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Research Article
Ravenelia piepenbringiae and Ravenelia hernandezii, two new rust species on Senegalia (Fabaceae, Mimosoideae) from Panama and Costa Rica
expand article infoM. Ebinghaus‡, D. Begerow‡
‡ Ruhr-University Bochum, Bochum, Germany

Corresponding author: M. Ebinghaus ( malte.ebinghaus@gmx.de )

Academic editor: Marco Thines
© 2018 M. Ebinghaus, D. Begerow.
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: Ebinghaus M, Begerow D (2018) Ravenelia piepenbringiae and Ravenelia hernandezii, two new rust species on Senegalia (Fabaceae, Mimosoideae) from Panama and Costa Rica. MycoKeys 41: 51-63. https://doi.org/10.3897/mycokeys.41.27694
Open Access

Abstract

Two new rust species, Ravenelia piepenbringiae and R. hernandezii (Pucciniales) on Senegalia spp. (Fabaceae) are described from the Neotropics (Panama, Costa Rica). A key to the species on neotropical Senegalia spp. is provided. Molecular phylogenetic analyses based on 28S rDNA sequence data suggest that the representatives of Senegalia rusts distributed in the neotropics evolved independently from species known from South Africa. This is further supported by the teliospore morphology, which is characterised by uniseriate cysts in the neotropical Senegalia rusts and contrasting multiseriate cysts in the paleotropic Ravenelia species that infect this host genus.

Keywords

Senegalia rust, rust fungi, Phylogeny, Taxonomy

Introduction

With more than 200 described species, the genus Ravenelia is amongst the most speciose genera within the rust fungi (Pucciniales) (Cummins and Hiratsuka 2003). In the tropics and subtropics, members of this genus parasitise a diverse range of hosts of the legume family (Fabaceae), including Caesalpinioideae, Faboideae and Mimosoideae. Numerous species of Ravenelia are known from the neotropics, mostly from Mexico (Cummins 1978), Brazil (Dianese et al. 1993, Rezende and Dianese 2001; Hennen et al. 2005) and Argentina (Hernández and Hennen 2002).

However, in the neotropics, occurrence of Ravenelia species is poorly known in other countries such as Panama and Costa Rica. Preliminary checklists of abundant fungi in Central America report only a single species of Ravenelia in Panama (R. entadae) (Piepenbring 2006) and 18 species of Ravenelia in Costa Rica, respectively (Berndt 2004).

Specimens of a rust fungus on Senegalia hayesii (Benth.) Britton and Rose were collected in Panama in 2013. Another species of Ravenelia was discovered through the analysis of herbarium specimens of the U.S. National Fungal Collections (BPI) on Senegalia tenuifolia (L.) Britton and Rose. On the basis of morphological and molecular data, these two specimens were herein analysed and described respectively as Ravenelia piepenbringiae and R. hernandezii.

Material and methods

Light- and electron microscopic investigations

Spores representing different spore stages were scraped from the leaf surfaces of dried herbarium specimens and stained in lactophenol solution on microscope slides. For the analysis of soral structures, hand sections were prepared under a stereomicroscope. Samples were microscopically studied with a Zeiss Axioplan Light Microscope and Zeiss AxioCam. Cellular structures were measured using ZEN 2 (Blue Edition) Software. Infected leaflets of the herbarium specimens were mounted on double-sided sticky carbon tape on metal stubs and coated with gold in a Sputtercoater BAL-TEC SCD OSO (Capovani Brothers Inc, USA). Superficial ornamentation of spores was investigated using a ZEISS Sigma VP scanning electron microscope at the Ruhr-University Bochum, Germany.

DNA extraction and PCR

Genomic DNA extractions were carried out using the INNUPrep Plant DNA Kit (Analytic Jena, Germany) according to the manufacturer’s protocol. Spores were milled in a Retsch Schwingmühle MM2000 (F. Kurt Retsch GmbH &Co KG, Haan, Germany), using two steel beads and liquid nitrogen in three consecutive cycles. An amount of 40 ml of lysis buffer was added to loosen spore remnants by vortexing from the Eppendorf tube lid, followed by centrifuging in a final cycle. Polymerase chain reaction (PCR) of 28S rDNA was conducted using the Taq-DNA-Polymerase Mix (PeqLab, Erlangen, Germany). To compensate for small amounts of spores applied for DNA extractions up to 5ml of genomic DNA extraction were used as the template in 25 ml reactions. Primer pair LR0R (Moncalvo et al. 1995) and LR6 (Vilgalys and Heester 1990) were used to obtain sequences of the 28S rDNA, with thermal cycling conditions set at 96 °C (3 min) followed by 40 cycles of 30 sec at 95 °C, 40 sec at 49 °C and 1 min at 72 °C, with a final extension for 7 min at 72 °C. PCR products, which showed only weak bands on agarose gels, were purified with Zymo Research DNA Clean & Concentrator-5 Kit (ZymoResearch Corp., Irvine, USA), according to the manufacturer’s protocol. The remaining PCR products were purified using Sephadex G-50 columns (Sigma-Aldrich Chemie GmbH, Taufkirchen, Germany). Sequencing was carried out in both directions using the same primers as in PCR at the sequencing service of the Faculty of Chemistry and Biochemistry of the Ruhr-University Bochum, Germany and by GATC (GATC Biotech, Konstanz, Germany)

Phylogenetic analyses

Sequences were screened against the NCBI Genbank using the BLAST algorithm to check for erroneously amplified contaminations and were afterwards edited manually using Sequencher 5.0 software (Gene Codes Corp., Michigan, USA). In total, 26 sequences were included (Table 1) to construct an alignment of the 28S rDNA-sequence data using MAFFT v6.832b (Katoh and Standley 2013). Maximum likelihood (ML) analyses were performed with RxML 8.0.26 (Stamatakis 2014) using RAxML GUI v. 1.31 (Silvestro and Michalak 2012) based on the General Time Reversible model of nucleotide substitution plus gamma distribution (GTR+G; Rodriguez et al. 1990) and 1000 generations. Four representative species of Endoraecium (KJ862335, KJ862298, KJ862337, KJ862344) were set as multiple outgroups. Maximum Parsimony (MP) analyses were carried out using MEGA6 (Tamura et al. 2013) using the heuristic search option with tree bisection-reconnection (TBR) branch swapping algorithm with 10 initial trees using random step-wise addition. The reliability of topology was tested using the bootstrap method with 1000 replicates.

Table 1.
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Specimens analysed in this study, including GenBank Accession Numbers. Published references are given for sequences obtained from GenBank. †: BPI (U.S. National Fungus Collections, USA); ‡: KR (Staatliches Museum für Naturkunde Karlsruhe, Germany); $: PREM (Plant Protection Research Institute, South Africa); |: Z+ZT (Universität Zürich, Switzerland and Eidgenössische Technische Hochschule Zürich, Switzerland); ¶: BRIP (Department of Agriculture and Fisheries, Australia); #: PMA (Universidad de Panamá, Panama).

Voucher Species Substrate Reference Origin LSU
GenBank
BPI841185† Ravenelia cohniana Henn. Senegalia praecox (Grieseb.) Seigler & Ebinger This work Catamarca Province, Argentina MG954487
BPI841034† Ravenelia echinata var. ectypa (Arthur & Holw.) Cummins Calliandra formosa (Kunth) Benth. Scholler and Aime, 2006 Tucuman Province, Argentina DQ323925*
KR-M-0043650‡ Ravenelia escharoides Syd. Senegalia burkei (Benth.) Kyal. & Boatwright This work Mpumalanga, South Africa MG954480
KR-M-0043651‡ Ravenelia escharoides Syd. Senegalia burkei (Benth.) Kyal. & Boatwright This work Limpopo, South Africa MG954481
KR-M-0043652‡ Ravenelia escharoides Syd. Senegalia burkei (Benth.) Kyal. & Boatwright This work Limpopo, South Africa MG954482
PREM61223$ Ravenelia evansii Syd. Vachellia sieberiana (Burtt Davy) Kyal. & Boatwr. This work KwaZulu-Natal, South Africa MG945988
PREM61228$ Ravenelia evansii Syd. Vachellia sieberiana (Burtt Davy) Kyal. & Boatwr. This work KwaZulu-Natal, South Africa MG945989
PREM61855$ Ravenelia halsei Doidge Senegalia ataxacantha (D.C) Kyal. & Boatwright This work Mpumalanga, South Africa MG954484
Z+ZT RB5788| Ravenelia havanensis Arthur Enterolobium contortisiliquum (Vell.) Morong Aime, 2006 Tucuman Province, Argentina DQ354557*
BPI872308† Ravenelia hernandezii Ebinghaus & Begerow Senegalia tenuifolia (L.) Britton & Rose This work Guanacaste, Costa Rica MG954488
PREM61222$ Ravenelia macowaniana Pazschke Vachellia karroo (Hayne) Banfi & Galasso This work Limpopo Province, South Africa MG946007
PREM61210$ Ravenelia macowaniana Pazschke Vachellia karroo (Hayne) Banfi & Galasso This work Eastern Cape Province, South Africa MG946004
PREM61221$ Ravenelia macowaniana Pazschke Vachellia karroo (Hayne) Banfi & Galasso This work North-West Province, South Africa MG946005
BPI841195† Ravenelia macrocarpa Syd. & Syd. Senna subulata (Griseb.) H.S. Irwin & Barneby Scholler and Aime 2006 Argentina DQ323926*
BRIP56908¶ Ravenelia neocaledoniensis Huguenin Vachellia farnesiana (L.) Wight & Arn. McTaggart et al. 2015 Kununurra, Australia KJ862348*
BRIP56907¶ Ravenelia neocaledoniensis Huguenin Vachellia farnesiana (L.) Wight & Arn. McTaggart et al. 2015 Northern Territory, Australia KJ862347*
KR-M-0045114‡ Ravenelia pienaarii Doidge Senegalia caffra (Thunb.) P.J.H. Hurter & Mabb. This work Gauteng, South Africa MG954483
PREM61892$ Ravenelia pienaarii Doidge Senegalia caffra (Thunb.) P.J.H. Hurter & Mabb. This work KwaZulu-Natal, South Africa MG954482
MP5157 (PMA)# Ravenelia piepenbringiae Ebinghaus & Begerow Senegalia hayesii (Benth.) Britton & Rose This work Chiriquí Province, Panama MG954489
BRIP56904¶ Ravenelia sp. Cassia sp. Mill. McTaggart et al. 2015 Northern Territory, Australia KJ862349*
PREM61858$ Ravenelia transvaalensis Doidge Senegalia mellifera (Vahl) Seibler & Ebinger This work North-West Province, South Africa MG954485
PREM61893$ Ravenelia transvaalensis Doidge Senegalia mellifera (Vahl) Seibler & Ebinger This work North-West Province, South Africa MG954486
BRIP56539¶ Endoraecium auriculiforme McTaggart & Shivas Acacia difficilis Maiden McTaggart et al., 2015 Northern Territory, Australia KJ862398*
BRIP27071¶ Endoraecium tierneyi (Walker & Shivas) Scholler & Aime Acacia harpophylla F.Muell. ex Benth. McTaggart et al. 2015 Queensland, Australia KJ862335*
BRIP56557¶ Endoraecium tropicum McTaggart & Shivas Acacia tropica (Maiden & Blakely) Tindale McTaggart et al. 2015 Northern Territory, Australia KJ862337*
BRIP56545¶ Endoraecium violae-faustiae Berndt Acacia difficilis Maiden McTaggart et al. 2015 Northern Territory, Australia KJ862344*

Results

Phylogenetic analyses

The alignment of the 28S rDNA sequence data consisted of 26 sequences representing 18 taxa and had a total length of 1015 nucleotides with 305 variable characters, 250 parsimony-informative sites and 55 singletons. The tree topologies of MP and ML analyses were identical and thus only the ML tree is shown. A clade, comprising rusts on neotropical Senegalia species, i.e. R. cohniana, R. hernandezii sp. nov. and R. piepenbringiae sp. nov., displays a robustly supported sister-group (MLBS/MPBS = 99/100) to two neotropically distributed rusts which infect non-Senegalia hosts (i.e. R. echinata var. ectypa on Calliandra formosa, DQ323925 and R. havanensis on Enterolobium contortisiliquumDQ354557) (Scholler and Aime 2006, Aime 2006). A second clade, based on sequences obtained from Ravenelia species on Senegalia spp. with paleotropical origin, appeared only distantly related to the former species cluster (MLBS/MPBS = 100/99) (Figure 1).

Figure 1. 

Maximum likelihood reconstruction of Ravenelia spp. based on 28S rDNA sequence data. Bootstrap values are shown above branches based on 1000 replicates (MLBS and MPBS, respectively), values below 75 are not shown. Names of species collected on neotropical Senegalia hosts including R. piepenbringiae and R. hernandezii are highlighted (bold, red box). For paleotropically distributed species of Senegalia rusts, see black box.

Taxonomy

Ravenelia piepenbringiae Ebinghaus & Begerow, sp. nov. on Senegalia hayesii (Benth.) Britton & Rose (Mimosoideae, Leguminosae)

MycoBank No: Mycobank: MB 824297
Fig. 2

Type

Panama, Chiriquí Province, Dolega District, Los Algarrobos, Casa de la Alemana, Bosquecito, approx. 150 m a.s.l., 8°29'45.31"N, 82°25'56.24"W on Senegalia hayesii (Benth.) Britton and Rose, 17 February 2013, coll. M. Piepenbring MP 5157 [holotype: s.n. (PMA), isotypes: KR-M-0043654 (KR). M-0141345 (M)]

Etymology

Named after M. Piepenbring, who discovered the rust fungus in her garden and provided the specimens.

Spermogonia and aecia not seen. Uredinia hypophyllous, single or in irregular groups, light brown, often associated with necrotic spots that are also evident on the adaxial surface, 0.1–0.8 mm in diameter, aparaphysate, subepidermal, covered by the epidermis when young, later erumpent. Urediniospores obovoidal, ellipsoidal or slightly curved, often limoniform with an acuminate apex, ochraceous brown, (18)21–25(29) × 12–15(20) mm; spore wall laterally 1–1.5 mm thick, apically and basally often slightly thickened, distinctly verrucose to echinulate; aculei 1.0–1.5 mm high, distances between aculei about 2 mm, germ pores 4–7, in equatorial position. Telia replacing uredinia or developing independently from uredinia, chestnut to dark brown, sometimes confluent. Teliospores roundish to broadly ellipsoidal to oblong in planar view, hemispherical in lateral view, with 4–6 probasidial cells across, single-layered, each teliospore formed by 9–13 probasidial cells, (44)58–73(78) mm in diameter, single probasidial cells (19)22–26(31) × (11)17–22(28) mm; cell wall thickened at the surface of the teliospore (epispore), 2–4(5) mm thick, often with a thin and hyaline outer layer, each probasidial cell with 7–11 rod-shaped, straight spines that are (1)2–3(4.5) mm long; cysts at the basis of the teliospores, uniseriate and in the same position and number as the peripheral probasidial cells, globose, hyaline, swelling in water, slightly swelling in lactophenol.

Further specimens. Type locality, 22 January 2014, M. Piepenbring 5203 [M-0141344 (M), s.n. (UCH)]. Type locality, 12 January 2017, M. Piepenbring & I. D. Quiroz González 5333 (UCH, s.n.).

Figure 2. 

Ravenelia piepenbringiae. A Telia in chlorotic spots associated with infection of Senegalia hayesii B, C sori showing uredinio- and teliospores and teliospores, respectively D SEM image of a telium E SEM view of a teliospore F, I LM images of teliospores G SEM image of urediniospores showing equatorially arranged germ pores H drawings of urediniospores. Scale bars: 3 mm (A); 0.1 mm (B); 0.2 mm (C); 40 mm(D); 10 mm (E); 20 mm(F); 5 mm(G); 10 mm(H); 20 mm(I).

Ravenelia hernandezii Ebinghaus & Begerow, sp. nov. on Senegalia tenuifolia (L.) Britton and Rose (Mimosoideae, Leguminosae)

MycoBank No: Mycobank: MB 824298
Fig. 3

Type

Costa Rica, Guanacaste, Area de Conservación Guanacaste, Sendero Bosque húmedo (10°50.702'N, 85°36.450'W) on Senegalia tenuifolia (L.) Britton and Rose, coll. J.R. Hernandez, 1. December 2003. Holotype: BPI 872308 (BPI).

Etymology

Named after J.R. Hernández who collected the type specimen.

Spermogonia and aecia not seen. Uredinia hypophyllous, minute, single or in small and often loose groups, ochraceous to light brown, 0.1–0.3 mm in diameter, aparaphysate, subepidermal, erumpent and surrounded by torn epidermis; urediniospores obovoidal, ellipsoidal, often reniform or slightly curved, ochraceous brown, often with an attached fragment of the pedicel, (17)18–21(24) × (8)9–10(12) mm; spore wall thin, laterally (0.5)1–1.5 mm thick, apically and basally slightly thickened, distinctly echinulate; aculei approximately 1.0–1.5 mm high, germ pores 5–6, in equatorial position. Telia replacing uredinia, chestnut- to dark brown. Teliospores (59)67–75(96) mm, roundish or broadly ellipsoidal to oblong in planar view, hemispherical in lateral view, 5–6 probasidial cells across, single-layered, central cells often arranged in two rows of 3 or 4 cells, each cell (19)22–25(39) × (11)17–22(28) mm, cell wall thickened at the apex, (2.5)3.0–4.5(6.0) mm thick, often with a thin and hyaline outer layer, probasidial cells each with 3–5 rod-shaped straight spines (1)3–4(6) mm long; cysts on the abaxial side of the teliospores, uniseriate and in same position and number as the peripheral probasidial cells, globose, hyaline, swelling in water, slight swelling in lactophenol.

Figure 3. 

Ravenelia hernandezii. A Infected leaflets of S. tenuifolia B Mixed sori containing urediniospores and teliospores C Teliospore seen in LM D telium seen by SEM E Adaxial view of a teliospore by LM, with arrows indicating the uniseriate cysts F SEM view of spinescent teliospores G LM view of the upper surface H drawing of a urediniospore. Scale Bars: 0.5 mm (A); 0.1 mm (B); 20 mm (C–G); 10 mm (H).

Discussion

A total of 10 species of Ravenelia have been described to date from the neotropics parasitising Senegalia trees: R. cohniana Hennings on S. praecox (Griseb.) Seigler & Ebinger, R. idonea Jackson & Holway, R. lata Hennen & Cummins on S. glomerosa (Benth.) Britton & Rose, R. monosticha Speg. on S. bonariensis (Gillies ex Hook. & Arn.) Seigler & Ebinger, R. pringlei Cummins on S. greggii (A. Gray) Britton & Rose, R. rata Jackson & Holway on S. pedicellata (Benth.) Seigler & Ebinger, R. roemerianae Long on S. roemeriana (Scheele) Britton & Rose, R. scopulata Cummins & Baxter on S. greggii (A. Gray) Britton & Rose, R. stevensii Arthur on S. riparia (Kunth) Britton & Rose ex Britton & Killip and R. versatilis (Peck) Dietel on S. anisophylla (Watson) Britton & Rose. No species of Ravenelia has been reported to affect Senegalia hayesii or S. tenuifolia. Most of these species known to parasitise Senegalia spp. are distinguished from species identified in this study by abundant paraphyses in the uredinia, except for Ravenelia rata which also lacks paraphyses in the uredinia. However, this species differs from R. piepenbringiae and R. hernandezii by abundant tuberculate teliospore ornamentations 2–3µm in length and by formation of only 2–4 cysts per teliospore. Both newly described species exhibit longer tuberculate spines and bear 6–8 cysts per teliospore. Ravenelia cohniana is the only species that resembles various teliospore and urediniospore characteristics of R. piepenbringiae and R. hernandezii (see Table 2). The teliospores of R. hernandezii, however, are larger in size than those of the latter two species (Table 2). In contrast to the teliospores, urediniospores of R. hernandezii tend to be smaller and more slender, while they mostly lack the characteristic acuminate apex present in urediniospores of R. piepenbringiae (Table 2; compare Figures 1H and 2H). Hernández and Hennen (2002) considered R. concinna Syd. on S. riparia (Kunth) Britton & Rose ex Britton & Killip and S. glomerosa, R. distans Arthur & Holway on an unidentified mimosoid host and R. lindquistii Hennen & Cummins on Senegalia praecox as synonyms of R. cohniana due to a nearly identical morphology. However, given the likewise close morphological resemblance in R. piepenbringiae, R. hernandezii and R. cohniana, despite being phylogenetic entities, this assumption needs revision by molecular phylogenetic means.

The resemblance of teliospore characters in R. cohniana and the species identified in the present study suggests a close relationship which is supported by the phylogenetic reconstructions. These neotropical rusts on Senegalia further appear to have evolved independently from those Senegalia rusts that have a paleotropic origin (Fig. 1, Table 1). The phylogenetic distinction of both lineages is also mirrored by a morphological feature: the arrangement of teliosporic cysts is uniseriate in the analysed neotropic species but multiseriate in all investigated paleotropic Senegalia rusts (Table 2).

Table 2.
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Summary of morphological characteristics of Ravenelia species infecting Senegalia trees in the neotropics. All measurements are given in mm. Absent characters are indicated with dashes.

Species Teliospore characters Source
Teliospore size Probasidial cell size Epispore Ornamentation Cells in Diameter Arrangement of Cysts
Number per cell length shape
R. cohniana (39)45–73(74) 16–22 × 13–15 not stated (2)3–5(8). 3–5 spinescent (3)4–5(6) uniseriate Hernández and Hennen (2002)
R. escharoides 55–90 30–35 × 16–20 up to 6 4–9 1–2 verrucose 6–8 multiseriate Doidge (1939)
R. halsei 80–112 25–30 × 10–15 5–6 – – smooth 9–11 uniseriate Doidge (1939)
R. hernandezii (59)67–75(96) (19)22–25(39) × (11)17–22(28) (2.5)3–4.5(6) 3–5 (1)3–4(6) spinescent 5–6 uniseriate This study
R. lata 53–64 (18)22–26 (width) not stated 6–20 not stated spinescent 4 multiseriate Hennen et al. (2005)
R. monosticha (50)53–55 × 65–70 16–19 × 13–15 not stated 4–8 not stated verrucose 4–6 uniseriate Spegazzini (1923)
R. pienaarii 80–120 25–30 × 10–15 up to 7 4–7 1–1.5(2) verrucose (6)7–10 multiseriate Doidge (1939)
R. piepenbringiae (44)58–73(78) (19)22–26(31) × (11)17–22(28) 2–4(5) 7–11 (1)2–3(4.5) spinescent 4–6 uniseriate This study
R. pringlei (55)70–95(105) (12)14–18(20) (width) not stated not stated not stated verrucose (5)6–8 uniseriate Cummins (1975)
R. rata (30)33–40(44) 14–20 × 12–17 1.5 not stated 2–3 verrucose 2–4 uniseriate Hennen et al. (2005)
R. roemerianae 63–100 Not stated not stated 3–10 2 verrucose 5–7 uniseriate Long (1917)
R. scopulata (55)65–100(110) (13)16–19(21) (width) not stated not stated not stated smooth 5–8 multiseriate Cummins and Baxter (1976)
R. stevensii 40–63 Not stated not stated 1–3 6–19 verrucose 3–6 multiseriate Arthur (1915)
R. transvaalensis 75–100 30–35 × 15–17.5 up to 6 – – smooth 5–6 multiseriate Doidge (1939)
R. versatilis 85–105 10–16 (width) not stated – – smooth 7–9 not stated Dietel (1894)
Paraphyses Urediniospore characters Source
Position Shape Size Cell wall Germ pores Shape
Number Position
R. cohniana – – (12)20–28(32) × (11)13–17(19) 1.5–2.5(3) (3)4(6) equatorial oblong-ellipsoidal Hernández and Hennen (2002)
R. escharoides – – 17–22×14–17 1.5 Not stated not stated obovoidal-ellipsoidal Doidge (1939)
R. halsei not stated not stated – – – – – Doidge (1939)
R. hernandezii – – (17)18–21(24) × (8)9–10(12) (0.5)1–1.5 5–6 equatorial obovoidal-ellipsoidal This study
R. lata peripheral capitate (22)25–32(36) × (12)14–17(18) 1.5–2 (4)5–6 equatorial obovoidal-oblong Hennen et al. (2005)
R. monosticha peripheral capitate (23)26–30(33) × (8)12–14(15) 1.5–2 4–5(6) equatorial obovoidal-ellipsoidal Spegazzini (1923)
R. pienaarii – – 20–25 × 15–19 1.5 6 equatorial ellipsoidal-subglobose Doidge (1939)
R. piepenbringiae – – (18)21–25(29) × 12–15(20) 1–1.5 4–7 equatorial obovoidal-limoniform This study
R. pringlei not stated clavate - capitate (10)11–15(17) × (20)26–33(35) (1)1.5(2) 8 bizonate oblong-ellipsoidal Cummins (1975)
R. rata – – – – – – – Hennen et al. (2005)
R. roemerianae intrasoral clavate 10–14 × 27–38 1–1.5 8 bizonate obovoidal-oblong Long (1917)
R. scopulata not stated clavate (17)19–24 × (11)12–14(15) (1)1.5(2) 6–8 bizonate oblong-ellipsoidal Cummins and Baxter (1976)
R. stevensii peripheral clavate - capitate 8–13 × 25–30 <1 4 equatorial oblong-obovoidal Arthur (1915)
R. transvaalensis – – – – – – – Doidge (1939)
R. versatilis intrasoral clavate - capitate 13–18 × 26–32 Not stated 8 bizonate obovoidal-oblong Dietel (1894)

Key to species of Ravenelia infecting neotropical Senegalia trees

1 Teliospores ≤64 mm; urediniospores with equatorially arranged germ pores 2
– Teliospores >64 mm; urediniospores with bizonate or equatorially arranged germ pores 4
2 Paraphyses present in uredinia 3
– Paraphyses absent in uredinia R. rata
3 Teliospores with <6 verrucae per cell; on S. riparia R. stevensii
– Teliospores with 6–20 spines per cell; on S. glomerosa R. lata
4 Urediniospores with 6–8 bizonate germ pores; teliospores verrucose or smooth 5
– Urediniospores if present with equatorially arranged germ pores; teliosporesspinescent or verrucose; teliospore cysts uniseriate 8
5 Teliospores smooth 6
– Teliospores verrucose 7
6 On S. anisophylla; urediniospores 12–14 × 19–24 mm R. versatilis
– On S. greggii; urediniospores 13–18 × 26–32 mm R. scopulata
7 With intrasoral paraphyses; on S. roemeriana R. roemerianae
– On S. greggii R. pringlei
8 Paraphyses present; teliospores verrucose; on S. bonariensis R. monosticha
– Paraphyses absent; teliospores spinescent 9
9 Teliospores with 7–11 spines per cell; urediniospores often limoniform; on S. hayesii R. piepenbringiae
– Teliospores with 3–5 spines per cell; urediniospores obovoidal to ellipsoidal,sometimes limoniform 10
10 Teliospores 59–96 mm in diameter; urediniospores <13mm in width; urediniospore wall laterally 1–1.5 mm; on S. tenuifolia R. hernandezii
– Teliospores 39–75 mm in diameter; urediniospores 11–19 mm in width; urediniospore wall laterally 1.5–2.5 mm; on S. praecox R. cohniana

Acknowledgements

We gratefully acknowledge Dr. Meike Piepenbring, the US National Fungus Collections (USDA-ARS) and the South African Mycology Collections (PREM) for providing herbarium specimens on loan. We also wish to thank Katharina Görges for providing drawings of the urediniospores of R. piepenbringia and R. hernandezii.

References

  • Berndt R (2004) A checklist of Costa Rican rust fungi. In: Agerer R, Piepenbring M, Blanz P (Eds) Frontiers in Basidiomycete Mycology.IHW Verlag, München, 185–236 .
  • Cummins GB, Hiratsuka Y (2003) Illustrated Genera of Rust Fungi (3rd edn). Phytopathological Society, St. Paul, MN, APS Press, St. Paul, MN.
  • Dianese JC, Medeiros RB, Santos LTP, Furlanetto C, Sanchez M, Dianese AC (1993) Batistopsora gen. nov. and new Phakopsora, Ravenelia, Cerotellium, and Skierka species from the Brazilian Cerrado. Fitopatologia Brasileira 18: 436–450.
  • Hennen JF, Figueiredo MB, de Carvalho Jr AA, Hennnen PG (2005) Catalogue of the species of plant rust fungi (Uredinales) of Brazil. Instituto de Pesquisas, Jardim Botanico do Rio de Janeiro: Rio de Janeiro, Brazil.
  • Hennings P (1896) Beiträge zur Pilzflora Südamerikas I. Myxomycetes, Phycomycetes, Ustilagineae und Uredineae. Hedwigia 35: 246.
  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
  • Moncalvo JM, Wang HH, Hseu RS (1995) Phylogenetic relationships in Ganoderma inferred from the internal transcribed spacers and 25S ribosomal DNA sequences. Mycologia 87: 223–238. https://doi.org/10.1080/00275514.1995.12026524
  • Piepenbring M (2006) Checklist of fungi in Panama. Puente Biológico Volume 1: 1–190.
  • Scholler M, Aime C (2006) On some rust fungi (Uredinales) collected in an Acacia koa–Metrosideros polymorpha woodland, Mauna Loa Road, Big Island, Hawaii. MycoScience 47: 159–165. https://doi.org/10.1007/S10267-006-0286-8
  • Silvestro D, Michalakis I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity and Evolution 12: 335–337. doi: 10.1007/s1127-011-0056-0
  • Spegazzini CL (1909) Mycetes Argentinenses. Anales del Museo Nacional de Buenos Aires. Series. 3, 12: 296.
  • Sydow H, Sydow P (1916) Fungi amazonici a cl. E. Ule lecti. Annales Mycologici 14: 65–97.
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
  • Vilgalys R, Hester M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (Eds) PCR Protocols: A Guide to Methods and Applications.Academic Press, Inc., New York, 315–324.
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