Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 December 2024 | 16(12): 26283–26290
ISSN 0974-7907 (Online)
| ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.6876.16.12.26283-26290
#6876 | Received 07
November 2020 | Final received 12 November 2024 | Finally accepted 21 November
2024
On the Maravalia echinulata
(Niessl ex Rabenh.) Ono (Pucciniales:
Chaconiaceae) with reference to its host range and
distribution
Sayantan Jash
1 & Asit
Baran De 2
1 Department of Botany
(UGC-Centre for Advanced Studies), The University of Burdwan, Golapbag, Bardhaman, Purba Bardhaman, West Bengal
713104, India.
2 Department of
Microbiology, The University of Burdwan, Golapbag, Bardhaman, Purba Bardhaman, West Bengal 713104, India.
1 sayantanjash.myco@gmail.com,
2 abde.brc@gmail.com (corresponding author)
Editor: K.R. Sridhar, Mangalore University,
Mangalore, India. Date of publication: 26 December
2024 (online & print)
Citation: Jash, S. & A.B. De (2024). On the Maravalia
echinulata (Niessl ex Rabenh.)
Ono (Pucciniales: Chaconiaceae)
with reference to its host range and distribution. Journal
of Threatened Taxa 16(12): 26283–26290. https://doi.org/10.11609/jott.6876.16.12.26283-26290
Copyright: © Jash & De 2024. Creative Commons
Attribution 4.0 International License. JoTT allows
unrestricted use, reproduction, and distribution of this article in any medium
by providing adequate credit to the author(s) and the source of publication.
Funding: Self-funded.
Competing interests: The authors declare no competing interests.
Author details: During this study, Mr. Sayantan Jash was a postgraduate student of Botany with keen interest in the field of mycology and plant pathology. Now he is working on the systematics of fungi as a junior research fellow at Botanical Survey of India. Dr. Asit Baran De is a retired associate professor of Botany with a great contribution to fungal research, especially fungal taxonomy. He has described eight taxa new to science. Dr. De is one of the authors of the very popular book ‘Polyporaceae of India’.
Author contributions: All authors have contributed equally throughout the study.
Acknowledgements: The authors are
grateful to Mr. Kajal Krishna Das of the Department of Botany, Burdwan Raj
College, and Mr. Rahul Goswami for their technical
support. The authors also want to acknowledge the subject editor and all
reviewers for their critical review and helpful suggestions on this paper.
Abstract: Maravalia echinulata (Niessl ex Rabenh.) Ono has been rediscovered from West Bengal, India,
after its last report in 1931. Sections of infected host leaves were cut, stained
in cotton blue, and mounted in lactophenol. All five spore forms of this
macrocyclic autoecious rust fungus are described in
detail, with notes on its world distribution, distribution in India, and host
range. Pycnia were found to be amphigenous,
whereas aecia, uredinia, and telia
were hypophyllous. Pycnia
subcuticular, globose with flexuous hyphae belonging to type 4 of Hiratsuka & Sato (1982)
containing chains of spermatia. Aeciospores are
spiny, and catenulate, forming long chains connected by hyaline disjunctor cells. Urediniospores
pedicellate, spiny, hyaline, and thin-walled when young, but brown and
thick-walled when mature, intermingled with paraphyses. Basidium cylindric with
a pedicel, 4-celled, tetrasterigmatic; basidiospores
globose. Discrepancies in descriptions of microscopic characters by different
authors with regard to the present observations have also been discussed.
Keywords: India, macrocyclic, rediscovery, rust
fungus, Scopella echinulata,
spore forms, West Bengal.
INTRODUCTION
Uromyces echinulatus Niessl ex Rabenhorst
was first described in 1881 (Rabenhorst 1881), which
parasitized Bassia latifolia
Roxb. (= Madhuca latifolia Macbr.). It was
described based on the collection made by Dr. S. Kruz from the Royal Botanic Garden, Calcutta (now Acharya
Jagadish Chandra Bose Indian Botanic Garden, Shibpur,
Howrah, West Bengal, India). In 1939, it was transferred to the genus Scopella Mains (Mains 1939) and then in 1984 to the
genus Maravalia Arth.
(Ono 1984). Therefore, the valid name of the species is Maravalia
echinulata (Niessl ex Rabenh.)
Ono.
From literature and also from available herbarium
specimens, it is evident that the world distribution of Maravalia
echinulata is restricted to only five Asian
countries, namely India (Ono 1984), Myanmar (Thaung
2005), Nepal (IMI 189185), Pakistan (Ahmad 1956), and Sri Lanka (Spaulding
1961). Its global distribution has been presented in an outline map of the
world (Figure 1).
Butler & Bisby
(1931) mentioned that Mitra collected this fungus
from West Bengal, India. But this report was not substantiated by any reference
or herbarium specimen. It has been rediscovered from West Bengal in 2019 by the
present authors, and was found to grow on the leaves of Madhuca
latifolia. This is the report of this fungus from
the state of West Bengal about 90 years after its last report (Butler & Bisby 1931). From the literature (Mains 1939; Cummins 1950;
Thirumalachar 1950; Verma
2015), it is evident that there is much controversy regarding its characters.
In the present study, the characteristics of M.
echinulata originating from West Bengal is
described, with special emphasis on its spore types and microscopic features.
The host range and distribution of this fungus have also been discussed.
MATERIAL AND METHODS
During a survey conducted in West Bengal
(October 2019–February 2020) to record naturally occurring host plants of
different rust fungi, some infected leaves of Madhuca
latifolia were found in some localities of Bardhaman town in Purba Bardhaman District. The infected leaves of different plants
were collected separately on 20 November 2019. Thin sections of infected leaves
were cut by using sharp blades. Staining of the sections was done with cotton
blue and mounted in lactophenol. After staining, some sections were teased
apart with sharp needles and then mounted in lactophenol. Microscopic
observations were made under ×600 and ×1,500 magnifications of a Nikon Ti-U inverted microscope. To determine the range of spore
sizes, 20 spores of each type were measured. Voucher specimens were properly
processed and then deposited in the herbarium of the Department of
Microbiology, The University of Burdwan (BURD), Bardhaman,
West Bengal, India. Identification of the fungus was done based on the
descriptions provided by different literatures, including Mains (1939), Cummins
(1950), and Ono (1984). The holdings of Maravalia
echinulata were also studied from different
internationally recognized herbaria, including Royal Botanic Garden, Kew (K),
The New York Botanical Garden (NY), Meise Botanic
Garden (BR), New Zealand Fungal Herbarium (PDD), University of Michigan (MICH),
and University of Minnesota (MIN), to record its host range and distribution.
RESULTS
Field observation
The fungus was regularly seen in the field
infecting leaves of Madhuca latifolia as very small dark brown somewhat elevated
pustules. Dark pustules were surrounded by irregular pale-green to yellowish
halo zones (Image 1). The infection started in October and remained up to
February. The survey showed that all the trees in the study area were infected.
Taxonomy
Each infected leaf collected from different
trees showed all of the five spore forms, confirming the species as macrocyclic
and autoecious. The species is described based on the
present collection, which is as follows:
Maravalia echinulata (Raben.) Ono, Mycologia 76(5): 924. 1984. (Image 2 & 3)
Uromyces echinulatus Niessl ex Raben., Hedwigia 20: 149. 1881.
Scopella echinulata (Raben.) Mains [as
(Niessl) Mains], Ann. Mycol. 37: 58. 1939.
Pycnia (Image 2a) amphigenous, sub-cuticular,
lenticular to hemispheric, 40.0–50.0 × 80.0–120.0 µm; spermatiophores
producing chains of spermatia, spermatia
(Image 2b) globose to elliptical, hyaline, thin- walled, 1.5–2.0 × 1.5–1.8 µm;
flexuous hyphae long and hyaline. Aecia hypophyllous,
sub-epidermal, more or less concentrically and densely grouped with pycnia, becoming confluent, causing reddish brown spots epiphyllously, about 0.2–1.0 mm in diameter, individual sori of about 0.1–0.2 mm diameter, chocolate-brown,
pulverulent; aeciospores forming chains (Image 2c,d) connected by hyaline disjunctors, asymmetrical, triangular in face view, obovate
or oblong-elliptic in lateral view, 26.0–32.0 × 31.0–42.0 µm, hyaline and thin-
walled when young but when mature dark cinnamon to chestnut-brown, coarsely
echinulate above (Image 2e), spore wall 2.0–3.0 µm thick. Uredinia
hypophyllous, sub-epidermal, very similar to aecia
but more scattered and chestnut-brown; urediniospores
(Image 2f,g) similar to aeciospores in shape and size, sometimes containing oil
droplets; spore wall densely covered by spines but with smooth area on one side
near the base; the urediniospores borne on long
pedicels, pedicels hyaline, up to 28.0 µm long. Telia
hypophyllous sub-epidermal, more or less rounded or
ovoid, 0.2–0.5 mm in diameter, crowded in irregular groups or often scattered
singly, yellowish or pale brownish; teliospores (Image 2h,i,j) obovoid or
sub-angular, apex broadly rounded to sub-truncate, pedicellate, 22.0–27.0 ×
34.0–50.0 µm; outer spore wall hyaline, very thin, about 0.5 µm, covered with
spines, whereas inner spore wall brownish, up to 1.5 µm thick; pedicels
hyaline, up to 30.0 µm long. Teliospores intermingled with numerous paraphyses,
teliospores and paraphyses arising from highly developed hyaline to yellowish
thin- to slightly thick-walled cylindrical basal cells (Image 2k). Paraphyses
(Image 2l) cyllindric to clavate, hyaline, aseptate,
longer than pedicellate teliospores. Basidia cyllindric
with a hyaline pedicel, 4-celled, tetrasterigmatic, tetrasporous (Image 2m,n); sterigmata short, hyaline
bearing single basidiospore on each; basidiospores globose, hyaline,
thin-walled.
Mycelia hyaline, thin-walled to slightly
thick-walled, simple-septate, up to 5.0 µm wide, intercellular (Image 3a), but
some are intracellular, forming hyaline, thin-walled and bulbous haustoria
(Image 3b). Abundant gummy substances (Image 3c) were secreted by the host
plant at the post infection stage to defend itself from further invasion by
this pathogen.
Specimens examined
On leaves of Madhuca
latifolia (Roxb.) Macbr., Leg. A.B. De & S. Jash;
20 November 2019; Bardhaman (23.233 0N,
87.863 0E, 30 m altitude), Purba Bardhaman, West Bengal, India--—BURD MCBH1939, BURD
MCBH1940, BURD MCBH1941.
Collections: INDIA: Bihar – Pusa, 21 December 1914,
leg. P.C. Kar (PDD 14053); locality not mentioned, 05 February 1986,
leg. J.N. Sinha (IMI 314115). Gujarat
– locality not mentioned, March 1984, leg. not mentioned (IMI 284368). Karnataka – Bangalore, 1 March 1946,
leg. M.J. Thirumalachar (WIS-f-0080583); 3 August
1946, leg. M.J. Thirumalachar (MICH 295078). Madhya Pradesh – locality not mentioned,
23 April 1980, leg. V.R. Neelay (IMI 248182); 21
October 1986, leg. K.S. Khan (IMI 311371). Maharashtra
– Palghar, 22 February 1912, leg. H.M. Chebber (MICH
295080); Poona, Maharashtra Assoc. for Cult. Sci., 19 March 1965, leg. M.N. Kamat (IMI 112556); Sirsi,
September 1912, leg. G.S. Kulkarni (PDD 9797). Uttar
Pradesh – Gorakhpur, 23 February 1984, leg. P. Narayan (IMI 283997); 22
October 1984, leg. not mentioned (IMI 290974); locality not mentioned, 05 March
1980, leg. R.P. Verma (IMI 246910). West Bengal – Bardhaman,
20 November 2019, leg. A.B. De & S. Jash (BUR
MCBH1939, BUR MCBH1940, BUR MCBH1941); Calcutta, H. Botanico,
– s.d., leg. Dr. S. Kruz 3551 (K-M000187873, K-M000187874, NY 00046133, NY
00046134, UC 1886570); s.d., leg. G. Rabenhorst s.n.
(BR5020078034467).
MYANMAR: Mandalay, 28 November
1974, leg. M.M. Thaung (LAM 220082, UC 1886570); s.d., leg. M.M. Thaung (IMI
161589).
NEPAL: locality not mentioned, 18th October 1974, leg. K.L. Manandhar (IMI 189185, IMI 189192).
SRI LANKA: Peradeniya, 16 June 1908,
leg. T. Petch (K-M000187875); August 1912, leg. T. Petch (BR5020078035471,
K-M000187876, MICH 295079, MICH 296112, MIN 1228326, MIN 1228327, MIN 1267657,
NY 03432410, WIS-f-0085023); locality not mentioned, s.d.,
leg. T. Ptech (IMI 67265).
DISCUSSION
Although Maravalia
echinulata (Niessl ex Rabenh.)
Ono has been found to cause rust disease in five Asian countries (India, Myanmar, Nepal,
Pakistan and Sri Lanka), it mostly affects its hosts growing in India except
its northern and northeastern parts (Figure 2).
Different localities of its occurrence in India are presented in Table 1 along
with its hosts recorded by different workers.
From Table 1 it is evident that Maravalia echinulata
(Niessl ex Rabenh.) Ono mostly grows on two species of Madhuca
Ham. ex Gmel., namely Madhuca
latifolia (Roxb.) Macbr. and Madhuca longifolia (Koenig ex L.) Macbr.
Rabenhorst (1881) described the species based on a
specimen infecting the leaves of Bassia latifolia Roxb. Several
authors, including Spaulding (1961), Sathe (1969),
Narayan & Kamal (1985), and Bilgrami et al.
(1991) reported Madhuca indica
Gmel. as its host. But Bassia
latifolia and Madhuca
indica are just synonymous with Madhuca latifolia.
Mains (1939) and Sathe (1969) mentioned the
occurrence of this rust fungus on Bassia longifolia, which is currently accepted as Madhuca longifolia.
Thirumalachar (1950) mentioned Bassia
bourdilli [correct name is Madhuca
bourdillonii (Gamble) H.J.Lam]
as a new host collected from Mysore (now Karnataka, India). In 1986, Dr. C.R. Patil collected the rust
fungi on leaves of Sideroxylon tomentosum Roxb. from Amboli (Maharashtra) and M.S. Patil
reported it as a new host of Maravalia echinulata (Patil 1991). So,
this fungus has, so far, been found to parasitize only four host species,
namely, M. bourdillonii, M. latifolia, M. longifolia,
and S. tomentosum. From all these reports, it
can be stated that the host range of this fungus is strictly restricted to the angiospermic family Sapotaceae to
date.
As regards characters of its different spore
forms, there are great controversies. According to Thirumalachar
(1950), its pycnium is conoid without conspicuous ostiolar paraphyses. But from the present observation, it
is evident that the pycnium of M. echinulata is globose with flexuous hyphae and,
therefore, belongs to type 4 of Hiratsuka & Sato (1982), not type 5 or 7.
Aeciospores were stated to be pedicellate and
uredinoid type (Thirumalachar
1950), but in our observation they are catenulate, forming long chains
connected by hyaline disjunctor cells.
Teliospores have been stated to be hyaline
and smooth (Mains 1939; Cummins 1950), but very thin-walled according to Mains
(1939) and slightly thick-walled according to Cummins (1950). Mains (1939) and
Cummins (1940) also found that teliospores of this species arise from highly
developed cylindric basal cells. Similar observations were made by the authors,
who also observed spiny teliospores as hyaline and thin-walled when young, but
brown and thick-walled when mature. Similar types of brown, thick-walled
teliospores with a spiny outer wall have been observed by Rabenhorst
(1881) and Pathak et al. (2015).
Teliospores are intermingled with numerous
paraphyses, which are cylindrical to clavate, hyaline, thin-walled and much
longer than pedicillate teliospores. Although Thaung (2005) has mentioned numerous fine paraphyses in Maravalia echinulata,
most of the authors had probably ignored this character in their description.
A gap in the secondary wall above the hilum
of urediniospores and teliospores has been observed,
which indicates the existence of continuous cytoplasmic communication of these
spores with their pedicels through the passage in the secondary wall.
Spines of aeciospores, urediniospores
and teliospores are formed in the centre of lumina
bordered by muri. These spores of Maravalia
echinulata, therefore, may be better described as
reticulate-spinulose rather than just reticulate or
just spinulose.
Ono (1984) reported that each metabasidium forms one short, apical sterigma, and from
this sterigma, globose to subglobose basidiospores
are formed successively. Thus, the basidiospores occur in clumps at the apex of
the metabasidium. Thirumalachar
(1950) had reported another type of metabasidium
divided into four cells and arranged in
a linear fashion. No sterigmata was reported. Moreover, the spore formation was
described by directly rounding off of basidial cells.
In the present observation, basidium was found with a linear row of four
cells. Typical short hyaline sterigmata
were found to develop from each cell bearing basidiospore on each. According to
Ono (1984), the basidiospore of the terminal cell of basidium is the largest
one and becomes successively smaller towards the basal cell.
Table 1.
Different localities and hosts of Maravalia
echinulata growing in India.
|
State |
Locality |
Host |
References |
|
Andhra Pradesh |
Amaravati |
Madhuca longifolia |
Hosagoudar 2013 |
|
Cuddapah |
Madhuca latifolia |
Cummins 1950 |
|
|
Penagaluru |
Madhuca latifolia |
Cummins 1950 |
|
|
Bihar |
Pusa |
Madhuca latifolia |
Butler & Bisby 1931 |
|
Gujarat |
Anand |
Madhuca latifolia |
Jamaluddin et al.
2004 |
|
Karnataka |
Bangalore |
Madhuca latifolia and Madhuca
bourdillonii |
Thirumalachar 1950 |
|
Kerala |
Palghat |
Madhuca latifolia |
Bilgrami et al. 1991 |
|
Madhya Pradesh |
Indore |
Madhuca latifolia |
Pathak et al. 2015 |
|
Jabalpur |
Madhuca latifolia |
Verma 2015 |
|
|
Maharashtra |
Amboli |
Sideroxylon tomentosum |
Patil 1991 |
|
Jalgaon |
Madhuca latifolia |
Firdousi 2020 |
|
|
Mumbai |
Madhuca longifolia |
Sathe 1969 |
|
|
Nagpur |
Madhuca latifolia |
Parandekar 1964 |
|
|
Palghar |
Madhuca latifolia |
MICH 295080 |
|
|
Poona |
Madhuca latifolia and Madhuca
longifolia |
IMI 112556, Sathe 1969 |
|
|
Sirsi |
Madhuca latifolia |
PDD 9797 |
|
|
Uttar Pradesh |
Benaras |
Madhuca latifolia |
Payak 1949 |
|
Gonda |
Madhuca latifolia |
Narayan & Kamal
1985 |
|
|
Gorakhpur |
Madhuca latifolia |
IMI 283997, IMI
290974 |
|
|
West Bengal |
Bardhaman |
Madhuca latifolia |
Present study |
|
Howrah |
Madhuca latifolia |
Rabenhorst 1881, Mains 1939,
Ono 1984 |
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