall-Stotler, John Engel, Matt von Konrat.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Larraín J, Carter B, Shaw B, Hentschel J, Strozier LS, Furuki T, Heinrichs J, Crandall-Stotler B, Engel J, von Konrat M (2015) The resurrection of Neohattoria Kamim. (Jubulaceae, Marchantiophyta): a six decade systematic conflict resolved through a molecular perspective. PhytoKeys 50: 101-122. https://doi.org/10.3897/phytokeys.50.4940
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The systematic placement of Frullania herzogii has been contentious since its description six decades ago. Over the years it has been interpreted as either a member of the genus Frullania or segregated into its own genus, Neohattoria, due to morphological similarities with both Frullania and Jubula. Here we provide molecular evidence that supports the recognition of the genus Neohattoria and its inclusion within the Jubulaceae, together with Jubula and Nipponolejeunea. Jubulaceae are placed sister to Lejeuneaceae rather than to the monogeneric Frullaniaceae.
DNA sequence data, Frullania , Frullaniaceae , Japan, Jubula , Jubulaceae , Lejeuneaceae , liverwort, Nipponolejeunea
The liverwort Frullania herzogii S.Hatt. was originally described by
Later
In
Lack of useable specimens has previously precluded inclusion of Neohattoria in molecular phylogenetic studies. As a result of recent collecting activities, fresh material became available that allowed for successful DNA extraction and amplification. In the present study, we use molecular sequence data to investigate the phylogenetic position of Neohattoria. We investigate whether the genus should be placed in the Frullaniaceae or the Jubulaceae and evaluate whether molecular evidence supports the recognition of Neohattoria as a distinct genus.
For the production of microscopic images an Olympus BX51 microscope was used, equipped with both a QICAM Fast1394 camera from QIMAGING (Surrey, Canada), and a slide scanner (moving platform stage attached between the objectives and the condenser) from Objective Imaging Ltd. (Cambridge, UK). The software “Surveyor” from the latter company was used for the digitally rendered images.
We worked with two independent datasets to address two different questions, (1) what is the position of Neohattoria relative to the Frullaniaceae, Jubulaceae and Lejeuneaceae, and once we obtained results from these analyses, we asked (2) what is the position of Neohattoria within the Jubulaceae. For dataset 1 sequences were generated for two mitochondrial (nad1, rps3), and two chloroplast loci (psbA, rbcL), following DNA extraction, amplification and sequencing methods described by
For dataset 1 seven species of Radula were selected as outgroup taxa following the results already published in recent liverwort phylogenies (
Both datasets were analysed with PartitionFinder v1.1.0 (
The complete alignment for dataset 1 including all four regions mentioned above, with flanking areas pruned to avoid ambiguous readings, comprised 4818 characters for 54 accessions, of which 694 were parsimony informative. A total of 101 new sequences were generated for this study (Appendix
The complete alignment for dataset 2 including all four regions included, and after pruning the flanking areas to avoid ambiguous readings and deleting unalignable areas of the ITS region, comprised 3737 characters for 55 accessions, of which 548 were parsimony informative. The four different regions were not equally represented in the matrix, as shown in Appendix
Maximum likelihood (ML) tree showing the systematic position of Neohattoria herzogii within the Jubulaceae. Only 1/2 of the length of the branch between the Frullaniaceae and the Lejeuneaceae/Jubulaceae clade is depicted. Wide black branches indicate ML bootstrap support > 90 % and PP > 0.95.
The voucher of Neohattoria herzogii used for DNA extraction is illustrated in Figure
Our molecular analyses support recognition of the genus Neohattoria as distinct from the genus Frullania, as first proposed by
Our results strongly support the position of the Jubulaceae (containing Jubula, Nipponolejeunea and Neohattoria) sister to the Lejeuneaceae, and the Frullaniaceae as sister of the latter clade, although without significant support (Fig.
These three families (Frullaniaceae, Jubulaceae and Lejeuneaceae) share several morphological characters, including the leaves divided into two (or three) parts [lobe, lobule (and stylus)], the beaked perianths, the sporophyte enclosed in a stalked true calyptra, the bistratose capsule wall, and the vertically aligned elaters that are attached to the valve apices (
Assessing the importance of different morphological characters in circumscribing Frullaniaceae, Jubulaceae and Lejeuneaceae has been a difficult problem, but there are several characters that are consistent with the molecular phylogenetic results presented here. In most Lejeuneaceae a true stylus does not develop, but instead a single, unstalked slime papilla is formed at the junction of the lobule base and the stem, while in Jubula and Neohattoria there is a one- or two-celled filament terminated by a slime papilla in this position (
Morphologically, the monogeneric Frullaniaceae can be differentiated from the Jubulaceae by: (1) plants usually with conspicuous secondary pigmentation, often reddish; (2) initial leaves of branches either trifid or bifid; and (3) spores with rosette-like protrusions. Conversely, in the Jubulaceae the plants are: (1) soft and without secondary pigmentation (thus usually dull green to pale brown); (2) the initial leaves of branches are small, subtriangular, and never tri- or bifid; and (3) the spores without rosette-like protrusions. The first two of these characters support the placement of Neohattoria within Jubulaceae rather than Frullaniaceae (spores remain unknown in Neohattoria).
Chemically, Frullania species in general, produce significant amounts of sesquiterpene lactones, diterpenoids, and bibenzyl derivatives, which are considered important chemosystematic markers of the group (
Interestingly,
Our results place Neohattoria in the Jubulaceae with strong support, together with Nipponolejeunea and Jubula. Within the Jubulaceae, Neohattoria is resolved as sister to Nipponolejeunea, and this latter clade sister to Jubula, although this relationship is sensitive to taxon sampling (cf. Figs
Oil-bodies in Neohattoria are homogenous, usually more than ten per cell, and similar in size to chloroplasts (
Neohattoria Kamim., Journal of Japanese Botany 37: 218. 1962.
≡ Frullania subg. Dentatilobi Stotler & Crand.-Stotl., Memoirs of The New York Botanical Garden 45: 542. 1987 (“Dentatiloba”). syn.nov. – Type: Frullania herzogii S.Hatt.
We thank Anders Hagborg (The Field Museum) and Lars Söderström (Norwegian University of Science and Technology) and the Early Land Plants Today (ELPT) project for access to nomenclatural data. Support from the Biodiversity Synthesis Center of the Encyclopedia of Life provided important funding to help foster international initiatives. The Biodiversity Heritage Library is acknowledged for the facility they provide that has greatly accelerated our effort. The generous support by the National Science Foundation (Awards No. 1145898, 1146168, and 0531730) is gratefully acknowledged. We also recognize the support of the Museum Collection Spending Fund, administered by The Field Museum, as well as curatorial support provided by Yarency Rodriguez, Lucia Kawasaki and Anna Balla (The Field Museum). Lauren Smith is acknowledged for providing the digital images used to compile the plates. Finally, we thank Matt Renner and an anonymous reviewer for their help in improving the manuscript.
Voucher information for data set 1. Information is presented in the following order: taxon name, collector followed by collection number (herbarium acronyms follow
Acanthocoleus madagascariensis (Steph.) Kruijt, Pócs 97145/AA (GOET), Uganda, EF011843/DQ983649/—/—; Blepharolejeunea chimantaensis van Slageren & Kruijt, Pócs & Rico 00234/A (F), Venezuela, KF851876/—/—/KF852465; Bryopteris filicina (Sw.) Nees, Churchill, Magombo & Price 19855 (NY), Bolivia, AY607930/DQ439681/KF851576/KF852481; Caudalejeunea reniloba (Gottsche) Steph., Pócs et al. 01090/AB (F), Australia, KF851845/KF852294/KF851541/KF852441; Ceratolejeunea coarina (Gottsche) Schiffn., Zartman 1235.1 (DUKE), Brazil, AY607934/AY608026/—/KF852489; Cololejeunea microscopica (Taylor) Schiffn., Long & Rothero 37789 (E), Scotland: Wester Ross, KF851954/KF852386/KF851651/KF852552; Colura conica (Sande Lac.) K.I.Goebel, Pócs & Streimann 9986/W (F), Australia: Queensland, KM817490*/KM817513*/KM817536*/KM817462*; Colura imperfecta Steph., Pócs & Pócs 07019/A (F), Thailand, KF851881/KF852327/—/KF852469; Drepanolejeunea erecta (Steph.) Mizut., Long 28691 (E), Bhutan, JF513393/JF513452/KF851515/JF513342; Frullania albertii Steph., Davis 295 (DUKE), Ecuador, AY607942/DQ439685/KM817549*/KM817477*; Frullania atrata (Sw.) Nees ex Mont., Dauphin 3306 (F), Costa Rica, KM817491*/—/KM817540*/KM817466*; Frullania caulisequa (Nees) Mont., Karst, Shaw & Gibbs 022 (DUKE), USA: North Carolina, KM817500*/KM817526*/KM817553*/KM817481*; Frullania dilatata (L.) Dumort., Stotler 4666 (SIU), Portugal, KM817502*/KM817528*/KM817555*/KM817482*; Frullania eboracensis Lehm., Stotler 80-4354 (ABSH), USA: Illinois, AY688827/AY688779/KM817547*/KM817475*; Frullania ecklonii (Spreng.) Spreng. ex Gottsche, Lindenb. & Nees, Pócs 02030/W (F), Kenya, KM817488*/KM817510*/KM817533*/KM817459*; Frullania ericoides (Nees) Mont., Long 35167 (E), China: Yunnan, KM817486*/KM817507*/KM817531*/KM817456*; Frullania falciloba Taylor ex Lehm., Engel, von Konrat & Braggins 26837 (F), New Zealand, KM817489*/KM817511*/KM817534*/KM817460*; Frullania moniliata (Reinw., Blume & Nees) Mont., Mizutani s.n. (ABSH), Japan, AY507484/AY507401/KM817548*/KM817476*; Frullania nodulosa (Reinw., Blume & Nees) Nees, Pócs & Pócs 03261/A (F) Fiji, KM817492*/KM817517*/KM817541*/KM817467*; Frullania parhamii (R.M.Schust.) R.M.Schust. ex von Konrat, L.Söderstr. & A.Hagborg, von Konrat, Braggins & Naikatini 6/16-5 (F), Fiji, —/KM817516*/KM817539*/KM817465*; Frullania pycnantha (Hook.f. & Taylor) Taylor ex Gottsche, Lindenb. & Nees, von Konrat 99/409 (F), New Zealand, KM817499*/KM817525*/—/KM817480*; Frullania rostrata (Hook.f. & Taylor) Hook.f. & Taylor ex Gottsche, Lindenb. & Nees, Engel, von Konrat & Braggins 27770 (F), New Zealand, —/KM817512*/KM817535*/KM817461*; Frullania tamarisci (L.) Dumort. 1, Stotler 4661 (SIU), Portugal: Sintra, KM817501*/KM817527*/KM817554*/—; Frullania tamarisci 2, Long 35371 (E), France, KM817487*/KM817508*/KM817532*/KM817457*; Frullanoides densifolia Raddi, Gradstein 10171 (GOET), Ecuador, KF851930/KF852371/KF851634/KF852530; Fulfordianthus pterobryoides (Spruce) Gradst., Gradstein & Varon 11069 (GOET), Colombia, KF851931/KF852372/KF851635/KF852531; Jubula hutchinsiae (Hook.) Dumort. 1, Long 29077 (E), UK: England, —/KM817509*/—/KM817458*; Jubula hutchinsiae 2, Drehwald 3007 (GOET), Portugal, EF011746/AY548101/—/—; Jubula hutchinsiae subsp. bogotensis (Steph.) Verd., Gradstein s.n. (GOET), Mexico, EF011758/AY548100/—/—; Jubula hutchinsiae subsp. javanica (Steph.) Verd. 1, Konstantinova & Savchenko K479/1-07 (F), Russia, —/KM817506*/KM817542*/KM817468*; Jubula hutchinsiae subsp. javanica 2, Kodama s.n. (ABSH), Japan: Wakayama Pref., AY507492/AY507408/KF851585/JF513366; Jubula hutchinsiae subsp. pennsylvanica (Steph.) Verd., Risk 11005 (DUKE), USA, AY607954/KM817523*/KM817550*/—; Lejeunea deplanata var. deplanata, Shaw F533 (DUKE), USA: North Carolina, KM817498*/KM817524*/KM817552*/KM817479*; Lejeunea japonica Mitt., Bakalin s.n. (F), Russia, —/KM817518*/KM817543*/KM817469*; Lejeunea tuberculosa Steph., Long 28596 (E), Bhutan, JF513394/JF513453/KF851518/JF513344; Leptolejeunea elliptica (Lehm.) Besch., Yamaguchi s.n. (F), Japan, KM817485*/KM817515*/KM817538*/KM817464*; Lopholejeunea eulopha (Taylor) Schiffn., Pócs et al. 08036/U (F), Fiji, KF851868/KF852314/—/—; Marchesinia mackaii (Hook.) Gray, Buryova 2181 (DUKE), UK: Wales, —/KF852356/KF851619/KF852515; Mastigolejeunea auriculata (Wilson) Steph., Shaw 6222 (DUKE), USA: Alabama, KF851917/KF852359/KF851622/KF852518; Neohattoria herzogii (S.Hatt.) Kamim., Furuki 22673 (F), Japan: Honshu, KM817504*/KM817530*/KM817557*/KM817484*; Nipponolejeunea pilifera (Steph.) S.Hatt., Ohnishi 5975 (HIRO), Japan, AM396291/AM392293/—/—; Nipponolejeunea subalpina (Horik.) S.Hatt., Ohnishi 5611 (GOET), Japan, AM396290/AM392292/—/—; Odontolejeunea lunulata (F.Weber) Schiffn., Picon et al. 00227/CE (F), Venezuela, —/KM817514*/KM817537*/KM817463*; Ptychanthus striatus (Lehm.) Nees, Pócs & Pócs 03288/O (F), Fiji, KF851872/KF852318/KF851558/KF852460; Radula buccinifera (Hook.f. & Taylor) Taylor ex Gottsche, Lindenb. & Nees, Engel, von Konrat & Braggins 23569 (F), New Zealand, KM817495*/KM817521*/KM817545*/KM817472*; Radula cuspidata Steph., Engel & von Konrat 23517 (F), New Zealand, KM817496*/—/KM817546*/KM817473*; Radula grandis Steph., Engel, von Konrat & Braggins 24847 (F), New Zealand, KM817494*/KM817520*/KM817544*/KM817471*; Radula lindenbergiana Gottsche ex C.Hartm., Stotler 4656 (SIU), Portugal, KM817503*/KM817529*/KM817556*/KM817483*; Radula perrottetii Gottsche ex Steph., Mizutani 15030 (F), Japan, —/DQ439700/KM817551*/KM817478*; Radula ratkowskiana K.Yamada, Engel, von Konrat & Braggins 24365 (F), New Zealand, KM817497*/KM817522*/—/KM817474*; Radula tasmanica Steph., Engel, von Konrat & Braggins 24874 (F), New Zealand, KM817493*/KM817519*/—/KM817470*; Spruceanthus thozetianus (Gottsche & F.Muell.) B.M.Thiers & Gradst., Pócs 01107/M (GOET), Australia, AM396273/AM384877/—/—; Stictolejeunea squamata (Willd. ex F.Weber) Schiffn., Dauphin & Gonzalez 2134 (GOET), Costa Rica: Alajeula, KF851951/—/—/KF852549; Thysananthus convolutus Lindenb., Gradstein 10205 (GOET), Indonesia: Java, KF851953/DQ983737/KF851650/KF852551.
Voucher information for data set 2. Information is presented in the following order: taxon name, collector followed by collection number (herbarium acronyms follow
Frullania kunzei (Lehm.) Lehm. & Lindenb., Costa & Gradstein 3769 (GOET), Brazil, FJ380536/FJ380863/FJ380387/FJ380697; Frullania nisquallensis Sull., Doyle 11001 (GOET), USA, FJ380503/FJ380826/FJ380349/FJ380661; Frullania peruviana Gottsche, Schaefer-Verwimp & al. 24356 (GOET), Ecuador, FJ380543/FJ380870/FJ380394/FJ380704; Frullanoides mexicana van Slageren, Burghardt 4421a, Mexico, DQ987366/DQ983682/DQ987464/EF011851; Fulfordianthus pterobryoides (Spruce) Gradst., Dauphin 2518, Costa Rica, AM237145/DQ983684/AM237198/EF011832; Jubula hutchinsiae (Hook.) Dumort., Ahonen, Huttunen et Virtanen 3190 (H), Taiwan, AY125350/AY125946/AY144477/—; Jubula hutchinsiae subsp. bogotensis (Steph.) Verd. 1, Gradstein s.n. (GOET), Mexico: Veracruz, FN396818/—/FN398013/—; Jubula hutchinsiae subsp. bogotensis 2, Gradstein s.n. (GOET?), Mexico, DQ987273/AY548100/DQ987388/AM396281; Jubula hutchinsiae subsp. bogotensis 3, Gradstein 9449 (GOET), Costa Rica, FN396817/—/FN398012/—; Jubula hutchinsiae subsp. bogotensis 4, Frahm et al. 1313 (GOET), Peru, FN396816/—/—/—; Jubula hutchinsiae subsp. caucasica Konstant. & Vilnet 1, Konstantinova K456-5-07 (KPABG), Russia: Caucasus, JN836964/—/JN836974/—; Jubula hutchinsiae subsp. caucasica 2, Konstantinova K429-3-08 (KPABG), Russia: Caucasus, JN836961/—/JN836971/—; Jubula hutchinsiae subsp. caucasica 3, Konstantinova K462-1-08 (KPABG), Russia: Caucasus, JN836960/—/JN836970/—; Jubula hutchinsiae subsp. caucasica 4, Konstantinova K463-1-07 (KPABG), Russia: Caucasus, JN836962/—/JN836972/—; Jubula hutchinsiae subsp. caucasica 5, Konstantinova K371-1-08 (KPABG), Russia: Caucasus, JN836958/—/JN836968/—; Jubula hutchinsiae subsp. caucasica 6, Konstantinova K446-7-08 (KPABG), Russia: Caucasus, JN836959/—/JN836969/—; Jubula hutchinsiae subsp. caucasica 7, Konstantinova K443-14-08 (KPABG), Russia: Caucasus, JN836963/—/JN836973/—; Jubula hutchinsiae subsp. hutchinsiae 1, Long 29077 (GOET), UK: Devon, FN396813/—/FN398010/—; Jubula hutchinsiae subsp. hutchinsiae 2, Long 35296 (GOET), UK: Wales, FN396814/—/FN398011/—; Jubula hutchinsiae subsp. hutchinsiae 3, Schaefer-Verwimp & Verwimp 25675 (GOET), Portugal: Madeira, FN396811/—/FN397099/—; Jubula hutchinsiae subsp. hutchinsiae 4, Schaefer-Verwimp & Verwimp 25796 (GOET), Portugal: Boaventura, FN396812/—/FN398009/—; Jubula hutchinsiae subsp. hutchinsiae 5, Drehwald & Reiner-Drehwald 3007 (GOET), Portugal, DQ987260/AY548101/DQ987380/AM396282; Jubula hutchinsiae subsp. japonica (Steph.) Horik. & Ando 1, Koponen et al. 54308 (H), China, AY125342/AY125938/AY144479/—; Jubula hutchinsiae subsp. japonica 2, Inoue BSE755 (GOET), Japan: Kochi, FN396809/—/—/—; Jubula hutchinsiae subsp. japonica 3, Gradstein & Mizutani 2958 (GOET), Japan: Miyazaki, FN396810/—/FN397098/—; Jubula hutchinsiae subsp. japonica 4, Bakalin P-68-10-08 (KPABG), Russia: Primorsky Kray, JN836967/—/JN836977/—; Jubula hutchinsiae subsp. javanica (Steph.) Verd. 1, Zhu et al. 3361 (HSNU), China: Hainan, FN396800/—/—/—; Jubula hutchinsiae subsp. javanica 2, Zhu et al. 20050903-7a (HSNU), China: Hainan, FN396801/—/—/—; Jubula hutchinsiae subsp. javanica 3, Long 34765 (GOET), China: Yunnan, FN396805/—/FN397095/—; Jubula hutchinsiae subsp. javanica 4, Pocs 98105/C (GOET), Viet Nam: Vin-Phuc, FN396807/—/—/—; Jubula hutchinsiae subsp. javanica 5, Pocs & Tran Ninh 98103/A2 (GOET), Viet Nam: Vin-Phuc, FN396808/—/FN397097/—; Jubula hutchinsiae subsp. javanica 6, Schaefer-Verwimp & Verwimp 18870/A (GOET), Malaysia: Pahang, FN396802/—/FN397094/—; Jubula hutchinsiae subsp. javanica 7, Zhu 555 (HSNU), China: Fujian, FN396806/—/FN397096/—; Jubula hutchinsiae subsp. javanica 8, Bakalin Kor-12-6-08 (KPABG), South Korea, JN836966/—/JN836976/—; Jubula hutchinsiae subsp. javanica 9, Schaefer-Verwimp & Verwimp 18935 (GOET), Malaysia: Pahang, FN396803/—/—/—; Jubula hutchinsiae subsp. javanica 10, Wang 685B (HSNU), China: Yunnan, FN396804/—/—/—; Jubula hutchinsiae subsp. pennsylvanica (Steph.) Verd. 1, Buck 39060 (H?), USA: West Virginia, AY776308/AY776303/AY776309/—; Jubula hutchinsiae subsp. pennsylvanica 2, Davison 5045 (UNAF), USA: Alabama, FN396819/—/—/—; Jubula hutchinsiae subsp. pennsylvanica 3, Davison 5201 (UNAF), USA: West Virginia, FN396821/—/FN398015/—; Jubula hutchinsiae subsp. pennsylvanica 4, Davison 4707 (UNAF), USA: Alabama, FN396822/—/FN398016/—; Jubula hutchinsiae subsp. pennsylvanica 5, Davison 3775a (UNAF), USA: Alabama, FN396823/—/FN398017/—; Jubula hutchinsiae subsp. pennsylvanica 6, Davison & Risk 2537 (UNAF), USA: Kentucky, FN396820/—/FN398014/—; Jubula hutchinsiae subsp. pennsylvanica 7, Konstantinova ACH-3-92 (KPABG), USA, JN836965/—/JN836975/—; Jubula hutchinsiae subsp. pennsylvanica 8, Davison 4690 (UNAF), USA, Alabama, FN396824/—/FN398018/—; Jubula hutchinsiae subsp. pennsylvanica 9, Hyatt 8212 (UNAF), USA: North Carolina, FN396825/—/FN398019/—; Jubula hutchinsiae subsp. pennsylvanica 10, Davison s.n. (UNAF), USA: North Carolina, FN396826/—/FN398020/—; Neohattoria herzogii (S.Hatt.) Kamim., Furuki 22673 (F), Japan: Honshu, KM817455*/KM817530*/KM817505*/KM817504*; Nipponolejeunea pilifera (Steph.) S.Hatt. 1, Ohnishi 5975 (HIRO), Japan, —/AM392293/FJ380228/AM396291; Nipponolejeunea pilifera 2, Higuchi 41359 (H?), Japan, AY776307/AY776304/AY776310/—; Nipponolejeunea pilifera 3, Masuzaki 510 (HIRO), Japan: Yakushima Is., —/AB476588/—/—; Nipponolejeunea pilifera 4, Ohnishi s.n. (H), Japan, AY125341/AY125937/AY144478/—; Nipponolejeunea subalpina (Horik.) S.Hatt. 1, Ohnishi 5611 (HIRO), Japan, DQ987289/AM392292/FJ380227/AM396290; Nipponolejeunea subalpina 2, Higuchi 41358 (H?), Japan, AY776306/AY776305/AY776311/—; Ptychanthus striatus (Lehm.) Nees, Gradstein 10217, Indonesia: Java, DQ987297/DQ983723/DQ987403/EF011777; Schiffneriolejeunea nymannii (Steph.) Gradst. & Terken, Gradstein et al. 10321, Malaysia, DQ987320/DQ983725/DQ987424/EF011801.