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Persoonia 40, 2018: 221–238 ISSN (Online) 1878-9080
www.ingentaconnect.com/content/nhn/pimj https://doi.org/10.3767/persoonia.2018.40.09
RESEARCH ARTICLE
INTRODUCTION
McAlpine (1905) established Uromycladium for rust fungi
(Pucciniales) on species of Acacia (Fabaceae) in Australia that
were characterised by single-celled teliospores on branched
and septate pedicels. Five species were described by Mc-
Alpine (1905) as new, namely, U. alpinum, U. bisporum (syn.
U. acaciae fide Sydow & Sydow 1915), U. maritimum, U. robin-
sonii and U. simplex. McAlpine (1905) additionally recombined
Uromyces tepperianus and Uredo notabilis as Uromycladium
tepperianum and Uromycladium notabile, respectively. Since
then, three additional species of Uromycladium have been de-
scribed, namely, U. fusisporum (Savile 1971), U. naracoortensis
(Berndt 2010) and U. falcatariae (type on Falcataria moluccana,
Doungsa-ard et al. 2015).
Uromycladium tepperianum s.lat. causes prominent galls on the
stems, phyllodes, inflorescences and pods of over 100 species
of Acacia (Morris 1991, Berndt 2010). Uromycladium tepperi-
anum has also been recorded on Paraserianthes lophantha
subsp. lophantha in Western Australia (Gathe 1971, Morris
1987), and Paraserianthes lophantha subsp. montana in Indo-
nesia (Magnus 1892, Boedjin 1959). Severe infection may lead
to the death of host plants (Gathe 1971, Morris 1997, Wood &
Morris 2007), and for this reason, U. tepperianum was intro-
duced as a biological control agent for the control of A. saligna
in the Eastern and Western Cape provinces of South Africa
(Morris 1991, Wood & Morris 2007, Wood 2012).
Samuel (1924) first suggested that U. tepperianum may be di-
visible into a number of biological species, each adapted to a
different host. Several authors have supported this hypothesis
based on observations of host range and intraspecific molecular
variation (Burges 1934, Walker 1983, Morris 1987, Berndt 2010,
Doungsa-ard et al. 2015). Morris (1987) inoculated isolates of
U. tepperianum from different host species onto a range of spe-
cies of Acacia and found there were host specific genotypes.
Doungsa-ard et al. (2015) used a molecular phylogenetic ap-
proach to show that the rust on Falcataria moluccana, which
had been attributed to U. tepperianum (Braza 1997, Old &
Cristovao 2003, Rahayu et al. 2010, Rahayu 2011, Widyastuti
et al. 2013), was a distinct species, U. falcatariae, and that
there was intraspecific variation within U. tepperianum s.lat.
This study investigated the diversity of Uromycladium spp. that
produce three teliospores per pedicel and form galls on their
hosts. The purpose of the study was to define U. tepperianum
in the strict sense, and resolve closely related species by a
combined biological (host range), morphological and phylo-
genetic species concept. Four gene regions from ribosomal
(rDNA) and mitochondrial DNA were analysed, together with
morphological characters, for 74 specimens on Acacia, two on
Falcataria and three on Paraserianthes lophantha.
MATERIALS AND METHODS
Specimen selection and morphological examination
During 2012–2015, specimens of Uromycladium spp. on spe-
cies of Acacia and P. lophantha were collected from various
locations in Australia (Table 1). All specimens were preserved
in the Plant Pathology Herbarium, Department of Agriculture
and Fisheries, Queensland (BRIP).
Rust spores were mounted on glass slides in 100 % lactic
acid and gently heated to boiling before microscopic examina-
tion. Ranges were expressed as either min.–max., or (min.–)
mean–SD – mean+ SD (–max.) with values rounded to 0.5 μm.
Diversity of gall-forming rusts (Uromycladium, Pucciniales)
on Acacia in Australia
C. Doungsa-ard1,2,3, A.R. McTaggart1,4, A.D.W. Geering1,2, R.G. Shivas2,5
1 Queensland Alliance for Agriculture and Food Innovation, The University
of Queensland, Ecosciences Precinct, GPO Box 267, Brisbane 4001,
Australia.
2 Plant Biosecurity Cooperative Research Centre, LPO Box 5012, Bruce
2617, Australia;
corresponding author e-mail: Roger.Shivas@daf.qld.gov.au.
3 Plant Pathology Research Group, Plant Protection Research and Develop-
ment Office, Department of Agriculture, Chatuchuk, Bangkok 10900,
Thailand.
4 Department of Microbiology and Plant Pathology, Tree Protection Co-
operative Programme (TPCP), Forestry and Agricultural Biotechnology
Institute (FABI), Private Bag X20, University of Pretoria, Pretoria, Gauteng,
South Africa.
5 Centre for Crop Health, University of Southern Queensland, Toowoomba
4350, Queensland, Australia.
Key words
cryptic species
Pucciniales
systematics
taxonomy
16 new taxa
Abstract Uromycladium tepperianum has been reported on over 100 species of Acacia, as well as on the closely
related plant genera, Falcataria, Racosperma and Paraserianthes. Previous studies have indicated that U. tep-
perianum may represent a complex of host-specific, cryptic species. The phylogenetic relationships between 79
specimens of Uromycladium were determined based on a concatenated dataset of the Small Subunit, the Internal
Transcribed Spacer and the Large Subunit regions of nuclear ribosomal DNA, and the mitochondrial cytochrome
c oxidase subunit 3. This study showed that the host range of U. tepperianum s.str. was restricted to species of
Acacia in the ‘A. bivenosa group’ sensu Chapman & Maslin (1992). An epitype of U. tepperianum on A. ligulata is
designated to create a stable taxonomy for the application of this name. Sixteen novel species of Uromycladium
are described, based on host preference, morphology and a phylogenetic species concept.
Article info Received: 23 October 2017; Accepted: 30 April 2018; Published: 16 May 2018.
222 Persoonia – Volume 40, 2018
Taxon Accession Host Statec, Country GenBank accession
number LSU ITS SSU CO3
Uromycladium brachycarpae BRIPa 58599 Acacia brachycarpa Qld, Australia KR994685 KR994736 KR994781 KR994986
U. falcatariae BRIP 57477 Falcataria moluccana Laguna, Philippines KJ632973d KJ633013d KJ632993d KJ639059d
BRIP 57990 F. moluccana Timor Leste KJ632974d KJ633014d KJ632994d KJ639060d
U. farinosae BRIP 58154 A. farinosa SA, Australia KR994686 KR994737 KR994782 KR994987
U. flavescentis BRIP 55385 A. flavescens Qld, Australia KR994687 KR994738 KR994783 KR994988
BRIP 57283 A. flavescens Qld, Australia KR994688 KR994739 KR994784 KR994989
U. fusisporum BRIP 57526 A. salicina Qld, Australia KJ632991d KJ633031d KJ633009d KJ639075d
U. holosericeae BRIP 56538 A. holosericea NT, Australia KR994689 KR994740 KR994785 KR994990
BRIP 56541 A. holosericea NT, Australia KJ632987d KJ633020d KJ633004d KJ639061d
BRIP 56543 A. holosericea NT, Australia KR994690 KR994741 KR994786 KR994991
BRIP 59653 A. holosericea Qld, Australia KJ632986 d KJ633028d KJ632998d KJ639062d
BRIP 61544 A. holosericea Qld, Australia KR994691 KR994742 KR994787 KR994992
U. implexae BRIP 57313 A. implexa Vic, Australia KR994692 KR994743 KR994788 KR994993
BRIP 57508 A. implexa NSW, Australia KR994693 KR994744 KR994789 KR994994
BRIP 57509 A. implexa NSW, Australia KJ632983d KJ633015d KJ633007d KJ639072d
BRIP 57628 A. implexa NSW, Australia KR994694 KR994745 KR994790 KR994995
BRIP 59220 A. implexa Vic, Australia KJ632984 d KJ633016d KJ633008d KJ639071d
U. leiocalycis BRIP 56928 A. leiocalyx Qld, Australia KJ632981d KJ633017d KJ633005d KJ639073d
BRIP 57285 A. leiocalyx Qld, Australia KR994695 KR994746 KR994791 KR994996
BRIP 57511 A. leiocalyx Qld, Australia KJ632982d KJ633018d KJ633006d KJ639074d
BRIP 57536 A. leiocalyx Qld, Australia KR994696 KR994747 KR994792 KR994997
BRIP 57582 A. leiocalyx NSW, Australia KR994697 KR994748 KR994793 KR994998
BRIP 59926 A. leiocalyx Qld, Australia KR994698 KR994749 KR994794 KR994999
U. ligustrinae BRIP 57708 A. ligustrina WA, Australia KR994699 KR994750 KR994795 KR995000
U. maslinii BRIP 57697 A. acuminata WA, Australia KR994700 KR994751 KR994796 KR995001
BRIP 57700 A. acuminata WA, Australia KR994701 KR994752 KR994797 KR995002
BRIP 57703 A. latior WA, Australia KJ632975d KJ632999d KJ633023d KJ639065d
BRIP 57704 A. incognita WA, Australia KR994702 N/A N/A N/A
BRIP 57743 A. resinimarginea WA, Australia KR994703 N/A N/A KR995003
BRIP 57744 A. gibbosa WA, Australia KR994704 N/A N/A KR995004
BRIP 57749 A. coolgardiensis WA, Australia KJ632976d KJ633024d KJ633003d KJ639066d
BRIP 57751 A. acuminata WA, Australia KR994705 KR994753 KR994798 KR995005
BRIP 57755 A. acuminata WA, Australia KR994706 KR994754 KR994799 KR995006
BRIP 57756 A. acuminata WA, Australia KJ632977d KJ633025d KJ633000d KJ639067d
BRIP 57819 A. acuminata WA, Australia KJ632978d KJ633026d KJ633001d KJ639068d
BRIP 57825 A. yorkrakinensis WA, Australia KR994707 N/A KR994800 KR995007
BRIP 57869 A. sibina WA, Australia KJ632979d KJ633019d KJ633002d KJ639070d
BRIP 57871 A. patagiata WA, Australia KR994708 N/A N/A KR995008
BRIP 57873 A. cyclops WA, Australia KR994709 KR994755 KR994801 KR995009
BRIP 61549 A. burkittii WA, Australia KR994710 KR994756 KR994802 KR995010
U. merrallii BRIP 58153 A. merrallii SA, Australia KR994711 KR994757 KR994803 KR995011
U. mitchellii BRIP 59355 A. trudgeniana WA, Australia KR994827 KR994836 KR994845 KR995036
U. morrisii BRIP 56962 A. saligna WA, Australia KJ632985d KJ633021d KJ632996d KJ639063d
BRIP 56963 A. saligna WA, Australia KJ632980d KJ633022d KJ632997d KJ639064d
BRIP 57860 A. saligna WA, Australia KJ632988d KJ633027d KJ632995d KJ639069d
U. murphyi BRIP 59234 A. dealbata Tas, Australia KJ632992 d KJ633030d KJ633011d KJ639076d
BRIP 55674 A. elata NSW, Australia KR994828d KR994837d N/A KR995037d
BRIP 57629 A. deccurens NSW, Australia KR994829d KR994838d KR994846d KR995038d
BRIP 57858 A. elata NSW, Australia KR994830d KR994839d KR994847d KR995039d
BRIP 57879 A. mearnsii NSW, Australia KR994831d KR994840d N/A KR995040d
BRIP 57929 A. rubida NSW, Australia KR994832 d KR994841d KR994848d KR995041d
BRIP 58300 A. penninervis NSW, Australia KR994833d KR994842d KR994849d KR995042d
BRIP 59219 A. dealbata Vic, Australia KR994834d KR994843d KR994850d KR995043d
BRIP 59233 A. mearnsii Tas, Australia KR994835 d KR994844d KR994851d KR995044d
U. paradoxae BRIP 58152 A. paradoxa SA, Australia KR994712 KR994758 KR994804 KR995012
BRIP 58602 A. stricta Qld, Australia KR994713 KR994759 KR994805 KR995013
BRIP 59204 A. paradoxa Vic, Australia KR994714 KR994760 KR994806 KR995014
BRIP 59221 A. montana Vic, Australia KR994715 KR994761 KR994807 KR995015
BRIP 59235 A. verniciflua Tas, Australia KR994716 KR994762 KR994808 KR995016
U. scirpifoliae BRIP 57817 A. scirpifolia WA, Australia KR994717 KR994763 KR994809 KR995017
BRIP 57827 A. scirpifolia WA, Australia KR994718 KR994764 KR994810 KR995018
U. simplex BRIP 59214 A. pycnantha Vic, Australia KJ632990 d KJ633029d KJ633010d KJ639078d
U. tepperianum BRIP 57307 A. ligulata WA, Australia KR994719 KR994765 KR994811 KR995019
BRIP 57596 A. ligulata WA, Australia KR994720 KR994766 KR994812 KR995020
BRIP 57707 A. rostellifera WA, Australia KR994721 KR994767 KR994813 KR995021
BRIP 57714 A. rostellifera WA, Australia KR994722 KR994768 KR994814 KR995022
BRIP 57742 A. cupularis WA, Australia KR994723 KR994769 KR994815 KR995023
BRIP 57816 A. cupularis WA, Australia KR994724 KR994770 KR994816 KR995024
BRIP 58146 A. cupularis SA, Australia KR994725 KR994771 KR994817 KR995025
BRIP 58147 A. cupularis SA, Australia KR994726 KR994772 KR994818 KR995026
BRIP 58160 A. cupularis SA, Australia KR994727 KR994773 KR994819 KR995027
BRIP 59439 A. xanthina WA, Australia KR994728 KR994774 KR994820 KR995028
BRIP 59895 A. ligulata SA, Australia KR994729 KR994775 KR994821 KR995029
BRIP 59899 A. ligulata SA, Australia KR994730 KR994776 KR994822 KR995030
BRIP 61265 A. sclerosperma WA, Australia KR994731 KR994777 KR994823 KR995031
U. tetragonophyllae BRIP 57748 A. tetragonophylla WA, Australia KR994732 KR994778 KR994824 KR995032
U. woodii BRIP 61600 Paraserianthes lophantha WA, Australia KR994733 KR994779 KR994825 KR995033
BRIP 62249 P. lophantha WA, Australia KR994734 KR994780 KR994826 KR995034
DARb 52697 P. lophantha WA, Australia KR994735 N/A N/A KR995035
a Queensland Plant Pathology Herbarium, Department of Agriculture and Fisheries, Australia.
b Plant Pathology Herbarium, Department of Primary Industries, New South Wales, Australia.
c NSW = New South Wales, NT = Northern Territory, Qld = Queensland, SA = South Australia, Tas = Tasmania, Vic = Victoria, WA = Western Australia.
d Doungsa-ard et al. (2015).
Table 1 List of rust specimens included in this study.
223
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
Fig. 1 Phylogram obtained in a maximum likelihood search in RAxML of concatenated SSU, ITS, LSU and CO3 gene regions. Bootstrap support values
(≥ 70 %) from 1 000 replicates above nodes. Posterior probabilities (≥ 0.95) summarised from 30 000 converged trees obtained in a Bayesian search are
shown below nodes.
0. 0 3
BRIP62249 Paraserianthes lophantha
BRIP59355 A. trudgeniana
BRIP57526 A. salicina
BRIP58599 A. brachycarpa
BRIP59234 A. dealbata
BRIP57744 A. gibbosa
BRIP55385 A. flavescens
BRIP56543 A. holosericea
BRIP59221 A. montana
BRIP58602 A. stricta
BRIP57509 A. implexa
BRIP55674 A. elata
BRIP58152 A. paradoxa
BRIP57869 A. sibina
BRIP61265 A. sclerosperma
BRIP58160 A. cupularis
BRIP56541 A. holosericea
BRIP59926 A. leiocalyx
BRIP57707 A. rostellifera
BRIP59235 A. verniciflua
BRIP61600 Paraserianthes lophantha
BRIP57929 A. rubida
BRIP57703 A. latior
BRIP57508 A. implexa
BRIP59895 A. ligulata
BRIP57283 A. flavescens
BRIP56538 A. holosericea
BRIP57873 A. cyclops
BRIP57816 A. cupularis
BRIP57749 A. coolgardiensis
BRIP57819 A. acuminata
BRIP58154 A. farinosa
BRIP57313 A. implexa
BRIP57714 A. rostellifera
BRIP57990 Falcataria moluccana
BRIP57743 A. resinimarginea
BRIP58300 A. penninervis
BRIP59220 A. implexa
BRIP57827 A. scirpifolia
BRIP56963 A. saligna
BRIP56928 A. leiocalyx
BRIP58146 A. cupularis
BRIP57628 A. implexa
BRIP57629 A. decurrens
BRIP57582 A. leiocalyx
BRIP57704 A. incognita
BRIP58153 A. merrallii
BRIP57536 A. leiocalyx
BRIP57825 A. yorkrakinensis
BRIP57697 A. acuminata
BRIP57742 A. cupularis
BRIP59439 A. xanthina
BRIP59899 A. ligulata
BRIP57596 A. ligulata
BRIP57871 A. patagiata
BRIP59233 A. dealbata
BRIP59653 A. holosericea
BRIP57817 A. scirpifolia
BRIP56962 A. saligna
BRIP57879 A. mearnsii
BRIP57708 A. ligustrina
BRIP57755 A. acuminata
BRIP57748 A. tetragonophylla
BRIP59219 A. dealbata
BRIP61549 A. burkittii
BRIP57285 A. leiocalyx
BRIP57878 A. elata
DAR52697 Paraserianthes lophantha
BRIP59204 A. paradoxa
BRIP58147 A. cupularis
BRIP57307 A. ligulata
BRIP57756 A. acuminata
BRIP57751 A. acuminata
BRIP57860 A. saligna
BRIP57511 A. leiocalyx
BRIP61544 A. holosericea
BRIP57700 A. acuminata
BRIP57477 Falcataria moluccana
BRIP59214 Acacia pycnantha
Uromycladium maslinii
Uromycladium scirpifoliae
Uromycladium holosericeae
Uromycladium flavescentis
Uromycladium implexae
Uromycladium paradoxae
Uromycladium leiocalycis
Uromycladium woodii
Uromycladium morrisii
Uromycladium merrallii
Uromycladium ligustrinae
Uromycladium brachycarpae
Uromycladium falcatariae
Uromycladium tepperianum
Uromycladium murphyi
Uromycladium mitchellii
Uromycladium simplex
Uromycladium fusisporum
Uromycladium farinosae
1.0
0.98
1.0
91
1.0
91
1.0
84 1.0
100
1.0
100
0.99
88
1.0
100
89
98
0.97
1.0
1.0
100
100
1.0
1.0
1.0
93
1.0
100 1.0
100
1.0
1.0
100 100
1.0
100
1.0
97
1.0
99
1.0
100
86
93
77
1.0
90
73
79
78
1.0
1.0
89
1.0
0.98
1.0
99
Uromycladium tetragonophyllae
224 Persoonia – Volume 40, 2018
Means and standard deviations (SD) were made from at least
30 measurements. Images were captured with a Leica DFC
500 camera attached to a Leica DMLB compound microscope
with Normarski differential interference contrast.
DNA extraction, PCR amplification and DNA sequencing
DNA was extracted as described by Doungsa-ard et al. (2015).
High fidelity Phusion® DNA Polymerase (New England Biolabs,
MA, USA) was used in PCR as per the manufacturer-specified
cycling and reaction conditions. The internal transcribed spacer
(ITS) region was amplified with ITS1F /ITS4B (Gardes & Bruns
1993). The large subunit (LSU) region was amplified with the
primers Rust2inv (Aime 2006)/LR7 (Vilgalys & Hester 1990)
and nested with the primers LROR/LR6 (Vilgalys & Hester
1990). The small subunit (SSU) region was amplified with
the primers NS1 (White et al. 1990)/Rust 18SR (Aime 2006).
Cytochrome c oxidase subunit 3 (CO3) in the mitochondrial
genome was amplified with the primers CO3_F1/CO3_R1
(Vialle et al. 2009). Annealing temperatures were: SSU, ITS and
nested LSU at 62 °C, the initial LSU at 60 °C, and CO3 at 55 °C.
PCR products were sent to Macrogen Korea for purification
and direct sequencing. Contigs were made from sequence
trace files with Sequencher v. 5.0 (Gene Codes Corporation,
Ann Arbor, Michigan).
Phylogenetic analyses
The LSU, ITS, SSU and CO3 sequences were aligned in SATe
v. 1.2 (Liu et al. 2012) with the MAFFT and MUSCLE algo-
rithms (Katoh & Toh 2008). DNA sequences were deposited in
GenBank with the accession numbers listed in Table 1 and the
final alignment and trees were deposited in TreeBASE (http://
purl.org/phylo/treebase/phylows/study/TB2:S18219). The
se quences from each locus were concatenated and run as a
partitioned dataset with maximum likelihood (ML) and Bayesian
inference as phylogenetic criteria. GTRGAMMA was specified
as the model of evolution for nucleotide sequence data for both
criteria. ML was implemented as a search criterion in RAxML
v. 8.1.15 (Stamatakis 2014). The RAxML analyses were run
with a rapid bootstrap analysis 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 v. 3.2 (Ronquist & Huelsenbeck
2003). Four runs, each consisting of four chains, were imple-
mented for 10 million generations. The cold chain was heated
at a temperature of 0.25. Substitution model parameters were
sampled every 1 000 generations and trees were saved every
1 000 generations. Convergence of the Bayesian analysis was
confirmed using the cumulative and compare functions in AWTY
(Nylander et al. 2008) (available at: ceb.csit.fsu.edu/ awty/) and
30 000 trees were summarized to create a consensus tree. The
ML and Bayesian analyses were run four times to test accuracy.
RESULTS
Phylogenetic relationships obtained with nuclear rDNA
and mitochondrial loci
Maximum likelihood and Bayesian inference recovered congru-
ent topologies (Fig. 1). The phylogenetic analyses recovered
18 species that could be differentiated from each other by
host range and a phylogenetic species concept. All species
with three, striate teliospores per pedicel were recovered in a
monophyletic group, and this character is considered a synapo-
morphy for this clade, which represents U. tepperianum s.lat.
Uromycladium tepperianum s.str., which was first described on
A. salicina (Saccardo 1889) in the ‘A. bivenosa group’ sensu
Chapman & Maslin (1992), was sister to other species of Uro-
mycladium with three, striate teliospores per pedicel.
Uromycladium falcatariae was distinguished from other gall-
forming species in the U. tepperianum s.lat. complex, by the
number of striae per spore (Doungsa-ard et al. 2015), but this
character was not informative for the remaining species. Based
on host range and a phylogenetic species concept from the
analysis of DNA sequences from four genes, 16 new species of
Uromycladium are described. Sequences obtained from holo-
type specimens were submitted to GenBank, and taxonomic
novelties were deposited in MycoBank (www.MycoBank.org;
Crous et al. 2004). The taxonomy of all species of Uromycla-
dium with three spores per pedicel is discussed below.
TAXONOMY
Uromycladium brachycarpae Doungsa-ard, McTaggart,
Geering & R.G. Shivas, sp. nov. — MycoBank MB818526;
Fig. 2
Etymology. Name refers to the host, Acacia brachycarpa, on which it was
found.
Type. AustrAliA, Queensland, Girraween (-28.8275, 151.9375), on A. bra-
chycarpa, 6 Mar. 2012, C. Doungsa-ard, D.J. Aster & A.R. McTaggart (holo-
type BRIP 58599), SSU, ITS, LSU and CO3 sequences GenBank KR994781,
KR994736, KR994685 and KR994986.
Galls along branches and stems, up to 7 cm long and 1 cm
diam. Spermogonia subepidermal, associated with telia. Telia
cinnamon brown, powdery. Teliospores in clusters of three,
depressed globose or subglobose, at first hyaline, later cin-
namon brown, with 37–44 equatorial striae and 25–31 striae
Fig. 2 Uromycladium brachycarpae on Acacia brachycarpa (BRIP 58599). a–b. Galls on branch; c. pedicellate teliospores; d. teliospores (equatorial view);
e. teliospores (surface view). — Scale bars: b = 1 cm; c– e = 10 μm.
225
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
convergent at the apex, margin crenulate in equatorial view,
(14–)15–17(–18) × (18 –)19–20(– 22) μm, apical germ pore
4–5.5 μm diam, deciduous or with a fragment of the pedicel
attached; wall 2.5 – 3.5 μm, thickened at the apex (2–)3 –4 μm;
pedicel branched, with a long axis (34–)39 –57(–58) × 4 – 5 μm
and two shorter lateral branches, pedicel wall 1 μm thick at
sides, septum situated near and above the basal branch and
about 8–11(–12) μm below the top fertile cell, hyaline.
On stems of A. brachycarpa.
Notes — Uromycladium brachycarpae is only known from
one specimen on A. brachycarpa in Queensland. Acacia brachy-
carpa is a member of the ‘Acacia ulicifolia group’, which includes
A. asparagoides, A. brownii, A. echinula, A. gunnii, A. saxicola
and A. ulicifolia (Maslin et al. 2001). None of these other spe-
cies of Acacia are recorded in Australian herbaria with gall rust.
Uromycladium brachycarpae was recovered as sister to all other
species of U. tepperianum s.lat. on Acacia.
Uromycladium falcatariae Doungsa-ard, McTaggart, Geering
& R.G. Shivas (as ‘falcatarium’), Australas. Pl. Pathol. 44:
28. 2015
Type. PhiliPPines, Magsaysay, Siniloan Laguna, University of the Philip-
pines Los Baños, Laguna-Quezon Land Grant, on Falcataria moluccana,
6 July 2012, K.L. Lancetta, V.A. Felices, T.U. Dalisay, A.I. Llano, A.R. McTag-
gart, M.D.E. & R.G. Shivas (holotype BRIP 57477), SSU, ITS, LSU and
CO3 sequences GenBank KJ633013, KJ632993, KJ632973 and KJ639059,
MycoBank MB808468.
Galls on swollen distorted stems, up to 20 cm long and 2 cm
wide, sometimes forming witches’ brooms. Spermogonia sub-
epidermal, scattered, associated with telia, 140 µm diam. Sper-
matia globose, ellipsoid or obovoid, hyaline, 3–4 × 3–7 µm.
Telia yellowish brown, powdery. Teliospores globose or subglo-
bose, yellowish brown, (13–)15–19(–21) × (17–)18–22(–24)
µm, in clusters of three on branched and septate pedicels,
with 25–32 striae converging at a solitary apical germ pore
2.5–4 µm diam, deciduous; wall 1.5–2.5 µm thick at sides
and 2–3.5 µm at apex; pedicel persistent, branched, with a
long axis 36–44 × 4–6 μm and two shorter lateral branches,
pedicel wall 1–1.5 μm thick at sides, septum situated near and
above the basal branch and about 14–16 μm below the upper
fertile cell, hyaline.
On stems of F. moluccana (tribe Ingeae).
Additional material examined. timor leste, on F. moluccana, Mar. 2011,
J.D. Ray & G. Soares, BRIP 57990, SSU, ITS, LSU and CO3 sequences
GenBank KJ633014, KJ632994, KJ632974 and KJ639060.
Notes — Uromycladium falcatariae occurs on F. moluccana
in the tribe Ingeae, which is a sister group to Australian Acacia
(Brown et al. 2011). Doungsa-ard et al. (2015) suggested that
U. falcatariae speciated by a host jump from Acacia (tribe Aca-
cieae) to Falcataria (as Paraserianthes) (tribe Ingeae), rather
than by coevolution on related host species.
Uromycladium farinosae Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818527; Fig. 3
Etymology. Name refers to host, Acacia farinosa, on which it was found.
Type. AustrAliA, South Australia, Warramboo, Nantuma Road, next to
railway line, 110 m from intersection with Tod Highway (-33.2967, 135.6261),
on A. farinosa, 24 Dec. 2012, A.D.W. Geering (holotype BRIP 58154), SSU,
ITS, LSU and CO3 sequences GenBank KR994782, KR994737, KR994686
and KR994987.
Galls on stems and phyllodes, up to 3 cm diam or confluent
to 7 cm long. Spermogonia subepidermal, embedded or asso-
ciated with telia, scattered, reddish brown to dark brown,
depressed globose, 200 – 220 μm wide and 80–110 μm high.
Telia scattered, young telia pale and velvet to powdery when
mature, cinnamon brown. Teliospores in clusters of three,
depressed globose, at first hyaline, later cinnamon brown,
with 31–40 equatorial striae and 22–25 striae convergent at
the apex, margin crenulate in equatorial view, 13–17(–20) ×
(16–)17–20 (–21) μm, apical germ pore 4 – 5 μm diam, decidu-
ous or sometimes with a fragment of the pedicel attached; wall
1.5–2.5 (–3) μm, thickened at the apex 2.5 – 4 μm; pedicel
branched, with a long axis 33–39(–43) × 4–5 μm and two
shorter lateral branches, pedicel wall 1–1.5 μm thick at sides,
septum situated near and above the basal branch and about
13–15 μm below the upper fertile cell, hyaline.
On phyllodes of A. farinosa.
Notes — Uromycladium farinosae is known from one speci-
men on A. farinosa in South Australia. It was recovered as sister
to U. ligustrinae and U. merrallii in the phylogenetic analyses.
Uromycladium flavescentis Doungsa-ard, McTaggart,
Geering & R.G. Shivas, sp. nov. — MycoBank MB818528;
Fig. 4
Etymology. Name refers to host, Acacia flavescens, on which it was found.
Type. AustrAliA, Queensland, Teewah, on A. flavescens, 6 Mar. 2012, A.R.
McTaggart (holotype BRIP 55385), SSU, ITS, LSU and CO3 sequences
GenBank KR994783, KR994738, KR994687 and KR994988.
Galls on stems and trunks, up to 10 cm long and 2 cm wide. Sper-
mogonia subepidermal, associated with telia, scattered, reddish
brown, depressed globose, 180–240 μm wide and 80–110 μm
high. Spermatia hyaline, ellipsoid to obovoid, (2.5 –)3 – 4 × 4–6 μm.
Fig. 3 Uromycladium farinosae on Acacia farinosa (BRIP 58154). a– b. Galls on branch; c. teliospores (equatorial view); d. teliospores (surface view). — Scale
bars: b = 1 cm; c– d = 10 μm.
226 Persoonia – Volume 40, 2018
Telia cinnamon brown, powdery. Teliospores in clusters of three,
vesicle absent, depressed globose or subglobose, at first
hyaline, later cinnamon brown, with 35–45 equatorial striae
and 24–28 striae convergent at the apex, margin crenulate
in equatorial view, (15–)16–18(–19) × (19–) 20 –23(– 24) μm,
apical germ pore 5–5.5 (– 6) μm diam, deciduous; wall 2 – 3 μm
diam; pedicels not seen.
On stems and trunks of A. flavescens.
Additional material examined. AustrAliA, Queensland, Noosa Heads
(-26.3789, 153.1069), on A. flavescens, 9 June 2012, C. Doungsa-ard, M.D.E.
& R.G. Shivas, BRIP 57283, SSU, ITS, LSU and CO3 sequences GenBank
KR994784, KR994739, KR994688 and KR994989.
Notes — Uromycladium flavescentis is specific to A. flave-
scens in subclade Plurinerves. It was sister to U. holosericeae
on A. holosericea in subclade Juliflorae. This may indicate
speciation occurred by a host shift of a recent common ancestor
between sympatric subclades of Acacia.
Uromycladium holosericeae Doungsa-ard, McTaggart,
Geering & R.G. Shivas, sp. nov. — MycoBank MB818529;
Fig. 5
Etymology. Name refers to host, Acacia holosericea, on which it was
found.
Type. AustrAliA, Queensland, Bowen, summit of Flagstaff Hill (-20.0172,
148.2666), on A. holosericea, 21 Sept. 2013, M.D.E. & R.G. Shivas (holotype
BRIP 59653), SSU, ITS, LSU and CO3 sequences GenBank KJ633028,
KJ632998, KJ632986 and KJ639062.
Galls on stems and phyllodes, up to 5 cm long and 3 cm wide.
Spermogonia subepidermal, associated with telia, scattered,
reddish brown, depressed globose, Telia erumpent, cinnamon
brown, powdery. Teliospores in clusters of three, vesicle absent,
depressed globose or subglobose, at first hyaline, later cin-
namon brown, with 35–40 equatorial striae and 24–27 striae
convergent at the apex, margin crenulate in equatorial view,
(16–)17–19(–20) × (18 –)20– 24 μm, apical germ pore 4–5.5
μm diam, deciduous; wall (1.5 –) 2–2.5 (–3) μm, thickened at the
apex (2–) 2.5–3.5 (–4) μm; pedicel branched, with a long axis,
55–80 × 4–5 μm, and two shorter lateral branches, pedicel wall
1–2 μm thick at sides, septum situated near and above the basal
branch and about 14–16 μm below the top fertile cell, hyaline.
On stems of A. holosericea.
Additional materials examined. AustrAliA, Northern Territory, Nitmiluk,
near Katherine Gorge (-14.3172, 132.4258), on A. holosericea, 20 Apr.
2012, C. Doungsa-ard, A.R. McTaggart, R. Berndt, V. Faust-Berndt, M.D.E.
& R.G. Shivas, BRIP 56541, SSU, ITS, LSU and CO3 sequences GenBank
KJ633020, KJ633004, KJ632987 and KJ639061; Northern Territory, Nitmiluk
(-14.3105, 132.4217), on A. holosericea, 20 Apr. 2012, C. Doungsa-ard, A.R.
McTaggart, R. Berndt, V. Faust-Berndt, M.D.E. & R.G. Shivas, BRIP 56543,
SSU, ITS, LSU and CO3 sequences GenBank KR994786, KR994741,
KR994690 and KR994991; Queensland, Laura, Peninsula Developmental
Road (-15.4394, 144.2114), on A. holosericea, 13 May 2014, W. Khemmuk &
A.D.W. Geering, BRIP 61544, SSU, ITS, LSU and CO3 sequences GenBank
KR994787, KR994742, KR994691 and KR994992.
Notes — There was intraspecific variation in the ITS and LSU
regions between isolates of U. holosericeae from the Northern
Territory and Queensland. The main distribution of A. holo-
sericea extends from Derby, Western Australia eastwards
Fig. 4 Uromycladium flavescentis on Acacia flavescens. a– b. Galls on trunk and branch (BRIP 57283); c. gall on branch (BRIP 55385); d. teliospores (equa-
torial view) (BRIP 55385); e. teliospores (surface view) (BRIP 55385). — Scale bars: c = 1 cm; d– e = 10 μm.
Fig. 5 Uromycladium holosericeae on Acacia holosericea. a. Galls on branches and phyllodes (BRIP 56538); b. gall on phyllodes (BRIP 59653); c. pedicellate
teliospores (BRIP 59653); d. teliospores (equatorial view) (BRIP 59653); e. teliospores (surface view) (BRIP 59653). — Scale bars: a– b = 1 cm; c– e = 10 μm.
227
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
across the Kimberley Region and Northern Territory to eastern
Queensland (Doran & Turnbull 1997). The variation observed
in rDNA may reflect genetic diversity of U. holosericeae across
the geographic range of A. holosericea.
Uromycladium implexae Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818530; Fig. 6
Etymology. Name refers to host, Acacia implexa, on which it was found.
Type. AustrAliA, Victoria, Euroa (-36.7742, 145.5139), on A. implexa, 12
May 2013, C. Doungsa-ard, W. Khemmuk & A.D.W. Geering (holotype BRIP
59220), SSU, ITS, LSU and CO3 sequences GenBank KJ633016, KJ633008,
KJ632984 and KJ639071.
Galls on branches, stems and phyllodes, confluent up to 50 cm
long, variable in shape and size. Spermogonia subepidermal,
associated with telia, reddish brown, depressed globose, 200–
240 μm wide and 100 –110 μm high. Spermatia hyaline, ellip-
soid, (2–)3–4(–5) × 4 – 5(– 6) μm. Telia erumpent, cinnamon
brown, powdery. Teliospores in clusters of three, vesicle absent,
depressed globose or subglobose, at first hyaline, later cin-
namon brown, with 32–39 equatorial striae and 21–27 striae
convergent at the apex, margin crenulate in equatorial view,
(12–)13–16(–17) × (16–)17–20 (–21) μm, apical germ pore
3–4.5 μm diam, deciduous; wall 1.5– 2.5 (–3) μm, thickened
at the apex 2 – 3.5 μm; pedicel branched, with a long axis
(42–)51–70 × 4 – 5 μm and two shorter lateral branches, pedicel
wall 1 μm thick at sides, septum situated near and above the
basal branch and about (15–)19–26 (–27) μm below the top
fertile cell, hyaline.
On stems, branches and phyllodes of A. implexa.
Additional materials examined. AustrAliA, New South Wales, Rookhurst,
Thunderbolts Way (-31.8681, 151.8628), on A. implexa, 13 June 2012,
A.J. Carnegie, BRIP 57508, SSU, ITS, LSU and CO3 sequences GenBank
KR994789, KR994744, KR994693 and KR994994; New South Wales, Stroud
Road, Bucketts Way (-32.3439, 151.9278), on A. implexa, 13 July 2012,
A.J. Carnegie, BRIP 57509, SSU, ITS, LSU and CO3 sequences GenBank
KJ633015, KJ633007, KJ632983 and KJ639072; New South Wales, Blax-
land, Great Western Highway, on A. implexa, 23 Aug. 2012, A.J. Carnegie,
BRIP 57628, SSU, ITS, LSU and CO3 sequences GenBank KR994790,
KR994745, KR994694 and KR994995; Victoria, Melbourne, along the Merri
Creek Trail between Glenlyon Road and Blyth Street-Separation Street, East
Brunswick, on A. implexa, 18 June 2012, J. Edwards, BRIP 57313, SSU,
ITS, LSU and CO3 sequences GenBank KR994788, KR994743, KR994692
and KR994993.
Notes — Uromycladium implexae occurs on A. implexa in
subclade Plurinerves. The host is similar in morphology to A. me-
lanoxylon, from which it is distinguished by the colour of the
funicle, time of flowering and phyllode shape (Gowers 1990).
Records of U. tepperianum s.lat. on A. melanoxylon (McAlpine
1905, Burges 1934) were unable to be verified as gall rust was
not found on A. melanoxylon in the present study.
Uromycladium leiocalycis Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818533; Fig. 7
Etymology. Name refers to host, Acacia leiocalyx, on which it was found.
Type. AustrAliA, Queensland, Seventeen Mile Rocks, 308 Seventeen Mile
Rocks Road, next to iSEE Church (-27.5497, 152.9581), on A. leiocalyx, 29
Nov. 2013, C. Doungsa-ard & A.D.W. Geering (holotype BRIP 59926), SSU,
ITS, LSU and CO3 sequences GenBank KR994794, KR994749, KR994698
and KR994999.
Fig. 6 Uromycladium implexae on Acacia implexa (BRIP 59220). a–b. Galls on branches and phyllodes; c. teliospores (equatorial view); d. teliospores
(surface view). — Scale bars: c– d = 10 μm.
Fig. 7 Uromycladium leiocalycis on Acacia leiocalyx. a. Galls on branch (BRIP 57536); b. galls on inflorescences (BRIP 59926); c. young pedicellate telio-
spores (BRIP 59926); d. teliospores (equatorial view) (BRIP 59926); e. teliospores (surface view) (BRIP 59926). — Scale bars: b = 1 cm; c– e = 10 μm.
228 Persoonia – Volume 40, 2018
Galls on branches, stems, phyllodes and inflorescences, glo-
bose to irregular, up to 5 cm diam. Spermogonia subepidermal,
associated with telia, scattered, reddish brown, depressed
globose, 200 – 240 μm wide and 80 –110 μm high. Spermatia
hyaline, ellipsoid, 4–5 × 3–4 μm. Telia on branches, erumpent,
cinnamon brown, powdery. Teliospores in clusters of three,
vesicle absent, depressed globose or subglobose, at first hya-
line, later cinnamon brown, with 31–38 equatorial striae and
22–27 striae convergent at the apex, margin crenulate in
equatorial view, 14–20(–27) × (19–)20 – 22(– 23) μm, apical
germ pore 4 – 4.5 μm diam, deciduous or with a fragment of
the pedicel attached; wall 2– 3 μm through the apex; pedicel
branched, with a long axis (26–)28–50(–53) × 4–5 μm and
two shorter lateral branches, pedicel wall 1 μm thick at sides,
septum situated near and above the basal branch and about
13–17(–18) μm below the top fertile cell, hyaline.
On branches, stems, phyllodes and inflorescences of A. leio-
calyx.
Additional materials examined. AustrAliA, Queensland, Wavell Heights,
end of Bilsen Road near Downfall Creek (-27.382475, 153.053798), on A. leio-
calyx, 17 May 2012, C. Doungsa-ard & R.G. Shivas, BRIP 56928, SSU, ITS,
LSU and CO3 sequences GenBank KJ633017, KJ633005, KJ632981 and
KJ639073; Queensland, Noosa Heads (-26.3778, 153.1150), on A. leiocalyx,
9 June 2012, C. Doungsa-ard, M.D.E. & R.G. Shivas, BRIP 57285, SSU, ITS,
LSU and CO3 sequences GenBank KR994791, KR994746, KR994695 and
KR994996; Queensland, Mount Coolum (-26.5622, 153.0942), on A. leio-
calyx, 28 July 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57511, SSU,
ITS, LSU and CO3 sequences GenBank KJ633018, KJ633006, KJ632982
and KJ639074; Queensland, Mount Alford, Mount Alford Road (-28.0717,
152.5742), on A. leiocalyx, 1 Aug. 2012, C. Doungsa-ard, A.R. McTaggart,
A.D.W. Geering & R.G. Shivas, BRIP 57536, SSU, ITS, LSU and CO3 se-
quences GenBank KR994792, KR994747, KR994696 and KR994997; New
South Wales, Maclean, Wharf Street approaching Highland Ridge (-29.4589,
153.2111), on A. leiocalyx, 12 Aug. 2012, C. Doungsa-ard, A.R. McTaggart
& A.M. Young, BRIP 57582, SSU, ITS, LSU and CO3 sequences GenBank
KR994793, KR994748, KR994697 and KR994998.
Notes — There was intraspecific variation in the ITS and LSU
regions of U. leiocalycis. These differences may reflect genetic
diversity of U. leiocalycis on A. leiocalyx, which contains two
subspecies, namely A. leiocalyx subsp. leiocalyx and subsp.
herveyensis (Pedley 1978).
Uromycladium ligustrinae Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818537; Fig. 8
Etymology. Name refers to host, Acacia ligustrina, on which it was found.
Type. AustrAliA, Western Australia, Kokeby, Southern Branch Road ap-
proaching Great Southern Highway (-32.2289, 116.9892), on A. ligustrina,
1 Oct. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering, Y.M. Li,
M.D.E. & R.G. Shivas (holotype BRIP 57708), SSU, ITS, LSU and CO3
sequences GenBank KR994795, KR994750, KR994699 and KR995000.
Galls on branches and phyllodes, up to 1 cm diam or conflu-
ent to 4 cm. Spermogonia subepidermal, associated with telia,
scattered, dark brown to black, depressed globose, 200 –250 μm
wide and 80 –120 μm high. Telia erumpent, cinnamon brown,
powdery. Teliospores in clusters of three, vesicle absent, de-
pressed globose or subglobose, at first hyaline, later cinnamon
brown, with 27–44 equatorial striae and 24–28 striae conver-
gent at the apex, margin crenulate in equatorial view, (14–)
16–18(–20) × (14–)19– 23(–26) μm, apical germ pore 4 – 5
μm diam, deciduous or with a fragment of the pedicel attached;
wall 2– 3(– 3.5) μm, thickened at the apex (2.5–) 3 –3.5(– 4) μm;
pedicel branched, with a long axis (48–)51–75(–84) × 4–6
μm and two shorter lateral branches, pedicel wall 1 μm thick
at sides, septum situated near and above the basal branch
and about (13–)18– 23 μm below the top fertile cell, hyaline.
On branches and phyllodes of A. ligustrina.
Notes — Uromycladium ligustrinae is known only from the
type specimen. The phylogenetic analyses showed that it was
sister to U. merrallii, which occurs on A. merrallii. Acacia ligus-
trina is closely related to A. merrallii and both are classified in
sect. Phyllodineae (Maslin 2013).
Uromycladium maslinii Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818539; Fig. 9
Etymology. Named after the Australian botanist, Bruce R. Maslin, who
generously identified many species of Acacia used in this study.
Type. AustrAliA, Western Australia, Mocardy, Koorda-Wongan Hills Road
(-30.8508, 116.8075), on A. acuminata, 6 Mar. 2012, C. Doungsa-ard, A.R.
McTaggart, A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shivas (holotype BRIP
57819), SSU, ITS, LSU and CO3 sequences GenBank KJ633026, KJ633001,
KJ632978 and KJ639068.
Galls on branches, confluent along the margin of phyllodes,
subglobose to irregular, up to 3 cm diam. Spermogonia subepi-
dermal, associated with telia, scattered, reddish brown to black,
depressed globose, 220–240 μm wide and 100–120 μm high.
Spermatia hyaline, ellipsoid, (3.5 –)4 – 6(– 8) × (2.5 –)3 – 4(– 5) μm.
Telia erumpent, cinnamon brown, powdery. Teliospores in clus-
ters of three, depressed globose or subglobose, at first hya-
line, later cinnamon brown, with 33–44 equatorial striae and
22–34 striae convergent at the apex, margin crenulate in
equatorial view, (12–)15–18(–20) × (17–)19– 23(– 26) μm,
apical germ pore 4–5 μm diam, deciduous or with a fragment
of the pedicel attached; wall (1.5–)2– 2.5(–3) μm, thickened at
the apex (2–) 2.5–3.5 (–4) μm; pedicel branched, with a long
axis (32–)37–64(–65) × 4.5 –5.5 μm and two shorter lateral
branches, pedicel wall 1–2 μm thick at sides, septum situated
near and above the basal branch and about (15–)16– 20(–21)
μm below the top fertile cell, hyaline.
Fig. 8 Uromycladium ligustrinae on Acacia ligustrina (BRIP 57708). a–c. Galls on branches; d. teliospores (equatorial view); e. teliospores (surface
view). — Scale bars: c = 1 cm; d– e = 10 μm.
229
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
On branches and phyllodes of A. acuminata, A. burkittii,
A. coolgardiensis, A. cyclops, A. gibbosa, A. incognita, A. latior,
A. patagiata, A. resinimarginea, A. sibina and A. yorkrakinensis.
Additional materials examined. AustrAliA, Western Australia, Yalgoo, 160
km west of Mount Magnet, off Geraldton-Mount Magnet Road (-28.3811,
116.3182), on A. acuminata, 29 Sept. 2012, A.D.W. Geering, Y.M. Li, M.D.E.
& R.G. Shivas, BRIP 57697, SSU, ITS, LSU and CO3 sequences GenBank
KR994796, KR994751, KR994700 and KR995001; Western Australia,
Mullewa, off Geraldton-Mount Magnet Road (-28.5783, 115.4503), on A. acu-
minata, 29 Sept. 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57700, SSU,
ITS, LSU and CO3 sequences GenBank KR994797, KR994752, KR994701
and KR995002; Western Australia, Yalgoo, Mount Magnet, off Geraldton-
Mount Magnet Road (-28.3811, 116.3182), on A. acuminata, 29 Sept. 2012,
A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57703, SSU, ITS,
LSU and CO3 sequences GenBank KJ633023, KJ632999, KJ632975 and
KJ639065; Western Australia, Pindar, Geraldton-Mount Magnet Road, Fegan
Road (-28.5201, 115.8678), on A. incognita, 29 Sept. 2012, A.D.W. Geering,
Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57704, LSU sequence GenBank
KR994702; Western Australia, Burakin, Dowerin-Kalannie Road, north west
of railway track (-30.5214, 117.1744), on A. resinimarginea, 30 Sept. 2012,
C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering, Y.M. Li, M.D.E. & R.G.
Shivas, BRIP 57743, LSU and CO3 sequences GenBank KR994703 and
KR995003; Western Australia, Cadoux, Hospital Road (-30.6433, 117.0100), on
A. gibbosa, 30 Sept. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering,
Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57744, LSU and CO3 sequences
GenBank KR994704 and KR995004; Western Australia, Pindar, Geraldton-
Mount Magnet Road, Fegan Road (-28.5070, 115.82699), on A. cool-
gardiensis, 29 Sept. 2012, A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shivas,
BRIP 57749, SSU, ITS, LSU and CO3 sequences GenBank KJ633024,
KJ633003, KJ632976 and KJ639066; Western Australia, York, end of Thorn
Street, in the park along Avon River (-31.8908, 116.7714), on A. acuminata,
1 Oct. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering, Y.M. Li,
M.D.E. & R.G. Shivas, BRIP 57751, SSU, ITS, LSU and CO3 sequences
GenBank KR994798, KR994753, KR994705 and KR995005; Western Aus-
tralia, Pingelly, 2 km north of Review Street, off Great Southern Highway,
next to railway track (-32.5133, 117.0764), on A. acuminata, 1 Oct. 2012,
C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shi-
vas, BRIP 57755, SSU, ITS, LSU and CO3 sequences GenBank KR994799,
KR994754, KR994706 and KR995006; Western Australia, Broomehill West,
13.1 km north of Tambellup, Great Southern Highway (-33.9331, 117.6456),
on A. acuminata, 1 Oct. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geer-
ing, Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57756, SSU, ITS, LSU and CO3 se-
quences GenBank KJ633025, KJ633000, KJ632977 and KJ639067; Western
Australia, Paynes Find, Goodlands Road, 6.3 km from intersection with Great
Northern Highway (-29.7711, 117.1017), on A. yorkrakinensis, 30 Sept. 2012,
C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering, Y.M. Li, M.D.E. & R.G.
Shivas, BRIP 57825, SSU, LSU and CO3 sequences GenBank KR994800,
KR994707 and KR995007; Western Australia, Carnamah, off Midlands Road,
600 m south-east of Carnamah railway station (-29.6944, 115.8889), on
A. sibina, 28 Sept. 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57869,
SSU, ITS, LSU and CO3 sequences GenBank KJ633019, KJ633002,
KJ632979 and KJ639070; Western Australia, Katanning, Great Southern
Highway (-33.7175, 117.5717), on A. patagiata, 1 Oct. 2012, C. Doungsa-ard,
A.R. McTaggart, A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57871,
LSU and CO3 sequences GenBank KR994708 and KR995008; Western
Australia, Amelup, off Chester Pass Road near Ongarup Creek (-34.2553,
118.2081), on A. cyclops, 2 Oct. 2012, C. Doungsa-ard, A.R. McTaggart,
A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57873, SSU, ITS,
LSU and CO3 sequences GenBank KR994801, KR994755, KR994709 and
KR995009; Western Australia, Mount Burges, southern Goldfields, Mount
Burges station, site 292 north of the Transline (-30.6925, 120.8192), on
A. burkittii, 3 Dec. 2013, A.A. Mitchell & P.J. Waddell, BRIP 61549, SSU,
ITS, LSU and CO3 sequences GenBank KR994802, KR994756, KR994710
and KR995010.
Notes — Uromycladium maslinii is restricted to Western Aus-
tralian on endemic species of Acacia. Uromycladium maslinii
was found on A. acuminata, A. burkittii, A. coolgardiensis, A. cy-
clops, A. gibbosa, A. incognita, A. latior, A. patagiata, A. resini-
marginea, A. sibina and A. yorkrakinensis. There was intra-
specific variation in the ITS region of U. maslinii from specimens
on different species of Acacia, indicating it may represent a
complex of cryptic species.
Uromycladium merrallii Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818545; Fig. 10
Etymology. Name refers to host, Acacia merrallii, on which it was found.
Type. AustrAliA, South Australia, Warramboo, Nantuma Road, next to
railway line, 110 m from intersection with Tod Highway (-33.2964, 135.6261),
on A. merrallii, 24 Dec. 2012, A.D.W. Geering (holotype BRIP 58153), SSU,
ITS, LSU and CO3 sequences GenBank KR994803, KR994757, KR994711
and KR995011.
Galls on stems and branches, up to 3 cm diam or confluent to
7 cm along branches. Spermogonia subepidermal, depressed
globose, associated with telia, scattered. Telia erumpent, cinna-
mon brown, powdery. Teliospores in clusters of three, vesicle
absent, depressed globose or subglobose, at first hyaline,
later cinnamon brown, with 33–43 equatorial striae and 24 –30
striae convergent at the apex, margin crenulate in equatorial
view, (13.5–)15–17.5(–18) × (16.5 –)20 – 24(–26) μm, apical
germ pore 4 – 5.5 μm diam, deciduous or with a fragment of
the pedicel attached; wall (2 –)2.5– 3(–3.5) μm, thickened at
the apex 2.5 – 3.5(– 4.5) μm; pedicel branched, with a long axis
(37–)42–71(–72) × (5 –) 5.5–6.5 (–7) μm and two shorter lateral
branches, pedicel wall 1–2 μm thick at sides, septum situated
near and above the basal branch and about (15.5–)16.5–20
(–21) μm below the top fertile cell, hyaline.
On branches of A. merrallii.
Notes — Uromycladium merrallii is only known from the type
specimen on A. merrallii. Uromycladium merrallii was sister to
U. ligustrinae, which occurs on A. ligustrina, a close relative of
A. merrallii (Maslin 2013).
Fig. 9 Uromycladium maslinii on Acacia acuminata (BRIP 57819). a–b. Galls on branches and phyllodes; c. teliospores (equatorial view); d. teliospores
(surface view). — Scale bars: b = 1 cm; c– d = 10 μm.
230 Persoonia – Volume 40, 2018
Uromycladium mitchellii Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818549; Fig. 11
Etymology. Named after the indefatigable Australian botanist, Andrew
A. Mitchell, who has collected many rust and smut fungi in Australia, including
this rust on A. trudgeniana.
Type. AustrAliA, Western Australia, Fortescue, West Pilbara, about 5 km
west of Yarraloola Station Homestead on Old Main Road (-21.5778, 115.8636),
on A. trudgeniana, 8 June 2013, A.A. Mitchell, (holotype BRIP 59355), SSU,
ITS, LSU and CO3 sequences GenBank KR994845, KR994836, KR994827
and KR995036.
Galls on stems, swollen or distorted, up to 5 cm diam. Spermo-
gonia subepidermal, dark brown to black, scattered, associated
with telia, 150 – 200 μm wide and 100–150 μm high. Spermatia
hyaline, ovate or ellipsoid, 2–3(–4) × (2 –)2.5–3.5 μm. Telia
powdery on gall and persistent when mature. Teliospores in
clusters of three, subglobose to depressed globose, at first hya-
line, later yellowish brown to cinnamon brown, densely covered
in randomly arranged warts, 13–17(–20) × (13–)15–18(–20)
μm, apical germ pore 3 – 4.5 μm diam; wall 2–3 μm, thickened at
the apex 2 – 4.5 μm; pedicel branched, with a long axis 55–70 ×
4.5–7.5 μm and two shorter lateral branches, pedicel wall 1–1.5
μm thick at sides, septum situated near and above the basal
branch and about 13–16 μm below the top fertile cell, hyaline.
On branches of A. trudgeniana.
Notes — Uromycladium mitchellii was sister to another
species (described below as U. murphyi sp. nov.) and together
formed a monophyletic group with a shared derived character
of three warted teliospores per pedicel. It is known from a sin-
gle specimen on A. trudgeniana in Western Australia. Acacia
trudgeniana belongs to a group of closely related species in
sect. Phyllodineae, referred to as the ‘A. pyrifolia group’ (Maslin
2013), which is sister to the ‘A. victoriae group’ (Murphy et al.
2010, Maslin 2013). Uromycladium mitchellii is the first rust
found on a host in this phylogenetic group and it is hypothesized
that collections of Uromycladium found on species of Acacia
in the A. victoriae and A. pyrifolia clade sensu Murphy et al.
(2010), will be closely related to each other.
Uromycladium morrisii Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818550; Fig. 12
Etymology. Named after Dr Michael J. Morris, a South African plant
pathologist who introduced this rust into South Africa in 1987 as a biological
control agent for A. saligna, where it has significantly helped to bring this
species under control.
Type. AustrAliA, Western Australia, Perth, 5 km north of The Vines Resort
(-31.7543, 116.0167), on A. saligna, 24 May 2012, R.G. Shivas (holotype
BRIP 56962), SSU, ITS, LSU and CO3 sequences GenBank KJ633021,
KJ632996, KJ632985 and KJ639063.
Galls on branches, stems, inflorescences, pods and phyllodes, ir-
regular, up to 20 cm in length or forming witches’ brooms up to
40 cm diam. Spermogonia subepidermal, depressed globose,
associated with telia, scattered, reddish brown, 200–250 μm
wide and 100 –120 μm high. Spermatia hyaline, ellipsoid, (3.5–)
4–6(–7) × (2 –)3–4 (–5) μm. Telia erumpent, cinnamon brown,
powdery. Teliospores in clusters of three, depressed globose
Fig. 10 Uromycladium merrallii on Acacia merrallii (BRIP 58153). a– b. Galls on branches; c. teliospores (equatorial view); d. teliospores (surface view). — Scale
bars: b = 1 cm; c– d = 10 μm.
Fig. 11 Uromycladium mitchellii on Acacia trudgeniana (BRIP 59355). a. Gall on branch; b. pedicellate teliospores; c. teliospores (equatorial view); d. telio-
spores (surface view). — Scale bars: a = 1 cm; b– d = 10 μm.
231
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
or subglobose, at first hyaline, later cinnamon brown, with
33–40 equatorial striae and 27–35 striae convergent at the
apex, margin crenulate in equatorial view, (11–)14–18(–20) ×
(17–)18–22 (–26) μm, apical germ pore 4– 5.5 μm diam, deci-
duous or with a fragment of the pedicel attached; wall 2–3 μm,
thickened at the apex, (2–)2.5 – 3.5(–4) μm; pedicel branched,
with a long axis (40–)42–58(–65) × 4.5 – 6.5 μm and two
shorter lateral branches, pedicel wall 1–1.5 μm thick at sides,
septum situated near and above the basal branch and about
(15–)16– 24 μm below the top fertile cell, hyaline.
On stems, branches, phyllodes, inflorescences or pods of
A. saligna.
Additional materials examined. AustrAliA, Western Australia, Bailup,
Toodyay Road, on A. saligna, 24 May 2012, R.G. Shivas, BRIP 56963, SSU,
ITS, LSU and CO3 sequences GenBank KJ633022, KJ632997, KJ632980
and KJ639064; Western Australia, Two Rocks, 4 km south of Breakwater
Drive (-31.5016, 115.6109), on A. saligna, 27 Sept. 2012, A.D.W. Geering,
Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57860, SSU, ITS, LSU and CO3 se-
quences GenBank KJ633027, KJ632995, KJ632988 and KJ639069.
Notes — Uromycladium morrisii is highly destructive on
A. saligna in south-western Western Australia (Morris 1987
as U. tepperianum). It was introduced as a biocontrol agent in
South Africa, where A. saligna is a noxious weed (Morris 1997,
Wood 2012). Experimental inoculations of 23 Australian spe-
cies of Acacia demonstrated gall formation only on A. saligna,
which indicated strong host-pathogen specificity (Morris 1987).
Intraspecific variation in the ITS region of U. morrisii may reflect
genetic variation of this pathogen on A. saligna, of which there
are at least four subspecies (Millar & Byrne 2007, Millar et al.
2008, 2011).
Uromycladium murphyi Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB824917; Fig. 13
Etymology. Named after Dr Daniel J. Murphy, an Australian botanist and
molecular systematist, who has focused much of his research on the taxo-
nomy, classification and biogeography of Acacia.
Type. AustrAliA, Victoria, Mount Macedon, 409 Cameron Drive (-37.3722,
144.5964), on A. dealbata, 12 May 2013, C. Doungsa-ard, W. Khemmuk &
A.D.W. Geering (holotype BRIP 59219), SSU, ITS, LSU and CO3 sequences
GenBank KR994850, KR994843, KR994834 and KR995043.
Galls on branches, stems, phyllodes, leaves and pods, swollen
or distorted with proliferating lobes up to 5 cm diam. Spermogo-
nia subepidermal, associated with telia, 160 – 240 μm wide and
100–170 μm high, punctiform, black, scattered. Spermatia hya-
line, ovate or ellipsoid, 2–3 × 4 μm. Telia powdery. Teliospores
in clusters of three, subglobose to depressed globose, yellowish
brown to cinnamon, with 35–44 equatorial striae composed of
warts that converge and become indistinct towards the apex,
margin verruculose in equatorial view, (15–)16 –20(–23) × (21–)
22–25 (–30) μm, apical germ pore 5–6.5 μm diam; wall 1– 4
μm at sides, thickened at apex 3 – 5.5 μm; pedicel branched,
with a long axis, 30–50 × 3.5 –6 μm, and two shorter lateral
branches, pedicel wall 1–1.5 μm thick at sides, septum situated
near and above the basal branch and about 13–18 μm below
the top fertile cell, hyaline.
On branches, stems, phyllodes, inflorescences and pods of
A. dealbata, A. decurrens, A. elata, A. mearnsii, A. penninervis
and A. rubida.
Additional materials examined. AustrAliA, New South Wales, Blackheath,
Blue Mountains, Grand Canyon, on A. elata, 16 Mar. 2012, R. Berndt &
Fig. 12 Uromycladium morrisii on Acacia saligna. a. Galls on branches and phyllodes (BRIP 57860); b. gall on branch (BRIP 56962); c. teliospores (equatorial
view) (BRIP 61661); d. teliospores (surface view) (BRIP 61661). — Scale bars: c– d = 10 μm.
Fig. 13 Uromycladium murphyi on Acacia dealbata (BRIP 59219). a– b. Galls on branch; c. pedicellate teliospores; d. teliospores (equatorial view); e. telio-
spores (surface view). — Scale bars: b = 1 cm; c– e = 10 μm.
232 Persoonia – Volume 40, 2018
V. Faust-Berndt, BRIP 55674, ITS, LSU and CO3 sequences GenBank
KR994837, KR994828 and KR995037; New South Wales, Mount Colah, Fox-
glove, on A. decurrens, 25 Aug. 2012, A.J. Carnegie, BRIP 57629, SSU, ITS,
LSU and CO3 sequences GenBank KR994846, KR994838, KR994829 and
KR995038; New South Wales, Captains Flat, Parkers Gap Road (-35.6061,
149.7581), on A. elata, 6 Oct. 2012, A.J. Carnegie, BRIP 57878, SSU, ITS,
LSU and CO3 sequences GenBank KR994847, KR994839, KR994830 and
KR995039; New South Wales, Calga, Peats Ridge (-33.3128, 151.2654),
on A. mearnsii, 11 Oct. 2012, A.J. Carnegie, BRIP 57879, ITS, LSU and
CO3 sequences GenBank KR994840, KR994831 and KR995040; New
South Wales, Jerangle, Bredbo-Jerangle Road (-35.9189, 149.2569), on
A. rubida, 6 Oct. 2012, A.J. Carnegie, BRIP 57929, SSU, ITS, LSU and CO3
sequences GenBank KR994848, KR994841, KR994832 and KR995041;
New South Wales, Riamukka, Brackendale Road (-31.4289, 151.6508), on
A. penninervis, 16 Oct. 2012, A.J. Carnegie, BRIP 58300, SSU, ITS, LSU and
CO3 sequences GenBank KR994849, KR994842, KR994833 and KR995042;
Victoria, Kergunyah (-36.3333, 147.0333), on A. dealbata, 30 Apr. 1905,
G.H. Robinson, VPRI 5830; Tasmania, Berriedale, Museum of Old and New
Art (-42.8122, 147.2619), on A. mearnsii, 12 May 2013, J. Edwards, BRIP
59233, SSU, ITS, LSU and CO3 sequences GenBank KR994851, KR994844,
KR994835 and KR995044; Tasmania, Tinderbox (-43.0347, 147.3325), on
A. dealbata, 2 Dec. 2012, M. Glenn, BRIP 59234, SSU, ITS, LSU and CO3
sequences GenBank KJ633030, KJ633011, KJ632992 and KJ639076.
Notes — Uromycladium murphyi differs from other gall-
forming species of Uromycladium by having teleospores with
striations comprised of warts rather than distinct striae as
in U. tepperianum (McAlpine 1905). Uromycladium murphyi
was identified on six species of Acacia in the Botrycephalae
subclade sensu Murphy et al. (2010). Many earlier records of
this rust species were likely identified as U. notabile, e.g., on
A. dealbata (McAlpine 1905, 1906, Barry 2003, Berndt 2010),
A. decurrens, A. elata (McAlpine 1905, 1906, Berndt 2010),
A. pruinosa (McAlpine 1905, 1906) and A. mearnsii (Barry 2003,
Berndt 2010). However, the name Uromycladium notabile is
a synonym for another rust Endoraecium digitatum (Fig. 14),
which is a nomenclatural consequence of McAlpine (1905)
basing his description of Uromycladium notabile on a mixed
collection of urediniospores of Endoraecium and teliospores of
Uromycladium. Berndt (2011) first recognised that McAlpine’s
(1905) description of Uromycladium notabile was based on a
mixed collection when he synonymised Uredo notabilis with
Endoraecium digitatum.
Intraspecific molecular diversity (single nucleotide polymor-
phisms (SNPs) and/or indel sites in the ITS and LSU regions)
was found amongst isolates of U. murphyi. It is possible that
further species diversity exists within U. murphyi. However, this
was not resolved with the species criteria used in the present
study and more sampling is needed to determine whether there
are cryptic species in this group.
Uromycladium paradoxae Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818551; Fig. 15
Etymology. Name refers to one of the hosts, Acacia paradoxa, on which
it was found.
Type. AustrAliA, Victoria, Tarrawingee (-36.3858, 146.4233), on A. para-
doxa, 12 May 2013, C. Doungsa-ard, W. Khemmuk & A.D.W. Geering (holo-
type BRIP 59204), SSU, ITS, LSU and CO3 sequences GenBank KR994806,
KR994760, KR994714 and KR995014.
Fig. 14 Uredo notabilis. a. Illustration of holotype showing host symptoms (III a) on A. notabilis and urediniospore ornamentation (III b, c, d) (Ludwig 1890);
b. galls on phyllodes of A. notabilis (isotype MEL 1054135); c. urediniospore showing reticulate surface. — Scale bar: c = 10 μm.
Fig. 15 Uromycladium paradoxae on Acacia paradoxa (BRIP 59204). a–b. Galls on branches; c. teliospores (equatorial view); d. teliospores (surface
view). — Scale bars: b = 1 cm; c– d = 10 μm.
233
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
Galls globose on stems and branches, up to 3 cm diam, con-
fluent along stems. Spermogonia subepidermal, associated
with telia, scattered, reddish brown to dark brown, depressed
globose, 200– 240 μm wide and 100–120 μm high. Spermatia
hyaline, ellipsoid, (3–)3.5–4.5(–5.5) × (3–)3.5 –6(–7.5) μm.
Telia erumpent, cinnamon brown, powdery. Teliospores in
clusters of three, depressed globose or subglobose, at first
hyaline, later cinnamon brown, with 30–44 equatorial striae
and 26–32 striae convergent at the apex, margin crenulate in
equatorial view, (15–)16–18.5(–20) × (18–) 20 –23(– 26) μm,
apical germ pore 3.5 – 5.5 μm diam, deciduous or with a frag-
ment of the pedicel attached; wall (1.5–) 2–2.5 μm, thickened
at the apex 2.5 – 3.5 μm; pedicel branched, with a long axis
(32–)33–57(–65) × 4 –5.5 μm and two shorter lateral branches,
pedicel wall 0.5–1 μm thick at sides, septum situated near and
above the basal branch and about (10–)11–17(–18.5) μm below
the top fertile cell, hyaline.
On branches and stems of A. montana, A. paradoxa, A. stricta
and A. verniciflua.
Additional specimens examined. AustrAliA, South Australia, Belair, Belair
National Park, Queen Jubilee Drive (-35.0075, 138.6428), on A. paradoxa, 20
Dec. 2012, A.D.W. Geering, BRIP 58152; Queensland, Girraween, Girraween
National Park, Pyramids Road (-28.8278, 151.5626), on A. stricta, 6 Mar.
2013, C. Doungsa-ard & A.R. McTaggart, BRIP 58602, SSU, ITS, LSU and
CO3 sequences GenBank KR994804, KR994758, KR994712 and KR995012;
Victoria, Ingliston, Werribee Gorge State Park, 138 Myers Road (-37.6556,
144.3650), on A. montana, 11 May 2013, C. Doungsa-ard, W. Khemmuk &
A.D.W. Geering, BRIP 59221, SSU, ITS, LSU and CO3 sequences GenBank
KR994807, KR994761, KR994715 and KR995015; Tasmania, St Marys, Ele-
phant Pass Road (-41.5989, 148.2042), on A. verniciflua, 7 Mar. 2013, M. Glenn,
BRIP 59235, SSU, ITS, LSU and CO3 sequences GenBank KR994808,
KR994762, KR994716 and KR995016.
Notes — There was intraspecific variation from SNPs and
indels in the ITS and LSU regions of U. paradoxae from five
specimens on four host species, namely A. montana, A. para-
doxa, A. stricta and A. verniciflua. This intraspecific variation
in U. paradoxae may correspond to host variation or location.
Uromycladium scirpifoliae Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818552; Fig. 16
Etymology. Name refers to one of hosts, Acacia scripifolia, on which it
was found.
Type. AustrAliA, Western Australia, Boothendarra, Watheroo National
Park (-30.3178, 115.8197), on A. scirpifolia, 28 Sept. 2012, C. Doungsa-ard &
A.R. McTaggart (holotype BRIP 57817), SSU, ITS, LSU and CO3 sequences
GenBank KR994809, KR994763, KR994717 and KR995017.
Galls on stems and branches, up to 8 cm long and 4 cm wide.
Spermogonia subepidermal, associated with telia, scattered,
reddish brown, depressed globose, 180–220 μm wide and 80–
110 μm high. Spermatia hyaline, ellipsoid, (2.5–)3–4.5(–5.5)
× 4.5–7(–7.5) μm. Telia erumpent, cinnamon brown, powdery.
Teliospores in clusters of three, vesicle absent, depressed
globose or subglobose, at first hyaline, later cinnamon brown,
with 36–44 equatorial striae and 26 –30 striae convergent at the
apex, margin crenulate in equatorial view, (14–)15.5 –19.5(– 20)
× (19.5 –)20– 23(–26) μm, apical germ pore 4.5 – 6 μm diam,
deciduous or with a fragment of the pedicel attached; wall
2–3 μm, thickened at the apex (2.5 –) 3–4(– 5) μm; pedicel
branched, with a long axis (25–)33–75(–80) × 4.5 – 6 μm and
two shorter lateral branches, pedicel wall 1– 2 μm thick at sides,
septum situated near and above the basal branch and about
(15–)17–23 (– 24) μm below the top fertile cell, hyaline.
On branches and stem of A. scirpifolia.
Additional specimen examined. AustrAliA, Western Australia, Coorow,
Midlands Road, 200 m north of Coorow Train Station (-29.8817, 116.0206),
on A. scirpifolia, 28 Sept. 2012, C. Doungsa-ard & A.R. McTaggart, BRIP
57827, SSU, ITS, LSU and CO3 sequences GenBank KR994810, KR994764,
KR994718 and KR995018.
Note — Uromycladium scirpifoliae occurs on A. scirpifolia
in Western Australia and is sister to U. morrisii. These two
species together form a sister clade to U. maslinii, which are
all restricted to Western Australia.
Uromycladium tepperianum (Sacc.) McAlpine, Ann. Mycol. 3:
310. 1905. emend. (s.str.) Doungsa-ard, McTaggart, Geering
& R.G. Shivas — MycoBank MBT373119; Fig. 17
Basionym. Uromyces tepperianus Sacc., Hedwigia 28: 126. 1889.
Synonym. Caeomurus tepperianus (Sacc.) Kuntze, Revis. Gen. Pl. 3:
451. 1898.
Type. AustrAliA, South Australia, on Acacia salicina s.lat., 1889, J.G.O.
Tepper, holotype PAD; South Australia, Black Hill, Sandy Creek, on A. salicina
s.lat., 1889, J.G.O. Tepper (MEL 2070213 presumed isotype); South Australia,
Walker Flat, Angus Valley Road (-34.7569, 139.5531), on A. ligulata, 22 Nov.
2013, A.D.W. Geering (BRIP 59895 here designated as epitype), SSU, ITS,
LSU and CO3 sequences GenBank KR994821, KR994775, KR994729 and
KR995029.
Galls on stems and branches, up to 15 cm long and 3–5 cm
wide, elongated, confluent. Spermogonia subepidermal, asso-
ciated with telia, scattered, reddish brown, depressed globose,
220–240 μm wide and 80 –110 μm high. Spermatia hyaline,
ellipsoid, 3–3.5 × 2 – 2.5 μm. Telia cinnamon brown, powdery.
Teliospores in clusters of three, vesicle absent, depressed
globose or subglobose, at first hyaline, later cinnamon brown,
with 28–44 equatorial striae and 22–26 striae convergent at
Fig. 16 Uromycladium scirpifoliae on Acacia scirpifoliae (BRIP 57817). a–b. Galls on branches; c. teliospores (equatorial view); d. teliospores (surface
view). — Scale bars: b = 1 cm; c– d = 10 μm.
234 Persoonia – Volume 40, 2018
the apex, margin crenulate in equatorial view, 14–16(–17) ×
(18–)19– 23(–25) μm, apical germ pore 4 –5 μm diam; wall
1.5–2.5 (–3) μm, thickened at the apex (2.5–)3 – 4 μm; pedicel
branched, with a long axis (23–)29 –55(–70) × 4 –5 μm and two
shorter lateral branches, pedicel wall 0.5–1 μm thick at sides,
septum above the basal branch, hyaline.
On stems or branches of A. cupularis, A. ligulata, A. rostelli-
fera, A. sclerosperma and A. xanthina (‘A. bivenosa group’).
Additional materials examined. AustrAliA, Western Australia, Leonora
(-29.5431, 122.4828), on A. ligulata, 1 Nov. 2011, A.A. Mitchell, A.M. Holm
& A.L. Payne, BRIP 57307, SSU, ITS, LSU and CO3 sequences GenBank
KR994811, KR994765, KR994719 and KR995019; Western Australia, Koo-
kynie, Lake Rebecca (-30.0517, 122.2992), on A. ligulata, 27 July 2012, A.A.
Mitchell & A.M. Holm, BRIP 57596, SSU, ITS, LSU and CO3 sequences
GenBank KR994812, KR994766, KR994720 and KR995020; Western
Australia, Mullewa, Geraldton-Mount Magnet Road (-28.5479, 115.5001), on
A. rostellifera, 29 Sept. 2012, A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shivas,
BRIP 57707, SSU, ITS, LSU and CO3 sequences GenBank KR994813,
KR994767, KR994721 and KR995021; Western Australia, Mullewa,
Geraldton-Mount Magnet Road (-28.5783, 115.4503), on A. rostelli fera, 29
Sept. 2012, C. Doungsa-ard & A.R. McTaggart, BRIP 57714, SSU, ITS,
LSU and CO3 sequences GenBank KR994814, KR994768, KR994722 and
KR995022; Western Australia, Amelup (-34.2531, 118.2092), on A. cupularis,
2 Oct. 2012, C. Doungsa-ard, A.R. McTaggart, A.D.W. Geering, Y.M. Li,
M.D.E. & R.G. Shivas, BRIP 57742, SSU, ITS, LSU and CO3 sequences Gen-
Bank KR994815, KR994769, KR994723 and KR995023; Western Australia,
Amelup (-34.2550, 118.2075), on A. cupularis, 2 Oct. 2012, C. Doungsa-ard,
A.R. McTaggart, A.D.W. Geering, Y.M. Li, M.D.E. & R.G. Shivas, BRIP 57816,
SSU, ITS, LSU and CO3 sequences GenBank KR994816, KR994770,
KR994724 and KR995024; Western Australia, Hamilton Hill, Manning
Park (-32.0908, 115.7689), on A. xanthina, 23 July 2013, A.A. Mitchell,
BRIP 59439, SSU, ITS, LSU and CO3 sequences GenBank KR994820,
KR994774, KR994728 and KR995028; Western Australia, Capricorn, Great
Northern Highway (-23.9925, 119.5664), on A. sclerosperma, 20 Apr. 2014,
A.A. Mitchell, BRIP 61265, SSU, ITS, LSU and CO3 sequences GenBank
KR994823, KR994777, KR994731 and KR995031; South Australia, Port
Lincoln, Cape Baron PI (-34.7472, 135.8681), on A. cupularis, 20 Dec. 2012,
A.D.W. Geering, BRIP 58146, SSU, ITS, LSU and CO3 sequences GenBank
KR994817, KR994771, KR994725 and KR995025; South Australia, Murdinga
(-33.6900, 135.6881), on A. cupularis, 23 Dec. 2012, A.D.W. Geering, BRIP
58147, SSU, ITS, LSU and CO3 sequences GenBank KR994818, KR994772,
KR994726 and KR995026; South Australia, Murdinga (-33.7408, 135.7067),
on A. cupularis, 24 Dec. 2012, A.D.W. Geering, BRIP 58160, SSU, ITS,
LSU and CO3 sequences GenBank KR994819, KR994773, KR994727 and
KR995027; South Australia, Hallett Cove, Hallett Cove Conservation Park
(-35.0764, 138.4975), on A. ligulata, 24 Nov. 2013, A.D.W. Geering, BRIP
59899, SSU, ITS, LSU and CO3 sequences GenBank KR994822, KR994776,
KR994730 and KR995030.
Notes — The holotype of Uromyces tepperianus was collect-
ed on Acacia salicina in South Australia by J.G.O. Tepper and des-
cribed by Saccardo (1889). McAlpine (1905) transferred this rust
to Uromycladium. The holotype of U. tepperianum is located
in Saccardo’s collection at PAD (University of Padova, Italy).
This specimen was examined by John Walker (pers. comm.),
who observed that the teliospores had 22–26 striae that con-
verged at the apex. A presumed isotype (MEL 2070213) of this
specimen was examined in the present study and had similar
morphology to the description given by Saccardo (1889). An
attempt was made to extract DNA from this specimen, but PCR
amplifications were unsuccessful.
Fig. 17 Uromycladium tepperianum s.str. a. Illustration of holotype showing host symptoms on A. salicina and teliospores with convergent striae (Saccardo
1889); b. drawing of holotype preserved in PAD (sketched by John Walker in 1971); c. elongated gall symptom on A. salicina (holotype in PAD); d– f. teliospores
from holotype specimen showing the longitudinal striae (micrographs were taken at the National Herbarium of New South Wales in 2001 by Carolyn Porter
using a Cambridge Stereoscan 360 electron microscope, after having gold sputter-coated the teliospores in a Dynavac minicoater SC110M for 1.5–2 min;
g– h. elongated gall on A. ligulata branches (BRIP 59895); i. cluster of three teliospores on a branched pedicel; j–k. teliospores (equatorial and surface view)
on A. ligulata (BRIP 59895). — Scale bars: c, h = 1 cm; d– f, i–k = 10 μm.
235
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
Acacia salicina, the originally labelled host of the holotype of
U. tepperianum, belongs to the ‘A. bivenosa group’ of closely re-
lated plant species, which also includes A. ampliceps, A. biveno-
sa, A. cupularis, A. didyma, A. ligulata, A. rostellifera, A. sclero-
sperma, A. startii, A. telmica, A. tysonii and A. xanthina (Chap-
man & Maslin 1992, Joseph et al. 2013a, b). Acacia ligulata
has been historically confused with A. salicina (Chapman &
Maslin 1992) and at the time of the original fungal description,
the two were considered conspecific. The only members of
the ‘A. bivenosa group’ that were recognised in the systematic
census of Australian plants by Baron Ferdinand von Mueller
were A. salicina and A. rostellifera (Von Mueller 1889). Speci-
mens of Uromycladium were examined on five species in the
‘A. bivenosa group’, namely A. cupularis, A. ligulata, A. rostel-
lifera, A. sclerosperma and A. xanthina. Both A. ligulata and
A. salicina occur in the type locality, i.e., the Black Hill region
near the Murray River in South Australia, but only A. ligulata
was observed with gall rust (A.D.W. Geering, unpubl. data). Gall
rust was not found on A. salicina at any other location during
the course of this study.
Saccardo (1889) described and illustrated Uromyces tepperi-
anus as having teliospores with prominent longitudinal striae,
formed on unbranched pedicels. McAlpine (1906) observed
that pedicels of Uromyces tepperianus were branched with
three teliospores in a head. McAlpine (1906) transferred this
species to Uromycladium, which he established for rust fungi
on Acacia with teliospores in heads, i.e., on branched pedicels.
The specimen of gall rust on A. ligulata at the type locality (BRIP
59895) had teliospores in agreement with the descriptions and
illustrations made by Saccardo (1889), McAlpine (1906) and
observed by John Walker (unpubl. data). Saccardo (1889) il-
lustrated a phyllode of the host of Uromyces tepperianus (Fig.
17a). The phyllode length in A. ligulata is 3–10 cm (Chapman
& Maslin 1992, Tame 1992), which overlaps with that for A. sali-
cina (4–18 cm) (Simmons 1981, Tame 1992). Saccardo (1889)
also illustrated Uromyces tepperianus on an elongated stem
gall (Fig. 17a), which is similar to the gall seen on A. ligulata
in the type locality. The teliospores of Uromyces tepperianus
illustrated by Saccardo (1889) are similar in shape (depressed
globose) and surface ornamentation (42–44 equatorial striae)
(Fig. 17c) to the rust on A. ligulata. We conclude that the
holotype of Uromyces tepperianus was actually collected from
A. ligulata. DNA sequence data has been obtained from a recent
South Australian collection (BRIP 59895), which is a suitable
epitype of U. tepperianum in order to provide nomenclatural
stability.
Uromycladium tepperianum is distinct from other species in the
genus as it infects hosts in the ‘A. bivenosa group’. Further,
U. tepperianum has elongated galls along stems and branches
rather than galls that are globose or with proliferating lobes.
Uromycladium tepperianum s.str. is known only from Western
Australia and South Australia.
Uromycladium tetragonophyllae Doungsa-ard, McTaggart,
Geering & R.G. Shivas, sp. nov. — MycoBank MB818554;
Fig. 18
Etymology. Name refers to the host, Acacia tetragonophylla, on which it
was found.
Type. AustrAliA, Western Australia, East Yuna, Yuna-Tenindewa Road
(-28.4289, 115.0833), on A. tetragonophylla, 29 Sept. 2012, C. Doungsa-ard &
A.R. McTaggart (holotype BRIP 57748), SSU, ITS, LSU and CO3 sequences
GenBank KR994824, KR994778, KR994732 and KR995032.
Galls on branches, up to 3 cm long and 1 cm wide. Spermogonia
subepidermal associated with telia, scattered, reddish brown
to dark brown, depressed globose, 180 – 220 μm wide and
80–100 μm high. Spermatia hyaline, ellipsoid, (3–) 3.5– 5(–5.5)
× (3.5–) 4 –8(–10) μm. Telia erumpent, cinnamon brown, pow-
dery. Teliospores in clusters of three, vesicle absent, depressed
globose or subglobose, at first hyaline, later cinnamon brown,
with 34–45 equatorial striae and 24 –30 striae convergent at the
apex, margin crenulate in equatorial view, (12.5–)14 –20(–22)
× (17.5 –)18–22.5 (– 25) μm, apical germ pore 3.5–5.5 μm
diam., deciduous or sometimes with a fragment of the pedicel
attached; wall (1.5 –)2– 2.5(–3) μm, thickened at the apex
(2–)2.5 – 3.5(– 4) μm; pedicel branched, with a long axis
(25–)28–60(–65) × 4 – 5.5 μm and two shorter lateral branches,
pedicel wall 1– 2 μm thick at sides, septum situated near and
above the basal branch and about (10 –)12 –20(– 21) μm below
the top fertile cell, hyaline.
On branches of A. tetragonophylla.
Notes — Uromycladium tetragonophyllae is only known from
the type specimen on A. tetragonophylla in Western Australia.
Uromycladium woodii Doungsa-ard, McTaggart, Geering
& R.G. Shivas, sp. nov. — MycoBank MB818556; Fig. 19
Etymology. Named after the South African plant pathologist, Dr Alan R.
Wood, who has discovered and collected many rusts in Australia and South
Africa.
Type. AustrAliA, Western Australia, Porongurup, on Paraserianthes lo-
phantha, July 2010, L. Braun (spores harvested by A.R. Wood on 24 Feb.
2011 from inoculated plants maintained at the Agricultural Research Council
– Plant Protection Research Institute; ARC-PPRI) (holotype BRIP 61600),
SSU, ITS, LSU and CO3 sequences GenBank KR994825, KR994779,
KR994733 and KR995033.
Fig. 18 Uromycladium tetragonophyllae on Acacia tetragonophylla (BRIP 57748). a–b. Galls on branches; c. teliospores (equatorial view); d. teliospores
(surface view). — Scale bars: b = 1 cm; c– d = 10 μm.
236 Persoonia – Volume 40, 2018
Galls on stems and branches, round to elongated, up to 3
cm diam. Spermogonia subepidermal, associated with telia,
scattered, reddish brown, depressed globose, 200 –240 μm
wide and 100–110 μm high. Spermatia hyaline, ellipsoid, (2–)
2.5–3.5(–4) × (3 –) 3.5–5 (–6) μm. Telia erumpent, cinnamon
brown, powdery. Teliospores in clusters of three, vesicle ab-
sent, depressed globose or subglobose, at first hyaline, later
cinnamon brown, with 35–45 equatorial striae and 22–35
striae convergent at the apex, margin crenulate in equatorial
view, (15.5–)17– 20(–21) × (21–)22–25 (– 27) μm, apical germ
pore 3.5– 5.5 μm diam, deciduous or with a fragment of the
pedicel attached; wall 2 – 2.5(– 3) μm, thickened at the apex
(2.5–)3 – 4.5(– 5) μm; pedicel branched, hyaline, with a long
axis (20–)29–80(–95) × 4 – 5.5 μm and two shorter lateral
branches, pedicel wall 0.5–1 μm thick at sides, septum situated
near and above the basal branch and about 10–23(– 27) μm
below the apical spore.
On stems of Paraserianthes lophantha (tribe Ingeae).
Additional materials examined. AustrAliA, Western Australia, Porongurup,
on P. lophantha, July 2010, L. Braun (spores harvested by A.R. Wood on 28
Aug. 2014, from inoculated plants maintained at ARC-PPRI), BRIP 62249,
SSU, ITS, LSU and CO3 sequences GenBank KR994826, KR994780,
KR994734 and KR995034; Western Australia, Gloucester National Park, near
Gloucester Tree, on P. lophantha, 1985, M.J. Morris (from rust maintained
on inoculated plants at Commonwealth Scientific and Industrial Research
Organisation (CSIRO), Australian Capital Territory), DAR 52697, LSU and
CO3 sequences GenBank KR994735 and KR995035.
Notes — Uromycladium woodii is highly specific to P. lo-
phantha ssp. lophantha (Morris 1987), which is an endemic
Western Australian species that has become weedy in South
Africa (Impson et al. 2011). This rust was collected from the
Porongurup Ranges, Western Australia and maintained on
living plants at CSIRO, Australia and the Agricultural Research
– Council Plant Protection Research Institute, South Africa,
where it was studied as a potential biological control agent
for P. lophantha (Impson et al. 2011), and efforts to establish
it are underway (A.R. Wood pers. comm.). Uromycladium tep-
perianum s.lat. was recorded on P. lophantha ssp. montana
from Java, Indonesia (Magnus 1892, Boedijn 1959), although
it has not been recorded there or on this plant recently. The
relationship of this rust on P. lophantha ssp. montana in Indo-
nesia to U. woodii should be determined, i.e., do they represent
one widely distributed species or two distinct species. These
rusts on P. lophantha represent a host jump from Acacia to
P. lophantha, a sister species to Acacia (Brown et al. 2011).
DISCUSSION
The present study defined U. tepperianum s.str. by host range
and a phylogenetic species concept. An epitype specimen
of U. tepperanium was designated to provide future nomen-
clatural stability for this taxon. The phylogenetic hypothesis in
this study has confirmed the observations by Samuel (1924),
Burges (1934) and Morris (1987) that U. tepperianum was a
species complex on multiple hosts, and a new taxonomy has
been proposed. Uromycladium tepperianum s.lat. was divided
into 16 species, which are formally described here. This takes
the number of rust fungi in Australia to over 370 reported spe-
cies (Shivas et al. 2014). Doungsa-ard (2015) determined that
the presence of three teliospores on branched pedicels with
striate teliospore walls was synapomorphic for U. tepperianum
s.lat., and this finding was supported by the present study. At
the species level, the morphology of spore characters is not
useful to separate many of these taxa with three, striate telio-
spores per pedicel.
Phylogenetic analyses of genes from nuclear rDNA and mito-
chondrial DNA showed that the majority of these new species of
Uromycladium were host specific on a single species of Acacia.
There were four exceptions, namely U. maslinii, U. murphyi,
U. paradoxae and U. tepperianum s.str., which occurred on
more than one closely-related host species of Acacia. Molecular
evidence from the ITS region indicated there was intraspecific
diversity in U. holosericeae, U. morrisii, U. murphyi and U. para-
doxae. This may reflect the intraspecific diversity of their host
species, such as in A. saligna for U. morrisii (Thompson 2012)
and species of the Botrycephaleae clade sensu Murphy et al.
(2010) for U. murphyi.
The identification of species of Uromycladium in the proposed
taxonomy depends on accurate identification of the host spe-
cies. The host range of taxa with three, striate teliospores per
pedicel in Uromycladium includes species of Acacia in sections
Phyllodineae, Plurinerves, Juliflorae, and the Pulchelloidea
clade, referred to in traditional classifications (Maslin 2013).
Based on recent systematic studies of Acacia, A. saligna (host
of U. morrisii) was transferred from sect. Phyllodineae and
placed in the Pulchelloidea clade sensu Murphy et al. (2010),
which also contains species of Acacia in sections Alatae, Lyco-
podifoliae and Pulchellae (Murphy et al. 2010). It is interesting
that species of Uromycladium with three, striate teliospores per
pedicel have not otherwise been recorded on host species in
these three sections.
McTaggart et al. (2016) determined that host jumps, followed
by shifts and coevolution, shaped the extant diversity of rust
Fig. 19 Uromycladium woodii on Paraserianthes lophantha. a. Galls on stems (image provided by A.R. Wood, taken at Boranup Road, Leeuwin Naturaliste
National Park, Western Australia); b. teliospores (surface view) (BRIP 61600); c. teliospores (equatorial view) (BRIP 61600). — Scale bars: a = 1 cm; b –c = 10 μm.
237
C. Doungsa-ard et al.: Diversity of Uromycladium spp. on Acacia
fungi in the last 115 million years. Uromycladium diversified
approximately 16 million years ago, with the three-celled spe-
cies of Uromycladium younger than 10 million years old. The
present study showed that Uromycladium diversified on Acacia,
with U. falcatariae and U. woodii as result of two independent
host jumps from Acacia to the tribe Ingeae (Doungsa-ard et
al. 2015). The evolutionary history of the 16 new species on
Acacia is still uncertain and warrants future study. For instance,
U. maslinii occurs on hosts in two closely related sections,
namely Juliflorae and Plurinerves (Murphy et al. 2010). We
hypothesize that the host range of U. maslinii across different
sections of Acacia may be the result of host jumps. On the other
hand, coevolution or shifts to closely related host species may
have occurred in species such as U. paradoxae and U. morrisii,
which occur on multiple species or subspecies of Acacia that
are closely related (Thompson 2012, Maslin 2013). Similarly,
coevolution or host shifts explained much of the observed
species diversity in Endoraecium, another genus of rust fungi
on Acacia (McTaggart et al. 2015). Further species diversity of
Uromycladium may be discovered when the numerous rusts
that produce galls on Acacia and closely related genera, are
examined with a phylogenetic approach, considered together
with host range.
Acknowledgements The authors would like to acknowledge the support
of the Australian Government’s Cooperative Research Centres Program
(Project No. PBCRC62081). We also thank John Walker for specimens of
Uromycladium and his insightful and helpful comments. We are grateful to
Reinhard Berndt, Angus Carnegie, Jacky Edwards, Morag Glenn, Andrew
Mitchell, Alan Wood, Marjan Shivas, Margaret Geering, Louise Shuey, and
the Thai Department of Agriculture for support and provision of specimens.
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