A co-evolutionary relationship exists between Endoraecium (Pucciniales) and its Acacia hosts in Australia

Abstract

Endoraecium is a genus of rust fungi that infects several species of Acacia in Australia, South-East Asia and Hawaii. This study investigated the systematics of Endoraecium from 55 specimens in Australia based on a combined morphological and molecular approach. Phylogenetic analyses were conducted on partitioned datasets of loci from ribosomal and mitochondrial DNA. The recovered molecular phylogeny supported a recently published taxonomy based on morphology and host range that divided Endoraecium digitatum into five species. Spore morphology is synapomorphic and there is evidence Endoraecium co-evolved with its Acacia hosts. The broad host ranges of E. digitatum, E. parvum, E. phyllodiorum and E. violae-faustiae are revised in light of this study, and nine new species of Endoraecium are described from Australia based on host taxonomy, morphology and phylogenetic concordance.

Full text

© 2015 Naturalis Biodiversity Center & Centraalbureau voor Schimmelcultures
You are free to share - to copy, distribute and transmit the work, under the following conditions:
Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work).
Non-commercial: You may not use this work for commercial purposes.
No derivative works: You may not alter, transform, or build upon this work.
For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be
waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights.
Persoonia 35, 2015: 50 – 62
www.ingentaconnect.com/content/nhn/pimj http://dx.doi.org/10.3767/003158515X687588
!"#"$!%&''$!()%*"
)+(!,-.%(),+
Endoraecium (Pucciniales, Raveneliaceae) was established
for two endocyclic species of rust fungi with pedicellate spores,
E. acaciae (the type species) and E. hawaiiense, which were
found on Acacia koa (Fabaceae, subfamily Mimosoideae) in
Hawaii (Hodges & Gardner 1984). There are over 1 000 spe-
cies of Acacia s.str. (hereafter referred to as Acacia) known in
Australia (Murphy et al. 2010, Maslin 2013). The classification
of Acacia has moved from a traditional morphological one based
on sections, to a molecular phylogenetic one based on clades
(Murphy et al. 2010, Miller et al. 2013). At the commencement
of this study, 20 species of Acacia were recorded as hosts
of seven species of Endoraecium in Australia (Berndt 2011).
These 20 host species fall within three clades of the plurinerved,
uninerved and Botrycephalae (p.u.b.) group of Acacia (Murphy
et al. 2010), namely the i) Botrycephalae subclade (Murphy
et al. 2010); ii) Juliflorae p.p. clade (Miller et al. 2013); and iii)
Plurinerves p.p. clade (Miller et al. 2013), hereafter referred
to as Botrycephalae, Juliflorae and Plurinerves, respectively.
Species of Endoraecium produce a range of symptoms on
Acacia that include bullate swellings or pulvinate sori on phyl-
lodes, or galls and witches’ brooms on stems. These rust fungi
produce spores of three types: i) spermogonia; ii) pedicellate
spores, which have reticulate to foveolate ornamentations and
were variously called aecial urediniospores (Walker 2001),
uredo-like aeciospores (Berndt 2011) or teliospores in the
endocyclic species (Hodges & Gardner 1984); iii) teliospores,
which are single celled, subhyaline and smooth walled. The
teliospores are morphologically similar to those of Uromyces
s.l. and several species of Endoraecium were at one time clas -
sified in that genus, including U. digitatus (Winter 1886), U. bi-
cintus (McAlpine 1906), U. phyllodiorum (McAlpine 1906),
U. hyalosporus (Sawada 1913) and U. koae (Stevens 1925). On
the basis of morphology, some species currently considered as
Endoraecium were previously placed in other genera, including
Pileolaria (Dietel 1921), Maravalia (Dietel 1924), Poliotelium
(Mains 1939), Atelocauda (Cummins & Hiratsuka 1983, Ono
1984, Gardner 1991), and Racospermyces (Walker 2001).
Gardner (1991) proposed that Endoraecium may be closely re-
lated to Uromycladium (Pileolariaceae), another genus of rust
that occurs on Acacia in Australia. However, in combined
analyses of the Large Subunit (LSU) and Small Subunit (SSU)
regions of ribosomal DNA (rDNA), the systematic position of
Endoraecium was shown by Scholler & Aime (2006) and Aime
(2006) to have an affinity with mimosoid rusts in the Ravenel-
iaceae rather than with the Pileolariaceae.
In this study, the systematic relationships of Endoraecium on
Acacia in Australia were investigated with freshly collected field
material and herbarium specimens. Currently, Endoraecium
contains 13 species, all on Acacia, with seven endemic to
Australia, one to South-East Asia and five to Hawaii (McAl-
pine 1906, Sawada 1913, Hodges & Gardner 1984, Berndt
2011). The species are E. acaciae (type on A. koa, Hawaii),
E. angustiphyllodium (type on A. koa, Hawaii), E. bicinctum
(type on A. fasciculifera, Australia), E. digitatum (type on A. no-
tabilis, Australia), E. hawaiiense (type on A. koa, Hawaii), E. hyalo-
sporum (type on A. confusa, Taiwan), E. kauaianum (type on
A. koa, Hawaii), E. koae (type on A. koa, Hawaii), E. parvum
(type on A. leiocalyx, Australia), E. phyllodiorum (type on
Acacia sp., Australia), E. tierneyi (type on A. harpophylla, Aus-
tralia), E. violae-faustiae (type on Acacia sp., Australia) and
E. walkerianum (type on A. penninervis, Australia). The SSU,
Internal Transcribed Spacer (ITS) and LSU regions of rDNA,
and cytochrome c oxidase subunit 3 (CO3) of mitochondrial
DNA, were used for phylogenetic reconstruction to determine
$'/012304567089:;':2496708<=7>'2?7<6<'@26A228'Endoraecium
BPuccinialesC'98D'76<'Acacia =0<6<'78'$5<6:9479
A.R. McTaggart1,2,3, C. Doungsa-ard1,4, A.D.W. Geering1, M.C. Aime5, R.G. Shivas2
1 Queensland Alliance for Agriculture and Food Innovation, The University of
Queensland, Ecosciences Precinct, GPO Box 267, Brisbane, Queensland
4001, Australia;
corresponding author e-mail: alistair.mctaggart@gmail.com.
2 Department of Agriculture, Fisheries and Forestry, Ecosciences Precinct,
GPO Box 267, Brisbane, Queensland 4001, Australia.
3 Department of Microbiology and Plant Pathology, Tree Protection Co-ope-
rative Programme (TPCP), Forestry and Agricultural Biotechnology Institute
(FABI), Private Bag X20, University of Pretoria, Pretoria, 0028, South Africa.
4 Plant Biosecurity Cooperative Research Centre, LPO Box 5012, Bruce
2617, Australia.
5 Department of Botany and Plant Pathology, Purdue University, 915 W. State
Street, West Lafayette, IN 47907, USA.
E2;'A0:D<
Atelocauda
endocyclic rusts
Mimosoideae
Racospermyces
Raveneliaceae
Uredinales
$@<6:9/6 Endoraecium is a genus of rust fungi that infects several species of Acacia in Australia, South-East
Asia and Hawaii. This study investigated the systematics of Endoraecium from 55 specimens in Australia based
on a combined morphological and molecular approach. Phylogenetic analyses were conducted on partitioned
datasets of loci from ribosomal and mitochondrial DNA. The recovered molecular phylogeny supported a recently
published taxonomy based on morphology and host range that divided Endoraecium digitatum into five species.
Spore morphology is synapomorphic and there is evidence Endoraecium co-evolved with its Acacia hosts. The
broad host ranges of E. digitatum, E. parvum, E. phyllodiorum and E. violae-faustiae are revised in light of this
study, and nine new species of Endoraecium are described from Australia based on host taxonomy, morphology
and phylogenetic concordance.
$:67/42'78F0 Received: 10 June 2014; Accepted: 18 December 2014; Published: 13 February 2015.

51
A.R. McTaggart et al.: Co-evolutionary relationship between Endoraecium and Acacia
Taxon Accession number Subclade 1 of Host GenBank accession
Acacia s.str.
LSU ITS SSU CO3
E. acaciae BPI 871098 Plurinerves A. koa DQ3239162 N/A DQ3239172 N/A
E. auriculiforme BRIP 55609 Juliflorae A. auriculiformis KJ862296 KJ862353 N/A KJ862430
BRIP 56550 Juliflorae A. auriculiformis KJ862297 KJ862354 N/A KJ862431
BRIP 56548* Juliflorae A. auriculiformis KJ862298 KJ862355 N/A KJ862432
BRIP 56549 Juliflorae A. auriculiformis KJ862299 KJ862356 N/A KJ862433
E. carnegiei BRIP 57926 Botrycephalae A. dealbata KJ862300 KJ862357 N/A KJ862434
BRIP 57924* Botrycephalae A. dealbata KJ862301 N/A N/A KJ862435
BRIP 59218 Botrycephalae A. dealbata KJ862302 N/A N/A N/A
E. disparrimum BRIP 55659 Juliflorae A. disparrima KJ862303 N/A KJ862402 KJ862436
BRIP 55626* Juliflorae A. disparrima KJ862304 KJ862358 KJ862403 KJ862437
BRIP 55632 Juliflorae A. disparrima KJ862305 KJ862359 KJ862404 KJ862438
E. falciforme BRIP 57583* Botrycephalae A. falciformis KJ862306 KJ862360 KJ862405 KJ862439
BRIP 57643 Botrycephalae A. falciformis KJ862307 N/A N/A N/A
E. hawaiiense BPI 871064 Plurinerves A. koa DQ3239202 N/A N/A N/A
E. irroratum BRIP 55671 Botrycephalae A. irrorata KJ862310 KJ862364 KJ862406 KJ862442
BRIP 57279 Botrycephalae A. irrorata KJ862311 KJ862365 N/A KJ862443
BRIP 57286* Botrycephalae A. irrorata KJ862312 KJ862366 KJ862407 N/A
BRIP 58054 Botrycephalae A. irrorata KJ862313 N/A N/A N/A
E. koae BPI 871071 Plurinerves A. koa DQ3239182 N/A DQ3239192 N/A
E. maslinii BRIP 57872* Botrycephalae A. daphnifolia KJ862314 KJ862367 KJ862408 KJ862444
E. parvum BRIP 57514 Juliflorae A. leiocalyx KJ862315 KJ862368 N/A N/A
BRIP 57524 Juliflorae A. leiocalyx KJ862316 KJ862369 KJ862409 KJ862445
BRIP 57527 Juliflorae A. leiocalyx KJ862317 KJ862370 N/A N/A
BRIP 57534 Juliflorae A. leiocalyx KJ862318 KJ862371 N/A N/A
BRIP 57568 Juliflorae A. leiocalyx KJ862319 KJ862372 N/A N/A
BRIP 57631 Juliflorae A. leiocalyx KJ862320 KJ862373 KJ862410 KJ862446
BRIP 57512 Juliflorae A. leiocalyx KJ862321 KJ862374 N/A N/A
BRIP 53616 Juliflorae A. leiocalyx KJ862322 KJ862375 N/A N/A
E. peggii BRIP 55602* Juliflorae A. holosericia KJ862308 KJ862361 N/A KJ862440
BRIP 55631 Juliflorae A. holosericia KJ862309 KJ862362 N/A KJ862441
BRIP 58324 Juliflorae A. holosericia N/A KJ862363 N/A N/A
E. phyllodiorum BRIP 57310 Juliflorae A. aulacocarpa KJ862323 KJ862377 N/A N/A
BRIP 57516 Juliflorae A. aulacocarpa KJ862324 KJ862378 KJ862411 KJ862447
BRIP 57569 Juliflorae A. aulacocarpa KJ862325 KJ862379 N/A N/A
BRIP 57570 Juliflorae A. aulacocarpa KJ862326 KJ862380 N/A N/A
BRIP 57578 Juliflorae A. aulacocarpa KJ862327 KJ862381 KJ862412 KJ862448
BRIP 57579 Juliflorae A. aulacocarpa KJ862328 N/A KJ862413 N/A
BRIP 57580 Juliflorae A. aulacocarpa KJ862329 KJ862382 N/A N/A
BRIP 57588 Juliflorae A. aulacocarpa KJ862330 KJ862383 N/A N/A
BRIP 57589 Juliflorae A. aulacocarpa KJ862331 KJ862384 N/A N/A
BRIP 57590 Juliflorae A. aulacocarpa KJ862332 KJ862385 N/A N/A
E. podalyriifolium BRIP 57294 Botrycephalae A. podalyriifolia KJ862333 KJ862386 N/A N/A
BRIP 57576* Botrycephalae A. podalyriifolia KJ862334 KJ862387 KJ862414 KJ862449
E. tierneyi BRIP 27071* Plurinerves A. harpophylla KJ862335 N/A KJ862415 KJ862450
BRIP 27880 Plurinerves A. harpophylla N/A KJ862388 N/A N/A
BRIP 27887 Plurinerves A. harpophylla N/A KJ862389 N/A N/A
E. tropicum BRIP 56555 Juliflorae A. tropica KJ862336 KJ862390 KJ862416 KJ862451
BRIP 56557* Juliflorae A. tropica KJ862337 KJ862391 KJ862417 KJ862452
E. violae-faustiae BRIP 55601 Juliflorae A. aulacocarpa KJ862338 KJ862392 KJ862418 KJ862453
BRIP 55629 Juliflorae A. aulacocarpa KJ862339 KJ862393 KJ862419 KJ862454
BRIP 55660 Juliflorae A. aulacocarpa KJ862340 N/A KJ862420 KJ862455
BRIP 56544 Juliflorae A. difficillis KJ862341 KJ862395 KJ862421 N/A
BRIP 55616 Juliflorae A. difficillis N/A KJ862396 KJ862422 KJ862456
BRIP 55611 Juliflorae A. difficillis N/A KJ862397 KJ862423 N/A
BRIP 56539 Juliflorae A. difficillis KJ862342 KJ862398 KJ862424 KJ862457
BRIP 56540 Juliflorae A. difficillis KJ862343 KJ862399 KJ862425 N/A
BRIP 56545 Juliflorae A. difficillis KJ862344 KJ862400 KJ862426 N/A
BRIP 56547 Juliflorae A. difficillis KJ862345 KJ862401 KJ862427 KJ862458
Kernkampella breyniae BRIP 56909 NA Breynia cernua (Euphorbiaceae) KJ862346 N/A KJ862428 KJ862459
Ravenelia neocaledoniensis BRIP 56907 NA Vachellia farnesiana KJ862347 N/A N/A N/A
BRIP 56908 NA V. farnesiana KJ862348 N/A N/A KJ862460
Ravenelia sp. BRIP 56904 NA Cassia sp. KJ862349 N/A N/A KJ862461
Sphaerophragmium sp. BRIP 56910 NA Albizia sp. KJ862350 N/A KJ862429 KJ862462
Uromycladium simplex BRIP 57571 Botrycephalae A. pycnantha KJ6329903 N/A N/A N/A
* Holotype
1 Botrycephalae = Botrycephalae subcade (Murphy et al. 2010); Juliflorae = Juliflorae p.p. clade (Miller et al. 2013); Plurinerves = Plurinerves p.p. clade (Miller et al. 2013).
2 Scholler & Aime (2006).
3 Doungsa-ard et al. (2014).
(9@42'G Specimens of Endoraecium included in this study.

52 Persoonia – Volume 35, 2015
whether the current taxonomy of Australian species was sup-
ported by molecular data and if further diversity existed within
Endoraecium.
H$("!)$*#'$+-'H"(&,-#
Taxon selection
Fresh specimens were collected from New South Wales, the
Northern Territory, Queensland, Victoria and Western Australia,
representing a broad diversity of Acacia (Table 1). Species
from representative genera of Raveneliaceae, namely Dior-
chidium, Kernkampella, Ravenelia and Sphaerophragmium,
were selected as outgroup taxa for the phylogenetic analyses.
Uromycladium simplex (Pileolariaceae) was included as an
outgroup to the Raveneliaceae, as it represented another Aus-
tralian endemic rust on Acacia.
Morphology
Spores were scraped from leaf material, mounted in lactic acid
and gently heated to boiling. Preparations were examined
with a Leica DMLB microscope and images were taken with
a Leica DFC500 camera. Measurements were made digitally
from photographed spores. All previous taxonomic studies of
Endoraecium have adopted an ontogenic approach to spore
classification (Hodges & Gardner 1984, Walker 2001, Scholler
& Aime 2006, Berndt 2011). Aeciospores, urediniospores and
I7JK'G Phylogram obtained in a maximum likelihood search in RAxML of the SSU, ITS, LSU and CO3 gene regions. Bootstrap support (≥ 70 %) values from
1 000 replicates above nodes. Posterior probabilities (≥ 0.95) from 4 200 trees in a Bayesian search are shown below nodes. Synapomorphic characters,
namely host subclade and morphology of urediniospores, are mapped on to the topology.
JF263493
Diorchidium polyalthiae
BRIP-56910
Sphaerophragmium
sp.
BRIP-56909
Kernkampella breyniae
BRIP-56904
Ravenelia
sp.
BRIP-56907
Ravenelia neocaledoniensis
BRIP-56908
Ravenelia neocaledoniensis
KJ6329903
Uromycladium simplex
BRIP-27880
E. tierneyi
BRIP-27071
E. tierneyi
BRIP-27887
Endoraecium tierneyi
DQ323916
E. acaciae
DQ323918
E. koae
DQ323920
E. hawaiiense
BRIP-58054
E. irroratum
BRIP-57279
E. irroratum
BRIP-57286
E. irroratum
BRIP-55671
E. irroratum
BRIP-57643
E. falciforme
BRIP-57583
E. falciforme
BRIP-57872
E. maslinii
/
Acacia daphnipholia
BRIP-57926
E. carnegiei
BRIP-57924
E. carnegiei
BRIP-59218
E. carnegiei
BRIP-57294
E. podalyriifolium
BRIP-57576
E. podalyriifolium
BRIP-57527
E. parvum
BRIP-57512
E. parvum
BRIP-53616
E. parvum
BRIP-57568
E. parvum
BRIP-57534
E. parvum
BRIP-57631
E. parvum
BRIP-57514
E. parvum
BRIP-57524
E. parvum
BRIP-56557
E. tropicum
BRIP-56555
E. tropicum
BRIP-58324
E. peggii
BRIP-55631
E. peggii
BRIP-55602
E. peggii
BRIP-55660
E. violae-faustiae
BRIP-56547
E. violae-faustiae
BRIP-56540
E. violae-faustiae
BRIP-56545
E. violae-faustiae
BRIP-56539
E. violae-faustiae
BRIP-56544
E. violae-faustiae
BRIP-55616
E. violae-faustiae
BRIP-55611
E. violae-faustiae
BRIP-55629
E. violae-faustiae
BRIP-55601
E. violae-faustiae
BRIP-55659
E. disparrimum
BRIP-55632
E. disparrimum
BRIP-55626
E. disparrimum
BRIP-57578
E. phyllodiorum
BRIP-57570
E. phyllodiorum
BRIP-57310
E. phyllodiorum
BRIP-57580
E. phyllodiorum
BRIP-57588
E. phyllodiorum
BRIP-57516
E. phyllodiorum
BRIP-57569
E. phyllodiorum
BRIP-57589
E. phyllodiorum
BRIP-57590
E. phyllodiorum
BRIP-57579
E. phyllodiorum
BRIP-56550
E. auriculiforme
BRIP-55609
E. auriculiforme
BRIP-56549
E. auriculiforme
BRIP-56548
E. auriculiforme
100
100
100
100
100
100
100
100
100
100
100
81
94
1.0
1.0
1.0
Acacia falciformis
Acacia podalyriifolia
Acacia leiocalyx
Acacia tropica
Acacia aulacocarpa
Acacia difficilis
Acacia disparrima
Acacia aulacocarpa
Acacia auriculiformis
Acacia holosericea
Acacia harpophylla
Acacia koa
Acacia dealbata
Acacia irrorata
Sub-clade of Acacia s. str.
according to Miller et al. (2013)
Juliflorae
Plurinerves
Botrycephalae
Morphology of urediniospore
Golden brown, reticulate to
foveolate
Subhyaline to yellow,
reticulate
85
77
70
100
87
97
98
100
100
99
100
82
100
83
100
83
100
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0

53
A.R. McTaggart et al.: Co-evolutionary relationship between Endoraecium and Acacia
in some cases teliospores, are often indistinguishable with this
approach. For this reason, we used a morphological approach
to classify spores (Laundon 1967), which recognises uredinio-
spores of Endoraecium as spores with reticulate ornamentation,
pedicels and germ pores.
DNA extractionL'PCR and sequencing
DNA was extracted from fresh or archived material. Spores
were obtained from leaf material according to the protocol in
McTaggart et al. (2014), and then extracted with the UltraClean
Microbial DNA Isolation Kit (MoBio Laboratories Inc., Solana
Beach, CA, USA).
The ITS region was amplified with ITS1F /ITS4B (Gardes &
Bruns 1993). The ITS2-LSU region was amplified with Rust2inv
(Aime 2006) / LR7 (Vilgalys & Hester 1990) and nested with
LROR/LR6 (Vilgalys & Hester 1990). The SSU region was am-
plified with NS1 (White et al. 1990) / Rust 18S-R (Aime 2006)
according to the protocol by Aime (2006). CO3 was amplified
with the primers CO3_F1/CO3_R1 (Vialle et al. 2009). All PCRs
were performed with high fidelity Phusion enzyme (New England
Biolabs Inc.) according to the manufacturer’s instructions. The
PCRs were performed with the following annealing tempera-
tures: SSU, ITS and nested LSU at 62 °C, the initial LSU at
60 °C, and CO3 at 55 °C. PCR products were sent to Macro-
gen Korea for direct sequencing. Sequences were uploaded
to GenBank under the accession numbers listed in Table 1.
Phylogenetic analyses
The SSU (19), ITS (47), LSU (51) and CO3 (29) sequences were
aligned separately in MAFFT (Katoh et al. 2009) (available: http://
www.ebi.ac.uk/Tools/ msa/ mafft/ ). Non-homologous regions in
the ITS alignment were removed using GBlocks (Castresana
2000). The sequences from each locus were concatenated in
a supermatrix and run as partitioned datasets with maximum
likelihood and Bayesian inference as phylogenetic criteria. CO3
was translated and included as amino acid coding sequence.
JTT was selected as a protein coding model of evolution in
MEGA5 (Tamura et al. 2011). Maximum likelihood was imple-
mented as a search criterion in RAxML (Stamatakis 2014).
GTRGAMMA was specified as the model of evolution for nucleo-
tide sequence data. The RAxML analyses were run with a rapid
Bootstrap analysis (command -f a) using a random starting tree
and 1 000 maximum likelihood bootstrap replicates. A Markov
Chain Monte Carlo (MCMC) search in a Bayesian analysis was
conducted with MrBayes (Ronquist & Huelsenbeck 2003). Four
runs, each consisting of four chains, were implemented for
5 million generations. The cold chain was heated at a tempera-
ture of 0.25. Substitution model parameters were sampled every
500 generations and trees were saved every 1 000 generations.
Convergence of the Bayesian analysis was confirmed using
AWTY (Nylander et al. 2008) (available at: ceb.csit.fsu.edu /
awty/) and a burn-in of 18 000 generations was calculated.
The ML and Bayesian analyses were run three times to test
accuracy. Alignments and trees were uploaded to TreeBASE
(http:// purl.org/phylo /treebase /phylows/study/TB2:S15410).
!"#.*(#
The topologies recovered by Bayesian inference and maximum
likelihood were identical (Fig. 1). No differences were recovered
in the tree topologies between nucleotide and amino acid coding
sequences of CO3. Endoraecium was recovered as a mono-
phyletic group sister to other members of the Raveneliaceae.
Three major clades of Endoraecium corresponded to three
clades in Acacia, namely Plurinerves, Juliflorae and Botryce pha-
lae. The clade of Endoraecium that diversified on Plurinerves
contained the Hawaiian species of Endoraecium and the Aus-
tralian species, E. tierneyi. Rust taxa formed well-supported
clades corresponding to host species. This is contrary to the
current broad host ranges proposed for E. digitatum, E. parvum,
E. phylliodorum and E. violae-faustiae (Berndt 2011).
Morphology of the urediniospores was a synapomorphic charac-
ter for the two large clades on Juliflorae and Botrycephalae (Fig. 1).
Urediniospores of species on Juliflorae were golden brown
with reticulate to foveolate ornamentation. Urediniospores of
those on Botrycephalae were subhyaline to pale yellow with
reticulate ornamentation.
($M,+,HN
Endoraecium auriculiforme McTaggart & R.G. Shivas, sp. nov.
― MycoBank MB808980; Fig. 2
Etymology. Name refers to the host, Acacia auriculiformis, on which it
was found.
Type. AustrAliA, Northern Territory, Darwin, Howard Springs (-12.4564,
131.0522), on A. auriculiformis, 15 Apr. 2012, C. Doungsa-ard, A.R. McTag-
gart, R. Berndt, V. Faust-Berndt, M.D.E. & R.G. Shivas (holotype BRIP
56548).
Uredinia on both phyllode surfaces, subepidermal, erumpent,
on bullate swellings up to 1 cm long, or pulverulent on phyl-
lode surface, linear to round, yellowish brown; paraphyses
intrasoral, cylindrical, apex 6– 9-digitate, subhyaline to yellow,
35–70 × 10–14 µm, thickened at apex, pedicel up to 40 µm.
Urediniospores obovoid, oval to fusiform, apex acute, yellow-
ish brown, 31–46 × 16– 20 µm; wall 3–5 µm thick at sides and
I7JK'O Endoraecium auriculiforme. a. Bullate sori on leaf (BRIP 56550); b, c. urediniospores (BRIP 55609); d. teliospores (BRIP 56550); e. germinating telio-
spore (BRIP 56549). — Scale bars: a = 1 cm; b– e = 10 µm.

54 Persoonia – Volume 35, 2015
5–9 µm thick at apex, foveolate, with 3 – 4 equatorial germ
pores; pedicel 3– 5 µm, or absent. Telia formed from uredinia,
erumpent, reddish brown. Teliospores cylindrical to fusiform,
apex rounded, 2 – 4-digitate, hyaline to subhyaline, 36–54
× 13–25 µm; wall 1.5 – 2.5 µm thick at sides, 6 – 8 µm thick
at apex; pedicel persistent, up to 38 µm. Basidia cylindrical,
3-septate, up to 35–40 × 8–12 µm. Basidiospores globose,
hyaline, 4–6 µm, smooth-walled.
On phyllodes of Acacia auriculiformis (Juliflorae).
Additional specimens examined. AustrAliA, Northern Territory, Howard
Springs, on A. auriculiformis, 9 May 2012, C. Doungsa-ard, A.R. McTaggart,
R. Berndt, V. F aus t- Ber ndt , M.D.E. & R .G. Shi va s, BRIP 55609; 15 Apr. 2012,
C. Doungsa-ard, A.R. McTaggart, R. Berndt, R.G. Shivas, BRIP 56550;
Northern Territory, Darwin, Bronzewing Ave, Howard Springs, 15 Apr. 2012,
C. Doungsa-ard, A.R. McTaggart, R. Berndt & R.G. Shivas, BRIP 56549.
Notes ― Endoraecium auriculiforme has foveolate uredinio-
spores with an acute and thickened apex, and digitate para-
physes that resemble narrow teliospores. Endoraecium violae-
faustiae and E. peggii also produce similar paraphyses. These
three species all occur on hosts in the Juliflorae, with E. auriculi-
forme restricted to A. auriculiformis; E. v iol ae-f aus tia e to A. aula-
cocarpa and A. crassicarpa, and E. peggii to A. holosericea.
In the phylogenetic analyses, E. auriculiforme was recovered
as sister to E. peggii (Fig. 1).
Endoraecium bicinctum (McAlpine) M. Scholler & Aime, Myco-
science 47: 163. 2006
Basionym. Uromyces bicinctus McAlpine, Rusts of Australia: 93. 1906.
≡ Pileolaria bicincta (McAlpine) Dietel, Ann. Mycol. 19: 302. 1921.
≡ Atelocauda bicincta (McAlpine) Cummins & Y. Hirats., Illustr. Gen. Rust
Fungi, rev. edn (St. Paul): 147. 1983.
≡ Racospermyces bicinctus (McAlpine) J. Walker, Australas. Mycol. 20:
16. 2001.
Type. AustrAliA, Queensland, Rockhampton, on A. fasciculifera, 30 Nov.
1866, G.H. Robinson (holotype VPRI 5751).
Notes ― Endoraecium bicinctum is known from four collec-
tions, which were examined by Walker (2001). It is only known
to occur on A. fasciculifera in Botrycephalae (Murphy et al.
2010, Maslin 2013).
Endoraecium carnegiei McTaggart & R.G. Shivas, sp. nov.
― MycoBank MB808981; Fig. 3
Etymology. Named after the Australian forest pathologist and fungal
taxonomist, Dr Angus J. Carnegie, who generously assisted this study by
collecting many specimens of rust on Acacia, including the type specimen
on which this taxon is based.
Type.
AustrAliA, New South Wales, Ando, Glen Allen State Forest, Poddy
Hut Road (-36.7150, 149.3486), on A. dealbata, 6 Oct. 2012, A.J. Carnegie
(holotype BRIP 57924).
Uredinia forming galls on stems, irregular, up to 3 cm, yellow-
ish brown. Urediniospores ellipsoidal to ovoid, subhyaline to
yellow, 34– 40 × 21– 25 µm; wall 4.0 –4.5 µm thick, uniform or
slightly thicker at sides, with 6– 8 equatorial germ pores. Telia
on leaves, pulverulent, erumpent, elliptical, less than 1 mm, yel-
lowish brown. Te l i ospor e s cylindrical to fusiform, apex rounded,
1–5-digitate, hyaline to subhyaline, 41–76 × 10–17 µm; wall
1.0–1.5 µm thick at sides, 6–19(– 32) µm thick at apex; pedicel
persistent, up to 51 µm.
On stems and leaves of A. dealbata (Botrycephalae).
Additional specimens examined. AustrAliA, New South Wales, Mila, Bondi
State Forest (-37.0847, 149.1078), on A. dealbata, 4 Oct. 2012, A.J. Carnegie,
BRIP 57926; Victoria, Kergunyah, Murramurrangbong Range, Simpson Road
(-36.3142, 146.9819), on A. dealbata, 13 May 2013, C. Doungsa-ard, W. Khem -
muk & A.D.W. Geering, BRIP 59218.
Notes ― Endoraecium carnegiei is one of three species that
forms galls on the stems of its host. The other two species,
E. digitatum and E. irroratum, also infect species of Acacia in
the Botrycephalae. Endoraecium carnegiei is only known to
occur on A. dealbata in south-eastern Australia.
Endoraecium digitatum (G. Winter) M. Scholler & Aime, Myco-
science 47: 163. 2006.
Basionym. Uromyces digitatus G. Winter, Rev. Mycol. (Toulouse) 8: 209.
1886.
≡ Coeomurus digitatus (G. Winter) Kuntze (as ‘Caeomurus’), Revis. Gen.
Pl. 3: 450. 1898.
≡ Atelocauda digitata (G. Winter) Cummins & Y. Hirats., Illustr. Gen. Rust
Fungi, rev. edn (St. Paul): 147. 1983.
≡ Racospermyces digitatus (G. Winter) J. Walker, Australas. Mycol. 20:
13. 2001.
Type.
AustrAliA, South Australia, near Gawler, on A. notabilis, 1 July 1885,
J.G.O. Tepper (holotype SF35352); South Australia, west of Gawler, along
road to Mallala (-34.5665, 138.7184), on A. notabilis, 16 Oct. 2009, V. F aus t-
Berndt & R. Berndt (epitype SF35352).
Notes ― Our study shows that the known host range of
E. digitatum s.str. is restricted to A. notabilis in Botrycephalae.
Walker (2001) adopted a broad host range for E. digitatum, but
suspected it was a complex of closely related taxa, confined to
one or a small group of hosts. Berndt (2011) divided E. digitatum
into five species in Australia. He accepted E. phyllodiorum as
distinct from E. digitatum, and further described three new taxa,
E. parvum, E. violae-faustiae an d E. walkerianum. Berndt (2011)
I7JK'P Endoraecium carnegiei. a. Telia on leaves (BRIP 59218); b. gall (BRIP 57924); c. urediniospores (BRIP 57924); d, e. teliospores (BRIP 57924). —
Scale bars: b = 1 cm; c– e = 10 µm.

55
A.R. McTaggart et al.: Co-evolutionary relationship between Endoraecium and Acacia
designated an epitype for E. digitatum on A. notabilis, and listed
six species of Acacia as hosts. We found four of these hosts,
A. dealbata, A. falciformis, A. irrorata and A. podalyriifolia, were
infected by novel species of Endoraecium. The remaining two
hosts, A. deanei and A. oshanesii, most likely represent two
new hosts of Endoraecium. The urediniospores of E. digitatum
were not examined in this study, however, the description of the
epitype (Berndt 2011) is similar to other species of Endoraecium
with subhyaline to golden yellow urediniospores and reticulate
ornamentation on species of Acacia in Botrycephalae.
Endoraecium disparrimum McTaggart & R.G. Shivas, sp. nov.''
― MycoBank MB808982; Fig. 4
Etymology. Name refers to the host, Acacia disparrima, on which it was
found.
Type. AustrAliA, Queensland, Babinda (-17.3397, 145.8675), on A. dis-
parrima, 3 Apr. 2012, C. Doungsa-ard, A.R. McTaggart, R. Berndt, V. Faust-
Berndt, M.D.E. & R.G. Shivas (holotype BRIP 55626).
Uredinia on both phyllode surfaces, forming bullate swellings
up to 1 cm long, or pulverulent, linear to round, up to 1 mm
diam, yellowish brown. Urediniospores subglobose to ovoid,
apex obtuse, yellowish brown, 29 –41 × 20 – 26 µm; wall 2 – 4
µm thick at sides and 5.5– 9.0 µm thick at apex, reticulate,
I7JK'Q Endoraecium disparrimum. a. Host (BRIP 55659); b, c. urediniospores (BRIP 55659); d. teliospores (BRIP 55626). — Scale bars: a = 1 cm; b– d = 10 µm.
I7JK'R Endoraecium falciforme (BRIP 57583). a. Uredinia and telia surrounding spermogonia; b. uredinium; c. teliospores; d, e. urediniospores. — Scale
bars: b = 1 cm; c– e = 10 µm.

56 Persoonia – Volume 35, 2015
I7JK'S Endoraecium irroratum. a. Stem gall (BRIP 55671); b, c. urediniospores (BRIP 55671); d. teliospore (BRIP 57286). — Scale bars: a = 1 cm; b–d = 10 µm.
with 2– 5 equatorial germ pores; pedicel 2 µm or absent. Telia
formed from uredinia, yellowish brown. Teliospores cylindrical
to fusiform, apex acuminate to rounded, hyaline to subhyaline,
31–50 × 20–26 µm; wall 1–2 µm thick at sides, 4–14 µm thick
at apex; pedicel persistent, up to 33 µm.
On phyllodes of A. disparrima (Juliflorae).
Additional specimens examined. AustrAliA, Queensland, Herberton, Silver
Valley Drive, on A. disparrima, 10 Apr. 2012, R. Berndt & V. Faust-Berndt,
BRIP 55659; Queensland, near Yungaburra, Danbulla State Forest, at the
Chimney’s Rest Area, on A. disparrima, 9 Apr. 2012, R. Berndt & V. Faust-
Berndt, BRIP 55632.
Notes ― Endoraecium disparrimum occurs on A. disparrima
in Juliflorae. It was recovered as sister to E. violae-faustiae,
which occurs on closely related species of Acacia. It differs from
E. violae-faustiae in that the urediniospores have an obtuse
apex with reticulate rather than foveolate ornamentation, and
paraphyses are absent.
Endoraecium falciforme McTaggart & R.G. Shivas, sp. nov.'
'― MycoBank MB808983; Fig. 5
Etymology. Name refers to the host, Acacia falciformis, on which it was
found.
Type. AustrAliA, Queensland, Mt Tibrogargan (-26.9283, 152.9494), on
A. falciformis, 15 Aug. 2012, C. Doungsa-ard & A.R. McTaggart (holotype
BRIP 57583).
Spermogonia on fruit or phyllodes, amphigenous, subepider-
mal, erumpent, c. 100 µm. Uredinia on fruit or on both phyl-
lode surfaces, causing distortion, surrounding spermogonia,
subepidermal, erumpent, pulverulent, linear, round to ellip-
soidal, greater than 10 mm, reddish brown. Urediniospores
ellipsoidal to ovoid, subhyaline to yellow, 34– 43 × 21– 25 µm;
wall unevenly thickened at equator, 3.0– 6.5 µm and 3 – 5 µm
thick at apex, reticulate, with 4– 9 equatorial germ pores; pedi-
cel 2 µm. Telia on both phyllode surfaces, formed separately
from uredinia, erumpent, c. 1 mm, orange to yellowish brown.
Teliospores cylindrical to clavate, apex rounded, 2– 5-digitate,
subhyaline, 47– 63 × (13–)15– 23 µm; wall 1.5 – 2.0 µm thick
at sides, 12–24 µm thick at apex; pedicel persistent, up to 64
µm long × 6–8 µm thick.
On phyllodes and fruit of A. falciformis (Botrycephalae).
Additional specimen examined. AustrAliA, Queensland, Mt Tibrogar gan,
4 Sept. 2012, K.M. Thomson, BRIP 57643.
Notes ― Endoraecium falciforme is morphologically similar
to E. walkerianum, which both occur on species of Acacia spe-
cies in Botrycephalae. Endo raeciu m fa lcif orm e has distinctively
thicker walls at the equator of the urediniospores (3.0–6.5 µm)
than E. walkerianum (3.0–4.5 µm). Endoraecium falciforme is
recorded from south-east Queensland, whereas E. walkerianum
is known from southern Australia. Urediniospores from a para-
type specimen of E. walkerianum (BRIP 14205) were found to
have thickened apices, whereas those of E. falciforme were
thickened at the equator, or the wall was of uniform thickness.
Endoraecium irroratum McTaggart & R.G. Shivas, sp. nov.'
'― MycoBank MB808984; Fig. 6
Etymology. Name refers to the host, Acacia irrorata, on which it was
found.
Type. AustrAliA, Queensland, Main Range National Park, on A. irrorata,
11 June 2012, A.D.W. Geering (holotype BRIP 57286).
Uredinia forming galls on stems, up to 2 cm long, yellowish
brown. Urediniospores ovoid, apex obtuse, subhyaline, yellow
to yellowish brown, 32– 42 × 17–24 µm; wall 2.0– 3.5 µm thick
at sides, apex sometimes thickened (up to 4 µm), reticulate,
with 4 –10 equatorial germ pores. Telia formed from uredinia,
yellowish brown. Teliospores cylindrical to subfusiform, apex
acuminate to rounded, 2–7-digitate, subhyaline to yellow, 47–73
× 15– 22 µm; wall 1.0–1.5 µm thick at sides, 11–21 µm thick at
apex; pedicel persistent, up to 46 µm.
On stems and phyllodes of A. irrorata (Botrycephalae).
Additional specimens examined. AustrAliA, New South Wales, Warrum-
bungle National Park, on A. irrorata, 20 Mar. 2012, R. Berndt & V. Faust-
Berndt, BRIP 55671; Queensland, Mt Mee, Mt Mee State Forest, on A. irro-
rata, 3 June 2012, C. Doungsa-ard & R.G. Shivas, BRIP 57279; Queensland,
Mt Glorious, Wivenhoe Dam lookout area (-27.3077, 152.7136), A. irrorata,
30 Nov. 2012, A.D.W. Geering, BRIP 58054.
Notes ― Endoraecium irroratum occurs on A. irrorata in
Botrycephalae. Berndt (2011) considered that the rust on A. irro-
rata was E. digitatum based on morphology. There are no clear
morphological differences that separate E. irroratum from the
epitype of E. digitatum (Berndt 2011). However, the results from
the molecular phylogenetic analysis in this study indicate the
rusts on Botrycephalae are each restricted to a single host
species.
Endoraecium maslinii McTaggart & R.G. Shivas, sp. nov.'―
MycoBank MB808985; Fig. 7
Etymology. Named after the Australian botanist Bruce R. Maslin, an expert
on Acacia taxonomy, who has published approximately 250 Acacia taxa and
kindly identified many specimens in this study.
Type.
AustrAliA, Western Australia, Midlands Rd, 10 km SE of Mingenew
(-29.2847, 115.5319), on A. daphnifolia, 28 Sept. 2012, C. Doungsa-ard &
A.R. McTaggart (holotype BRIP 57872).

57
A.R. McTaggart et al.: Co-evolutionary relationship between Endoraecium and Acacia
Uredinia forming bullate swellings on fruit and both phyllode
surfaces, round, up to 1 cm, yellowish brown. Urediniospores
ellipsoidal, ovoid to fusiform, apex obtuse, subhyaline to yel-
lowish brown, 37– 46 × 20 –26 µm; wall 2.5 – 5.0 µm thick at
side, apex slightly thickened, 3.5–6.0 µm, reticulate, with 6– 8
equatorial germ pores; pedicel absent or up to 2.5 µm.
On phyllodes of A. daphnifolia (Botrycephalae).
Notes ― Endoraecium maslinii occurs on A. daphnifolia in
Botrycephalae and is the only species of Endoraecium known
from Western Australia. Only urediniospores have been found,
which are yellowish brown and reticulate, and morphologically
similar to other species on Acacia in Botrycephalae.
Endoraecium parvum Berndt, Mycol. Progr. 10: 510. 2011
Type. AustrAliA, Queensland, Caloundra, on A. leiocalyx, 25 Aug. 1932,
S.T. Blake (holotype BRIP 7543!).
Uredinia on both phyllode surfaces, subepidermal, erumpent,
pulverulent, linear to round, yellowish brown. Urediniospores
globose, subglobose to obovoid, apex obtuse, yellowish brown
to reddish brown, 25–38 × 16 – 22 µm; wall 3 – 4 µm thick at
equator, hardly thickened at apex, reticulate, with 2–4 equato-
rial germ pores, pedicel 1.5– 3.0 µm. Telia formed from uredinia,
erumpent, linear to dome-shaped, reddish brown. Teliospores
oval, apex rounded, 1– 3-digitate, hyaline to subhyaline, 31–60
× 13–27 µm; wall 1–2 µm thick, mostly thickened at apex (5–14
µm); pedicel persistent, up to 66 µm.
Additional specimens examined. AustrAliA, Queensland, Caloundra, on
A. leiocalyx, 25 Aug. 1932, S.T. Blake, BRIP 7543; Queensland, Mt Coolum
(-26.5656, 153.0969), on A. leiocalyx, 28 July 2012, C. Doungsa-ard & A.R.
McTaggart, BRIP 57512; Queensland, Mt Coolum (-26.5622, 153.0942), on
A. leiocalyx, 28 July 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57514;
Queensland, Cunningham Highway (-28.0317, 152.4697), on A. leiocalyx,
1 Aug. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering & R.G. Shivas,
BRIP 57524; Queensland, Lake Moogerah Road (-28.0247, 152.5189), on
A. leiocalyx, 1 Aug. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering
& R.G. Shivas, BRIP 57527; Queensland, West Haldon (-27.7722, 152.0903),
on A. leiocalyx, 1 Aug. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geer-
ing & R.G. Shivas, BRIP 57534; Queensland, Brisbane, Geebung (-27.3375,
153.0511), on A. leiocalyx, 2 Sept. 2012, R.G. & M.D.E. Shivas, BRIP 57631;
New South Wales, Shark Creek (-29.5664, 153.2003), on A. leiocalyx, 13
Aug. 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57568.
Notes ― Endoraceium parvum is distinguished from other
species by the comparatively short (25–38 µm) urediniospores
(Berndt 2011). Berndt (2011) described E. parvum from A. leio-
calyx (as A. concurrens) and A. mangium. Specimens of rust
on A. mangium were not included in this study and these war-
rant further study.
Endoraecium peggii McTaggart & R.G. Shivas, sp. nov.'―
MycoBank MB808986; Fig. 8
Etymology. Named after the Australian forest pathologist and rust special-
ist, Dr Geoff S. Pegg, who has discovered several new plant pathogens in
Australia.
Type. AustrAliA, Northern Territory, Darwin, 8 km from airport, on A. holo-
sericea, 7 May 2012, R.G. Shivas (holotype BRIP 55602).
Uredinia on both phyllode surfaces, pulverulent, subepider-
mal, erumpent, linear to round, up to 2 mm, yellowish brown;
paraphyses intrasoral, cylindrical, yellow, with pedicel, 37– 84
× 9–10 µm, thickened at apex, digitate. Urediniospores ovoid,
apex obtuse, yellowish brown to reddish brown, 31– 45 ×
20–25 µm; wall 3 – 5 µm thick at sides, apex 4 –10 µm thick,
foveolate to reticulate, with 2–3 equatorial germ pores; pedicel
3–6 µm. Telia rare, on both surfaces of phyllode, darker than
uredinia, erumpent, linear, brown to black. Teliospores oval,
apex rounded, no digitations, hyaline to subhyaline, 45–60 ×
(15–)19–27 µm; wall 1.5 – 2.0 µm thick at sides, sometimes
thickened at apex, 7–17 µm; pedicel persistent, up to 52 µm.
On phyllodes of A. holosericea (Juliflorae).
Additional specimens examined. AustrAliA, Queensland, Dimbulah,
Bourke Developmental Road, on A. holosericea, 6 Apr. 2012, C. Doungsa-
ard, A.R. McTaggart, R. Berndt, V. Fa us t-B ern dt , M.D.E. & R.G. Shivas, BRIP
55631; Queensland, Brisbane, Mt Coot-tha Botanic Gardens (-27.477655,
152.972270), on A. holosericea, Nov. 2012, C. Doungsa-ard & A.R. Mc-
Taggart, BRIP 58324.
Notes ― Endoraecium peggii is known from A. holosericea
in Juliflorae. This species of Acacia is native to northern Aus-
tralia (Maslin 2013). The rust was also collected in south-east
Queensland on a plant in the Mt Coot-tha Botanic Gardens.
The teliospores of E. peggii lack the apical digitations found in
all other species of Endoraecium, although this ornamentation
is present on the paraphyses.
Endoraecium phyllodiorum (Berk. & Broome) Berndt, Mycol.
Progr. 10: 503. 2011
Basionym. Melampsora phyllodiorum Berk. & Broome, Trans. Linn. Soc.
London 2, ser. 2: 67. 1883.
≡ Uromyces phyllodiorum (Berk. & Broome) McAlpine, The Rusts of
Australia: 95. 1906. (McAlpine (1906) described teliospores from the type
specimen, which were overlooked by Berkeley & Broome (1883). Under
previous rules of nomenclature, U. phyllodiorum was considered the name
of a new species with a teleomorphic type (Berndt 2011). Under the current
system of nomenclature, the name is cited as originally published, and is
typified by the type of the basionym.)
≡ Pileolaria phyllodiorum (Berk. & Broome) Dietel, Ann. Mycol. 19: 302.
1921.
I7JK'T Endoraecium maslinii (BRIP 57872). a– c. Bullate swellings on leaves; d, e. urediniospores. — Scale bars: c = 1 cm; d, e = 10 µm.

58 Persoonia – Volume 35, 2015
= Uromyces phyllodii Cooke & Massee (as ‘phyllodiae’), in Cooke, Grevil-
lea 17: 70. 1889.
≡ Coeomurus phyllodii (Cooke & Massee) Kuntze (as ‘Caeomurus’),
Revis. Gen. Pl. 3: 450. 1898.
Type. AustrAliA, Queensland, Brisbane, on Acacia sp., F.M. Bailey no.
269, K(M) 146703.
Uredinia on both phyllode surfaces, subepidermal, erumpent,
pulverulent or on bullate swellings, linear, round to irregular, yel-
lowish brown. Urediniospores subglobose to oval, apex obtuse,
yellowish brown, (28 –)30–52 × 17–26 µm; wall 2.5 – 4.0 µm
thick at sides, 5–10 µm thick at apex, reticulate, with 3 –7 equa-
torial germ pores; pedicel absent or 1.5–3.5 µm. Telia form-
ed from uredinia, erumpent, linear, reddish brown. Telio spores
cylindrical to oval, apex rounded, 1–4-digitate, hyaline to sub-
hyaline, 38– 58 × 17– 28 µm; wall 1–2 µm thick at sides, 6–17
µm thick at apex; pedicel persistent, up to 30 µm.
Additional specimens examined. AustrAliA, Queensland, Mount Coolum
(-26.5611, 153.0839), on A. aulacocarpa, 28 July 2012, C. Doungsa-ard & A.R.
McTaggart, BRIP 57310; Queensland, Mt Coolum (-26.5611, 153.0839), on
A. aulacocarpa, 28 July 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57516;
New South Wales, Woombah, at the beginning of Iluka Road (-29.3544,
153.2492), on A. aulacocarpa, 11 Aug. 2012, C. Doungsa-ard & A.R. McTag-
gart, BRIP 57578; New South Wales, Woombah, at the beginning of Iluka
Road (-29.3544, 153.2492), on A. aulacocarpa, 11 Aug. 2012, C. Doungsa-
ard & A.R. McTaggart, BRIP 57580; New South Wales, Woombah, Iluka Bluff
(-29.3967, 153.3722), on A. aulacocarpa, 11 Aug. 2012, C. Doungsa-ard &
A.R. McTaggart, BRIP 57579; New South Wales, Shark Creek (-29.5664,
153.2003), on A. aulacocarpa, 13 Aug. 2012, C. Doungsa-ard & A.R. McTag-
gart, BRIP 57569; New South Wales, Shark Creek (-29.5664, 153.2003),
on A. aulacocarpa, 13 Aug. 2012, C. Doungsa-ard & A.R. McTaggart, BRIP
57570; Queensland, Mt Tibrogargan (-26.9264, 152.9417), on A. aulaco carpa,
15 Aug. 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57588; Queens-
land, Mt Tibrogargan (-26.9258, 152.9508), on A. aulaco carpa, 15 Aug. 2012,
C. Doungsa-ard & A.R. McTaggart, BRIP 57589; Queensland, Mt Tibrogargan
(-26.9278, 152.9378), on A. aulacocarpa, 15 Aug. 2012, C. Doungsa-ard &
A.R. McTaggart, BRIP 57590.
Notes ― Berndt (2011) discussed the taxonomy of E. phyl-
lodiorum, and listed the hosts as A. aulacocarpa, A. crassicarpa,
A. holosericea, A. mangium and tentatively A. auriculiformis.
The type specimens of Melampsora phyllodiorum and Uromy-
ces phyllodii were collected on unidentified species of Acacia
in Brisbane, Australia. Acacia aulacocarpa is the only host
species listed by Berndt (2011) that occurs naturally in or near
to Brisbane. The other four species of Acacia are restricted to
northern Queensland and the Northern Territory (Maslin 2013).
Herbarium records and field observations by the authors show
that Endoraecium spp. occur on four species, A. aulacocarpa,
A. irrorata, A. leiocalyx and A. podalyriifolia, in the Brisbane
region. The rust on A. aulacocarpa forms bullate swellings on
phyllodes, very similar to those seen in the type specimen of
E. phyllodiorum and illustrated by Berndt (2011). Consequently,
we suggest that A. aulacocarpa is the host of the type of
E. phyllodiorum. Berndt (2011) proposed that E. phyllodiorum
had a wide host range, including A. aulacocarpa, A. auriculi-
formis, A. holosericea and A. mangium. The rusts on A. auri-
culiformis and A. holosericea are now identified as E. auriculi-
forme and E. peggii, respectively. The rust on A. mangium is
unknown. Acacia aulacocarpa is the only species of Acacia
known to host two species of Endoraecium, E. phyllodiorum
and E. violae-faustiae.
I7JK'U Endoraecium peggii. a. Uredinia (BRIP 55631); b. teliospores (BRIP 55602); c, d. urediniospores (BRIP 55631). — Scale bars: a = 1 cm; b– d = 10 µm.

59
A.R. McTaggart et al.: Co-evolutionary relationship between Endoraecium and Acacia
Endoraecium podalyriifolium McTaggart & R.G. Shivas, sp.
nov.'― MycoBank MB808987; Fig. 9
Etymology. Name refers to the host, Acacia podalyriifolia, on which it was
found.
Type. AustrAliA, New South Wales, Maclean, Wharf Street (-29.4589,
153.2111), on A. podalyriifolia, 12 Aug. 2012, C. Doungsa-ard & A.R. McTag-
gart (holotype BRIP 57576).
Uredinia on both phyllode surfaces, subepidermal, erumpent,
pulverulent, round, 0.5 –10.0 mm, yellow to yellowish brown.
Urediniospores cylindrical to ovoid, apex obtuse, subhyaline to
yellow, (30–) 33 – 44 × 23 – 27 µm; wall 3–4 µm thick, reticulate,
with 4 – 6 germ pores. Telia formed from uredinia, subepider-
mal, erumpent, yellow. Te l i ospor e s cylindrical to fusiform, apex
rounded, 2 – 5-digitate, subhyaline to yellow, 44 – 60 × 12 –19
µm; wall 1 µm thick at sides, 6 –12 µm thick at apex; pedicel
persistent, over 60 µm.
On phyllodes of A. podalyriifolia (Botrycephalae).
Additional specimen examined. AustrAliA, Queensland, South Ripley,
Ripley Road, on A. podalyriifolia, 17 July 2012, A.D.W. Geering, BRIP 57294.
Notes ― Berndt (2011) considered the rust on A. podaly-
riifolia was E. digitatum based on morphology and the close
relationships of host species within this group. However, the
results from the molecular phylogenetic analysis in this study
indicate the rusts on Botrycephalae are each restricted to a
single host species.
Endoraecium tierneyi (J. Walker & R.G. Shivas) M. Scholler
& Aime, Mycoscience 47: 163. 2006
Basionym. Racospermyces tierneyi J. Walker & R.G. Shivas, in Walker,
Australas. Mycol. 20: 23. 2001.
Type.
AustrAliA, Queensland, Tambo, near Castlevale, on A. harpophylla,
6 June 2000, G.S. Pegg (holotype BRIP 27071!).
Uredinia on both phyllode surfaces, subepidermal, erumpent,
linear, up to 500 µm, yellowish brown. Urediniospores cylindri-
cal, oval to broadly fusiform, apex obtuse, reddish brown, 26 –36
× 13–18 µm; wall 2.0 – 2.5 µm thick at sides, 4.0– 4.5 µm thick at
apex, reticulate, with 4– 8 equatorial germ pores. Telia on both
phyllode surfaces, erumpent. Teliospores subglobose, ovoid
to obovoid, apex rounded, reddish brown, darker at the apex,
27–41 × 20–26 µm; wall 1.0 µm thick at sides, 7–13 µm thick
at apex, smooth; pedicel persistent, 50–55 µm long.
Additional specimens examined. AustrAliA, Queensland, Springsure,
on A. harpophylla, 27 Feb. 2001, G.S. Pegg, BRIP 27887; Queensland,
Caldervale, on A. harpophylla, 1 Mar. 2001, G.S. Pegg, BRIP 27880.
Notes ― Endoraecium tierneyi occurs on A. harpophylla in
Plurinerves. It was recovered in the phylogenetic analyses as
sister to three species of Endoraecium in Hawaii that occur on
A. koa, also in Plurinerves. The teliospores are subglobose to
obovoid, while other species of Endoraecium in Australia have
clavate teliospores.
I7JK'V Endoraecium podalyriifolium (BRIP 57576). a, b. Pulverulent sori on leaves and stems; c. teliospores; d, e. urediniospores. — Scale bars: b = 1 cm;
c– e = 10 µm.

60 Persoonia – Volume 35, 2015
Endoraecium tropicum McTaggart & R.G. Shivas, sp. nov.'―
MycoBank MB808988; Fig. 10
Etymology. Name refers to the host, Acacia tropica, on which it was found.
Type.
AustrAliA, Northern Territory, Gregory, Victoria Highway (-15.6003,
131.2136), on A. tropica, 20 Apr. 2012, C. Doungsa-ard, A.R. McTaggart,
R. Berndt, V. Faust-Berndt, M.D.E. & R.G. Shivas (holotype BRIP 56557).
Uredinia on both phyllode surfaces, subepidermal, pulverulent,
up to 2 mm, brown. Urediniospores ovoid to fusiform, apex ob-
tuse, yellowish brown, 30–40 × 17–22 µm; wall 3–4 µm thick at
sides, apex usually 3–4 µm thick, sometimes slightly thickened
(4–5 µm), reticulate, with 3– 4, equatorial germ pores; pedicel
3–4 µm. Telia formed from uredinia, erumpent. Teliospores
clavate, apex rounded, papillate rather than digitate, 40–53 ×
16–23 µm; wall 1.5 – 2.0 µm thick at sides, 8–11 µm thick at
apex; pedicel persistent, 5 µm.
On phyllodes of A. tropica (Juliflorae).
Additional specimen examined. AustrAliA, Northern Territory, Gregory, Vic-
toria Highway (-15.6014, 131.2136), on A. tropica, 20 Apr. 2012, C. Doungsa-
ard, A.R. McTaggart, R. Berndt, V. Faust-Berndt, M.D.E. & R.G. Shivas,
BRIP 56555.
Notes ― Endoraecium tropicum was closely related to E. par-
vum in the phylogenetic analysis. Both species have ure-
diniospores with uniformly thickened spore walls. The distri-
bution of A. tropica is restricted to the Northern Territory and
north-west Queensland. Acacia leiocalyx, the host of E. parvum,
occurs in eastern Australia (Maslin 2013).
Endoraecium violae-faustiae Berndt, (as ‘violae-faustae’)
Mycol. Progr. 10: 513. 2011
Type. AustrAliA, Queensland, Cairns, Barron Gorge, MacDonald’s trail,
on A. crassicarpa (as Acacia sp.), 18 Aug. 2006, V. Fa us t-B ern dt & R. Ber ndt
(holotype BRIP 53388!).
Uredinia on both phyllode surfaces, subepidermal, erumpent,
pulverulent, linear to round, yellowish brown, not forming bul-
late sori; paraphyses cylindrical with digitate heads, subhyaline
to yellow, 35– 88 × 6–15 µm thick at sides, thickened at apex.
Urediniospores globose, subglobose, obovoid to oval, apex
acute, yellowish brown, 28–53 × 17– 26 µm; wall 2.5 – 4.5
µm thick at sides, apex mostly thickened, 5.0 –10.5 µm thick,
foveolate, with 3 – 5 equatorial germ pores; pedicel 3 – 5 µm.
Telia formed from uredinia, erumpent, reddish brown. Telio-
spores obovoid to oval, apex rounded, 1– 4-digitate, hyaline
to subhyaline, 41– 53 × 20 – 28 µm; wall 1.5 – 3.0 µm thick at
sides, 5–14 µm thick at apex; pedicel persistent, up to 43 µm.
Additional specimens examined. AustrAliA, Queensland, Coen, Peach No. 7,
on A. crassicarpa 18 July 1999, R.G. Shivas & M. Gunther, paratype BRIP
25816; Queensland, Julatten, Abbatoir Swamp (-16.6074, 145.3428), on
A. aulacocarpa, 5 Apr. 2012, C. Doungsa-ard, A.R. McTaggart, R. Berndt,
V. Faust-Berndt, M.D.E. & R.G. Shivas, BRIP 55601; Queensland, Mareeba
(-16.9414, 145.5411), on A. difficilis, 6 Apr. 2012, C. Doungsa-ard, A.R. Mc-
Taggart, R. Berndt, V. Faust-Berndt, M.D.E. & R.G. Shivas, BRIP 55611;
Queensland, Innisfail (-17.5003, 146.0756), on A. difficilis, 7 Apr. 2012,
C. Doungsa-ard, A.R. McTaggart, R. Berndt, V. Faust-Berndt, M.D.E. & R.G.
Shivas, BRIP 55616; Queensland, Dimbulah (-17.2967, 144.9736), on A. aula-
cocarpa, 6 Apr. 2012, C. Doungsa-ard, A.R. McTaggart, R. Berndt, V. Faust-
Berndt, M.D.E. & R.G. Shivas, BRIP 55629; Northern Territory, Humpty Doo
(-12.5964, 131.2083), on A. difficilis, 22 Apr. 2012, C. Doungsa-ard, A.R.
McTaggart, R. Berndt & R.G. Shivas, BRIP 56539; Northern Territory, Humpty
Doo (-12.5964, 131.2083), on A. difficilis, 22 Apr. 2012, C. Doungsa-ard, A.R.
McTaggart, R. Berndt & R.G. Shivas, BRIP 56540; Northern Territory, Humpty
Doo (-12.5964, 131.2083), on A. difficilis, 22 Apr. 2012, C. Doungsa-ard, A.R.
McTaggart, R. Berndt & R.G. Shivas, BRIP 56545; Northern Territory, Humpty
Doo (-12.5964, 131.2083), on A. difficilis, 22 Apr. 2012, C. Doungsa-ard, A.R.
McTaggart, R. Berndt & R.G. Shivas, BRIP 56547.
Notes ― Berndt (2011) described the urediniospores of
E. violae-faustiae as foveolate, with a thickened and acute apex.
The most distinctive character was the variable paraphyses,
which resembled thin teliospores, similar to those found in
E. auriculiforme and E. peggii. Endoraecium violae-faustiae
was reported on A. aulacocarpa and A. crassicarpa, also in Juli-
florae, as well as A. flavescens in Plurinerves (Berndt 2011).
The host of the holotype (BRIP 53388), was re-identified as
A. crassicarpa, which is closely related to A. aulacocarpa (Maslin
2013). The host plant of the specimen on A. flavescens (BRIP
25816) was re-identified as A. crassicarpa. The distribution of
E. violae-faustiae is restricted to the northern parts of Australia
on A. aulacocarpa, A. crassicarpa and A. difficilis.
Endoraecium walkerianum Berndt, Mycol. Progr. 10: 509.
2011
Type. AustrAliA, New South Wales, Cavan Gap near Yass, on A. penni-
nervis, 20 Nov. 1951, E. Gauba (holotype SF35354).
Additional specimen examined. AustrAliA, New South Wales, Bald Rock,
on A. penninervis, 26 Feb. 1984, J.W. Tierney, paratype BRIP 14205.
Notes ― Endoraecium walkerianum was reported from
A. penninervis and A. obliquinervia (Berndt 2011) in Botrycepha-
lae (Maslin 2013).
I7JK'GW Endoraecium tropicum. a. Pulverulent sori (BRIP 56557); b, c. urediniospores (BRIP 56557); d. teliospores (BRIP 56555). — Scale bars: a = 1 cm;
b– d = 10 µm.

61
A.R. McTaggart et al.: Co-evolutionary relationship between Endoraecium and Acacia
$'E"N'(,'(&"'E+,X+'#Y"%)"#',I'"+-,!$"%).H )+'
$.#(!$*)$
1. Urediniospores hyaline to pale yellow (on Botrycepha-
lae) ........................................2
1. Urediniospores golden or reddish brown ............ 7
2. Urediniospore wall up to 5 µm or thicker at sides ..... 3
2. Urediniospore wall 2.0– 4.5 µm thick at sides . . . . . . . . 4
3. Forming galls on stems of A. notabilis......E. digitatum
3. Forming hypertrophied lesions on A. falciformis ........
................................... E. falciforme
3. Forming hypertrophied lesions on A. daphnifolia . . . . . .
.....................................E. maslinii
4. Forming hypertrophied lesions on phyllodes......... 5
4. Forming galls on stem .......................... 6
5. On A. fasciculifera . . . . . . . . . . . . . . . . . . . . E. bicinctum
5. On A. podalyriifolia . . . . . . . . . . . . . . . E. podalyriifolium
5. On A. penninervis ..................E. walkerianum
6. On A. irrorata.........................E. irroratum
6. On A. dealbata........................E. carnegiei
7. Teliospores globose to ellipsoid on A. harpophylla .....
..................................... E. tierneyi
7. Teliospores clavate to obovoid or absent (on Juliflorae) 8
8. Urediniospore wall uniform ...................... 9
8. Urediniospore with thickened apex ............... 10
9. Teliospores digitate, on A. leiocalyx ........E. parvum
9. Teliospores not digitate, on A. tropica ......E. tropicum
10. Urediniospores foveolate, paraphyses present ...... 11
10. Urediniospores reticulate, paraphyses absent . . . . . . 13
11. Urediniospores with an acute apex . . . . . . . . . . . . . . . 12
11. Urediniospores not acute, on A. holosericea . . E. peggii
12. On A. auriculiformis .................E. auriculiforme
12. On A. aulacocarpa, A. crassicarpa or A. difficilis.......
............................... E. violae-faustiae
13. On A. disparrima ...................E. disparrimum
13. On A. aulacocarpa..................E. phyllodiorum
-)#%.##),+
Phylogenetic analyses of loci from nuclear rDNA and mitochon-
drial DNA showed that species of Endoraecium in Australia
have narrow host ranges. Savile (1971) hypothesised that
rusts speciated either by divergence with their hosts or by
host jumps. The close relationship between Endoraecium and
species/ subclades of Acacia observed in this study indicates
that Endoraecium diversified by co-evolution with its hosts. For
example, the five species of Endoraecium on Botrycephalae,
namely, E. carnegiei, E. falciforme, E. irroratum, E. maslinii and
E. podalyriifolium, were closely related with few differences
in the studied genes and short branch lengths between spe-
cies in the recovered phylogenetic trees. Species of Acacia in
Botrycephalae diversified c. 3.4–3.8 million years ago (Miller
et al. 2013), which would represent the maximum age of the
corresponding Endoraecium species.
Endoraecium tierneyi on A. harpophylla in Australia was reco-
vered as sister to the Hawaiian species, E. acaciae, E. hawaii-
ense and E. koae, on A. koa. These Australian and Hawaiian
rusts all occur on species of Acacia in Plurinerves. Hodges &
Gardner (1984) and Walker (2001) proposed that the Austra-
lian species of Endoraecium were the ancestor of the Hawaiian
rusts. Our study supports this view by showing the rusts on
Plurinerves had an Australian ancestor (plesiomorphic state).
Further, the three rusts on Acacia in Hawaii have differences in
life cycle and morphology, but are identical in the LSU region of
rDNA. These rusts have diversified on A. koae after its relatively
recent split from Australian species of Acacia (Brown et al.
2012). Endocyclic species occur in Hawaii but not in Australia,
which shows that a reduced life cycle is a derived character
in Endoraecium.
Endoraecium hyalosporum from South-East Asia infects A. con-
fusa, which is the only example of a species of Endoraecium
on a host outside of the p.u.b. clade of Acacia (Brown et al.
2012). This may represent an example of a host jump. However
the systematic position of E. hyalosporum is unknown, and it is
possible that it does not have a close phylogenetic relationship
to other species of Endoraecium. It is noteworthy that E. hya-
losporum has been assigned to other genera at various times,
namely, Maravalia (Dietel 1924), Poliotelium (Mains 1939) and
Atelocauda (Ono 1984).
The morphology of urediniospores may be synapomorphic for
the three clades of Endoraecium. For example, the rusts on
Juliflorae have reticulate to foveolate ornamentation on golden-
brown urediniospores. The rusts on Botrycephalae have a
raised reticulate ornamentation on subhyaline to pale yel-
low urediniospores. Endoraecium tierneyi was the only rust
examined on Plurinerves, and it had reticulate, reddish brown
urediniospores. Berndt (2011) noted the urediniospores of
species of Endoraecium on A. koa have similar morpho logy
to the rusts on Juliflorae, such as E. phyllodiorum. We cannot
propose any apomorphies for the rusts on Plurinerves at this
stage. The rusts on Juliflorae, namely E. auriculiforme, E. dis-
parrimum, E. peggii, E. phyllodiorum and E. violae-faustiae,
have urediniospores with thickened apices, whereas their sister
rusts E. parvum and E. tropicum, also in Juliflorae, have uni-
formly thickened spore walls.
Other morphological characters were less useful for species
delimitation in Endoraecium. In general, the teliospores of rusts
on species of Acacia in Botrycephalae had numerous (up to
15) apical digitations and were clavate. The teliospores of rusts
on species of Acacia in Juliflorae had fewer (up to four) apical
digitations and were obovoid. The presence of a gall or bullate
swelling is not a useful character for species delimitation. For
example, the sori of E. auriculiforme and E. phyllodiorum may
occur on bullate swellings or on undistorted phyllodes (Berndt
2011).
Endoraecium is likely to show further diversity. Only 14 species
of Acacia were sampled in this study. Other species such as
A. glaucocarpa (Botrycephalae), A. juliflorae (Juliflorae) and
A. viscidula (Plurinerves) were observed by the authors as hosts
for potentially new species of Endoraecium. New taxa will need
to be classified by a combined morphological, ecological (host
range) and molecular approach. We predict that many new
species of Endoraecium, which have diversified by coevolution
with their Acacia hosts, remain to be found in Australia.
$/Z80A42DJ2[286< This work was funded by the Australian Biological
Resources Study, grant number RFL212-33. CD would like to acknowledge
the support of the Australian Government’s Cooperative Research Centres
Program (Project No. PBCRC62081). Thank you to the anonymous reviewers
whose suggestions helped improve this manuscript.
!"I"!"+%"#
Aime MC. 2006. Toward resolving family-level relationships in rust fungi
(Uredinales). Mycoscience 47: 112–122.
Berkeley MJ, Broome CE. 1883. List of fungi from Brisbane, Queensland;
with descriptions of new species (part II). Transactions of the Linnean
Society of London 2: 53–73.
Berndt R. 2011. Taxonomic revision of Endoraecium digitatum (rust fungi,
Uredinales) with description of four new species from Australia and Hawaii.
Mycological Progress 10: 497–517.

62 Persoonia – Volume 35, 2015
Brown GK, Murphy DJ, Kidman J, et al. 2012. Phylogenetic connections of
phyllodinous species of Acacia outside Australia are explained by geologi-
cal history and human-mediated dispersal. Australian Systematic Botany
25: 390– 403.
Castresana J. 2000. Selection of conserved blocks from multiple alignments
for their use in phylogenetic analysis. Molecular Biology and Evolution
17: 540– 552.
Cummins GB, Hiratsuka Y. 1983. Illustrated genera of rust fungi. APS, St.
Paul, MN.
Dietel P. 1921. Zur Umgrenzung der Gattung Pileolaria Cast. Annales Myco-
logici 19: 300– 303.
Dietel P. 1924. Kleine Beiträge zur Systematik der Uredineen. IV. Annales
Mycologici 22: 269– 273.
Doungsa-ard C, McTaggart AR, Geering ADW, et al. 2014. Uromycladium
falcatarium sp. nov., the cause of gall rust on Paraserianthes falcataria
in South-East Asia. Australasian Plant Pathology: doi 10.1007/s13313-
014-0301-z.
Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basi-
diomycetes – application to the identification of mycorrhizae and rusts.
Molecular Ecology 2: 113–118.
Gardner DE. 1991. Atelocauda angustiphylloda n. sp., a microcyclic rust on
Acacia koa in Hawaii. Mycologia 83: 650– 653.
Hodges Jr CS, Gardner DE. 1984. Hawaiian forest fungi. IV. Rusts on endemic
Acacia species. Mycologia 76: 332– 349.
Katoh K, Asimenos G, Toh H. 2009. Multiple alignment of DNA sequences
with MAFFT. In: Posada D (ed), Bioinformatics for DNA sequence analysis.
Humana Press, New York, USA: 39–64.
Laundon GF. 1967. Terminology in the rust fungi. Transactions of the British
Mycological Society 50: 189–194.
Mains EB. 1939. Studies in the Uredinales, the genus Maravalia. Bulletin of
the Torrey Botanical Club 66: 173–179.
Maslin BR. 2013. World Wide Wattle. Available: http://www.worldwidewattle.
com/ Accessed: January 2014.
McAlpine D. 1906. The rusts of Australia: Their structure, nature and classi-
fication. Government Printer, Melbourne.
McTaggart AR, Geering ADW, Shivas RG. 2014. The rusts on Goodeniaceae
and Stylidiaceae. Mycological Progress 13: 1017–1025.
Miller JT, Murphy DJ, Ho SYW, et al. 2013. Comparative dating of Acacia:
combining fossils and multiple phylogenies to infer ages of clades with poor
fossil records. Australian Journal of Botany 61: 436– 445.
Murphy DJ, Brown GK, Miller JT, et al. 2010. Molecular phylogeny of Acacia
Mill. (Mimosoideae: Leguminosae): evidence for major clades and informal
classification. Taxon 59: 7–19.
Nylander JAA, Wilgenbusch JC, Warren DL, et al. 2008. AWTY (are we
there yet?): a system for graphical exploration of MCMC convergence in
Bayesian phylogenetics. Bioinformatics 24: 581–583.
Ono Y. 1984. A monograph of Maravalia (Uredinales). Mycologia 76: 892– 911.
Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic infer-
ence under mixed models. Bioinformatics 19: 1572–1574.
Savile DBO. 1971. Coevolution of the rust fungi and their hosts. The Quarterly
Review of Biology 46: 211–218.
Sawada K. 1913. Uromyces hyalosporus Sawada. sp. nov. causing the
disease to the shoots of Acacia confusa Merrill. The Botanical Magazine
27: 16– 20.
Scholler M, Aime MC. 2006. On some rust fungi (Uredinales) collected in an
Acacia koa – Metrosideros polymorpha woodland, Mauna Loa Road, Big
Island, Hawaii. Mycoscience 47: 159–165.
Stamatakis A. 2014. RAxML Version 8: A tool for phylogenetic analysis and
post-analysis of large phylogenies. Bioinformatics: doi 10.1093/bioinfor-
matics/ btu033.
Stevens FL. 1925. Hawaiian fungi. Bernice P. Bishop Museum, Honolulu, USA.
Tamura K, Peterson D, Peterson N, et al. 2011. MEGA5: Molecular evolu-
tionary genetics analysis using maximum likelihood, evolutionary distance,
and maximum parsimony methods. Molecular Biology and Evolution 28:
2731–2739.
Vialle A, Feau N, Allaire M, et al. 2009. Evaluation of mitochondrial genes as
DNA barcode for basidiomycota. Molecular Ecology Resources 9: 99–113.
Vilgalys R, Hester M. 1990. Rapid genetic identification and mapping of en-
zymatically amplified ribosomal DNA from several Cryptococcus species.
Journal of Bacteriology 172: 4238– 4246.
Walker J. 20 01. A revisio n of the genu s Atel ocauda (Uredinales) and descrip-
tion of Racospermyces gen. nov. for some rusts of Acacia. Australasian
Mycologist 20: 3– 28.
White TJ, Bruns TD, Lee S, et al. 1990. Amplification and direct sequencing
of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand
DH, Sninsky JJ, et al. (eds), PCR protocols: a guide to methods and ap-
plications: 315– 322. Academic Press Inc., San Diego, USA.
Winter G. 1886. Fungi Australienses. Revue Mycologique 8: 207–213.