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Two new species of Geejayessia (Hypocreales) from Asia as evidenced by morphology and multi-gene analyses
expand article infoZhao-Qing Zeng, Wen-Ying Zhuang
‡ Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
Open Access

Abstract

Two new species of Geejayessia are introduced, based on materials collected from central China. Geejayessia clavata sp. nov. is characterised by gregarious, red brownish to dark red, oval-subglobose to globose perithecia that are formed on a basal stroma; (4–7-)8-spored cylindrical asci; ellipsoidal or rarely broadly ellipsoidal, uniseptate, smooth or finely verruculose ascospores; clavate, aseptate microconidia and absence of macroconidia. Geejayessia sinica sp. nov. is characterised by red to bright red, pyriform, subglobose to globose, perithecia on a basal stroma, collapsing laterally when dry; subcylindrical to clavate asci with a rounded apex; ellipsoidal, uniseptate ascospores; and falcate, multiseptate macroconidia with an arcuate tip. Morphological distinctions of the new species from the related fungi are discussed. This is the first report of Geejayessia from Asia.

Keywords

Cosmospora-like fungi, Nectriaceae, Systematic, Taxonomy

Introduction

Some fusarium-like species having gregarious, multicoloured, broadly ampulliform short-necked or broadly ellipsoidal perithecia were previously placed in Cosmospora Rabenh. and Nectria (Fr.) Fr. (Booth 1959; Samuels and Rogerson 1984; Nirenberg and Samuels 2000) until the genus Geejayessia Schroers, Gräfenhan & Seifert, typified by G. cicatricum (Berk.) Schroers, was introduced (Schroers et al. 2011). The genus is characterised by prosenchymatous stromata erumpent through substrates, caespitose, broadly pyriform, pale orange, brownish to reddish-orange, bright red to black perithecia, reacting to potassium hydroxide (KOH) and lactic acid (LA); cylindrical or clavate asci with eight ascospores; broadly ellipsoidal to ellipsoidal ascospores that are uniseptate, slightly constricted at the septum, hyaline or pale brown to yellowish-brown, smooth or verruculose at maturity; and multiseptate, slightly curved macroconidia with conspicuous pedicellate foot cell (Schroers et al. 2011; Lombard et al. 2015). Members of Geejayessia exhibit host specificity and mainly occur on Buxus spp., Celtis occidentalis and Staphylea trifolia and were reported only from Europe, North America and Oceania (Samuels and Rogerson 1984; Nirenberg and Samuels 2000; Schroers et al. 2011).

In our examinations of nectriaceous collections from central China, two cosmospora-like fungi were encountered. Judging by perithecial gross morphology, anatomic structures and culture characteristics, they represented two previously undescribed species of Geejayessia. Their taxonomic placements were confirmed by multigene phylogenetic analyses. Distinctions between the new species and their closely related fungi are discussed.

Materials and methods

Sampling and morphological studies

Specimens were collected from Shennongjia National Nature Reserve and Longyuwan National Forest Park and were deposited in the Herbarium Mycologicum Academiae Sinicae (HMAS). Methods used by Luo and Zhuang (2010) and Schroers et al. (2011) were generally followed for morphological observations. The test for colour changes of the perithecial wall was made with 3% KOH and 100% LA. To observe internal and microscopic characteristics of the perithecial wall, longitudinal sections through ascomata were made with a freezing microtome (YD-1508-III, Jinhua, China) at a thickness of 6–8 μm. Microscopic examinations and measurements were taken from longitudinal sections and squash mounts in lactophenol cotton blue solution using an Olympus BH-2 microscope (Tokyo, Japan). Photographs were taken with a Leica DFC450 digital camera (Wetzlar, Germany) attached to a Leica M125 stereomicroscope (Milton Keynes, UK) for gross morphology and a Zeiss AxioCam MRc 5 digital camera (Jena, Germany) attached to a Zeiss Axio Imager A2 microscope (Göttingen, Germany) for anatomical structures. Measurements of individual structures were based on 30 units, except when otherwise noted. Cultures were obtained by single ascospore isolation from fresh ascomata. To determine colony features, isolates were grown on cornmeal dextrose agar [CMD, 4% (w/v) cornmeal + 2% (w/v) dextrose + 2% (w/v) agar], potato dextrose agar [PDA, 20% (w/v) potato + 2% (w/v) dextrose + 2% (w/v) agar] and synthetic nutrient-poor agar (SNA; Nirenberg 1976) in 90 mm plastic dishes at 25 °C for 7 d. For the observation of conidiophores, macroconidia and microconidia, cultures were grown on SNA at 25 °C with alternating periods of light/darkness (12 h/12 h). Colony growth rates were measured after 7 d.

DNA extraction, PCR amplification and sequencing

The genomic DNA was extracted from fresh mycelium following the methods of Wang and Zhuang (2004). Three primer pairs, acl1-230up/acl1-1220low (Gräfenhan et al. 2011), ITS5/ITS4 (White et al. 1990) and fRPB2-5F/fRPB2-7cR (Liu et al. 1999) were used to amplify the sequences or partial sequences of the larger subunit of the ATP citrate lyase (ACL1), the internal transcribed spacers with the 5.8S nuclear ribosomal DNA (ITS) and the second largest subunit of the RNA polymerase II (RPB2), respectively. PCR reactions were performed on an ABI 2720 Thermal Cycler (Applied Biosciences, Foster City, California, USA), based on the procedures detailed in Gräfenhan et al. (2011), White et al. (1990) and Liu et al. (1999). DNA sequencing was carried out in both directions on an ABI 3730XL DNA Sequencer (Applied Biosciences).

Sequence alignment and phylogenetic analyses

Newly generated sequences and those retrieved from GenBank are listed in Table 1. Nalanthamala psidii (Sawada & Kuros.) Schroers & M.J. Wingf. and Thyronectria concentrica (Mont. & Fr.) Voglmayr & Jaklitsch were used as outgroup taxa. Sequences were assembled, aligned and the primer sequences were trimmed with BioEdit 7.0.5 (Hall 1999) and converted to NEXUS files by ClustalX 1.8 (Thompson et al. 1997). The partition homogeneity test of ACL1, ITS and RPB2 regions was performed with PAUP 4.0b10 (Swofford 2002). To confirm the phylogenetic positions of the new species, sequences of ACL1, ITS and RPB2 were combined and analysed with Bayesian Inference (BI) and Maximum Parsimony (MP) analyses. The MP analysis was performed with PAUP 4.0b10 (Swofford 2002) using 1000 replicates of heuristic search with random addition of sequences and subsequent TBR (tree bisection and reconnection) branch swapping. Topological confidence of resulted trees was tested by maximum parsimony bootstrap proportion (MPBP) with 1000 replications, each with 10 replicates of random addition of taxa. The BI analysis was conducted by MrBayes 3.1.2 (Ronquist and Huelsenbeck 2003) using a Markov chain Monte Carlo algorithm. Nucleotide substitution models were determined by MrModeltest 2.3 (Nylander 2004). GTR+I+G was shown to be the best-fit model for the combined sequences in the BI analysis. Four Markov chains were run simultaneously for 1,000,000 generations with the trees sampled every 100 generations. A 50% majority rule consensus tree was computed after excluding the first 2500 trees as ‘burn-in’. Bayesian inference posterior probability (BIPP) was determined from the remaining trees. Trees were examined in TreeView 1.6.6 (Page 1996). BIPP greater than 90% and MPBP greater than 50% are shown at the nodes.

List of species, herbarium/strain numbers and GenBank accession numbers of materials used in this study.

Species Herbarium/strain numbers GenBank accession numbers
acl1 ITS rpb2
Albonectria albosuccinea (Pat.) Rossman & Samuels BBA 64502 HQ897837 HQ897788 HQ897699
A. rigidiuscula (Berk. & Broome) Rossman & Samuels CBS 122570 HQ897896 HQ897815 HQ897760
Cyanonectria buxi (Fuckel) Schroers, Gräfenhan & Seifert CBS 125554 HM626629 HM626660 HM626688
C. cyanostoma (Sacc. & Flageolet) Samuels & P. Chaverri CBS 101734 HQ897895 FJ474076 HQ897759
Dialonectria episphaeria (Tode) Cooke CBS 125494 HQ897892 HQ897811 HQ897756
D. ullevolea Seifert & Gräfenhan CBS 125493 HQ897918 KM231821 HQ897782
Fusarium sambucinum Fuckel CBS 14695 KM231015 KM231813 KM232381
F. sublunatum Reinking BBA 62431 HM897916 HQ897830 HQ897780
Fusicolla acetilerea (Tubaki, C. Booth & T. Harada) Gräfenhan & Seifert BBA 63789 HQ897839 HQ897790 HQ897701
F. matuoi (Hosoya & Tubaki) Gräfenhan & Seifert CBS 58178 HQ897858 KM231822 HQ897720
Geejayessia atrofusca (Schwein.) Schroers & Gräfenhan CBS 125505 HM626628 HM626659 HM626682
G. celtidicola Gräfenhan & Schroers CBS 125502 HM626625 HM626657 HM626685
G. cicatricum (Berk.) Schroers CBS 125552 HQ728171 HQ728145 HQ728153
G. desmazieri (De Not. & Becc.) Schroers CBS 125507 HM626633 HM626651 HM626675
G. clavata Z.Q. Zeng & W.Y. Zhuang HMAS 248725 KY873305 a KY873307 KY873309
G. sinica Z.Q. Zeng & W.Y. Zhuang HMA S248726 KY873306 KY873308 KY873310
G. zealandica (Cooke) Schroers CBS 11193 HM626626 HM626658 HM626684
Macroconia leptosphaeriae (Niessl) Gräfenhan & Schroers CBS 100001 HQ897891 HQ897810 HQ897755
M. papilionacearum (Seaver) Gräfenhan & Seifert CBS 125495 HQ897912 HQ897826 HQ897776
Microcera coccophila Desm. CBS 31034 HQ897843 HQ897794 HQ897705
M. diploa (Berk. & M.A. Curtis) Gräfenhan & Seifert BBA 62173 HQ897899 HQ897817 HQ897763
Nalanthamala psidii (Sawada & Kuros.) Schroers & M.J. Wingf. CBS 116952 KM231073 AY864836 KM232401
Neocosmospora ramosa (Bat. & H. Maia) L. Lombard & Crous CBS 50963 KM231004 KM231802 KM232369
N. vasinfecta E.F. Sm. CBS 32554 KM231005 KM231803 KM232370
Stylonectria applanata Höhn. CBS 125489 HQ897875 HQ897805 HQ897739
S. purtonii (Grev.) Gräfenhan DAOM 235818 HQ897919 HQ897831 HQ897783
Thyronectria concentrica (Mont. & Fr.) Voglmayr & Jaklitsch CBS 47469 KM231080 KM231835 KM232408

Results

Sequence comparison and phylogenetic inference

The ACL1, ITS and RPB2 sequences of 25 taxa belonging to 10 genera having fusarium-like asexual states were analysed through the methods of BI and MP. The PHT (P = 0.01) indicated that the individual partitions were not highly incongruent (Cunningham 1997); the three loci were thus combined for phylogenetic analyses. The combined datasets include 2258 characters, of which 1085 were constant, 173 variable and parsimony-uninformative and 1000 parsimony-informative. The MP analysis resulted in a single most parsimonious tree (tree length = 4885, CI = 0.4491, HI = 0.5509, RI = 0.5638, RCI = 0.2532). The final matrix was deposited in TreeBASE with accession No. S20853. The BI tree generated is shown (Figure 1). The topology of the BI tree is similar to that of the MP tree. The 25 investigated species were grouped together (BIPP/MPBP = 100%/96%) and further segregated into two main clades (Figure 1). Species of Geejayessia clustered into one clade together with Albonectria Rossman & Samuels, Cyanonectria Samuels & P. Chaverri, Fusarium and Neocosmospora E.F. Sm. (BIPP/MPBP = 100%/100%) and those of Dialonectria (Sacc.) Cooke, Fusicolla Bonord., Macroconia (Wollenw.) Gräfenhan, Seifert & Schroers, Microcera Desm. and Stylonectria Höhn. formed another clade (BIPP/MPBP = 100%/98%). HMAS 248725, HMAS 248726 and other representatives of Geejayessia formed a highly supported monophyletic group (BIPP/MPBP = 100%/100%), which confirmed their taxonomic positions in the genus.

Figure 1. 

A Bayesian Inference trees inferred from the combined ACL1, ITS and RPB2 sequences. BIPP (left) above 90% and MPBP (right) above 50% are indicated at nodes.

Taxonomy

Geejayessia clavata Z.Q. Zeng & W.Y. Zhuang, sp. nov.

Fungal Names: FN570429
Figures 2, 3

Holotype

CHINA, Henan Province, Longyuwan, 33°40'45"N, 111°46'26"E, alt. 1500 m, on bark of Buxus sp., 17 September 2013, H.D. Zheng, Z.Q. Zeng & Z.X. Zhu 8728 (holotype: HMAS 275654), dried ex-type culture HMAS 248725.

Etymology

The specific epithet refers to the clavate microconidia.

Description

Mycelium not visible around ascomata or on host. Ascomata perithecial, crowded in group of 5 to 40, on basal stroma, oval, subglobose to globose, smooth, bright red when fresh, red brownish to dark red when dry, with a darker red ostiolar region, turning purple red in KOH and orange yellow in LA, 128–175 × 206–255 μm (n = 17). Perithecial wall consisting of a single layer, 15–25 μm thick, cells forming textura prismatica, 2–12 × 2–6 μm, walls 1–1.2 μm thick. Asci cylindrical, with a rounded apex, (4–7-)8-spored, 55–75 × 5–9 μm. Ascospores ellipsoidal to broadly ellipsoidal, equally 2-celled, slightly constricted at septum, smooth or finely verruculose, hyaline or pale brown, obliquely uniseriate in ascus often with ends overlapping, 7.5–12 × 4.5–5.5 μm.

Culture characteristics

Colony on PDA 48 mm diam. after 7 d at 25 °C, surface cottony, aerial mycelium white, producing vinaceous pigment in medium. Colony on SNA 30 mm diam. after 7 d at 25 °C, surface slightly floccose, with sparse whitish aerial mycelium. Colony on CMD 56 mm diam. after 7 d at 25 °C, surface floccose, with sparse whitish aerial mycelium, producing vinaceous pigment in medium. Conidiophores with short simple branches. Conidiogenous cells monophialidic, cylindrical, tapering toward the tip, 12–63 × 1.5–3.5 μm. Conidia clavate, not in chains, hyaline, aseptate, 4–7 × 0.8–2 μm (n = 60). Macroconidia and chlamydospores not observed.

Notes. Attempts were made to obtain macroconidia of the fungus in culture, but failed. Although the falcate macroconidia are lacking, the major phenotypic features of the fungus, such as occurrence on bark of Buxus sp., perithecia broadly ampulliform with a short neck, asci cylindrical with a rounded apex, ellipsoidal ascospores uniseptate and conidiophores monophialidic, fit well with the generic concept of Geejayessia. The molecular data confirm the taxonomic placement and indicate its close relationship with G. atrofusca (Figure 1, BIPP/MPBP = 100%/89%). Geejayessia atrofusca differs significantly in dark brown to black ascomata that do not change colour in KOH or LA, wider asci [(7.5-)9.8-13.3(-15) μm wide] and longer ascospores [(10-)11.2-14.2(-17.0) μm long]. Its microconidia are oblong to slightly curved and falcate but not clavate and are longer and wider (Samuels and Rogerson 1984).

Figure 2. 

Geejayessia clavata sexual state (holotype, HMAS 275654): a–c Ascomata on natural substrate d–f colour of perithecium in water (d), 3% KOH (e) and 100% lactic acid (f) g median section through perithecium h–k Asci with ascospores l–o Ascospores. Scale bars: 1 mm (a–c); 100 μm (d–f); 50 μm (g); 10 μm (h–k), 5 μm (l–o).

Figure 3. 

Geejayessia clavata asexual state (HMAS 248725): a–c colony on PDA (a) SNA (b) and CMD (c) d–j conidiophores, phialides and/or microconidia on SNA. Scale bar: 10 μm (d–j).

Geejayessia sinica Z.Q. Zeng & W.Y. Zhuang, sp. nov.

Fungal Names: FN570430
Figures 4, 5

Type

CHINA, Hubei Province, Shennongjia, 31°29'17"N, 110°20'58"E, alt. 2800 m, on bark of Buxus sp., 15 September 2014, Z.Q. Zeng, H.D. Zheng, W.T. Qin & K. Chen 9606 (holotype: HMAS 254520), dried ex-type culture HMAS 248726.

Etymology

Specific epithet refers to the type locality China.

Description

Mycelium not visible around ascomata or on host. Ascomata perithecial, solitary or in groups of 5 to 40, with a basal stroma, pyriform or subglobose to globose, smooth, collapsing laterally when dry, red to bright red with a dark red ostiolar region, turning dark purple red in KOH and light yellow in LA, 255–343 × 176–314 μm (n = 14). Perithecial wall of a single layer, 18–38 μm thick, of textura prismatica, cells 8–23 × 2–6 μm, walls 1.2–1.5 μm thick. Asci subcylindrical to clavate, with a rounded apex, 6(–8)-spored, 88–123 × 7–10(–12.5) μm. Ascospores ellipsoidal, hyaline or pale brown, smooth or finely warted, bicellular, slightly constricted at septum, obliquely uniseriate, 10–18(–20) × 5–7.5 μm.

Culture characteristics

Colony on PDA 42 mm diam. after 7 d at 25 °C, surface cottony, with whitish aerial mycelium, forming concentric rings, with pale vinaceous pigment produced in medium. Colony on SNA 26 mm diam. after 7 d at 25 °C, surface slightly velvet, with sparse whitish aerial mycelium. Colony on CMD 40 mm diam. after 7 d at 25 °C, surface radial, slightly floccose, with sparse whitish aerial mycelium. Conidiophores with short simple branches. Conidiogenous cells monophialidic, cylindrical, slightly tapering toward the tip, indefinite in length. Macroconidia falcate, with an arcuate tip and a pedicellate foot cell, hyaline, (3–4–)5-septate, 3-septate: 30–53 × 4–5 μm, 4-septate: 50–60 × 4.5–5.2 μm, 5-septate: 53–80 × 4.6–5.3 μm. Microconidia and chlamydospores not observed.

Notes

Geejayessia sinica is phylogenetically related to and morphologically similar to G. cicatricum and G. desmazieri in perithecial gross morphology, subcylindrical to clavate asci, ellipsoidal to broadly ellipsoidal, uniseptate ascospores, falcate macroconidia (Schroers et al. 2011). Geejayessia cicatricum differs from G. sinica in having smaller perithecia (160–260 × 125–250 μm) and ascospores [(9.5–)11.5–13(–14.5) × (4.5–)5.0–6(–6.5) μm], thinner perithecial wall [(12–)13.5–18(–21) μm thick), shorter asci [(65.5–)73–92.5(–103) μm long), macroconidia with more septa [(2–)5–7(–8)] and slow growth on PDA (15–20 mm diam. after 7 d at 25 °C) (Schroers et al. 2011). Geejayessia desmazieri is distinguished by shorter asci [(75.5–)85(–100) μm long], smaller ascospores [(9.5–)11–12.5(–15) × (4.5–)5.5–6(–7) μm] and slow growth on PDA (20 mm diam. after 7 d at 25 °C) (Schroers et al. 2011). The ITS sequence of G. sinica differs from that of the other two species by 29 bp and 29 bp divergences in total length of 521 bp. The protein-encoding gene sequences of G. sinica differ from those of G. cicatricum (G. desmazieri) by 59 (66) bp differences of 815 bp long ACL1 fragment and 34 (35) bp differences of the 672 bp long RPB2 region.

Figure 4. 

Geejayessia sinica sexual state (holotype, HMAS 254520): a–c ascomata on natural substrate d–f colour of perithecium in water (d), 3% KOH (e) and 100% lactic acid (f) g median section through perithecium h–j asci with ascospores k–m ascospores. Scale bars: 1 mm (a–c); 100 μm (d–f); 50 μm (g); 10 μm (h–m).

Figure 5. 

Geejayessia sinica asexual state (HMAS 248726): a–c colony on PDA (a), SNA (b) and CMD (c) d conidiophores, conidiogenous cells and macroconidia on SNA e–l Macroconidia on SNA. Scale bars: 50 μm (d–h); 10 μm (i–l).

Discussion

Schroers et al. (2011) recognised five species of Geejayessia. Geejayessia montana Lechat & J. Fourn was recently described and its placement was supported by morphological characteristics of both sexual and asexual states, as well as analysis of ITS sequences (Lechat and Fournier 2017). Meanwhile, a new combination, G. hispanica (Lechat & Priou) Lechat & J. Fourn was proposed based on the ITS sequence of Geejayessia sp. BRFM 1015 (GenBank accession no. JX082350) (Lechat and Fournier 2017). However, ‘Geejayessia hispanica’ grows on Phoenix canariensis rather than Buxus, Celtis or Staphylea, which deviates from the original generic concept of the genus (Schroers et al. 2011). This fungus was treated as Cosmospora hispanica Lechat & Priou in the present study. Cosmospora matuoi Hosoya & Tubaki was also combined with Geejayessia as G. matuoi (Hosoya & Tubaki) Lechat & Rossman (Lechat and Rossman 2017). Nevertheless, Gräfenhan et al. (2011) and Lombard et al. (2015) treated Cosmospora matuoi as a member of Fusicolla, which is followed in this study. To clarify the taxonomic positions of ‘G. hispanica’ and ‘G. matuoi’, more evidence is certainly required.

According to the International Code of Nomenclature for algae, fungi and plants (McNeill et al. 2012), the name Fusarium is accepted as the correct generic name for fungi with Gibberella Sacc. sexual states (Rossman et al. 2013). The asexual states of other genera are marked as fusarium-like (Lombard et al. 2015). In the present study, the phylogeny, based on analyses of the combined ACL1, ITS and RPB2 sequences, recognised nine clades amongst the investigated taxa which are in accordance with the genera Albonectria, Cyanonectria, Dialonectria, Fusicolla, Geejayessia, Macroconia, Microcera, Neocosmospora and Stylonectria. This result is basically consistent with that by Schroers et al. (2011).

Joining the two new species to the Geejayessia clade, the tree topology (Figure 1) remains basically the same as that revealed by Schroers et al. (2011). Our result showed G. clavata and G. atrofusca both forming microconidia in culture, grouped together with relatively high statistical supports (Figure 1, BIPP/MPBP = 100%/89%). Geejayessia sinica, G. cicatricum and G. desmazieri, as sister-groups, are poorly supported (BIPP/MPBP less than 50%).

Host specificity has been shown in some fungi of Nectriaceae; for example, Thyronectria aurigera (Berk. & Ravenel) Jaklitsch & Voglmayr occurs only on Oleaceae, T. berolinensis (Sacc.) Seaver on Ribes and T. aquifolii (Fr.) Jaklitsch & Voglmayr on Ilex aquifolium (Jaklitsch and Voglmayr 2014; Zeng and Zhuang 2016). Species of Geejayessia are also host-specific. As known currently, G. clavata, G. sinica, G. cicatricum and G. desmazieri occur only on Buxus spp., G. celtidicola only on Celtis occidentalis and G. atrofusca only on Staphylea trifolia (Schroers et al. 2011).

The genus Geejayessia was previously known from Europe, North America and Oceania (Samuels and Rogerson 1984; Nirenberg and Samuels 2000; Schroers et al. 2011). The new species discovered from central China extends the distribution of the genus to Asia.

Acknowledgements

We are very grateful to Drs. H.D. Zheng, Z.X. Zhu, W.T. Qin and K. Chen for collecting specimens jointly for this study and to Dr. X.C. Wang for technical help. This work was supported by the National Key Research and Development Program of China (no. 2017YFD0200600), the National Natural Science Foundation of China (no. 31750001) and Frontier Key Program of Chinese Academy of Sciences (no. QYZDY-SSW-SMC029).

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