A new species of rust fungi from the middle Eocene Sakhalinian amber

Abstract

Nyssopsora eocaenica Tykhonenko and Hayova sp. nov., the
only fossil species of the genus Nyssopsora (Pucciniales),
is described from the middle Eocene Sakhalinian amber
(Russian Far East). It differs from the other known representatives
of the genus by the presence of unbranched
hooked appendages on the surface of teliospores. The
spores are embedded in the amber sample in close proximity
to a syninclusion, Heterotrissocladius naibuchi (Diptera,
Chironomidae); most of them are clinged to the insect’s
wing or entangled in the bristles on its legs and body. This
fossil is ca. 45 myr old and provides useful information for
future phylogeny-based calibration and dating of the rust
fungi.

Full text

Acta Palaeontol. Pol. 66 (4): 921–924, 2021 https://doi.org/10.4202/app.00917.2021
A new species of rust fungi from the middle Eocene Sakhalinian
amber
YURI TYKHONENKO, VERA HAYOVA, MIKHAIL IGNATOV, DMITRY VASILENKO,
and EVGENY E. PERKOVSKY
Nyssopsora eocaenica Tykhonenko and Hayova sp. nov., the
only fossil species of the genus Nyssopsora (Pucciniales),
is described from the middle Eocene Sakhalinian amber
(Russian Far East). It differs from the other known rep-
resentatives of the genus by the presence of unbranched
hooked appendages on the surface of teliospores. The
spores are embedded in the amber sample in close proxim-
ity to a syninclusion, Heterotrissocladius naibuchi (Diptera,
Chironomidae); most of them are clinged to the insect’s
wing or entangled in the bristles on its legs and body. This
fossil is ca. 45 myr old and provides useful information for
future phylogeny-based calibration and dating of the rust
fungi.
Introduction
The order Pucciniales (rust fungi) currently accommodates
about 7800 species of obligate parasites of vascular plants
(Kirk et al. 2008). According to the most recent phylogenetic
research, rust fungi have separated from their closest relatives
in Jurassic, at around 175 Ma (Aime and McTaggart 2020). Due
to scarce fossil data, the time of origin of the order Pucciniales
and divergence dates for its main clades were calibrated mainly
by the age of the host plants and fossil evidences of other
groups of fungi (McTaggart et al. 2016; Aime et al. 2018). The
Nyssopsora Arthur, 1906, was established to accommodate
the species with triquetrous teliospores bearing appendages
on their surface (Arthur 1906). According to modern views, it
belongs to the suborder Uredinineae but its taxonomic position
within this taxon is not confidently resolved and the genus is
not yet assigned to any family (Aime and McTaggart 2020).
Currently, Nyssopsora comprises 10 species of autoecious par-
asites of plants of the orders Apiales and Sapindales. The pres-
ent-day geographic range of the genus includes all continents
except Africa and Antarctica; the centre of species diversity
is located in East Asia, where six species of Nyssopsora are
reported. Three of four species of Nyssopsora parasiting plants
of Sapindales are confined to East and South Asia. Nyssopsora
echinata reveals a prominent pattern of disjunctive distribution
between Europe and western North America. In the Eocene,
North Atlantic became suff iciently wide to make extremely
difficult any direct migration of plants and associated obligate
parasites between the continents (Milne and Abbott 2002); it
therefore implies that N. echinata may have originated in the
Eocene or earlier. More information on the extant species of
the Nyssopsora is available in publications by Lohsomboon et
al. (1990) and Carvalho Junior et al. (2014).
Over the last decade, Sakhalinian amber has yielded nu-
merous fossil arthropods of various taxa (e.g., Simutnik
2014, 2015; Fedotova and Perkovsky 2016; Radchenko and
Perkovsky 2016; Marusik et al. 2018; Dietrich and Perkovsky
2019; Kazantsev and Perkovsky 2019; Davidian et al. 2021;
Perkovsky et al. 2021; Simutnik et al. 2021 and references
therein). In our previous publication (Tykhonenko et al. 2021),
we reported the finding of few teliospores of rust fungus
similar to those of the modern species Nyssopsora trevesiae
(Gäumann, 1921) Tranzschel, 1925 in a sample of Sakhalinian
amber. Here we describe a new species of the fossil rust fungus
from another sample of Sakhalinian amber. For information
on the age, outcrop, and fossils from the Naibuchi Formation,
where the specimen of Sakhalinian amber was found in situ,
see Kodrul (1999).
Institutional abbreviations.—PIN, Borissiak Paleontological
Institute, Moscow, Russia.
Nomenclatural acts.—This published work and the nomencla-
tural act it contains, have been registered in Index Fungorum:
IF558 769.
Material and methods
The type of Nyssopsora eocaenica Tykhonenko and Hayova sp.
nov. is embedded in a small (7×4×3 mm) clear piece of amber.
In the previously published article (Baranov et al. 2015), the in-
ventory number of syninclused holoty pe of Heterotrissocladius
naibuchi Baranov, Andersen, and Perkovsky, 2015, was erro-
neously indicated as PIN 3387/150; the correct number is PIN
3387/147a. Photos were taken with an Olympus CX-41 trans-
mitted light microscope (10× and 20× lenses), with additional
illumination from above with a Motic fiber optic illuminator,
and an Infinity 2-2 digital camera.
The specimen PIN 3387/147 is deposited in the A.A. Boris-
siak Paleontological Institute, Russian Academy of Sciences,
Moscow.

922 ACTA PALAEONTOLOGICA POLONICA 66 (4), 2021
Systematic palaeontology
Kingdom Fungi Moore, 1980
Division Basidiomycota Moore, 1980
Class Pucciniomycetes Bauer, Begerow, Sampaio,
Weiss, and Oberwinkler, 2006
Order Pucciniales Caruel, 1881
Suborder Uredinineae Engler, 1892 emend. Aime and
McTaggart, 2020
Genus Nyssopsora Arthur, 1906
Type species: Nyssopsora echinata (Léveillé, 1848) Arthur, 1906; Re-
cent, Europe and western North America.
Fig. 1. Rust fungus Nyssopsora eocaenica Tykhonenko and Hayova sp. nov., holotype PIN 3387/147 Starodubskoye, Sakhalin, Russia; middle Eocene
Sakhalinian amber, Naibuchi Formation. General view of teliospores and part of the holotype of chironomid dipteran Heterotrissocladius naibuchi Bara nov,
Andersen, and Perkovsky, 2015 (A1), teliospores with appendages (A2, A3, A4).

BRIEF REPORT 923
Nyssopsora eocaenica Tykhonenko and Hayova sp.
nov.
Fig. 1.
Index Fungorum: IF558769
Etymology: Feminine adjective from Eocene, referring to its occur-
rence in that epoch.
Holotype: PIN 3387/147 (more than 200 detached teliospores).
Type locality: Starodubskoye village, Dolinsky District, Sakhalin Ob-
last, Russia.
Type horizon: Sakhalinian amber, Naibuchi Formation, middle Eocene,
48.6–40.4 Ma.
Diagnosis.—It is easily distinguishable from other hitherto des-
cribed species of the Nyssopsora by the presence of unbranched
hooked appendages on the surface of teliospores.
Description.—Teliospores consist of 3 cells; the basal one is
slightly larger than each of the other two which are both the
apical cells. The contours resemble almost equilateral trian-
gles with rounded corners, moderately constricted at the septa
(Fig. 1). Spores are coloured, but translucent, so that the septa
are clearly visible. Spore sizes vary within 33–38 × 34–37 μm.
Pedicels of teliospores are not observed. The outer walls of
all cells are covered with numerous simple appendages up to
6–7 μm long, hooked at the apex (Fig. 1). Host plant is un-
known.
Remarks.—In the article by Baranov et al. (2015), particles
adjacent to the holotype of the non-biting midge, Hetero trisso-
cladius naibuchi Bara nov, Andersen, and Perkovsky, 2015,
were considered as angiosperm pollen, but our further careful
examination has revealed that undoubtedly they are teliospores
of the Pucciniales fungus.
Studying of detached fungal spores is always hard because
the absence of sporogenous structures and associated substrate
makes correct identification extremely difficult. It is a serendip-
ity that mor phological features of the spores in the specimen PIN
3387/147 are sufficient for reliable identification of the fungus.
Indeed, due to triquetrous teliospores with appendages it can be
assigned to Nyssopsora with enough confidence, whereas un-
branched and hooked at the tips appendages clearly distinguish
the fossil from all previously described species of the extant ge-
nus. Since there are no plant inclusions in the amber sample, no
reliable assumption about a host plant of Nyssopsora eocaenica
Tykhonenko and Hayova sp. nov. can be made.
The left wing membrane of Heterotrissocladius naibuchi
(the right wing is lost) is densely covered with setae (Baranov
et al. 2015) and about 80% of all teliospores visible in the
specimen PIN 3387/147 are clinged to the wing (Fig. 1A1). The
position of the spores corroborates the assumption by Savile
(1989) that appendages on the surface of the teliospores of rust
fungi contribute to the inadvertent transfer of spores by entan-
glement in the bristles on the legs and body of insects.
Taxonomic identity of the Nyssopsora teliospores repor ted
in our recent publication (Tykhonenko et al. 2021) remains un-
clear. PIN 3387/147 and PIN 3387/973 are both collected in the
same locality and originated from the same stratigraphic hori-
zon; however, we cannot claim conspecificity of teliospores
in PIN 3387/147 and PIN 3387/973 due to a small number of
spores in the latter and due to a rather uncertain morphology
of their appendages.
Stratigraphic and geographic range.—Type locality and hori-
zon only.
Concluding remarks
The age of the amber sample containing Nyssopsora eocaenica
Tykhonenko and Hayova sp. nov. is reliably determined as
ca. 43–47 Ma (Radchenko and Perkovsky 2016). It indica-
tes that Nyssopsora must have originated before that time,
which is in concordance with cur rent estimation of age (53–
83 Ma) for the most recent common ancestor of Nyssopsora,
Sphaerophragmiaceae and Pucciniaceae (Aime and McTaggart
2020). Thus information on this newly described middle
Eocene-aged species of rust fungi can provide some evidence
and contribute to estimation of divergence times for the clades
of the suborder Uredinineae and the order Pucciniales as a
whole in future phylogenetic analyses.
Acknowledgements.—We greatly thank Alexandr Rasnitsyn and Irina
Sukacheva (both PIN) for the possibility to study Sakhalinian amber
inclusions. Useful comments on the manuscript of Alistair McTaggart
(The University of Queensland, Brisbane, Australia) and of two anon-
ymous reviewers are much appreciated and were gratefully accepted in
the final version. Ministry of Higher Education and Science of Russian
Federation is thanked for the support provided to the Center of Collec-
tive Use “Herbarium MBG RAS” Grant 075-15-2021-678.
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Yuri Tykhonenko [yu.ya.tykhonenko@gmail.com; ORCID: https://orcid.org/0000-0001-9000-7406] and Vera Hayova [v.hayova@gmail.com, https://or-
cid.org/0000-0002-7038-1633] (corresponding author); Kholodny Institute of Botany, National Academy of Sciences of Ukraine, 2 Tereshchenkivska Str.,
Kyiv, 01601, Ukraine.
Mikhail Ignatov [misha_ignatov@list.ru; ORCID: https://orcid.org/0000-0001-6096-6315], Tsytsin Main Moscow Botanical Garden of Academy of Sci-
ences, Russian Academy of Sciences, 4 Botanicheskaya Str., Moscow,127276, Russia.
Dmitry Vasilenko [damageplant@mail.ru], Borissiak Paleontological Institute, Russian Academy of Sciences, 123 Profsoyuznaya Str, Moscow, 117647,
Russia and Cherepovets State University, Lunacharsky Avenue, 5, Cherepovets, 162600, Russia.
Evgeny E. Perkovsky [perkovsk@gmail.com; ORCID: https://orcid.org/0000-0002-7959-4379], Schmalhausen Institute of Zoology, National Academy of
Sciences of Ukraine, 15 Bogdan Khmelnitski Str., Kyiv, 01601, Ukraine.
Received 13 June 2021, accepted 13 September 2021, available online 19 November 2021.
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