A new desert-dwelling oomycete, Pustula persica sp. nov ...

Short communication

A new desert-dwelling oomycete, Pustula persica sp. nov., on

Gymnarrhena micrantha (Asteraceae) from Iran

Mohammad Reza Mirzaee1, Sebastian Ploch2, Marco Thines2,3,*

1 Plant Protection Research Department, South Khorasan Agricultural and Natural Resources

Research and Education Center, AREEO, Birjand, Iran

2 Senckenberg Biodiversity and Climate Research Centre, Senckenberganlage 25, 60325

Frankfurt am Main, Germany

3 Goethe University, Department of Biological Sciences, Institute of Ecology, Evolution and

Diversity, Max-von-Laue-Str. 13, 60483 Frankfurt am Main, Germany

* Corresponding author. Senckenberg Biodiversity and Climate Research Centre,

Senckenberg Gesellschaft für Naturforschung, Mertonstr. 17-21, 60325 Frankfurt am Main,

Germany

E-Mail address: [email protected] (M.Thines)

ABSTRACT

The obligate biotrophic oomycete genus Pustula is one of the four major linages of white

blister rusts (Albuginaceae) identified so far. Species of the genus Pustula cause white blister

rust on numerous genera in the asterids, represented by several phylogenetically distinct

genus-specific lineages, most of which still await formal description. Thus, the observation

of the species of Pustula on the Asteraceae subfamily Gymnorhenoideae, pointed out to the

existence of a hitherto undescribed species. By the morphological and molecular

phylogenetic investigation conducted in this study it is concluded that the pathogen on

Mycoscience: Advance Publication doi: 10.47371/mycosci.2021.03.006

Short communication (Received January 13, 2021; Accepted March 16, 2021)

J-STAGE Advance Published Date:May 1, 2021

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Gymnarrhena micrantha from Iran indeed represents a hitherto unknown species and is

described as P. persica. This species has apparently adapted to desert condition and is, after

Albugo arenosa, the second species of white blister rust from Iranian deserts, highlighting

the adaptability of white blister rusts to hot and dry habitats.

Keywords: Albuginales, cox2, one new species, phylogeny

Despite similarities, such as filamentous growth and osmotrophic nutrient uptake,

the phylum Oomycota is unrelated to fungi of the kingdom Mycota, but instead belong to

the kingdom Straminipila, which also contains diatoms and brown seaweeds (Beakes &

Thines, 2017). Organisms in the Oomycota have adapted to a wide range of climate

conditions and lifestyles (Thines, 2014) and can be found in both arctic habitats (Hassett,

Thines, Buaya, Ploch, & Gradinger, 2019) and hot deserts (Mirzaee et al., 2013). The highest

diversity has so far been found among the two independently-evolved, obligate biotrophic

lineages parasitizing angiosperm plants, the downy mildews and white blister rusts (Thines,

2014; Wijayawardene et al., 2020). The white blister rusts have evolved to sporulate below

the epidermis of their hosts and to liberate their spores by enzymatic digestion of the

epidermal layer covering the pustules (Heller & Thines, 2009). The family Albuginaceae

contains the three genera that cause white blister disease of angiosperms, Albugo, Pustula,

and Wilsoniana. The latter two have been segregated from Albugo based on their largely

different cytology, differences in sporangia and oospore morphology, as well as deep

phylogenetic divide (Thines & Spring, 2005). In total, there are four major lineages in the

Albuginaceae (Voglmayr & Riethmüller, 2006), each with a specific host range. Albugo s.str.

parasitizes mostly Brassicales, but a few lineages are present on other orders (Choi, Shin,

Ploch, & Thines, 2011b; Ploch, Choi, & Thines, 2018). Albugo s.l. parasitizes members of the

Convolvulaceae and is distinguishable from Albugo s.str. by a pronounced oogonium

ornamentation (Voglmayr & Riethmüller, 2006; Thines & Voglmayr, 2009). Wilsoniana is

parasitic to caryophyllids and features broadly pear-shaped sporangia and densely ridged or

reticulate oospores (Thines & Spring, 2005; Thines & Voglmayr, 2009). Pustula parasitizes

various asterids, in particular Asteraceae, and is characterised by usually densely reticulate

oospores and sporangia with an equatorial wall thickening (Thines & Spring, 2005; Choi,

Thines, Tek, & Shin, 2012). Traditionally, it has been assumed that species causing white

blister rust disease are specific mostly on the host family level (Wilson, 1907; Biga, 1955;

Choi & Priest, 1995). However, phylogenetic investigations have revealed that in Albugo,

besides the generalist species, A. candida (Pers.) Roussel, several distinct, host-specific

species exist, which seem to be specific below the host genus level (Choi, Shin, Hong, &

Thines, 2007; Choi, Shin, Ploch, & Thines, 2008; Choi, Shin, & Thines, 2009; Thines et al.,

2009; Ploch et al., 2010; Choi & Thines, 2011). Also in the genus Pustula, species seem to be

specific on at least the host genus level (Ploch et al., 2011), leading to the description of P.

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Mycoscience: Advance Publication

helianthicola C. Rost & Thines affecting sunflower (Rost & Thines, 2011), and the re-

appraisal of several species previously thought to be synonyms of P. obtusata (Link) C. Rost

(syn. P. tragopogonis (Pers.) Thines) (Choi et al., 2012). In line with this, three new species of

Pustula were recently introduced from the Junggar Basin in China (Xu, Song, Xi, & Jiang,

2016; Xu et al., 2018).

During field trips in Iran, the occurrence of Pustula on Gymnarrhena micrantha Desf.

was noticed. Gymnarrhena micrantha is a hardy member of Asteraceae growing in dry,

mostly bare and sandy areas in the deserts of Iran. It is an ephemeric, amphicarpic, dwarf

desert annual herb which mainly distributed in the drier parts of Mediterranean biome of

North Africa and the Middle East. Although, some variation across the distribution range has

been noticed in collections, there is one species recognized in the genus. In a study of the

tribe Inuleae using the cpDNA gene ndhF, it was found that Gymnarrhena did not belonging

to Asteroideae as previously thought, but rather to the paraphyletic Cichorioideae complex

or sister to the entire Asteroideae, and was, thus, proposed as the sole member of the

subfamily Gymnarrhenoideae (Anderberg, Eldenäs, Bayer, & Englund, 2005; Funk &

Fragman-Sapir, 2009).

Given the host specificity previously observed for the genus Pustula (Ploch et al.,

2011; Xu et al., 2016, 2018), it seemed plausible that the Pustula species occurring on

Gymnarrhena does not belong to any Pustula species described so far. Therefore, it was the

aim of this study to clarify the phylogenetic relationships of the potential new species and to

investigate its morphology.

Specimens sequenced in this study have been deposited in the Herbarium

Senckenbergianum in Frankfurt (international herbarium code FR). The collection details are

given in Table 1. Thin cross sections using a razor blade were done on wetted herbarium

specimens with white blister symptoms. Sections were transferred to 60% lactic acid or 5%

aqueous chloral hydrate solution on a slide. The preparations for microscopy were warmed

up covered with coverslips and screened in bright-field using a compound light microscope

(VWR TR 500 PH, VWR International, Darmstadt, Germany). Subsequently, suitable

preparations were investigated in differential interference contrast (DIC) using a using a

compound light microscope (Zeiss Imager2, Carl Zeiss, Jena, Germany) for measurements

and photographs. Measurements were performed at ×1,000 magnification. Measurements

are presented as (minimum–)mean minus standard deviation–mean–mean plus standard

deviation(–maxiumum), with all values apart from the mean rounded to the nearest 0.5 µm

increment, followed by the number of measurements done for the respective organ.

Genomic DNA was extracted from small pieces of leave tissue with pustules of

Pustula from dried specimens. DNA extraction and PCR were performed as reported before

(Mirzaee et al., 2013). In short, the innuPREP plant DNA extraction kit (Analytik Jena GmbH,

Jena, Germany) was used for DNA extraction and PCR was performed using cox2 primers

reported previously (Hudspeth, Nadler, & Hudspeth, 2000). PCR products were sequenced

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A new desert-dwelling oomycete, Pustula persica sp. nov., on Gymnarrhena micrantha (Asteraceae) from Iran

by the laboratory centre of the Senckenberg Biodiversity and Climate Research Centre, with

the primers used in PCR. GenBank accession numbers for the sequences obtained in this

study are given in Table 1.

The partial cox2 sequences from the specimens were edited using the DNASTAR

computer package version 8 (Lasergene, Madison, WI, USA), and Geneious version 5.3.4

(Biomatters Ltd., Auckland, New Zealand). Subsequently, they were added to the dataset of

Ploch et al. (2011). In addition, the sequences of two Pustula species recently described

were added (Xu et al., 2016, 2018). Sequences were aligned on the Mafft webserver (Katoh,

Rozewicki, & Yamada, 2019) using default settings. Phylogenetic analyses were done on the

TrEase webserver (http://thines-lab.senckenberg.de/trease/) using FastTree2 (Price, Dehal,

& Arkin, 2010) for Minimum Evolution inference, RAxML (Stamatakis, 2014) for Maximum

Likelihood inference with 1,000 bootstrap replicates, and Bayesian inference using MrBayes,

version 3.2 (Ronquist et al., 2012) with 5 Million generations, while other parameters were

set to default.

In the phylogenetic reconstructions (Fig. 1), Pustula sp. from infecting Gymnarrhena

micrantha is occupying an isolated position, with no clear affinities to any other lineage. The

two specimens from G. micrantha were identical in sequence and clustered together with

maximum support in all analyses. The specimens from P. obtusata s.lat. infecting

Tragopogon graminifolius DC. clustered with P. obtusata from other species of Tragopogon

with high to maximum support. However, some genetic divergence between the two groups

was observed. Apart from a sister-group relationship of P. obtusata and P. junggarensis B.

Xu & Z. D. Jiang, which received strong to maximum support, no other subdivisions in

Pustula received strong support in all analyses.

Pustula is a cosmopolitan genus of white blister rusts, reported from all continents

except for Antarctica, and affecting a wide range of members of the Asterales (Ploch et al.,

2011). Most species of Pustula have been observed in the Asteraceae subfamilies

Lactucoideae, Carduoideae and Asteroideae. So far, there has been no occurrence reported

in the subfamily Gymnarrhenoideae (Funk & Fragman-Sapir, 2009), and also no other

pathogen is known to affect genus Gymnarrhena. Therefore, Pustula persica, causing white

blister rust disease, is the first pathogen reported in this subfamily. Interestingly, this is the

forth species of Pustula described from arid regions (Xu et al., 2016, 2018) this species in

desert regions supporting that this genus is able colonise a broad range of climates and is

well-adapted to dry conditions.

The morphological features that distinguish P. persica from other members of

Pustula are a combination of oospore, oogonium, primary and secondary sporangia sizes, in

line with previous publications (Rost & Thines, 2011; Choi et al., 2012; Xu et al., 2016, 2018).

As especially the often-neglected primary sporangia seem to be informative (Constantinescu

& Thines, 2006; Choi et al., 2012), these should always be considered when investigating

species of Pustula.

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While several new, host-specific species have been described or confirmed in the

genus Albugo (Choi et al., 2007, 2008; Thines et al., 2009; Ploch et al., 2010, 2018; Choi &

Thines, 2011; Choi, Thines, & Shin, 2011a), there are so far rather few articles on

undescribed Pustula species (Ploch et al., 2011; Rost & Thines, 2011; Xu et al., 2016, 2018).

Probably, this is because the variation in the oospore ornamentation is often less

conspicuous than in Albugo (Ploch et al., 2010; Choi et al., 2012). As a result, with the

exception of P. helianthicola (Rost & Thines, 2011), all of the undescribed lineages found in

Ploch et al. (2011) still await description. Apart from the species P. chardiniae (Bremer &

Petr.) Thines, P. hydrocotyles (Petr.) Thines, P. obtusata (as P. tragopogonis), and P.

spinulosa (de Bary) Thines, originally included in Pustula by Thines and Spring (2005), only

nine new species or combinations have been introduced to date, including P. obtusata, P.

centaurii Thines, C. Rost & Y. J. Choi, P. helianthicola and P. obtusata (Rost & Thines, 2011),

P. brasiliensis (Speg.) Y. J. Choi & Thines 2012 and P. swertiae (Berl. & Kom.) Y. J. Choi & H. D.

Shin 2012 (Choi et al., 2012), as well as P. junggarensis (Xu et al., 2016), P. cancriniae B. Xu &

Z. D. Jiang, and P. xinyuanensis B. Xu, Y. J. Choi & Z. D. Jiang (Xu et al., 2018).

Generally, Pustula species seem to be host specific on the host genus level (Ploch et

al., 2011; Choi et al., 2012), but in this study, we found some sequence divergence for P.

obtusata s.lat. on T. graminifolius as compared to P. obtusata from other Tragopogon

species. Further investigations, ideally including inoculation experiments and multigene

phylogenies are necessary to elucidate, if this variation can be considered as an intra-

species variation or if there are two distinct species of Pustula occurring in this host genus.

Taxonomy

Pustula persica Mirzaee & Thines, sp. nov. Fig. 2.

MycoBank no.: MB 838463.

Type: IRAN, Ferdows, on G. micrantha, Apr 2010, leg. M. R. Mirzaee (holotype,

Herbarium Senckenbergianum FR0046081).

Gene sequence in GenBank: MW450684 (cox2).

Etymology: “persica” refers to the Latin name of Iran, the country in which the

species was first collected.

Description: Hyphae intercellular. Sori mostly hypophyllous, 0.5–2 mm diam, distinct

or confluent, rounded or irregular, whitish to cream in colour. Sporogenous hyphae hyaline,

unbranched, clavate to cylindrical, head 13.5–16 μm diam, 25.5–39 μm long. Sporangia

arranged in basipetal chains, hyaline, of two types. Primary sporangia hyaline with an overall

thickened wall, except for the distal wall mostly 17–20.5 μm diam. Secondary sporangia

hyaline, subglobose to cylindrical, with pronounced equatorial wall thickening, mostly 18–22

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μm long, 18.5–23 μm diam. Oogonia globose to irregular, hyaline to yellowish, wall smooth,

mostly 63–80 µm diam. Oospores globose, yellowish brown to dark brown, mostly 49.2–

60.5 diam. Oospore ornamentation predominantly finely reticulate, sometimes appearing

wrinkly and with a discontinuous, wider net and rounded protuberances with fine ridges,

fine ornamentation with an irregularly bulged pattern within the areolae.

Habitat and known distribution: On living leaves of G. micrantha in Iran.

Other specimens examined: IRAN, Khorsan, Mohammadiah, April 2009, leg. M. R.

Mirzaee, Herbarium Senckenbergianum FR0046083.

Notes: Sori of P. persica on G. micrantha were mostly hypophyllous, 0.5–2 mm diam,

distinct or confluent, rounded or irregular, and whitish to cream in colour. The hyaline

primary sporangia had an overall thickened wall, except for the distal wall, and measured

(15–)17–18.7–20.5(–24) μm diam (n=100). The secondary sporangia were hyaline,

subglobose to cylindrical, with a pronounced equatorial wall thickening. They were (15.5–

)18–19.8–22(–27.5) μm long (n=100) and (17–)18.5–20.8–23(–27.5) μm diam (n=90).

Oogonia were globose to irregular, hyaline to yellowish, with a smooth wall, (57.7–)63–72–

81(–89) µm diam (n = 41). Oospores were globose, yellowish brown to dark brown, (40.5–

)49–54.9–60.5(–67.9) µm diam (n=70). Oospore ornamentation was predominantly finely

reticulate, but sometimes also wrinkly and with a discontinuous wider net and

protuberances with fine ridges. Apart from the generally finely reticulate coarse

ornamentation, a fine ornamentation with an irregularly bulged pattern within the areolae

was observed. A comparison with P. obtusata from T. graminifolius from Iran to P. persica

on G. micrantha showed differences in oospore size. While the oospore size of P. obtusata

was (42.5–)46–48.7–51.5(–56.5) µm diam, P. persica on G. micrantha, had larger oospores

with (40.5–)49–54.9–60.5(–68) µm diam. Primary sporangia of P. obtusata were larger than

in P. persica, with (15–)18–21.2–24.5(–30) µm diam in the former species and (15–)17–

18.7–20.5(–24) μm diam in the latter.

Disclosure

The authors declare no conflicts of interest. All the experiments undertaken in this study

comply with the current laws of the country where they were performed.

Acknowledgements

Support by the Iranian Research Institute of Plant Protection (IRIPP) to MRM is gratefully

acknowledged. This study was supported by the LOEWE initiative in the framework of the

Biodiversity and Climate Research Centre (BiK-F). Lisa Nigrelli and Sabine Telle are gratefully

acknowledged for laboratory support. Following the suggestion of Thines et al. (2020), all

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scientific names, regardless of rank are given in italics. Author contributions – MRM and MT

conceived the study, MRM provided materials, processed the specimens and did the

microscopy work. SP and MRM did the laboratory work, MT performed phylogenetic

reconstructions, MT and MRM wrote the manuscript with contributions from SP.

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Figure legends

Figure 1. Phylogenetic reconstruction in Minimum Evolution (ME) based on partial cox2

sequences. Support values for specific nodes in ME, Maximum Likelihood (ML), and

Bayesian inference (BI) are given on the branches next to the nodes if greater than 65% for

ME and ML, and greater than 0.8 for BI, in the respective order. A dash indicates lack of

support for the presented topology, and the letter x indicates support greater 69% in ME or

ML, or greater 0.9 in BI for conflicting topologies. Sequences obtained in this study are set in

bold.

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Figure 2. Micrographs of Pustula persica on Gymnarrhena micrantha. A: Primary sporangia

with pronounced thickening. B: Secondary sporangia with typical equatorial wall thickening

(arrow). C: Surface ornamentation with the fine structure within the areolae. D: Overview of

an oospore with reticulate surface ornamentation. Bars: A, B 20 μm; C, D 25 μm.

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Table

Table 1. Specimens sequenced in this study

Pathogen Host Collection details GenBank

accession #

for cox2

(mtDNA)

Herbarium

accession #

Pustula

obtusata

s.lat.

Tragopogon

graminifolius

Iran, Birjand, Mohammadiah, leg.

Mohammad Reza Mirzaee, Apr 2009

MW450686 FR0046065

P. obtusata

s.lat.

T. graminifolius Iran, Birjand, Mohammadiah, leg.


MW450687 FR0046066

P. persica sp.

nov.

Gymnarrhena

micrantha

Iran, Ferdows, leg. Mohammad Reza

Mirzaee, Apr 2010

MW450684 FR0046081

P. persica sp.

nov.

G. micrantha Iran, Khorsan, Mohammadiah, leg.


MW450685 FR0046083

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A new desert-dwelling oomycete, Pustula persica sp. nov ...

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