ZANCO Journal of Pure and Applied Sciences

The official scientific journal of Salahaddin University-Erbil ZJPAS (2017), 29 (s4); 300-309 http://dx.doi.org/10.21271/ZJPAS.29.s4.34

Seed-borne fungi of durum wheat (Triticum durum Desf) cultivars grown in Duhok province, Kurdistan Region, Iraq

Samir K. Abdullah1* and Helben I. M. Atroshi2

1 Biology Department, Faculty of Science, University of Zakho 2 Plant Protection Department, College of Agriculture and Forestry, Duhok University, Iraq

A R T I C L E I N F O A B S T R A C T

Article History: The study was carried out to investigate the seed borne fungi associated with Received: 01/06/2017 different cultivars of durum wheat (Triticum durum Desf.) grown in Duhok Accepted: 05/08/2017 province, Kurdistan region, Iraq. A total of 12 seed samples were surveyed for Published: 20/12/2017 the associated mycoflora using standard agar plate, blotter paper and freezing Keywords: methods. A total of 21 fungal species assigned to 14 genera were identified. Durum wheat, The most common genera in descending order of their isolation frequency were Seed-borne fungi, Cladosporium, Penicillium, Alternaria, Aspergillus, Ulocladium, Arthrinium Iraq and . Alternaria alternata,Cladosporium herbarum,Aspergillus flavus, A.niger, and Arthrinium phaeospermum were the most frequent species. *Corresponding Author: Ascad cultivar showed the highest number of detected species (13 species), Samir K. Abdullah whereas the lowest number (7 species) were isolated from Sham 3 cultivar. [email protected] Ascad cultivar (sample 2). Sham 3 (sample 5) and Simeto (sample 7) showed the highest mean percentage contamination (71.0%, 68.5% and 57.0%) respectively. The results showed a variation in the fungal composition, number of detected species and percentage contamination according to detection method and cultivar type.

1. INTRODUCTION cultivated areas of wheat in Iraq are estimated Wheat is the most important in the at 2.3 million hectares and the total production world and was one of the first crops that could is 3.4 million metric tonnes. and However, be easily cultivated on a large scale giving Iraqi wheat consumption is currently estimated about one third of total production followed by at 5.8 million tonnes a year (USDA,2016). rice (Wiese,1987). Durum wheat (Triticum Fungi associated with seeds prove to be durum Desf) has a high amount of proteins (12- hazardous causes several diseases, production 16%) which is good for pasta of poor quality grains, reduced yields and products/macaroni, spaghetti and other reduced grain germination (Neergard,1979). noodles(Beuerlein,2001). The actual planted Several pathogenic and saprophytic fungi have areas with wheat in Kurdistan region are been reported from durum wheat. Among them 600.000 hectares, yielded 912.000 metric is Fusarium spp.,causing head blight that tonnes in 2015 (Abdullah,2015) . The total reduces grain quality (Fernandez et al.2001; 301 Abdullah S. K. and Atroshi H. /ZJPAS: 2017, 29(s4): 300-309

Wright et al.2010; Fakhfakh et al.2011; Fields Crops, Duhok University(4 samples) and Alkadri et al.2013). Other important pathogens local Silos at Duhok Governorate(4 samples). A such as Alternaria alternata, Bipolaris working sample of each cultivar was obtained sorokiniana,Microdochium nivale and Tilletia according to the International Rules of Seed Testing (ISTA,2009). spp., were also regularly detected from wheat grains (Ioos et al.2004; Prescot et al.2006; 2.2. Detection of seed-borne Fungi Gargouri-Kammoun et al.2009; 2014; Hajihasani et al.2012; Majunder et al.2013; The seed-borne fungi were isolated using three Atroshi and Abdullah,2016). Seed-borne different detecting standard methods (agar plate, blotter paper and deep freezing techniques) saprophytic species in the genera Aspergillus according to International rules of seed Testing .Penicillium and Fusarium may also produce (ISTA,2009). A total of 200 seeds in four replicates several volatile metabolites including alcohol, were tested from each sample. Procedure details for ketone and aromatic compounds (Laddomada each isolation technique and media used were given et al.2014) and mycotoxins which may alter in (Abdullah and Atroshi,2016). The fungi growing grain composition or imposing high risk to from the grains were either identified directly from human or animals after consumption the plates or were sub cultured onto other (Christensen and Kaufman,1965;Abramson et appropriate media used for identification. al.1990;Gallo et al.2008; Al-Sagga et al.2015). The percentage frequency of occurrence (FO) Studies on the seed-borne fungi associated with of fungi in the seeds of each cultivar and durum wheat grains have been made by percentage contamination (PC) was calculated. researchers in different parts of the world Number of grains on which a (Flannigan,1970; Bokhary,1986; Clear et Fungal species was identified al.2005; Mavragani et al.2007; Plaskowska and FO%=______×100 Chrzanowska-Drozdz,2009;Gargouri- Total number of tested grains Kammoun et al.2009,2014; Alkadri et al.2013;

Belkacem-Hanfi et al.2013). However, in Iraq only few studies have been performed on the Number of infected grains from each subject (Sulaiman and Husain,1985; Juber and cultivar Al-Salahi,2006; Al-Taae and Al-Ameery,2010; PC%=------x100 Hassan et al.2010; Atroshi and Abdullah,2016) . The purposes of this study was to identify the Total number of grains in each cultivar fungi associated with grain samples of durum wheat cultivars from Duhok province 2.3. Fungal Identification Kurdistan Region of Iraq using different detecting methods and to assess the percentage All species were identified according to the keys of seed contamination with fungi for each and descriptions provided byEllis,1971,1976; cultivar. Arx,Von, et al.1986; Samson et al.2000; Klich,2002; Watanabe,2002;Prescott et al.2006; 2. MATERIALS AND METHODS Leslie and Summerell,2006; Guarro et al.2012). 2.1-Samples collection

A total of 12 seed samples of durum wheat were obtained in an amount of 250-500 gm/sample during 2.4.Data Analysis the year 2012-2013 from Directorate of Agricultural A factorial experiment (12×4) t was conducted Research in Duhok (4 samples), the Department of by Completely Randomized Design and replicate 302 Abdullah S. K. and Atroshi H. /ZJPAS: 2017, 29(s4): 300-309

five times with 10 seeds for each replicate. The data 3.2. Frequency of fungal genera on durum has been analyzed by using computer through the wheat grains SAS program (SAS,2001) and the means comparison was done by Duncan’s Multiple Fourteen fungal genera have been detected Ranges Test under 5% which was claimed by from durum wheat grains,(Figure 1).The (SAS,2001). highest isolation frequency was displayed by the genus Cladosporium (100%) followed by

Penicillium (91.665), Alternaria and 3. RESULTS AND DISCUSSION Aspergillus(83.33% each), Ulocladium 3.1.Contamination of wheat grains by fungi (66.66%), Arth rinium (58.33%) and Chaetomium (41.66%). Other fungal genera The results of percentage contamination of showed low isolation frequency (8.33% each). durum wheat grains of different cultivars by Sulaiman and Husain (1985). also reported fungi as detected by different isolation methods higher incidence for the genera Aspergillus, are presented in Table 1.The degree of fungal Alternaria, Rhizopus, Penicillium and contamination for the 12 durum cultivars as Cladosporium in stored wheat grains in silos in detected by blotter method ranged from 0.0 to Iraq. Fungal analysis of 48 samples from 70%, by deep freeze from 0.0 to 42%.Detection Syrian wheat grains reported Alternaria and of fungal contamination by using agar plate Cladosporium as the most frequent genera, method was higher (2.0 to 100%) for each of followed by Penicillium and Aspergillus PDA and OTA media as compared to both (Alkadri et al.2013), whereas, Aspergillus blotter methods and deep freeze (0.0 to 70% followed by Fusarium,Penicillium and and 0.0 to 0.42%) respectively. showed a high isolation rate in wheat grains from Turkey (Askun,2007). The cultivars Doar (1) and Acsad (1) showed the lowest fungal contamination (0.0 to 18.0% In Poland,Fusarium and Alternaria were the and 0.0 to 24.0%) respectively, whereas, the most common fungi colonizing winter durum highest fungal contamination was displayed by wheat, whereas, Aspergillus and Penicillium cultivars Acsad(2)(26.0 to 100%) and cultivar were present in low frequencies( Plaskowska Simeto(1)(24.0 to 100%).The mean value of and Chrzanowska-Drozdz,2009). The genera contamination percentage of each cultivar was Alternaria, Fusarium and Microdochium were significantly different using different isolation reported with high incidence on freshly method (Table 2). harvested durum wheat grains in the main production areas of Tunisia (Bensassi et The degree of percentage of fungal al.2009) whereas, the most predominant contamination varied among wheat cultivars. postharvest mould genera were Alternaria, Such variations may be attributed to the Fusarium, Penicillium, Aspergillus, Mucor and differences in geographical locality of Rhizipous ( Belkacem-Hanfi et al.2013). cultivations, storage conditions or to differences in physico-chemical nature of 3.3. Frequency of fungal species on durum different wheat genotypes and may be due to wheat grains. isolation techniques used in the present study. This is in line with results obtained by Twenty one species assigned to 14 genera (Christensen,1955; Singh et al.2011) . have been identified (Table 2). Ten species viz. Acremonium strictum, Aspergillus glucus, A.

303 Abdullah S. K. and Atroshi H. /ZJPAS: 2017, 29(s4): 300-309

rugulovalvus Bipolaris sorokinina were reported among the dominant post- ,Chaetomium globosum,Corynascella sp., harvest moulds isolated from durum wheat Curvalaria spicifera, Fusarium cultivated in Tunisia (Belkacem-Hanfi et graminearum,Nigrospora state of Khuskia al.2013). oryzae and Microdochium sp. were detected from one cultivar each. Arthrinium phaeospermum was detected in 7 cultivars at a percentage frequency ranged from Alternaria was represented by two species, 0.5% to 3.0%. The species was also reported A.alternata and A.tenuissima. The former on soft wheat grains from Iraq (Abdullah and species was the most frequent among the genus Atroshi,2016). The species was reported in detected from 10 cultivars at a percentage several surveys on seed-borne fungi of wheat frequency ranged between 0.5% to 12.5%, grains from different regions of the world whereas, A. tenuissima was reported from 4 (Flannigan,1970; Clear and Patrick,1993; cultivars with low isolation frequency ranged Broggi et al.2007). between 1.0% to 2.5%%. A.alternata and A.tenuissima were reported as the most Bipolaris sorokiniana and Curvularia spicifera frequently isolated species on grains of durum were detected in one occasion each at a wheat in Tunnisia with a prevalence of 36.1% isolation frequency of 1.5% and 0.55% and 30.6% respectively ( Gargouri-Kammoun respectively. B.sorokiniana was previously et al. 2014). A.alternata was also reported as reported on soft wheat grains in Iraq (Abdullah the most frequently isolated species from and Atroshi,2016) and also reported as a causal grains of durum wheat in Western Canada pathogen of root rot of winter wheat from (Clear et al.2005). The two species were middle of Iraq (Sarhan.2013). The was reported in association with black point of reported in association with various diseases wheat in Tunisia (Bensassi et al.2011). In such as root rot, seedling blight, black point Argentina, Patriarca et al.(2007). showed that and head blight on wheat in different regions of Alternaria species were present in 100% of the world (Wiese,1998; Bhatti and wheat samples and demonstrated that most of Bhutta,2002; Acharya,2011). strains were able to synthesize more than one Chaetomium was represented by two species, Alternaria toxins. C.elatum and C.globosum .The former species Among the five reported species of Aspergillus was detected from 4 cultivars at low isolation ,A.flavus and A.niger were detected from 8 frequency (0.5%-1.0%), whereas, C.globosum cultivars each at isolation frequency between was found on one cultivar at 1.0% isolation 1.0% to 5.5% and 0.55 to 6.0% respectively. frequency. The two species were previously A.terreus was detected from 3 cultivars, reported from Iraq on wheat grains (Abdullah whereas, A.glucus and A.rugulovalvus were and Atroshi,2014). C.globosum was reported detected each from one cultivar at low isolation on stored wheat grains worldwide frequency. Aspergillus amd Penicillium were (Flannigan,1970; Wiese.1998; Habib et reported at low levels from freshly harvested al.2011). durum wheat grains in the main productions Fusarium graminearum was detected in one areas in Tunisia compared with high levels of occasion on durum wheat. The species was occurrence for Alternaria,Fusarium and reported as the causal agent of crown rot Microdochium species (Bensassi et al.2011). disease in Iraq (Khalifa and Matny,2013). However,Aspergillus and Penicillium species 304 Abdullah S. K. and Atroshi H. /ZJPAS: 2017, 29(s4): 300-309

F.graminearum was reported as the most was more common and detected from six frequent species on durum and soft wheat cultivars at a percentage occurrence ranging grains in from 2000 to 2002 (Ioos et between 0.5 %– 2.5 %, whereas. A.alternaria al.2004). The fungus was also detected was found on two cultivars at 1.0% isolation predominantly from wheat grains in Western frequency. The two species were previously Australia ( Wright et al.2010) . reported on wheat grains from Iraq (Juber and F.graminearum and other species of Fusarium Al-Salahi, 2006; Abdullah and were detected from wheat grains ( soft and Atroshi,2014,2016). U. alternariae was also durum wheat ) worldwide (Clear and reported on wheat grains in Kerman province, Patrick,1993; Gargouri-Kammoun et al. 2009; Iran (Gohari et al.2007). Rehman et al.2011 ;Hajihasani et al.2012; Alkadri et al.2013). Conclusion

Microdochium sp., was detected from one In Iraq, little information is available on cultivar (cv.Simeto) at low isolation frequency seed-borne fungi of cereal grains. Our survey (0.5%). M. nivale was reported as the most showed that durum wheat grains from Iraq frequent species (63.5%) isolated from were contaminated with a diverse mycoflora diseased durum wheat spikes in Northern that included saprophytic, pathogenic and Tunisia( Gargouri-Kammoun et al. 2009). The mycotoxin producing fungi. A particular fungus was reported along with several attention should be paid to the presence of Fusarium species associated with Fusarium Alternaria spp.,B.sorokiniana, F. graminearum head blight on durum wheat in France (Ioos et and Microdochium sp., for their pathogenic and al.2004). toxigenic potentials.

Two species of Ulocladium viz. U. atrum and U. alternaria were detected .The first species

120

100

80

60

40

20

0

Figure 1 Isolation Frequency percentage for fungal genera detected from durum wheat grains

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Table.1.Contamination Percentage of durum wheat grains of different cultivars by fungi as detected by different isolation methods.

Method of isolation

Cultivar % Contamination by fungi

Blotter Deep PDA Oatmeal agar Mean method freezing

1-Acsad (1) 0.0 b* 24.0ab 14.0 c 4.0 d 10.5 ef

2- Acsad (2) 70.0 a 26.0ab 88.0ab 100 a 71.0 a

3-Creso (1) 8.0 b 34.0ab 12.0 c 20.0 cd 18.5 e

4-Creso (2) 28.0 b 26.0ab 14.0 c 68.0ab 34.0 cd

5-Sham 3 56.0 a 42.0 a 78.0 b 98.0 a 68.5 ab

6-Doar (1) 0.0 b 18.0 b 2.0 c 0.0 d 5.0 f

7-Simeto (1) 24.0 b 22.0ab 100 a 82.0 a 57.0 b

8-Simeto (2) 26.0 b 32.0ab 10.0 c 2.0 d 17.5 ef

9-Unknown cultivar 1 8.0 b 0.0 c 6.0 c 40.0bc 13.5 ef

10-Unknown cultivar 2 18.0 b 22.0ab 24.0 c 76.0 a 35.0 c

11-Unknown cultivar 3 8.0 b 42.0 a 4.0 c 36.0 c 22.5 de

12-Doar (2) 0.0 b 36.0ab 2.0 c 2.0 d 10.0 ef

Mean 20.5 c 27.0 bc 29.5 b 44.0 a ___

*Means followed by different letters in the same column are significantly different based on Duncan’s Multiple Range Test (P=0.05).

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Table 2. Percentage frequency of occurrence of fungi on durum wheat grains and their sources

Fungi species % infected grains of the particular cultivar

1* 2 3 4 5 6 7 8 9 10 11 12

Acremonium strirctum 1.0

Alternaria alternata 1.0 12.5 0.5 4.0 12.5 1.5 1.0 0.5 1.0 1.0

Alternaria tenuissima 2.0 1.0 2.0 2.5

Arthrinium 2.0 1.5 1.5 0.5 0.5 1.5 3.0 phaeospermum

Aspergillus flavus 1.5 2.0 1.5 1.0 5.5 1.0 6.0 1.0

A. glucus 0.5

Aspergillus niger 1.0 2.0 0.5 3.0 3.0 1.0 6.0 0.5

Aspergillus terreus 0.5 1.0 2.5

A.rugulovalvus 1.5

Bipolaris sorokiniana 1.5

Chaetomium elatum 0.5 1.0 1.0 0.5

Chaetomium globosum 1.0

Cladosporium 1.5 1.0 2.0 0.5 1.5 2.5 8.0 0.5 6.0 herbarum

Corynascela sp. 0.5

Curvularia spicifera 0.5

Fusarium 0.5 graminearum.

Nigrospora state of 1.0 khuskia oryzae

Microdochium sp 0.5

Penicillium spp . 1.5 1.0 1.5 2.5 2.5 2.0 4.0 0.5 3.0 4.0 3.0

Ulocladium atrum 1.0 0.5 2.0 1.0 2.5 0.5

Ulocladium alternariae 1.0 1.0

*1-2 Acsad ; 3-4 Creso ; 5-Sham3 ; 6- Doar ; 7-8 Simeto ; 9-11 mixed cultivars ;12- Doar .Based on 200 grains of each cultivar.

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