Identification and pathogenicity of fungal species associated with grapevine trunk diseases in Khorasan-Razavi province, Iran

Document Type : Original Article

Authors

1 Department of Plant Protection, Faculty of Agronomic Sciences, Sari Agricultural Sciences and Natural Resources University, Sari, Iran

2 Department of Plant Protection, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran

Abstract

Grapevine trunk diseases (GTDs)are known as the most important factors in crop reduction and cause considerable economic problems in grapevines worldwide. During 2016 to 2018, several field surveys were conducted on numerous vineyards in Khorasan-Razavi province to study fungal species associated with grapevine trunk diseases. In this study, samples were collected from trunk and branches of trees showing yellowing, stunted growth, dieback and wood discoloration in cross sections. In this study, 258 fungal isolates were obtained and identified based on morphological characteristics and comparison of DNA sequence data (ITS-rDNA region and a part of β-tubulin gene). These isolates were identified as Phaeoacremonium minimum (75 isolates), P. parasiticum (19 isolates), P. iranianum (52 isolates), P. tuscanum (8 isolates), Fomitiporia mediterranea (56 isolates) and Seimatosporium vitis (48 isolates). Pathogenicity of the selected isolates was verified by inoculation of potted grapevines shoots under greenhouse conditions. Based on the mean length of wood discoloration in the wood, P. minimum and F. mediterranea were the most and least virulent species, respectively. Our findings indicated that known fungal trunk pathogens such as Phaeoacremonium species and F. mediterranea occur on grapevine in Khorasan-Razavi province. This study is the first report of S. vitis associated with grapevine decline in Iran.

Keywords

Full Text

INTRODUCTION

Vitis L., with more than 100 species is one of the oldest and most important fruit crop genera all over the world (Mullins et al. 1992). Vitis vinifera L. (grapevine) is among the most widely cultivated species in Iran and Khorasan province is also considered as one of the most important grape growing areas in the country. In the past few decades, several studies have shown that more than 30 fungal diseases can affect the health of grapevines worldwide (Wilcox et al. 2015). However, in recent years, great emphasis has been laid on grapevine trunk diseases (GTDs) in Iran (Arabnezhad & Mohammadi, 2012, Arabnezhad et al. 2013, Mohammadi & Banihashemi 2007, Mohammadi et al. 2013a, b, Narmani & Arzanlou, 2017, Abed-Ashtiani et al. 2019) as well as many other countries in the world (Larignon & Dubos 1997, Mugnai et al. 1999, Armengol et al. 2001, Gramaje & Di Marco 2015). Currently, GTDs are known as one of the most destructive fungal diseases and serious threats to the future economic sustainability of viticulture in the world (Bertsch et al. 2013, Gramaje et al. 2016, 2018, Guerin-Dubrana et al. 2019). The term GTDs was first introduced by Chiarappa for a range of leaf disease symptoms and necrosis in the wood tissues of affected trees (Gramaje et al. 2018). GTDs are caused by different groups of fungal pathogens (Bruez et al. 2016). Based on the available references, more than 138 species of 35 different fungal genera have been isolated and reported from a grapevine showing trunk diseases worldwide (Gramaje et al. 2018, Raimondo et al. 2019). Several fungal species belonging to the family Botryosphaeriaceae (Van Niekerk et al. 2004, Úrbez-Torres 2011, Xie et al. 2010, Yang et al. 2017), Togniniaceae (Edwards & Pascoe 2004, Mostert et al. 2006, Gramaje et al. 2011, Raimondo et al. 2014, Gramaje & Di Marco 2015, Da Silva et al. 2017), Diatrypaceae (Dumot et al. 2004, Butterworth et al. 2005, Trouillas & Gubler, 2010, Trouillas et al. 2010, Sosnowski et al. 2016, Pitt et al. 2013), Phaeomoniella (Pa.) chlamydospora (Edwards & Pascoe 2004, Gramaje et al. 2009b, Fleurat-Lessard et al. 2010), Phomopsis spp. (Phillips 2000, Baumgartner et al. 2013, Úrbez-Torres et al. 2013, Senanayake et al. 2015), Pleurostoma (Pl.) richardsiae (Carlucci et al. 2015, Pintos Varela et al. 2016), Cadophora spp. (Gramaje et al. 2011, Travadon et al. 2015) and basidiomycetous species (Fischer 2002, Cloete et al. 2015) have been reported as components of the grapevine trunk-disease complex, although pathogenicity tests have not been completed for all of these taxa. Several studies conducted in Iran have also shown that grapevine cultivars can be affected by various fungal trunk pathogens including Botryosphaeriaceae, Pa. chlamydospora, Phaeoacremonium species, Pl. richardsiae, Cylindrocarpon liriodendri and basidiomycetous species (Karimi et al. 2001, Mohammadi & Banihashemi 2007, Mohammadi et al. 2009, Mohammadi 2012, Arabnezhad et al, 2013, Arzanlou et al. 2013, Mohammadi et al. 2013a, b). Although various fungal species have been isolated and reported from grapevines in Iran, the identity of the fungal trunk pathogens on this host plant have not yet been investigated in Khorasan-Razavi province. During the survey carried out on some vineyards in Khorasan-Razavi province, 258 fungal isolates were obtained from grapevines showing trunk disease symptoms. The aim of this study was to identify these isolates and to evaluate their pathogenicity on the grapevine.

 

MATERIALS AND METHODS

 

Field survey, sampling and fungal isolation

In order to study fungi associated with grapevine trunk diseases, several field surveys were conducted on various vineyards in Khorasan-Razavi province (northeastern Iran) between May 2016 and August 2018. Samples were collected from trunk and branches of affected trees showing disease symptoms, including yellowing, stunted growth, dieback and internal wood lesions in cross sections. Fungal isolation was conducted from each collected sample. Small pieces of tissue (about 5 × 5 mm in size) were cut from the margin between necrotic and apparently healthy wood tissues, surface-disinfected for 2 min in a 0.5 % sodium hypochlorite solution, washed twice with sterile distilled water and then cultures on potato dextrose agar plates (PDA, Merck, Darmstadt, Germany) supplemented with 100 mg l-1 streptomycin sulfate (PDAS). All the plates were incubated at 25 °C and the emerging colonies were transferred to fresh PDA. Fungal colonies were purified using single-spore or hyphal-tipping methods.

 

Morphological identification

All fungal isolates were initially grouped by comparing the main morphological characteristics and cultural appearance. Cultures characters and pigment production on PDA, malt extract agar (MEA, 2% malt extract, Merck, Darmstadt, Germany) and oatmeal agar (OA, 60 g oatmeal, 12.5 g agar, Difco, France) as well as the main microscopic structures including conidiophore morphology, size of hyphal warts, phialide type and shape and conidial size and shape were used to conduct morphological identification of Phaeoacremonium isolates (Crous et al. 1996, Mostert et al. 2006, Spies et al. 2018). Seimatosporium isolates were identified based on colony and cultural characteristics on PDA and pycnidia and conidial morphology as described by Senanayake et al (2015). Morphological and microscopic analyses of mycelial culture of basidiomycetous isolates were studied according to Fischer (2002). For these isolates, general colony characteristics on cultures including shape, color, surface aspect and reverse were evaluated and recorded.

 

DNA extraction, amplification and sequencing

Representative fungal isolates of each group were selected for molecular identification. These isolates were grown on PDA and incubated in the dark at 25 °C. Produced mycelia and conidia were scraped with a sterile scalpel from the surface of 10-15-day-old cultures and then total genomic DNA was extracted using CTAB method (Doyle & Doyle 1987). All samples were incubated at −20 °C until conducting of PCR amplification. The internal transcribed spacer 1 and 2 including the intervening 5.8S nrDNA gene (ITS) and a part of β-tubulin gene (BT) were amplified using primer sets ITS1/ITS4 (White et al. 1990) and T1 and Bt2b (Glass & Donaldson 1995), respectively. All the polymerase chain reactions (PCRs) were performed in Techne TC-312 Thermal Cycler (Techne, Cambridge, U.K.) as described by Hashemi & Mohammadi (2016). DNA samples and PCR products were evaluated on 0.1% agarose gels stained with ethidium bromide and visualized under ultraviolet light. A 100-bp ladder (GeneRuler DNA Ladder Mix, Fermentas, Vilnius, Lithuania) was used for evaluation of the band sizes. Purification and sequencing of the PCR products were performed using Bioneer Corporation (Daejeon, South Korea). All the sequences were read and edited by BioEdit Sequence Alignment Editor v. 7.0.9.0 (Hall 2006) and then run through the MegaBLAST function of the National Center for Biotechnology Information’s GenBank nucleotide database (https://www.ncbi.nlm.nih.gov/) for initial identification.

 

Phylogenetic analysis

Phylogenetic analysis was performed only for Phaeoacremonium isolates. Beta-tubulin sequences of Iranian Phaeoacremonium isolates obtained from grapevine in this study and reference sequences of Phaeoacremonium species taken from the GenBank were aligned using default settings of Clustal W algorithm (Thompson et al. 1994) included within MEGAX software package (Kumar et al. 2018). Pleurostoma richardsiae (CBS 270.33, accession no. AY579334) was used as an out-group. The alignment results were checked and manually improved where necessary. Maximum Likelihood (ML) analysis was performed in MEGAX. Bootstrap support was estimated using 1000 replicates to assess the robustness of each clade.

 

Pathogenicity tests

The pathogenicity of one isolate from each identified species was tested on two-year-old rooted cuttings of grapevine (cultivar Kolahdari) under controlled greenhouse conditions (at 23 ±2 °C). The inoculated region was surface-disinfested with 75% ethyl alcohol for 10 min. After air drying, a wound was made between two nodes of each cutting using a cork borer of 5 mm diameter. Wounds were inoculated with mycelial plugs (5 mm in diameter) taken from 2-week-old cultures on PDA and then protected by moist cotton and a strip of Parafilm ® (Pechiney Plastic Packaging, enasha, USA). A total number of 10 rooted cuttings per fungal isolate were used and 10 rooted cuttings were inoculated with sterile PDA plugs, as the control treatments. All the inoculated cuttings were arranged in a completely randomized design and disease symptoms and the length of wood discoloration were measured after 10 months. Re-isolations of the inoculated isolates were conducted from the symptomatic wood tissues of the treatments and control plants and cultured on PDA plates. Petri dishes were incubated at 25 °C and re-isolated fungi were identified based on the colony and conidial morphology. One-way analyses of variance (ANOVA) in SAS v 9.1 (SAS Institute, Cary, NC, USA) was performed in order to assess differences in the extent of wood discoloration induced by the inoculated isolates. Moreover, the LSD test was used for comparison of treatment means at p < 0.05.

 

RESULTS

 

Sample collection and disease symptoms

In this study, the wood samples were collected from the trunk and branches of 115 diseased grapevine showing yellowing, stunted growth and dieback. Various wood lesion types include wedge-shaped necrosis, irregular wood necrosis, central necrosis, black spots and wood decay were also observed and recorded in cross sections of collected trunk and branches (Fig. 1).

 

Fig 1. Internal wood disease symptoms on grapevine in Khorasan-Razavi province: Co-occurrence of irregular wood necrosis (1), central necrosis (2) and black spot (3) symptoms (a); irregular wood necrosis (b and c); wood decay (d); wedge-shaped necrosis (e); co-occurrence of wedge-shaped necrosis (1), central necrosis (2) and black spot (3) symptoms in cross-section of an infected branch.

 

Table1. Geographical origin and number of the fungal isolates recovered from diseased grapevines collected from Khorasan-Razavi province (Iran), during 2016-2018.

Fungal species

Region

Number of the isolates

From each region

Total and percentages (%) *

Phaeoacremonium minimum

Neghab

34

75 (29.1)

 

Quchan

15

 

 

Neyshabur

7

 

 

Kashmar

19

 

P. iranianum

Neghab

24

52 (20.1)

 

Quchan

9

 

 

Neyshabur

7

 

 

Kashmar

12

 

P. tuscanum

Neghab

8

8 (3.0)

P. parasiticum

Neghab

19

19 (7.4)

Fomitiporia mediterranea

Neghab

27

56 (21.8)

 

Quchan

8

 

 

Neyshabur

3

 

 

Kashmar

18

 

Seimatosporium vitis

Neghab

27

48 (18.6)

 

Quchan

4

 

 

Neyshabur

3

 

 

Kashmar

14

 

* percentage based on the total number of fungal isolates.

 

 

Fungal isolation and morphological identification

 

In this study, a total number of 258 fungal isolates were obtained. Isolation, frequency and geographical distribution of the isolates recovered from diseased grapevines in Khorasan-Razavi province are shown in Table 1. Based on colony appearance, culture characteristics, and microscopic structures, the main fungal isolates were divided in three groups.

Group one: One hundred and fifty-four isolates (59.7% of total isolates) were classified in this group. These isolates were characterized by beige medium brown, pale to pale brown to reddish brown flat slow-growing cultures on PDA. Sporulation was abundant, conidia were hyaline and aseptate, hyphae were single or fasciculate, and three types of phialides (I, II, and III types), that were different in size and shape were observed in these isolates. All of these isolates were tentatively identified as Phaeoacremonium (Crous et al. 1996, Mostert et al. 2006, Spies et al. 2018).

Group two: Forty-eight isolates (18.6 % of total isolates) as 'pestalotioid fungi' were placed in this group. These isolates were characterized by white to medium-brown, margin uneven and flat slow-growing cultures on PDA. Hyphae hyaline, straight, branched, and septate. Conidiomata pycnidioid, solitary or aggregate, dark, 95−345 μm diam. Conidiophores 7−18 × 2−3 μm,Conidia abundant, single,obovoid to fusiform, straight to slightly curved, 12−19 × 4−6 μm, with 3 dark brown transverse septa, hyaline to sub-hyaline basal and apical cell and two hyaline, unbranched and short flexuous appendages (Fig. 2). These morphological features were compatible with the description of Seimatosporium spp. (Senanayake et al. 2015, Wijayawardene et al. 2015, Lawrence et al. 2018).

Group three: Fifty-six isolates (21.7 % of total isolates) were classified in this group. These isolates were characterized by white and medium-growing mycelium on PDA (28 mm at 25 within 8 days) that became yellow-orange and brown in color with age. These morphological features were not sufficient to identify these isolates at the generic level; however, they were considered as basidiomycetous fungi (Sigler & Abbott 1997, Markakis et al. 2017. Brown et al. 2019).

 

Molecular identification and phylogenetic analysis

 

To confirm the identification based on morphology and cultural characteristics, BLASTn searches in GenBank showed that ITS sequences of basidiomycetous isolates had 100 % identity with Fomitiporia mediterranea (isolate: CB6, accession no.  EU477476). Beta tubulin sequences of Seimatosporium isolates were also 100 % identical to that of Seimatosporium vitis Napa776 (accession no. KY706252). For phylogenetic analyses, the BT sequences of 17 suspected Phaeoacremonium isolates were aligned with 34 sequences of reference isolates and Pleurostoma richardsiae (CBS270.33) was used as out-group. The alignment consisted of 628 characters (including gaps), of which 215 were constant and 292 parsimony informative. Maximum parsimony analysis resulted in 4 equally most parsimonious trees (TL=1303, CI=0.475, RI=0.765, RC=0.363). Analysis of the BT clearly separated Iranian isolates in 4 clades including P. iranianum (52 isolates), P. tuscanum (8 isolates), P. minimum (75 isolates) and P. parasiticum (19 isolates). One of the ML trees is shown in Fig. 3 with bootstrap support values at the nodes.

 

Pathogenicity tests

Mean lengths of wood discolorations caused by inoculated isolates on rooted grapevines are shown in Fig 4. All the inoculated isolates produced wood lesion lengths were significantly different from those in the control plants (P<0.05). Phaeoacremonium minimum was the most aggressive fungal species and produced the longest necrotic wood lesions (29.8 mm) on the inoculated shoots followed by S. viticola (27.8 mm) and F. mediterranea (12.1 mm). No significant difference was observed between P. minimum and S. viticola. Re-isolation percentages were between 60.0 % (F. mediterranea) and 100 % (P. minimum and S. viticola) on inoculated plants, and no fungal isolateswere isolated from control treatments.

 

DISCUSSION

 

Nowadays, GTDs are considered as the most destructive diseases of grapevine (Gramaje et al. 2018, Guerin-Dubrana et al. 2019) and to date, more than 138 fungal species have been associated with GTDs (Gramaje et al. 2018, Raimondo et al. 2019) worldwide. The results of this study showed that grapevines in Khorasan-Razavi province are infected with known fungi causing decline diseases. In this province, morphological and molecular data provided evidence that at least Phaeoacremonium spp., F. mediterranea and S. vitis occur on grapevines in this region. In addition to these taxa, several isolates of Aspergillus, Penicillium, Alternaria, Fusarium, Bipolaris and Coniothyrium species, were also isolated from affected grapevines in this province, which were not considered in this paper. Phaeoacremonium isolates were the most abundant fungal groups isolated from affected trees. More than 60 species of Phaeoacremonium have been isolated and reported from different woody plant hosts around the world, among which grapevine is known as one of the most important host of this group of fungi (Crous et al. 1996, Mostert et al. 2006, Essakhi et al. 2008, Graham et al. 2009, Ariyawansa et al. 2015, Gramaje & Di Marco 2015, Crous et al. 2016, Da Silva et al. 2017, Spies et al. 2018). Throughout this work, four Phaeoacremonium species, including P. parasiticum, P. minimum, P. iranianum and P. tuscanum were recovered from grapevines showing decline symptoms. The first three species are relatively widespread and have been reported from grapevine in various countries around the world (Mostert et al. 2006, Spies et al. 2018), while, P. tuscanum is reported only from grapevines in Italy (Essakhi et al. 2008) and Iran (Mohammadi 2012, Arabnezhad & Mohammadi 2014). 

 

Fig 2. Seimatosporium vitis: Colonies on PDA (a-c), Pycnidia on PDA at 25°C in the dark conditions (d-g) and Conidia (h-j).

Fig 3. Maximum likelihood tree generated based on beta tubulin (BT) gene sequences data for Phaeoacremonium isolates. Bootstrap values are given at the nodes. The tree was rooted by Pleurostoma richardsiae (CBS 270.33). Iranian isolates indicated by red color in each colored rectangle.

Fig 4. Wood lesion size produced by inoculated fungal species on rooted grapevine shoots, 10 months after inoculation. Means followed by the same letter are not significantly different (at P < 0.05) and bars represent standard error of the means.

 

In this study, P. minimum was the dominant Phaeoacremonium species obtained from diseased grapevines. This is in agreement with the previous studies on grapevine in France (Larignon & Dubos 1997), Italy (Mugnai et al. 1999), Australia (Pascoe & Cottral 2000), South Africa (Groenewald et al. 2001), Spain (Armengol et al. 2001), Argentina (Dupont et al. 2002), Chile (Auger et al. 2005) as well as Iran (Mohammadi & Banihashemi, 2007, Arabnezhad & Mohammadi, 2012. Mohammadi et al. 2013a, Arabnezhad et al. 2013). All of the four species of Phaeoacremonium isolated during this study, have previously been reported from grapevines and other woody plants in various provinces of Iran. For instance, P. minimum has previously been reported affecting grapevines in Fars, Hamadan, Isfahan, Yazd, Kerman, Kohgiluyeh and Boirahmad, and West and East Azerbaijan provinces (Arabnezhad & Mohammadi, 2012, 2014, Arzanlou et al. 2013, Mohammadi et al. 2013a, Narmani et al. 2014, Faraji & Mohammadi, 2015). Phaeoacremoniumparasiticum was associated with grapevine trunk diseases in Fars and Kerman provinces and stone and pome fruit trees (Arzanlou et al. 2014, Sami et al. 2014, Soltaninejad et al. 2017), cypress (Mohammadi et al. 2014), date palm (Mohammadi, 2014), poplar trees (Hashemi & Mohammadi, 2016, Kazemzadeh Chakusary et al. 2017) and some other forest trees (Kazemzadeh Chakusary et al. 2017) in Iran. Phaeoacremonium iranianum was isolated and recorded from grapevines in Fars and South Khorasan and also from alder (Kazemzadeh Chakusary et al. 2017), hawthorn, quince(Sami et al. 2014), apple (Arzanlou et al. 2014, Sami et al. 2014) and pomegranate (Kazemzadeh Chakusary et al. 2017) trees in various provinces of this country. Phaeoacremonium tuscanum has previously been reported affecting grapevines in Kohgiluyeh and Boirahmad province (Arabnezhad & Mohammadi 2012) and peach trees in Kerman province (Soltaninejad et al. 2017). Therefore, the current study is the first report on the occurrence of these species on grapevine in Khorasan-Razavi province.

Fomitiporia mediterranea was another fungal species that was isolated from grapevine in this study. Wood-rotting basidiomycete fungi, including Fomitiporia spp., are known as grapevine trunk pathogens (Bertsch et al. 2013, Brown et al. 2019). Fomitiporia mediterranea introduced by Fischer (2002) and as a fungal trunk pathogen on grapevine is widespread in the Mediterranean area (Fischer & Kassemeyer 2003). The importance of thisbasidiomycete as a fungal trunk pathogen has been widely investigated (Mugnai et al. 1999, Fischer 2002, Fischer & Binder 2004). This fungus is the main wood-decaying pathogen in some wine-growing areas of southern Italy (Ciccarone et al. 2004) and Greece (Markakis et al. 2017). In Iran, this taxon has been previously reported to affect grapevines in Northern Khorasan province (Farashiyani et al. 2010, Rajaiyan et al. 2013), Russian olive (Ahmadyusefi Sarhadi & Mohammadi, 2019) and elm trees (Mirsoleymani & Mostowfizadeh Ghalamfarsa 2019) in Fars province. To the best of our knowledge, this study is the first report of the occurrence of F. mediterranea on grapevine in Khorasan-Razavi province.

The genus Seimatosporium Corda, with S. rosae Corda as the type species, was first described and introduced by Corda (1833). Various Seimatosporium species have been isolated and reported from symptomatic or dead parts of grapevines in different countries (Diaz et al. 2012, Vaczy 2017, Farr & Rossman, 2018, Lawrence et al. 2018, Camele & Mang, 2019, Liu et al. 2019). In this study, 48 isolates of S. vitis were obtained from necrotic wood tissues of grapevines in Khorasan-Razavi province. This species has also been reported from symptomatic grapevines in Hungary (Vàczy 2017), North Carolina, USA (Lawrence et al. 2018) and Italy (Camele & Mang, 2019). To date, there has only been one report of the sexual morph of S. vitis on a dead branch of Vitis sp. in Iran (Mehrabi et al. 2017). Therefore, this study is the first report of this species from necrotic wood tissues of grapevine in Iran.

The results of the pathogenicity tests showed that all the inoculated species on the rooted cuttings of the grapevines were pathogenic and produced wood discoloration on inoculated shoots, developing from the point of inoculation. Phaeoacremonium minimum showed the longest lesions and were the most virulent species on the rooted cuttings of the grapevines. The findings of this study are in accordance with the results previously reported by other researches on grapevine (Feliciano et al. 2004, Halleen et al. 2007, Aroca & Raposo 2009, Gramaje et al. 2010). Mohammadi et al. (2013a) reported P. minimum causing significantly longer lesions than the other Phaeoacremonium species tested on grapevine shoots under field conditions in Iran. Similar results were also reported for this fungus on green shoots of grapevine under greenhouse conditions in this country (Mohammadi et al. 2014). Our findings for the first time in Iran, indicated that S. vitis is involved in the grapevine trunk-disease complex. Relatively, little is known regarding the importance of this species on grapevine. However, pathogenicity tests in Hungary (Vaczy 2017), Italy (Camale & Mang 2019) and the USA (Lawrence et al. 2018) have also shown that S. vitis can be considered as a fungal trunk pathogen on grapevine. Overall, all the fungal species were identified in this study, have previously been isolated and reported from grapevine in other provinces of Iran with the exception of S. vitis, which was reported here for the first time associated with wood necrosis of grapevine in this country. Further research is required to provide better understanding of the role of various fungal species on grapevine GTDs in Iran especially Khorasan-Razavi province.

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