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Ascochyta Rabiei from Pakistan and the United States

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Ascochyta Rabiei from Pakistan and the United States 010_JPP834RP_Ali_99 19-03-2012 16:51 Pagina 99 Journal of Plant Pathology (2012), 94 (1), 99-108 Edizioni ETS Pisa, 2012 99 POPULATION STRUCTURE AND MATING TYPE DISTRIBUTION OF THE CHICKPEA BLIGHT PATHOGEN ASCOCHYTA RABIEI FROM PAKISTAN AND THE UNITED STATES H. Ali1, S.S. Alam1, R.N. Attanayake2, M. Rahman3 and W. Chen2 1 Nuclear Institute for Agriculture and Biology, Faisalabad, Pakistan 2 USDA-ARS, Washington State University, Pullman, WA, USA 3 National Institute for Biotechnology and Genetic Engineering, Faisalabad, Pakistan SUMMARY INTRODUCTION Ascochyta blight caused by the fungus Ascochyta ra- Chickpea (Cicer arietinum), a cool season grain biei (AR) depresses chickpea production in Pakistan legume grown on a surface of 11 million ha with world- and worldwide. Thirty two AR isolates representing six wide production of about 9 million tons (FAOSTAT, geographical regions of Pakistan were compared with a 2009), is cultivated in more than 45 countries through- US-AR population for mating type frequency and genet- out the world including Pakistan where it is grown ic variation. Mating type results showed that the Pak- mostly in rainfed areas and on marginal lands in the istani AR (PAR) population had an apparent skewed (3 province of Punjab. Its yield in Pakistan is about 583 kg Mat1-2: 1 Mat1-1) distribution, although Chi-square ha-1 (GOP, 2009), much lower than its potential yield as tests showed non-significant deviation from equal distri- its production is under the constant threat of diseases bution due to small sample sizes. The US population and pests (Akhtar et al., 2008, 2009, 2011). Among fun- showed a 1:1 distribution of the two mating types. The gal diseases, wilt and blight are the two most important uneven distribution of mating types indicates that sexu- limiting factors to chickpea productivity. al reproduction among the PAR is rare due to either un- Chickpea blight is caused by Ascochyta rabiei (Pass.) availability of both mating types or lack of conducive Lab. (AR), whose perfect stage [telemorph: Didymella ra- environment, but statistical analysis showed that pan- biei (Kovachevski) von Arx] was discovered by Ko- mixia is there reflecting past recombinational events. vachevski in 1936 on overwintering chickpea debris in Genetic variation at six microsatellite loci was assessed southern Bulgaria (Kaiser, 1997). AR has been reported and each isolate was assigned to a microsatellite haplo- from 29 countries including the Middle East and the type. Population structure of the isolates was inferred Mediterranean and is usually associated with severe re- using Bayesian analyses implemented in the structure duction in chickpea yield and quality, especially under software which differentiated isolates into three distinct cool and wet weather conditions (Kaiser, 1997; Singh and clusters, two clusters of PAR and one of the US isolates. Reddy, 1996). It attacks all of the above-ground parts of However, few isolates from the US shared the same ge- the plant including stems, leaflets, pods and seeds, caus- netic background with one cluster of the PAR isolates, ing necrotic lesions that are circular on leaves and pods providing a link of inter-continental migration of the and elongate on petioles and stems. The disease may pathogen. Additionally, the two clusters of PAR-isolates cause a total yield loss if the environmental conditions are are not strictly associated with geographic locations in favourable to both the crop and the pathogen (>350 mm Pakistan, suggesting frequent gene flow of AR among annual rainfall, 20-22°C) (Nene and Reddy, 1987; different locations. Future studies should extend the Jimenez-Diaz et al., 1993; Acikgoz et al., 1994). sampling of representative populations to overcome the AR survives in plant debris, soil and infected seeds limitations of the small sample size for more accurate as- and it reproduces asexually, through the production of sessment of population structure. conidia in flask-shaped pycnidia, and sexually, through the production of ascospores from pseudothecia. As- Key words: mating type, chickpea, Ascochyta rabiei, cospores and conidia spread through wind and rain simple sequence repeats, genetic diversity. splashes, travelling distances up to hundreds of meters (Rhaiem et al., 2007). AR is heterothallic with two mat- ing types encoded by alternate alleles at a single mating type (MAT) locus. The MAT specific locus is governed by a single gene and its idiomorphs exist in the forms MAT1-1 and MAT1-2 (Turgeon and Yoder, 2000). The Corresponding author: H. Ali advantage of sexual reproduction is the adaptation to Fax: +92.419201776 E-mail: [email protected] new environment through recombination of genetic ma- 010_JPP834RP_Ali_99 19-03-2012 16:51 Pagina 100 100 Ascochyta rabies population structure in Pakistan and the US Journal of Plant Pathology (2012), 94 (1), 99-108 terial between the two mating strains. It also helps over- of the fact that less virulent pathotypes (pathotype I and coming the selection pressure imposed by the introduc- II) prevail there (Chen et al., 2004) as compared to Pak- tion of resistant host genotypes and fungicides. Deter- istan (Jamil et al., 2000; H. Ali, personal communication). mining the frequency of mating types in a fungal popu- The present study was undertaken to: (i) generate lation may help to infer the frequency and the relative knowledge about the genetic diversity of PAR isolates in importance of the sexual stage in the production region comparison with the US isolates; (ii) assess the mating (Cherif et al., 2006). Both AR mating types have been type distribution in Pakistan using MAT specific primers; reported in at least 15 countries including Tunisia, (iii) determine the AR reproductive mode in Pakistan. Turkey, USA, Canada and Spain (Rhaiem et al., 2007). Initially, mating types were identified by crossing iso- lates of unknown mating type with known tester strains MATERIAL AND METHODS (Wilson and Kaiser, 1995; Kaiser and Kusmenoglu, 1997), a time-consuming and laborious method. A spe- Fungal isolates. A total of 71 AR isolates were used cific-PCR assay has more recently been developed by in this study to analyze mating types and genetic vari- Barve et al. (2003), using multiplex PCR specific for ability. Thirtyfour isolates were collected during 2000- each idiomorph at the MAT locus. 2006 from six different geographical locations of Pak- Knowledge of the genetic structure of the fungal istan, namely Chakwal, Islamabad (northern Punjab), population is useful for predicting the genetic variation, Thal (central Punjab), Swabi, Karak and Attock (Khy- as the level of variability reflects the genetic evolution in ber Pakhtunkhwa), whereas 37 isolates were collected the fungal population. Genetic diversity of AR in differ- from one field in North Dakota, USA (Table 1). ent regions of the world has been studied using differ- ent DNA based approaches like restriction fragment DNA extraction. The isolates were purified using length polymorphism (RFLP), random amplified poly- single spore technique. Conidial suspensions of each morphic DNA (RAPD) and simple sequence repeats isolate were spread on potato dextrose agar with lactic (SSRs) markers (Geistlinger et al., 1997; Udupa and acid (APDA). After two or three days, single germinat- Weigand, 1998; Geistlinger et al., 2000; Santra et al., ing conidia were picked up, transferred and cultivated 2001; Vail and Banniza, 2009; Varshney et al., 2009; on PDA. DNA was extracted from fungal mycelium Nourollahi et al., 2010). Only a single study has been and isolated using FastDNA Kits (MP Biomedicals, conducted on the diversity and mating types of Pak- USA) according to manufacturer’s instructions. DNA istani AR (PAR) isolates using RAPD marker (Jamil et concentration was checked on Nano drop (USA). DNA al., 2000, 2010). Since RAPDs are dominant markers was diluted in sterile deionized distilled water to 10 known to be poorly reproducible (Jones et al., 1997), ng/µl before use in PCR. we have used the more robust SSR markers to detect ge- netic variation in PAR isolates collected from different Mating type assay. Mating types of all the 71 AR iso- geographical locations of Pakistan. lates (34 from Pakistan and 37 from USA) were deter- Pakistan has faced AR epidemics from 1928 to 1982 mined using the multiplex MAT-specific PCR assay which resulted in very heavy economic losses to farmers (Barve et al., 2003). Primer combinations of SP21, Tail5 (Kauser, 1965). Therefore, Ascochyta blight is a constant and Com1 were used in a single PCR carried out in 25 threat for Pakistani agriculture for the cold and humid µl vol containing 10 ng of genomic DNA, 1X PCR climate together provide congenial conditions to its at- buffer (containing 1.5 mM MgCl2), 0.2 mM dNTPs, 1 tacks. In the US, the disease causes severe losses in spite unit Taq DNA polymerase (Promega, USA) and 10-20 Table 1. Isolates of Ascochyta rabiei collected from different areas of Pakistan and the US and their mating types as determined by PCR. Province /State Geographic region Isolates (No.) Mat 1-1 Mat1-2 X2 P value Northern Punjab Islamabad 4 1 3 1.000 0.317 Chakwal 18 5 13 3.556 0.059 Khyber Pakhtunkhwa Swabi 2 0 2 - Karak 1 0 1 - Attock 2 0 2 - Central Punjab Thal 7 1 6 3.571 0.059 North Dakota, USA Minot 37 22 15 1.324 0.250 010_JPP834RP_Ali_99 19-03-2012 16:51 Pagina 101 Journal of Plant Pathology (2012), 94 (1), 99-108 Ali et al. 101 pMol each of the primers. Amplification was performed SSR amplification and analyses. PCR was performed in BioRad Cycler thermal cycler (Bio-Rad Laboratories, in a 12 µl reaction mixture containing 0.2 mM dNTP, USA) and cycling conditions consisted of an initial de- 1X PCR buffer, 1.5 mM MgCl2, and 1 unit Taq DNA naturation at 95°C for 3 min followed by 35 cycles of polymerase (Promega, USA), with the addition of 1 ng 94°C for 20 sec, 58°C for 20 sec, 72°C for 40 sec, and a genomic DNA, 0.24 µl (10 nM) of the forward primer final extension at 72°C for 10 min.
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