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ORIGINAL ARTICLE
Chaconia heliconiae and C. clusiae sp. novae from French
Guiana with notes on the genus Chaconia
(Uredinales/Pucciniales) in the neotropics
Reinhard Berndt &Ludwig Beenken
Received: 9 May 2012 /Revised: 29 June 2012 /Accepted: 2 July 2012
#German Mycological Society and Springer 2012
Abstract Chaconia clusiae on Clusia cf. palmicida
(Clusiaceae) and C. heliconiae on Heliconia psittacorum,
H. bihai and Heliconia sp. (Heliconiaceae) are described as
new from French Guiana in northern South America. Clusia-
ceae and Heliconiaceae are new host families for members of
Chaconia, Heliconiaceae is the first one from Monocotyledo-
neae. Chaconia clusiae,C. heliconiae and C. maprouneae
formed tuberous to worm-like D-haustoria originating from
haustorial mother cells that were part of the intercellular
parasitic mycelium. A key to the recognized Chaconia spp.
is provided.
Keywords Chaconiaceae .Clusiaceae .D-haustorium .
Heliconiaceae .Rust fungi .Teliospore
Introduction
The rust genus Chaconia Juel, based on C. alutacea Juel,
comprises eight recognized species that occur in warm parts
of the world on host plants belonging to the families Euphor-
biaceae, Fabaceae, Mimosaceae, Oleaceae (Ono and Hennen
1983) and perhaps Bignoniaceae (Ono et al. 1988). Its mem-
bers are characterised by one-celled, thin-walled, ellipsoid or
club-shaped sessile teliospores that are formed by basal mer-
istematic cells and germinate upon maturity by elongation of
the apex.
Five of the described species are known from the New
Worl d : C. alutacea Juel, C. braziliensis Y. Ono & J.F. Hennen,
and C. ingae (Syd.) Cummins are found on Mimosaceae, C.
hennenii Berndt on Moraceae, and C. maprouneae (Viégas) Y.
Ono & J.F. Hennen on Euphorbiaceae. Chaconia texensis
Arthur on Loranthaceae may not be a rust fungus (Ono and
Hennen 1983) and is not considered here.
This paper describes two new species of Chaconia from
French Guiana and presents a key to the recognized species
of the genus.
Materials and methods
The studied rust specimens are listed under the respective
species. They are located in Herbarium Turicense (Z+ZT),
the holotypes in Paris (PC). ‘FG’and ‘HeRB’numbers are
collection numbers.
Infected host leaves of Clusia were photographed with
a Nikon D90 DSLR and picture files processed using
Adobe Photoshop CS4. Spores and hand sections obtained
from herbarium material were mounted and gently heated
in lactophenol or lactic acid on microscopic slides.
Hoyer’s Fluid (Cunningham 1972) mixed with a small
droplet of cotton blue dissolved in lactic acid was used
to clear and stain thicker sections. Preparations were ex-
amined with an Olympus BX51 compound microscope
equipped with a ColorView IIIu camera. The software
package Cell B (Software Imaging System) was used to
capture micrographs and to measure spores and details of
the spore ornament. The ranges of measurements, fol-
lowed by the arithmetic means (in parentheses), represent
at least 30 measured spores. If fewer spores were studied,
this is indicated in the text. Spore states were designated
according to the ontogenic terminology (Hiratsuka 1973).
The Roman numeral II stands for the presence of uredinia,
III for telia.
R. Berndt (*):L. Beenken
Institute of Integrative Biology (IBZ), Plant Ecological Genetics,
ETH Zürich,
Universitätstr. 16,
8092 Zürich, Switzerland
e-mail: reinhard.berndt@env.ethz.ch
Mycol Progress
DOI 10.1007/s11557-012-0845-7
Results
Chaconia clusiae Berndt sp. nov. (Figs. 1,2and 3).
Etymology: Clusia, the host genus.
Mycobank MB 519741
Spermogonia, aecia and uredinia not seen, probably
microcyclic. Telia densely aggregated on abaxial side of
host leaves covering large, slightly hypertrophied and bright
orange patches of leaves; telia develop originally in substo-
matal cavities, then form tiny, pulvinate and more or less
superstomatal sori, later they become larger and tend to
coalesce with adjacent sori; teliospores formed by two or
three on meristematic hymenial cells, 28–41× 12–19 μm
(35.2×15.6 μm), clavate, subclavate or ellipsoid, wall
smooth, colourless and less than 1 μm thick, germinating
at maturity with stout, often bent or sickle-shaped phragmo-
basidia by elongation of the apex. Stalked D-haustoria
present.
On leaves of Clusia cf. palmicida Rich. ex Planch. &
Triana (Clusiaceae).
Holotype (PC). French Guiana: Sinnamary canton, road
to Barrage de Petit Saut some 100 m after turn-off from
route nationale 1, on Clusia cf. palmicida, leg. R. Berndt &
L. Beenken, 17 Jul 2009 (FG09/111. III). Isotype Z+ZT (ZT
Myc 3558).
Infected host leaves generally bore one conspicuous,
large telial patch of several centimetres diameter (Fig. 1).
The slightly hypertrophied patches were bright orange, later
dark orange or ferrugineous and bordered by a pale green
front. Chaconia clusiae differs from other described Chaco-
nia spp. in the host family and the apparently microcyclic
life cycle. Only two other rust fungi are known on Clusia-
ceae, the anamorphic Uredo clusiae Arthur and U. zarumae
H.S. Jacks. & Holw. Because C. clusiae has the aspect of a
microcyclic rust, it is unlikely to comprise one of these
anamorphs in its life cycle.
We compared the present rust fungus also with species
from genera similar to Chaconia, namely Aplopsora Mains,
Chrysocelis Lagerh. & Dietel, Olivea Arthur, Ceraceopsora
Kakish., T. Sato & S. Sato and Maravalia Arthur, but did
not find coincidences.
The basidia, produced by apical elongation of the proba-
sidia, appeared to collapse rapidly after formation and ba-
sidiospore discharge. Only remnants of four-celled basidia
were observed or a few with single cells still turgescent.
Delicately stalked D-haustoria with an elongated haustorial
body tapering into a worm-like distal part were found in
infected host cells under the telia (Fig. 3).
Chaconia heliconiae Berndt, sp. nov. (Figs. 4,5,6and 7).
Etymology: Heliconia, the host genus.
Mycobank MB 519742
Spermogonia and aecia unknown. Uredinia mainly scat-
tered on abaxial side of leaves, tiny, subepidermal, Uredo-
type, lacking sterile bounding structures; urediniospores short-
ly and inconspicuously stalked, broadly ellipsoid, obovoid or
Fig. 1 Leaves of Clusia cf. palmicida infected with Chaconia clusiae
(type). Telia cover the abaxial side of large, slightly hypertrophied
patches of leaves and induce bright orange decolouration (dark in
B&W reproduction) bordered by a bleached rim. Bar 2cm
Fig. 2 Chaconia clusiae (type). Section through telium showing sub-
epidermal position of sorus (ed epidermis) and a probasidium (pb)
germinating by apical elongation (arrow). Bar 20 μm
Fig. 3 Chaconia clusiae (type). Section through telium showing
young and germinating probasidia and developing basidia. D-
haustoria are indicated by arrows. The section is shown upside down
for easier orientation. Bar 20 μm
Mycol Progress
ellipsoid, more rarely subglobose to pyriform, 25–31(35)×
19–25.5 μm(27.2×24.0μm), wall 1–1.5 μm thick, golden
brown, evenly covered with moderately coarse spines ca. 2.5–
3.5(4) μm apart, germ pores obscure. Telia among uredinia on
abaxial side of leaves, tiny, ferrugineous, bullate or forming
small crusts, with waxy consistency; teliospores ellipsoid,
formed on 2–3 loci on slightly thick- and pale golden-walled
meristematic hymenial cells, 27–36 × 8–11 μm (20 spores
measured), wall colourless, smooth, ca. 0.5 μm thick; phrag-
mobasidia narrowly cylindrical, produced upon maturity by
elongation of apex of probasidia. Delicately stalked bulbous
D-haustoria present.
On leaves of Heliconia spp. (Heliconiaceae).
Holotype (PC). French Guiana: Kourou canton, hiking trail
on golf course adjacent to Kourou Space Center, on Heliconia
cf. psittacorum L. f., leg. R. Berndt & L. Beenken, 16 Jul 2009
(FG09/106. II, III). Isotype Z+ZT (ZT Myc 3559).
Additional material studied. French Guiana: Kourou can-
ton, hiking trail on golf course next to Kourou Space Center,
on Heliconia sp., leg. R. Berndt & L. Beenken, 16 Jul 2009
(FG09/97. II). Sinnamary canton, Piste de St. Elie, degraded
savannah and swampy area shortly after turn-off from route
nationale 1, on H. psittacorum,leg.R.Berndt&L.
Beenken, 24 Jul 2009 (FG09/68. II). Roura canton,
Montagne de Kaw, “sentier botanique”,onH. bihai L.
f., leg. R. Berndt & L. Beenken, 25 Jul 2009 (FG09/69. II).
Matoury canton, Massif de Mirande, “sentier de Mirande”,on
Heliconia sp., leg. R. Berndt & L. Beenken, 15 Jul 2009
(FG09/96. [II], III).
Chaconia maprouneae (Viégas) Y. Ono & J.F. Hennen.
French Guiana: Matoury canton, savannah at route nationale 2
shortly W of the Roura crossing, On Maprounea guianensis
Aubl., leg. R. Berndt & L. Beenken, 26 Jul 2009 (FG09/29. II).
Puccinia heliconiae Arthur. Costa Rica: Province Alajuela,
San Ramón, Reserva Forestal “Alberto Brenes”at Río San
Lorencito, on Heliconia sp., leg. R. Berndt 14 Mar 1991 (HeRB
2501. II, III). Province Puntarenas, Osa Peninsula, entrance to
Corcovado National Park at “Los Patos”,onH. cf. latispatha
Benth., leg. R. Berndt, 24 Mar 1992 (HeRB 3087. II).
Chaconia heliconiae differs from the known members of
Chaconia in its monocot host Heliconia. Waxy telia were also
Fig. 4 Chaconia heliconiae (FG09/96). Section through telium show-
ing young and germinated probasidia and basidia embedded in a
gelatinous matrix (indicated by dotting). Basidia are generally bent
and their remnants often border the outside of the sorus. Development
of telium originates between the epidermis (ed) and the hypodermis
(hd). D-haustoria are indicated by arrows. The section is oriented
upside down for easier orientation. Bar 20 μm
Fig. 5 Chaconia heliconiae (type). Section through subepidermal
telium. The outside of the gelatinous matrix is covered by basidial
remnants, basidiospores and undefined debris. Bar 50 μm
Fig. 6 Chaconia heliconiae (FG09/96). Section through lateral part of
telium showing the torn epidermis (ed) and young and germinated
probasidia. Germinated probasidia are collapsed; the bent basidia more
or less line the gelatinous matrix of the sorus (arrow). Bar 20 μm
Fig. 7 Chaconia heliconiae (FG09/69). Section through uredinium
showing the hymenial sporogenous cells (hym) initially formed be-
tween hypo- and epidermis (hd,ed). Bar 20 μm
Mycol Progress
described in C. butleri (Syd.) Mains on Jasminum from India
(Sydow et al. 1912)andinC. braziliensis. Both differ from C.
heliconiae in other morphological characters (Ono and Hennen
1983). Species of Goplana Racib. have very similar gelatinous
telia but none occur on Heliconiaceae (Ono and Hennen 1983).
The rust fungi described from Heliconia,Cerotelium rec-
tangulata Buriticá & J.F. Hennen and Puccinia heliconiae are
entirely different from the present species in the telial state.
Farr and Rossman (2011)listMaravalia sp. on H. caribaea
Lam. from Venezuela, but apparently this species has not been
described. Puccinia heliconiae could be confused with C.
heliconiae in the uredinial state but it has urediniospores with
slightly thicker and paler spore wall and two inconspicuous
germ pores according to Arthur (1922) and Dietel (1897).
Germ pores could not be seen in the urediniospores of two
specimens of P. heliconiae from Costa Rica, indicating that
the thicker, pale spore wall is the main feature to tell its
urediniospores apart from C. heliconiae.
Uredinia and telia of C. heliconiae developed between the
epi- and hypodermis of the host leaves (Fig. 7). The uredinio-
spores had short, evanescent and easily overlooked stalks. The
bases of the stalks were surrounded by membranous sheaths,
probably remnants of pedicels of discharged spores, that indi-
cate that the spores are successively produced on sporogenous
loci of meristematic cells. Uredinia of C. maprouneae were
similar but sometimes showed a few peripheral sterile cells
that did not form a well-defined bordering layer.
Delicately stalked bulbous D-haustoria (Fig. 4) similar to the
ones observed in C. clusiae (Fig. 3) were found in infected host
cells. Similar D-haustoria were also encountered in C.
maprouneae.
Key to the species of Chaconia
This key is based on morphological characters and host taxa
(data taken from Berndt 2008; Hernández and Hennen 2003;
Ono and Hennen 1983; Ono et al. 1988; Sydow 1937, and
unpublished results).
1Telia tiny, densely aggregated on large, bright orange and
slightly hypertrophied leaf areas (Fig. 1); probably
microcyclic; on Clusia (Clusiaceae) ............... C. clusiae
–With other characters, not on Clusia ............................. 2
2Aecia and/or uredinia paraphysate (Physopella-type) .. 3
–Aecia and/or uredinia paraphysate (a few peripheral ster-
ile cells may occur in C. maprouneae but do not form a
well defined border) ....................................................... 5
3Teliospores apically thickened, germinating from a sub-
apical pore; urediniospores with 4(−6), often bipolar
germ pores; on Maclura (Moraceae) .......... C. hennenii
–Teliospores apically not thickened, germinating by apical
elongation ...................................................................... 4
4Aecio- and urediniospores cinnamon-brown, with 3
equatorial germ pores positioned on projecting lobes;
spore wall 1.5–2.5 μm thick, slightly thicker at the
apex; on Millettia (Fabaceae)....................C. coaetanea
–Urediniospores (sub)hyaline; spore wall ca. 1 μm
thick, germ pores obscure; on cf. Bignoniaceae
sp..........................................................C. thailandica
5(2) Aecio- and/or urediniospores longitudinally striate
or almost reticulate, or with longitudinal lines of warts,
not echinate ................................................................ 6
–Aecio- and/or urediniospores echinate ....................... 7
6Aecio- and urediniospores with longitudinal ridges usu-
ally connected by cross ridges, hence almost reticulate;
spore wall 2–4μm thick, slightly thicker at the apex
and base, germ pores 3–4 equatorial; on Inga
(Mimosaceae) ................................................ C. ingae
–Urediniospores with delicate longitudinal ridges
composed of rod-like tiny warts, not connected by
cross ridges; spore wall evenly ca. 1.5 μmthick
(without ridges), germ pores obscure; on Jasminum
(Oleaceae) ................................................. C. butleri
7(5) On monocots (Heliconia, Heliconiaceae); telia waxy,
crustose; urediniospores broadly ellipsoid, obovoid or
ellipsoid ...................................................... C. heliconiae
–On dicots......................................................................8
8(7) On Maprounea (Euphorbiaceae); urediniospores
pyriform to subreniform ....................... C. maprouneae
–On Pithecellobium or Stryphnodendron (Mimosaceae)....9
9On Pithecellobium; demicyclic; aecia Uredo-like, aecio-
spores symmetric, 20–26 × 16–20 μm ......... C. alutacea
–On Stryphnodendron; uredinia and telia known; uredinio-
spores asymmetric, 23–38 × 18–25 μm...C. braziliensis
Mycol Progress
Discussion
Family Chaconiaceae was proposed by Cummins and
Hiratsuka (1983) to accommodate genera of rust fungi with
usually thin-walled, stalked or sessile teliospores (probasidia)
that germinate by elongation of the apex. Ono and Hennen
(1983) pointed out that Chaconiaceae as circumscribed by
Cummins and Hiratsuka (1983) may not be a natural group.
As a first step towards a more natural classification, they
excluded all genera with pedicellate teliospores. Cummins
and Hiratsuka (2003) did not follow this treatment, but ex-
cluded Chrysocelis from Chaconiaceae which differs from the
other genera in the spermogonial type and Petersonia-like
aecia. Ono and Harada (1994) emphasized that genera
assigned to Chaconiaceae were not clearly circumscribed
because of incomplete knowledge of life cycles and morpho-
logical characters of the sori.
The type genus Chaconia is also vaguely defined and can
only be characterized by a combination of traits of which
each is widespread in rust fungi: the teliospore morphology
and germination as described above, spermogonia of type 5
or 7, and uredinia assignable to the anamorph genera Uredo
Pers. or Physopella Arthur. In addition, all known Chaconia
spp. are autoecious. As a consequence, a rust fungus cannot
be assigned to Chaconia with certainty based on telial or
even telial plus uredinial characters. Both C. heliconiae,
collected with uredinia and telia, and C. clusiae, only with
telia, could have been assigned to Chrysocelis with equal
justification. Chaconia heliconiae might have been placed
alternatively in Goplana due to the consistency of the telia.
To affiliate both species with Chaconia was essentially a gut
decision that may in future turn out to be wrong. Evidence
from DNA sequences is still unavailable as the type species
of the genera in question have not so far been sequenced
(e.g. Aime 2006).
With the species described in this paper, Chaconia
comprises ten recognized species of which seven occur
in the New World, and three in India, Thailand or West
Africa. They inhabit a broad range of mostly unrelated
host families encompassing members of the dicotyledon-
ous Clusiaceae, Euphorbiaceae, Fabaceae, Mimosaceae,
Moraceae, Oleaceae and possibly Bignoniaceae, as well
as the monocotyledonous Heliconiaceae. Given the possi-
bility that Chaconia is heterogeneous, it seems idle to try
to interpret this host diversity.
This paper describes the D-haustoria of C. clusiae,C.
heliconiae and, for the first time, of C. maprouneae. They
had ‘ordinary’D-haustoria (cf. Littlefield and Heath 1979,
pp. 128–158) formed by haustorial mother cells that were
part of the intercellular mycelium. This is in contrast to C.
ingae, in which the entire parasitic mycelium grew within
the host cells and formed intracellular hyphae and D-haustoria
(Berndt 2012). Different haustorial types and colonization
strategies were also found in the well-circumscribed genus
Ravenelia (Berndt 1997). This indicates that these haustorial
characters are not fixed within a genus and cannot be used as
taxonomic markers.
Acknowledgments Field work in French Guiana was financed by
the Swiss National Fund (Project no. 31003A-116095).
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