Alternaria telliensis, a new causal agent of cabbage leaf spot disease in Iran

Document Type : Short Article


1 Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

2 Department of Plant Protection, Faculty of Agriculture and Natural Resources, Urmia University, Urmia, Iran


In order to study of cabbage leaf spot disease in Damavand region, Tehran province, Iran, symptomatic cabbage leaves (Brassica oleracea var. capitata) were collected during the late summer and fall of 2017. Twenty-one isolates with the main characteristics of the genus Alternaria were isolated from lesions on the cabbage leaves. Based on morphological characteristics and phylogenetic analysis using multi-gene sequences, they were identified as Alternaria telliensis. Pathogenicity tests were conducted on cabbage leaves under greenhouse conditions and characteristic lesions were formed on inoculated leaves. Re-isolation of the inoculated fungus from the treated leaves confirmed Koch’s postulates. Based on the available information, this is the first occurrence of A. telliensis as a new species and pathogen to cabbage plants in Iran.




Cabbage or headed cabbage (Brassica oleracea var. capitata), a member of Brassicaceae family, is an economically important leafy biennial vegetable crop grown worldwide as an annual crop for head harvest. Cabbages are used fresh in salads, as pickles, stir-fried and a fermented product (Wouters et al. 2013, Šamec et al. 2017) with antioxidant, antibacterial, anti-inflammatory, anti-obesity, anti-cancer, gastrointestinal and health-promoting effects (Podȿedek et al. 2006, Singh et al. 2006, Rokayya et al. 2013, Park et al. 2014, Lee et al. 2018). In 2017, the global production of cabbages and other related brassicas was 71.2 million tonnes (FAO 2018). In Iran, cabbage is cultivated on 6979 ha with a total annual production of 306781 tonnes (FAO 2018). Tehran province is one of the main cabbages-growing areas in Iran (Koocheki et al. 2013).

Cabbages and other cruciferous crops are severely affected by different pathogens, causing economic losses in yield and crop quality. Leaf spot diseases caused by Alternaria spp. are the most prevalent and destructive diseases of these plants worldwide as well as in Iran (Humpherson-Jones 1992, Nowicki et al. 2012, Kumar et al. 2014, Rahimloo & Ghosta 2015). These diseases are characterized by small, dark specks that enlarge into relatively large, circular, brown to black lesions with concentric rings and are sometimes surrounded by chlorotic halos (Koike et al. 2007, Siciliano et al. 2017). Historically, Alternaria brassicicola and A. brassicae have been considered as the main causative agents of dark leaf spot disease in cruciferous plants (Maude & Humpherson-Jones 1980, Rotem 1994, Pedras et al. 2009, Michereff et al. 2012). Seeds, seedlings and pods are also damaged by these pathogens (Köhl et al. 2010). In a monographic study on Alternaria diseases of crucifers, four species i.e., A. alternata, A. brassicae, A. brassicicola and A. japonica (as A. raphani) were reported to cause heavy losses in the crops (Verma & Saharan 1994). All four Alternaria species have been reported to be seed-borne and were detected from all parts of infected seeds (Saharan et al. 2016).

In a study on Alternaria species associated with cabbage leaf spot disease in Urmia, Iran, eight species were identified based only on morphological characteristics (Rahimloo & Ghosta 2015). In the most recent study on the incidence and diversity of Alternaria species associated with leaf spot disease of Brassica napus, 12 species were identified indicating high diversity of Alternaria species associated with the disease (Al-Lami et al. 2019). In the present study, a set of Alternaria isolates was isolated from cabbage plants representing leaf spot symptoms. Based on the combination of morphological characteristics and molecular data obtained from four genomic loci (ITS-rDNA, glyceraldehyde-3- phosphate dehydrogenase, the second-largest subunit of RNA Polymerase II and translation elongation factor 1-alpha), the isolates grouped well in Alternaria section Japonicae in close affinity with A. telliensis N. Bessadat, Ayad & P. Simoneau. Pathogenicity tests confirmed the pathogenic nature of the isolates on cabbage leaves. To our knowledge, this is the first occurrence of A. telliensis and its pathogenicity on cabbage plants in Iran.




Sample collection and fungal isolation

Cabbage (Brassica oleracea var. capitata) leaves with necrotic leaf spot symptoms were collected randomly from different cabbage growing fields in Damavand city, Tehran province, Iran during the late summer and fall of 2017. Leaf samples were placed in new separate paper bags, transferred to the laboratory and processed immediately. Symptomatic leaf samples were washed gently under running tap water and surface disinfested by submerging in 70% ethanol for 2 min and washed again with sterile distilled water. Small pieces at the interfaces of healthy and necrotic areas were excised and plated directly onto potato dextrose agar (PDA, Merck, 39 g/L) medium. Also, some of the leaves were kept in moist chambers. The samples were examined at 48 h intervals for fungal growth, and the growing fungi were transferred onto new PDA Petri dishes. Purification of the fungi was done based on the single spore method. Pure cultures were grown on potato carrot agar slants (PCA, 20g carrot, 20g white potato, 20g agar in 1L distilled water) supplemented with twice-autoclaved pieces of filter papers and kept at 4°C.


Morphological characterization

Morphological characteristics were examined according to Simmons (2007). Briefly, recovered isolates were cultured on PCA medium and incubated at 24 ± 1 °C with 8/16 h light/dark photoperiod under cool white fluorescent light without humidity control. Sporulation pattern was observed after 5–7 days at 64× magnification using a stereo-microscope. Microscopic slides were prepared using transparent clear tape and 25% lactic acid solution as mounting fluid (Schubert et al. 2007). Micro-morphological characteristics including dimensions, septation, color and surface ornamentation were recorded for 50 conidiophores and conidia. Colony characteristics were observed on PCA, PDA, hay decoction agar (HA) and V8 juice agar (V8-A) culture media after 7 days (Simmons 2007). The living cultures of examined isolates were deposited in the fungal culture collection of Agricultural Biotechnology Research Institute of Iran (ABRIICC) and additional isolates were kept in the fungal culture collection of Urmia University (FCCUU).


DNA extraction, amplification and sequencing

Freshly harvested mycelium from 5-day-old cultures grown in potato dextrose broth (PDB) was used for DNA isolation. Total genomic DNA was extracted using the Exgene™ Cell SV mini kit (GeneAll Biotechnology Co., Korea) following the manufacturer’s instruction. Polymerase chain reaction amplification of ITS-rDNA region and parts of TEF1-α, RPB2 and GAPDH gene regions were performed using primer pairs ITS1/ITS4 (White et al. 1990) for ITS-rDNA region, EF1-728F/EF1-986R (Carbone and Kohn 1999) for TEF1-α, fRPB2-5F/fRPB2-7cR (Liu et al. 1999; Sung et al. 2007) for RPB2 and gpd1/gpd2 (Berbee et al. 1999) for GAPDH. The thermal conditions for PCR amplification and the reaction mixtures were the same as Hashemlou et al. (2020). PCR products were cleaned up and sequenced by Microsynth DNA company (Balgach, Switzerland).


Phylogenetic analysis

Multiple sequence alignments were produced using the type or ex-type strains sequences retrieved from GenBank according to Woudenberg et al. (2013, 2015), Lawrence et al. (2014), Deng et al. (2018), Poursafar et al. (2018, 2019) and Bessadat et al. (2020) (Table 1), and aligned with MAFFT online service ( Concatenated sequence dataset (ITS-rDNA + GAPDH + RPB2 + TEF1-α) was produced and proofed in Mesquite v. 2.74 (Maddison and Maddison 2010). Maximum likelihood analysis (ML) was performed on a concatenated dataset in RAxML-HPC BlackBox v. 8.2.12 (Stamatakis, 2014) through the CIPRES Science Gateway v 3.3 (Miller et al. 2010) using the GTRGAMMA+I as substitution model. The resultant phylogenetic tree was observed in FigTree v. 1.4.4 (Rambaut 2019). Sequences of Stemphylium vesicarium (formerly as S. herbarum) CBS 191.86 and S. botryosum strain CBS 714.68 served as the outgroup taxa.


Pathogenicity test

The healthy plants of white cabbage cv. Glory of Enkhuizen without any leaf symptoms were chosen for fungal inoculation. Cabbage leaves were firstly cleaned with moist cotton balls, then were sprayed with 70% ethanol and cleaned again with sterile distilled water. Mycelial plugs (5 mm diameter) containing fungal spores were taken from the edges of actively growing colonies (5-day-old) on PDA plates and placed upside down on cabbage leaves, both with and without small wounding caused by sterile needle. In the controls, only sterile agar plugs (without fungal mycelia or spores) were used. In addition, pathogenicity tests were done using the spore suspension (106 spores/mL) prepared from PCA cultures. The inoculated plants were covered with plastic bags for 48 h in order to maintain high humidity. Disease symptoms were evaluated 10 days after inoculation. Four replicates were used for each isolate and all the experiments were repeated once. Re-isolation of the inoculated fungi was made from the necrotic lesions formed on the inoculated leaves after surface disinfestation and morphologically compared to the inoculated isolates to fulfill Koch’s postulates.



Table 1. Strains used for phylogenetic analysis in this study. Newly generated sequences are shown in bold.


Collection numbers


Host/ substrate

GenBank accession numbers






Alternaria anigozanthi

CBS 121920


Anigozanthus sp.





Woudenberg et al. 2013

A. armoraciae

CBS 118702


Armoracia rusticana





Woudenberg et al. 2013

A. avenicola

CBS 121459


Avena sp.





Woudenberg et al. 2013

A. botryospora

CBS 478.90


Leptinella dioica





Woudenberg et al. 2013

A. brassicae

CBS 116528


Brassica oleracea





Woudenberg et al. 2013

A. brassicae-pekinensis

CBS 121493


Brassica pekinensis





Woudenberg et al. 2013

A. brassicicola

CBS 118699


Brassica oleracea





Woudenberg et al. 2013

A. ershadii



Triticum aestivum





Poursafar et al. 2019

A. ershadii



Triticum aestivum





Poursafar et al. 2019

A. kordkuyana

IRAN 2764C


Triticum aestivum





Poursafar et al. 2018

A. rosae

EGS 41-30


Rosa rubiginosa





Lawrence et al. 2014

A. brassicinae (A. alternata)

CBS 118811


Brassica oleracea





Woudenberg et al. 2015

A. broccoli-italicae

EGS 40-134


Br. oleracea var. italica





Deng et al. 2018

A. burnsii

CBS 107.38


Cuminum cyminum





Woudenberg et al. 2015

A. caricis

CBS 480.90


Carex hoodii





Woudenberg et al. 2013

A. cetera

CBS 121340


Elymus scabrus





Woudenberg et al. 2013

A. cheiranthi

CBS 109384


Cheiranthus cheiri





Woudenberg et al. 2013

A. chlamydospora

CBS 491.72







Woudenberg et al. 2013

A. consortialis

CBS 104.31







Woudenberg et al. 2013

A. dianthicola

CBS 116491


Dianthus × allwoodii





Woudenberg et al. 2013

A. ethzedia

CBS 197.86


Brassica napus





Woudenberg et al. 2013

A. japonica

CBS 118390


Brassica chinensis





Woudenberg et al. 2013

A. leucanthemi

CBS 421.65


Chrysanthemum maximum





Woudenberg et al. 2013

A. mimicula

CBS 118696


Lycopersicon esculentum





Woudenberg et al. 2013

A. mouchaccae

CBS 119671







Woudenberg et al. 2013

A. nepalensis

CBS 118700


Brassica sp.





Woudenberg et al. 2013

A. panax

CBS 482.81


Aralia racemosa





Woudenberg et al. 2013

A. telliensis



Solanum tuberosum





Bessadat et al. 2020

A. telliensis



Lycopersicum esculentum





Bessadat et al. 2020

A. telliensis



Lycopersicum esculentum





Bessadat et al. 2020

A. telliensis



Br. oleracea var. capitata





This study

A. telliensis



B. oleracea var. capitata





This study

A. petroselini

CBS 112.41


Petroselinum sativum





Woudenberg et al. 2013

A. proteae

CBS 475.90


Protea sp.





Woudenberg et al. 2013

A. radicina

CBS 245.67


Daucus carota





Woudenberg et al. 2013

A. resedae (Alternaria sp.)

CBS 115.44


Reseda odorata





Woudenberg et al. 2013

A. scirpicola

CBS 481.90


Scirpus sp.





Woudenberg et al. 2013

A. subcucurbitae

CBS 121491


Chenopodium glaucum





Woudenberg et al. 2013

A. triglochinicola

CBS 119676


Triglochin procera





Woudenberg et al. 2013

Stemphylium botryosum

CBS 714.68


Medicago sativa





Woudenberg et al. 2013

S. vesicarium

CBS 191.86


Medicago sativa





Woudenberg et al. 2013





Morphological characterization

Twenty-one Alternaria isolates with similar morphological characteristics were recovered from collected samples from different fields in Damavand city, Tehran province. Based on morphological characteristics, they were identified as A. telliensis.


Phylogenetic analysis

PCR amplifications produced band sizes approximately 480 bp for ITS-rDNA, 531 bp for GAPDH, 909 bp for RPB2 and 224 bp for TEF-1α. Sequence combination of four loci for a total of 41 fungal strains including ingroup and outgroup taxa contained 1919-characters. The best scoring RaxML tree with the final ML optimization likelihood value of -11504.616823 (ln) is selected to demonstrate the phylogenetic relationships among the studied strains (Fig. 1). The results of the phylogenetic analysis revealed that the two studied Iranian Alternaria strains were closely related to the members of Alternaria section Japonicae with the nodal bootstrap support of 100% and clustered well in the subclade along with the strains of A. telliensis (Fig. 1), confirmed morphological identification.


Alternaria telliensis N. Bessadat, D. Ayad & P. Simoneau, Phytotaxa 440 (2): 92. 2020

Colonies on PCA reached 60 mm diam after 7 days, greenish olivaceous at the center and olivaceous grey at margins, with four well-defined concentric rings of growth and sporulation; 64 mm diam on PDA, smoke gray to whitish-grey; 54 mm diam on HA, hazel to brown and 65 mm diam on V-8 agar, greyish sepia to olivaceous. White aerial hyphae are present at the colony center of all media (Fig. 2a–c). Sporulation abundant after 4 days on PCA, HA and V8-A. On PCA, conidiophores arise directly from hyphae growing on agar surface or from aerial hyphae, mostly simple with an apical conidiogenous locus, sometimes with 2–3 geniculations, 20–90 × 3.5–5 µm; conidia mostly solitary, sometimes in chains of 2–3(–4) spores. Juvenile conidia are ovoid to ellipsoid, pale brown to brown, distinctly constricted at transverse septa, beakless, with 1–3 transverse septa and 0–1(–2) longitudinal septa, 17–40 × 10–17.5 µm. Mature conidia are long ovoid to cylindrical, brown to dark brown, outer wall punctate to verrucose, distinctly constricted at the transverse septa, 3–4(–5) transverse septa, 1–3 oblique septa and 1–3 longitudinal septa in the broadest transverse divisions, 40–65 × 18–43 µm, septa darker black-brown, 3–5 µm wide. In some of the conidia, body cells are enlarged and deformed the spore body. The apical secondary conidiophores that initiate chain formation are as single cells, slightly paler than that of the spore body, 5–8 × 5 µm, or a well-differentiated apical outgrowth up to ca 17–48 × 5 µm. A distinct feature of the studied isolates is the transformation of all cells of some of the conidiophores into chlamydospore-like structures, 8.5–12.5 × 5.5–10 µm (Fig. 3a–z). The sexual form was not formed.

Specimens examined. IRAN, Tehran province, Damavand City, on cabbage leaf (Brassica oleracea var. capitata) with leaf spot symptoms, Oct. 6, 2017. A. Poursafar, ABRIICC 10148, GenBank accession numbers : MK660798, ITS ; MK660796, GAPDH ; MK660800, RPB2 ; MK660802, TEF1-α ; Sep. 25, 2017. A. Poursafar, ABRIICC 10150, GenBank accession numbers : MK660799, ITS ; MK660797, GAPDH ; MK660801, RPB2 ; MK660803, TEF1-α.


Note. Alternaria telliensis is phylogenetically closely related to A. japonica and A. nepalensis in the Alternaria section Japonicae, but in a well-supported and distinct subclade. Alternaria japonica can easily be differentiated from A. telliensis by the production of distinctive chains of dark, thick-walled and often ornamented cells (micro-chlamydospores) in surface and subsurface hyphae and conidia with a smooth outer wall (Simmons 2007, Bessadat et al. 2020). Also, A. nepalensis can be differentiated from A. telliensis based on conidia with a smooth outer wall and with no formation of chlamydospores (Simmons 2007, Bessadat et al. 2020).


Pathogenicity test

All Alternaria isolates were used in pathogenicity experiments, and they produced conspicuous lesions on white cabbage leaves similar to those of naturally occurred under field conditions (Fig. 4a–e). No symptoms were formed on the control plants (Fig. 4f). Re-isolation of the inoculated fungus confirmed Koch’s postulates.


Fig. 1. Phylogenetic tree generated from maximum likelihood (ML) analysis based on the combined dataset of ITS, TEF1-α, GAPDH and RPB2 sequences of 39 Alternaria strains. The RAxML maximum likelihood bootstrap values (>50%) are given at the nodes. The tree was rooted to Stemphylium vesicarium strain CBS 191.86 and S. botryosum strain CBS 714.68. The bar indicates the number of substitutions per position. T: Ex-type strain. R: Representative strain.

Fig. 2. Alternaria telliensis (ABRIICC 10148). Colony after 7 d on: a. PCA; b. PDA; c. V8-A; d. HA.

Fig. 3. Alternaria telliensis (ABRIICC 10148). a. Sporulation pattern on PCA; b–c. Primary conidiophores; d–g. Chlamydospore-like structures formed from the transformation of primary conidiophore cells; h–z. Conidia. Bars: 20 µm.

Fig. 4. a-e. Symptoms formed on cabbage leaves 10 days post-inoculation with agar plugs containing fungal mycelia and spores in greenhouse conditions; f. Control treatment.



Cabbage, because of its high nutritional value and high levels of anthocyanins and flavonoids and antimicrobial, antioxidant, anticancer and anti-inflammatory properties is one of the most commonly grown vegetables all around the world. It has been widely used as herbal medicine to treat different disorders (Rokkaya et al. 2013, Sarandy et al. 2015, Lee et al. 2018). Different biotic and abiotic stresses affect negatively plant growth and yield. Leaf spot diseases caused by different species of Alternaria,are among the most common and destructive diseases of cabbage and other cruciferous crops (Maude & Humpherson-Jones 1980, Yu et al. 1991, Cucuzza et al. 1994; Reis & Boiteux 2010). Although different species of Alternaria have been reported as causal agents of the disease (Verma & Saharan 1994, Simmons 2007, Rahimloo & Ghosta 2015, Siciliano et al. 2017), A. brassicicola and A. brassicae have commonly been recognized as the most prevalent species (Pedras et al. 2009, Köhl et al. 2010).

A review of available literature reveals the report of 17 Alternaria morpho-species associated with leaf spot disease of cabbage and other cruciferous plants around the world (Peruch et al. 2006, Aneja et al. 2014, Rahimloo & Ghosta 2015, Al-Lami et al. 2019). Alternaria alternata, A. arborescens, A. destruens, A. malvae, A. perangusta, A. tenuissima, A. turkisafria and A. vaccini which were originally classified as small-spored Alternaria, are characterized by the production of relatively long to long, simple or branched chains of conidia and short to relatively long primary and secondary conidiophores (Simmons 2007).

In a recent comprehensive study using molecular and morphological characters, all these species (except for A. arborescens and A. arbusti) were synonymized under the single name A. alternata andplaced in Alternaria section Alternaria. Alternaria arborescens and A. arbusti stillexist as valid names within the section Alternaria (Woudenberg et al. 2015). Alternaria telliensis can easily be differentiated from species in section Alternaria based on its three-dimensional pattern of conidial chains as well as their morphologies. Alternaria brassicicola (Alternaria section Brassicicola), another important species reported from cabbage and other cruciferous plants, is characterized by the production of long branched chains of small, narrow conidia (30–60 × 6–17 µm) with few longitudinal septa (0–2) and formation of loose tufts of 50–60 or more conidia. Alternaria species reported on cabbage plants from Alternaria section Infectoriae such as A. ethzedia and A. broccoli-italicae, are characterized by the production of branched chains of small conidia, with more prominent secondary conidiophores and tufts of more than 50 conidia (Simmons 2007).

Alternaria brassicae (a monotypic lineage which is not placed in any section yet) has been classified as large-spored Alternaria (spore length >100 µm) (Simmons 2007), is characterized by the production of solitary or more frequently short chains of conidia (2–3), long secondary conidiophores and relatively large conidia [60–200(–250) × 13–35(–40) µm] with 3–12 transverse septa. A large percentage of conidia have no longitudinal septa, but in some, 3–8 longitudinal septa are present. Currently, three species viz. A. japonica and A. nepalensis and A. telliensis are placed in Alternaria section Japonicae. Our morphological and multi-gene phylogenetic analysis strongly confirm the placement of the newly recovered isolates within this section. Due to the widespread occurrence of the disease symptoms under field conditions in the studied area and the results of pathogenicity tests, it can be claimed that A. telliensis is a potential leaf spot pathogen in cabbage plantations. Alternaris telliensis was originally isolated and described from the two solanaceous plants, Lycopersicum esculentum and Solanum tuberosum, showing leaf spot symptoms (Bessadat et al. 2020). Although in their pathogenicity tests, the isolates of this species were weakly pathogenic on their natural hosts, they were identified as highly virulent on cabbage (Brassica oleracea), radish (Raphanus sativus) and turnip (Brassica rapa) plants in laboratory conditions.

Here we report cabbage as a natural host of A. telliensis. Previous studies indicated that Alternaria species infecting cabbage plants are all transmitted via infected seeds (Saharan et al. 2016), so additional studies are needed to explore seed transmissibility of this species and its pathogenicity on different cruciferous crops and weeds. Furthermore, since cabbage and other cruciferous plants are grown annually in different regions in Iran with diverse climatic conditions, more studies should be done in different locations to determine species diversity and richness for carefully planning efficient disease management programs.



The authors would like to acknowledge Mahdieh Mousavi (Ph.D. student, Department of Plant Protection, Faculty of Agriculture and Natural Resources, Urmia University, Iran) for her kind help and useful recommendations.



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