Mycol Progress (2014) 13:1097–1104 DOI 10.1007/s11557-014-0997-8
ORIGINAL ARTICLE
Morphology and phylogenetics of Stomatisora, including Stomatisora psychotriicola sp. nov. Alan R. Wood & Matthias Lutz & Robert Bauer & Franz Oberwinkler
Received: 25 April 2014 / Revised: 17 June 2014 / Accepted: 23 June 2014 / Published online: 10 July 2014 # German Mycological Society and Springer-Verlag Berlin Heidelberg 2014
Abstract The morphology of the type specimen of Stomatisora geophilicola, the only species of the genus Stomatisora (Pucciniales) recognised till now, was restudied. Thin-walled probasidia (teliospores) develop exclusively in substomatal chambers, and mature metabasidia emerge through the stomata and develop suprastomatally. Uredinia are erumpent through the upper epidermis. A new species, S. psychotriicola, parasitizing Psychotria capensis (Rubiaceae) from South Africa, is described and illustrated. Only telia have been found which also develop in stomatal cavities, and, as in the type species, have partly repetitive probasidia and suprastomatal metabasidia that easily detach from fragile stalks. The similarities of telial morphology, as well as the same host family, indicate a close relationship and a generic separation from other rust genera. Molecular data support this interpretation and a possible relationship within a phakopsoroid clade. Keywords Pucciniales . Taxonomy . Psychotria capensis
Yen (1971) created the genus Stomatisora (Pucciniales) to accommodate S. geophilicola J.M. Yen, a new rust fungus on Geophila lancistipula Hiern (Rubiaceae) collected in Gabon. Yen (1971) described this fungus as having peridiate uredinia and substomatal telia, the probasidia (= teliospores)
A. R. Wood (*) ARC-Plant Protection Research Institute, P. Bag X5017, Stellenbosch 7599, South Africa e-mail:
[email protected] M. Lutz : R. Bauer : F. Oberwinkler Plant Evolutionary Ecology, Institute of Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 1, 72076 Tübingen, Germany
being thin-walled, laterally free, without germ pores, and germinating by extension of the tips forming metabasidia which extended through the stomata. Because the metabasidia were suprastomatal, Yen (1971) considered the telia as semi-suprastomatal (‘semi-superstomatiques’), and therefore compared it with truly suprastomatal genera such as Blastospora, Gerwasia and Hemileia. However, in suprastomatal genera, the probasidia occur above the stomata and not within the stomatal cavity as in S. geophilicola (Ono and Hennen 1983). Cummins and Hiratsuka (1983) considered its substomatal character to be insufficient to distinguish this species from Chrysocelis, a genus characterized by having Type 4 or 12 spermogonia and subepidermal, 1-celled, thinwalled and laterally free probasidia, and concluded that Stomatisora should be considered a synonym of Chrysocelis and combined the species as C. geophilicola (J.M. Yen) Cummins & Y. Hirats. Cummins and Hiratsuka (1983) placed Chrysocelis in the Chaconiaceae, a group characterized by having laterally free, thin-walled probasidia germinating without dormancy. It differed from other genera in this family by having Type 12 or 4 spermogonia, the others having Type 5 or 7. Later, they transferred Chrysocelis to the Mikronegeriaceae (Cummins and Hiratsuka 2003) due to its Petersonia aecia and Type 12 or 4 spermogonia. The genera of Chaconiaceae are poorly circumscribed (Ono 2006; Berndt and Beenken 2013). Chrysocelis and Chaconia differ in morphology of their spermogonia and aecia, and therefore the assignment of species to genera is difficult in the absence of these structures. The probasidia of these two genera are identical, except that they are borne singly on basidiogenous cells in Chrysocelis, and in groups in Chaconia (Ono and Hennen 1983). The type specimen of S. geophilicola, as well as specimens of a morphologically similar fungus recently collected from South Africa, were examined to determine their generic placement.
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Materials and methods Specimen sampling and documentation Free-hand transverse sections through infected portions of specimens were examined with a Nikon E600 or a Zeiss Standard 25 microscope. Measurements were made of 25 of each structure examined. Specimens observed and sequenced are detailed below. Nomenclatural novelties were registered in MycoBank (www.MycoBank.org, Crous et al. 2004). The genetype concept proposed by Chakrabarty (2010) was followed. DNA extraction, PCR and sequencing For methods of isolation and crushing of fungal material, DNA extraction, amplification of the ITS 1 and ITS 2 regions of the rDNA including the 5.8S r DNA (ITS) and the 5´-end of the nuclear large subunit ribosomal DNA (LSU), purification of PCR products, sequencing, and processing of the raw data, see Lutz et al. (2004a), and Piątek et al. (2011). The DNA sequences determined for this study were deposited in GenBank, GenBank accession numbers (ITS/LSU) are KC709671/KC709669 (KR-M-0034441) and KC709672/ KC709670 (KR-M-0034442) for two specimens on P. capensis, and KJ162157 (ITS) for a specimen of Chrysocelis lupini Lagerh. & Dietel (private collection of R. Berndt HeRB A-34 in Z+ZT). Phylogenetic analyses To elucidate the phylogenetic position of the rust specimens from P. capensis within the Pucciniales, their LSU sequences were analysed within a dataset covering all rust fungus genera of which sequences were available in GenBank. If present in GenBank, the respective type species were used. Additionally, all sequences that showed a similarity of greater than 89 % in a BLAST search using the Psychotria rust sequences, were added. GenBank accession numbers of the sequences used (Aime 2006; Aime et al. 2007; Alaei et al. 2012; Barnes and Szabo 2007; Beenken et al. 2012; Berres et al. 1995; Blomquist et al. 2009; Chung et al. 2004; Deadman et al. 2011; Dervis et al. 2010; Feau et al. 2011; Henk and Vilgalys 2007; Hernández et al. 2004; Lutz et al. 2004b; Maier et al. 2003, 2007; Scholler and Aime 2006; Yun et al. 2011; Zuluaga et al. 2011) are given in Fig. 5. Sequence alignment was obtained using MAFFT 6.853 (Katoh et al. 2002, 2005; Katoh and Toh 2008) using the LINS-i option. To obtain reproducible results, manipulation of the alignment by hand as well as manual exclusion of ambiguous sites were avoided as suggested by Giribet and Wheeler (1999) and Gatesy et al. (1993), respectively. Instead, highly divergent portions of the alignment were omitted using
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GBlocks 0.91b (Castresana 2000) with the following options. ‘Minimum Number of Sequences for a Conserved Position’: 32, ‘Minimum Number of Sequences for a Flank Position’: 32, ‘Maximum Number of Contiguous Non-conserved Positions’: 8, ‘Minimum Length of a Block’: 5, and ‘Allowed Gap Positions’ to ‘With half’. The resulting alignment [new number of positions: 952 (42 % of the original 2218 positions), number of variable sites: 438] was used for phylogenetic analyses using a Bayesian Approach (BA), and Maximum Likelihood (ML) according to Piątek et al. (2012). Trees were rooted with the Pucciniomycetes genera Eocronartium, Helicobasidium, Pachnocybe, Platygloea, and Septobasidium, which do not belong to the Pucciniales.
Results Morphology of Stomatisora species No peridium was observed in cross-sections of uredinia of S. geophilicola, instead there was a layer of deformed urediniospores on the outer edge of these sori (Fig. 1). The telia were strictly substomatal, the probasidia did not extend through the stomata. The probasidia germinated by apical elongation and formed auricularioid metabasidia which emerged through the stomatal opening and developed basidiospores on sterigmata (Fig. 2). A rust fungus collected in forests of KwaZulu-Natal, South Africa, on the small tree Psychotria capensis (Eckl.) Vatke (Rubiaceae), had similar substomatal telia with thin-walled, laterally free probasidia which germinated by extension of their tips which developed into metabasidia that emerged through the stomatal openings (Fig. 3). These collections differed from S. geophilicola by causing much larger lesions and only telia were present (Fig. 4). In addition intercellular hyphae of S. geophilicola were typically thick-walled whereas those in the specimens from South Africa were thin-walled. Probasidia developed singly on branched sporogenous cells, with repetitive development of new probasidia from the same cells so that remnants of old probasidia were visible at the base of the new probasidia (percurrent proliferation) (Figs. 2, 3). Taxonomy of Stomatisora species Stomatisora geophilicola J.M. Yen (Figs. 1, 2) Hyphae hyaline, intercellular, 2–4 μm in diameter, most hyphae thick-walled becoming thin-walled in close contact with host cells, in haustorial mother cells, and in subhymenial layers of uredinia and telia. D-haustoria penetrating host cell
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Fig. 1 Stomatisora geophilicola, from isotype. a Urediniospores in different views. b Cross-section through a leaf of Geophila lancistipula showing the position of a uredinium on the leaf upperside. c D-Haustorium in cells of palisade parenchyma below upper epidermis. d DHaustoria in mesophyll cells. Bars (a, c, d) 10 μm, (b) 50 μm
walls via extremely narrow penetration pegs, and expanding and ramifying coral-like inside the host cells. Spermogonia and aecia not observed. Uredinia adaxial, scattered singly, deeply immersed in host tissue, 200–400 μm in diameter; urediniospores developing successively from generative basal cells, not on pedicels, subglobose, 15–20×22–25 μm, thickwalled, hyaline to cream coloured, conspicuously spiny, the spines hyaline, 1–1.5 × 2–3 μm; marginal urediniospore chains somewhat deformed, thus recalling peridial cells, however not forming a bounding structure composed of morphologically distinct cells. Telia developing in substomatal chambers. Probasidia (teliospores) generated by thin-walled hyphae of the subhymenium, often originating inside old probasidia that can be traced as hyphal sheaths (percurrent proliferation), hyaline, thin-walled, clavate, 10–25×25–40 μm, germinating by apical elongation and extending through the stomatal pore to form a 4-celled metabasidium, 6–8×50–80 μm. Sterigmata curved, rather stout, 2–3×5–12 μm. Basidiospores ellipsoidal, hyaline, thin-walled, 6–7×8–10 μm, sometimes germinating by repetition. Specimens examined Gabon: à Libreville, forêt de la Mondat, km 31.8, on Geophila lancistipula, 20 Dec. 1969, leg. G. Gilles (PG No. 32), isotype in PUR F19416.
Stomatisora psychotriicola A.R. Wood, M. Lutz, Bauer & Oberw., sp. nov (Figs. 3, 4) Hyphae thin-walled, intercellular, forming short side branches (haustorial mother cells) from which very thin penetration pegs penetrate the host cell walls. D-haustoria expanding inside the plant cells and producing ramified protuberances. Spermogonia, aecia and uredinia unknown. Telia abaxial, scattered singly in circular to oblong leaf spots which are up to 4×7 cm, chlorotic becoming brown coloured, often with a white surface bloom consisting of massed metabasidia and basidiospores; probasidia (teliospores) substomatal, 15–25× 60–90 μm, in dense clusters, often developing by percurrent proliferation, thin-walled and hyaline, basally strongly swollen, tapering to very thin tubes that protrude into the stomatal pore, germinating by apical elongation and extending through the stomatal pore. Metabasidia 8–12×40–60 μm, five-celled. The basal cell of the metabasidia stalk-like being extremely thin-walled and narrow facilitating easy detachment, the upper part broader and consisting of four cells, each cell producing one curved sterigma, 3–5×8–12 μm. Basidiospores ellipsoidal, hyaline, thin-walled, (7)–8–10×(8)–10–12–(14) μm, producing short to very short hyphal tubes; germination by repetition not observed.
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The main morphological difference between these species is thick-walled intercellular hyphae in the type species, while hyphae of S. psychotriicola always are thin-walled. Uredinia have not so far been found in specimens of S. psychotriicola despite careful searching. Basidiospore germination by repetition was found in the type species but not in the new species. Phylogenetic analyses The LSU sequences of the two rust specimens from Psychotria capensis were identical whereas their ITS sequences differed in three positions. The different runs of BA that were performed and the ML analyses yielded consistent topologies for supported relationships. The phylogenetic hypothesis resulting from the BA analyses is presented in Fig. 5. Estimates for a posteriori probabilities are indicated on branches before slashes, ML bootstrap support values after slashes. In all analyses, the two rust specimens from P. capensis clustered together and on a common branch with two specimens of Kweilingia divina (Syd.) Buriticá and Uredo chusqueae Pardo-Card.
Discussion Fig. 2 Stomatisora geophilicola, from isotype. a Cross-section through a leaf of Geophila lancistipula showing the position of a telium on the leaf underside. b Part of the hymenium showing percurrent proliferation of probasidia and basidia in different stages of development. c Basidiospores, two germinating with secondary spores. Bars (a) 50 μm, (b, c) 10 μm
Mycobank no.: MB 807851 Etymology: Named for its host plant Psychotria capensis (Rubiaceae; Psychotrieae) Specimens examined South Africa: KwaZulu-Natal: Kloof nature reserve, Kloof, on Psychotria capensis, 15 June 2009, leg. A.R. Wood 805 (PREM 60886, holotype; KR-M0034441, ZT Myc 56727, isotypes); Paradise Valley nature reserve, Durban, on Psychotria capensis, 25 Nov. 2010, leg. A.R. Wood 797 (PREM 60887, KR-M-0034442, ZT Myc 56726, paratypes). Stomatisora psychotriicola shares important characteristics with S. geophilicola. In both, host species belong to the family Rubiaceae, probasidia (teliospores) develop in substomatal chambers, are thin-walled and hyaline, basally strongly swollen and apically tapered, frequently developing repetitively by percurrent proliferation (Figs. 2b, 3b). Metabasidia develop suprastomatally on narrow necks of the probasidia, and detach easily from these in the newly described species.
The newly described rust fungus from South Africa was placed in Stomatisora, a genus introduced by Yen (1971) for S. geophilicola. This genus was not accepted by Cummins and Hiratsuka (1983, 2003), who included it in Chrysocelis. They were of the opinion that substomatal localization of telia cannot be used as a generic character, and that other differentiating features were also of minor importance. In both studied species, the probasidia develop singly on branched sporogenous cells similar to Chrysocelis (Ono and Hennen 1983). Cummins and Hiratsuka (2003) report spermogonia of Group III (Type 12) or Group V (Type 4), and aecia without peridia or intercalary cells (Petersonia-like) for the Chrysocelis spp. accepted by them. The type species of Chrysocelis, C. lupini, is autoecious and has Petersonia-like aecia and uredinia, whereas in C. globbae Syd. the uredinia are Uredo-like (Ono and Hennen 1983). However, spermogonia and aecia are not known in Stomatisora spp. We did not find uredinia in S. psychotriicola, while they are present in S. geophilicola. Yen (1971) described and illustrated uredinia of S. geophilicola with marginal, peridial cells. However, structural details of these cells are very difficult to ascertain, and we consider them to be deformed urediniospores. The uredinia are deep seated and the urediniospores are not pedicellate, and are neither Petersonia-like nor Uredo-like as in Chrysocelis (Cummins and Hiratsuka 2003). Only a few species of rust fungi have been described with substomatal telia (Ono et al. 1988), including Maravalia
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Fig. 3 Stomatisora psychotriicola, a, d, e from PREM 60887 (A.R. Wood 797); b, c from PREM 60886 (A.R. Wood 805). a Partial crosssection through a leaf of Psychotria capensis showing the position of telia in the leaf underside; two in young developmental stages, and one with mature metabasidia emerging through a stomatum. b, Probasidia of different developmental stages showing percurrent proliferation. c Three D-haustoria in mesophyll cells. d Basidiospores, two germinated. e detached, nearly mature, fourcelled metabasidia. Bars (a) 100 μm, (b–e) 25 μm
guianensis Y. Ono (Ono 1984), M. pseudosuprastomatalis Y. Ono & Kakish., Puccinia paullula Syd. & P. Syd. (Ono et al. 1988), Puccinia aframomicola (J.M. Yen) J.F. Hennen & Y. Ono (Yen 1969), as well as the two Stomatisora species Fig. 4 Stomatisora psychotriicola, a, b, c from PREM 60887 (A.R. Wood 797). a Large chlorotic lesions on the abaxial leaf surface of Psychotria capensis (circled). b Metabasidia and basidiospores scraped off surface of a lesion. c Crosssection through a leaf of Psychotria capensis showing a telium
discussed here. Of these, only M. pseudosuprastomatalis and Stomatisora produce probasidia within the substomatal cavity. In Stomatisora, probasidia elongate apically through the stomatal openings to produce narrow (S. geophilicola) to
1102 Fig. 5 Phylogenetic relationships of Stomatisora psychotriicola within the Pucciniales: Markov chain Monte Carlo analysis of an alignment of LSU rDNA sequences using the GTR+I+G model of DNA substitution with gamma distributed substitution rates and an estimated proportion of invariant sites, random starting trees and default starting parameters of the DNA substitution model. A 50 % majority-rule consensus tree is shown computed from 75 000 trees that were sampled after the process had reached stationarity. The tree was rooted with the pucciniomycetous genera Eocronartium, Helicobasidium, Pachnocybe, Platygloea, and Septobasidium. Numbers on branches before slashes are estimates for a posteriori probabilities, numbers on branches after slashes are ML bootstrap support values. Branch lengths were averaged over the sampled trees. They are scaled in terms of expected numbers of nucleotide substitutions per site
Mycol Progress (2014) 13:1097–1104 Olivea scitula DQ354541 Ravenelia macrocarpa DQ323926 100/100 Endoraecium acaciae DQ323916 Endoraecium koae DQ323918 Arthuria sp. EU851162 99/- 99/89 100/ Phakopsora meibomiae EU851164 97 Batistopsora crucis-filii DQ354539 Uromycladium fusisporum DQ323921 Tranzschelia pruni-spinosae AF426224 76/86/70 Kuehneola uredinis DQ354551 100/94 Phragmidium mucronatum HQ412646 98/65 Triphragmium ulmariae JF907676 67/Trachyspora intrusa DQ354550 81/Porotenus biporus JF263494 Gymnoconia peckiana JF907677 Miyagia pseudosphaeria DQ354517 80/63 91/69 Dietelia portoricensis DQ354516 Uromyces appendiculatus AB115646 60/Chrysocelis lupini KJ162157 87/Maravalia guianensis EU851143 Sphenospora kevorkianii DQ354521 Cumminsiella mirabilissima DQ354531 84/Endophyllum sempervivi DQ917747 Puccinia graminis DQ417388 Chardoniella gynoxidis GU936636 54/Pucciniosira solani EU851137 Aecidium kalanchoe AY463163 100/100 Kweilingia divina DQ354554 68/54 Kweilingia divina EF192212 98/78 Uredo chusqueae EU851156 53/100/100 Stomatisora psychotriicola KC709669 Stomatisora psychotriicola KC709670 Uredo alpestris AF426212 74/Allodus podophylli DQ354543 100/88 Gymnosporangium sabinae HM114221 94/88 Diorchidium polyalthiae JF263493 Dasyspora nitidae JF263487 94/64 Ochropsora ariae AF426221 Prospodium lippiae DQ354555 95/Pileolaria terebinthi HM639742 Chrysocelis muehlenbeckiae EU851158 Chrysocyclus cestri EU851157 57/- Chrysomyxa woroninii GU049540 Cronartium ribicola DQ354560 64/- Endocronartium harknessii AY700193 Melampsora euphorbiae DQ437504 84/73/Thekopsora areolata AF426235 Coleosporium ipomoeae EU851159 Melampsorella caryophyllacearum AF426232 66/88/63 Pucciniastrum epilobii AF426226 Naohidemyces vaccinii DQ354563 91/56 80/Milesia scolopendri AF426236 Uredinopsis filicina AF426237 100/98 Hyalopsora polypodii AY512852 93/69 Melampsoridium betulinum DQ354561 Hemileia vastatrix DQ354566 100/89 Mikronegeria alba DQ354569 Blastospora smilacis DQ354568 Caeoma torreyae AF522183 Septobasidium velutinum DQ241500 Platygloea vestita AY512872 63/Pachnocybe ferruginea L20284 Helicobasidium purpureum AY254180 Eocronartium muscicola AY512844 82/60/50
0.05 substitutions/site
very narrow necks (S. psychotriicola) at the end of which, with septum development, the metabasidia become four- or five-celled, respectively. Each cell develops a curved sterigma
and a basidiospore. In both Stomatisora spp., new probasidia develop from the same sporogenous cells as the previous probasidia, and become sheathed by the remnants of the older
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probasidia (Figs. 2b, 3b). No phylogenetic conclusions can be made from this as the suprastomatal and substomatal habits are found in widely divergent lineages of rust fungi (Ritschel et al. 2005). Recent molecular evidence suggests that certain families, and often also the genera, as accepted by Cummins and Hiratsuka (2003), are polyphyletic (Aime 2006; Beenken et al. 2012; Minnis et al. 2012). Sequence data obtained suggest Chrysocelis in the sense of Cummins and Hiratsuka (2003) is polyphyletic (Fig. 5). There are few sequences available from representatives of genera with thin-walled, laterally free probasidia. Thus the phylogenetic placement of the genera and species with such probasidia is uncertain at present. If spermogonia and aecia are unknown, as is the case in Stomatisora, an affiliation with species that are grouped in Chaconiaceae or Mikronegeriaceae would only be tentative. Berndt and Beenken (2013) came to similar conclusions in the case of newly described species in Chaconia for which Chrysocelis could also have been chosen as being the correct placement. The Phakopsoraceae as defined by Cummins and Hiratsuka (2003) has the same morphological type of spermogonia as the Chaconiaceae (Group VI, Types 5 and 7). Ono (1995) noted the similarity in morphology between certain species of Cerotelium (Phakopsoraceae) and Aplopsora (Chaconiaceae). Buriticá (1998) placed Aplopsora in the Phakopsoraceae, and transferred Cerotelium tanakae S. Ito to Aplopsora. Cummins and Hiratsuka (2003) maintained Aplopsora in the Chaconiaceae. This suggests that thin-walled, laterally free probasidia cannot be considered as a phylogenetically important characteristic, and that the Chaconiaceae sensu Ono and Hennen (1983) or Cummins and Hiratsuka (2003) will be found to be paraphyletic. Kweilingia divina plus Uredo chusqueae appeared as sister group to Stomatisora in our phylogram. Kweilingia belongs to the likely paraphyletic Phakopsoraceae (Aime 2006). Thick-walled intercellular hyphae, as reported herein as occurring in S. geophilicola, have been reported in K. bambusae (Teng) Teng (Berndt 1997), though the significance of this is uncertain. This relationship, the large distance of S. psychotriicola from C. lupini and C. muehlenbeckiae Lagerh. & Dietel in the phylogenetic analysis, and the different morphological characteristics indicate that Stomatisora is not a synonym of Chrysocelis but represents a well-defined genus. Additional sequences would be required to determine the true phylogenetic position of Stomatisora in the Uredinales. Acknowledgment R. Berndt provided valuable comments on an earlier draft of the manuscript.
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