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��ࡱ�>��	������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������	��x�bjbj[�[�	>�9�9�R],�������66������������8�\8 ,��^fd z � � � !�!�!u]w]w]w]w]w]w]$�_��bB�]���!!!�!�!�]��� � �L^�'�'�'�!��� �� u]�'�!u]�'�'��HX�L� ����@�Ix9�������$�I(a]b^0�^J��b�%D�bP�L�L��b�EM�!�!�'�!�!�!�!�!�]�]�'�!�!�!�^�!�!�!�!���������������������������������������������������������������������b�!�!�!�!�!�!�!�!�!6 V:	@Pathogenic variability of Ascochyta rabiei causing blight of chickpea in India
Mathew Seikholen Baite1*and Sunil Chandra Dubey2

Division of Plant Pathology, ICAR� Indian Agricultural Research Institute, New Delhi, 110012, India 
1Present address; ICAR- National Rice Research Institute, Cuttack, Odisha, 753006
2Division of Plant Quarantine, ICAR� National Bureau of Plant Genetic Resources, New Delhi, 110 012, India
*Corresponding author: Mathew Seikholen Baite
ICAR- National Rice Research Institute, Cuttack, Odisha, 753006 India
Email:  HYPERLINK "mailto:mathew.baite@gmail.com" mathew.baite@gmail.com
	
Ascochyta blight caused by Ascochyta rabiei (Pass.) Labr. is one of the major diseases of chickpea worldwide. Since there is report of variable number of races and no common set of International differential genotypes available to determine the races, an attempt was made to develop a set of differential genotypes and investigate the existing race (s) of the pathogen, which will be helpful in improving/breeding resistant variety of chickpea. The virulence of 25 isolates of A. rabiei from different parts of India were analysed on 10 differential genotypes showing different levels of resistant and susceptible reactions under artificially inoculation (105conidia/ml) in controlled environment. Based on the reactions, the population of A. Rabiei were grouped into seven races using the 1-9 rating scale. The genotype ICC 4991 showed susceptible reaction against all the isolates of the pathogen. Five genotypes, ICC 11879, ICC 3996, ICC 15978, GL 26054 and H00 108 exhibited resistant to moderately resistant reactions against the isolates of A. rabiei. Distribution of races was mapped. Race 1 widely prevalent in 5 states namely, Delhi, Himachal Pradesh and Jammu and Kashmir whereas, the most virulent is race 7 found in Uttar Pradesh. This study standardized a set of differential genotypes of chickpea for race identification and established 7 races of Ascochyta rabiei. The race pattern of A. rabiei would be helpful in breeding resistant chickpea variety. The information is entirely new in respect of differential genotypes and distribution pattern of races of A. rabiei in India.
Key words: Chickpea, Ascochyta blight, Ascochyta rabiei, pathogenic variability, race 
Introduction 
Chickpea (Cicer arietinum L.) is an important pulse crop grown and consumed across the world, particularly in the African and Asian countries. The crop is a good source of carbohydrates and proteins and the protein quality is regarded to be much better in comparison to other pulses1. Even though India is the largest chickpea producing country with an average production of 8.8 million tonnes and cultivated in an area of 9.6 million ha2, the productivity is low as compared to other major chickpea producing countries which are largely due to biotic and abiotic stresses. One of the major drawbacks limiting chickpea productivity is the Ascochyta blight.
Ascochyta blight of chickpea is caused by Ascochyta rabiei (Pass.) Labr. (teleomorph: Didymella rabiei (Kov.) v. Arx). It is a serious foliar disease of chickpea problematic in areas where cool (15-25�C) and humid weather (>150 mm rainfall) prevails during the crop season3. The disease occurs in several major chickpea growing parts of the world4. In India, the disease is very serious in north-western region, in the states of Punjab, Haryana, Himachal Pradesh, Jammu and Kashmir, Uttar Pradesh and Rajasthan5.  The disease sporadically occurred in Himachal Pradesh and Jammu and Kashmir and losses were observed upto 5%6.
Six races of A. rabiei using six chickpea differentials were identified from Syria and Lebanon7. Forty four isolates of the pathogen originated from India, Pakistan, Spain and the United States were grouped into 11 pathotypes using 7 differentials8. Forty Canadian isolates were assembled into 14 pathotypes based on pathogenicity on 8 chickpea differentials9. Thus, it is obvious that a variable number of races of A. rabiei have been reported by various researchers. The probable reasons might be unavailability of standardized International differentials for the purpose and highly variable populations. Earlier to this study, no systematic attempt was made to standardized differentials based on large scale screening of available genotypes or differentials used by other workers.
For ascochyta blight, the cultivation of resistant chickpea varieties is the most economical and effective management strategy10. However, breeding for resistance to blight is problematic due to frequent collapse of host plant resistance, perhaps due to variable nature of the pathogen11. Therefore, in order to identify stable and durable sources of resistance against the prevailing pathotypes of A. rabiei that occur in the target areas, it is vital to study the pathogenic variability among A. rabiei isolates12. The evolution of new races has made the plant breeders to alter their tactic from oligogenic resistance to pyramiding of genes to deliver long-lasting resistance. It is also imperative to comprehend the race distribution of A. rabiei in different chickpea growing areas, which will assist in selective deployment of varieties to deliver effective resistance and to save resistance genes from being overcome by the races of the pathogen. It becomes necessary to track fluctuations in the pathogen population to expect the collapse of resistance in prevailing chickpea cultivars. Hence, it is necessary to understand the pathogenic variation in the populations of the pathogen to sustain a proficient resistance-breeding programme. No clear-cut information on the prevalence of races in India is available.
Therefore, the present study was aimed to standardized a set of differential genotypes and determine the races of A. rabiei present in chickpea growing states of Northern India suitable for disease development. This study will add new knowledge about a set of differential genotypes of chickpea against ascochyta blight and will comprehensively identify the existing races of A. rabiei in India.   

Materials and Methods
Collection, isolation and maintenance of pathogen. Ascochyta blight infected chickpea plant samples were collected from chickpea growing states of Northern India namely, Haryana, Himachal Pradesh, Jammu and Kashmir, Punjab, Rajasthan, Uttarakhand, Uttar Pradesh and Delhi during 2012-2013. The pot experiments were conducted during 2014 and 2015 at IARI, New Delhi. The associated fungus, A. rabiei was isolated from stem, leaves and pods of chickpea on chickpea dextrose agar medium (CDA) medium (chickpea flour (besan) - 60 gm, dextrose - 20 gm and agar - 20 gm and distilled water � 1L) following standard tissue isolation procedures. The pycnidium of the isolated fungus was spherical or pear-shaped with an ostiole. The conidia were oval to oblong, hyaline, occasionally bi-celled, rounded at both ends under compound microscope. They developed on conidiophores and embedded in a mucilaginous mass of cream�pink to light tan. The fungus was flat, submerged with sparse mycelium on artificial media. Throughout the study, the single spore isolates were maintained by transferring periodically on CDA slants and stored at 4�1�C for further use. Altogether, 25 isolates of A. rabiei were used in the present experiment (Table 1). 
Pathogenicity test. The isolates collected from different parts of the country were tested for their pathogenicity on susceptible chickpea cultivar under artificially inoculated conditions following standard procedures. Seeds of the susceptible chickpea cultivar, JG-62 were sown in pots containing sterilized soil. Single-spore cultures of A. rabiei isolates were grown on CDA at 20�1�C for 15 days. The conidia were harvested and 100 ml suspension of desired concentration (105conidia/ml) was prepared in sterile distilled water (SDW) for inoculation. The morphological characteristics of the re-isolated fungus were similar to the original fungus used for pathogenicity.
Thirty days old plants were inoculated with such spore suspensions using a hand atomizer in three replications. Control plants were sprayed with SDW. The plants were concealed with plastic bags for 72 h and after that the � upper cover of the plastic bags were cut open using a scissor for proper aeration and sunlight but effectively prohibit the spread of spores from plants of one pot to another. The relative humidity above 90% was maintained by spraying of sterile water 5 times daily for 6 days and after symptom initiation, the water was sprayed 3 times daily. Disease reaction was evaluated at 15 days after inoculation using 1-9 rating scale13. Re-isolation of the pathogen was made from the diseased plants to confirm the identity of the pathogen and establish the Koch�s postulates. 
Standardization of differential genotypes. The 91 chickpea genotypes were screened to obtain a new set of differentials following the procedures described in the pathogenicity test. These 91 genotypes included the majority of genotypes used earlier for race determination in different parts of the world by earlier workers as per their availability in genebanks and institutions14. Out of this, 10 chickpea genotypes were identified as differentials in the present study representing various degree of resistant (GL 26054, H00 108, ICC 1467, ICC 1903, ICC 3996 and ICC 15978), moderately resistant (GPF 2, ICC 1527 and ICC 11879) and highly susceptible (ICC 4991) reactions.
Virulence analysis. The standardized differential genotypes were used to determine the races of A. rabiei isolates. The experiment was conducted twice under controlled environmental conditions at phytotron following completely randomized design. Following standard procedures, the differentials were sown in pots filled with sterilized soil. The seeds of each genotype were sown in each pot in three replications. Fifteen days old plants were inoculated by 25 isolates of A. rabiei separately for all 10 genotypes by spraying of conidial suspension (105conidia/ml). The plants were incubated in a growth chamber at 18-25�C and 12 h photoperiod.The inoculum was prepared as mentioned earlier. The control (uninoculated) set of plants were maintained by spraying sterile water only. Before inoculation, the pots were irrigated heavily and after inoculation the plants were instantly covered all around with transparent polythene sheets to maintain humidity (>80% RH) and avoid chances of contamination.
Observations on disease severity were recorded at 15 days after inoculation. Randomly 5 plants from each pot were selected to record the observations in terms of disease development. The genotypes were assessed for disease development using 1-9 rating scale where grading 1.0 to 3.0 represented resistant (R); 4 to 5 as moderately resistant (MR) and 6 to 9 were considered as susceptible (S). 
Data analysis. The date on disease grade was recorded in each treatment using 1-9 rating scale and analysed in completely randomized block design. The genotypes differentiating the isolates among each other by showing different reactions as resistant/moderately resistant to susceptible were identified for race/pathotype of the pathogen. 
Results
The disease symptoms appeared in about five days after inoculation by displaying minute brown lesions on leaves and stems of the inoculated seedlings which gradually increase in size and girdle the stem causing its breakage and death of the plants. Abundant pycnidia developed on the necrotic lesions. All the isolates of A. rabiei proved pathogenic on the susceptible chickpea host, JG 62 by showing 7-9 virulence (susceptible) grades on 1-9 rating scale (Table 1). 
On virulence analysis of the 25 isolates of A. rabiei showed varying disease grades and reactions on the differentials andtypical ascochyta blight symptoms were observed on the susceptible genotypes. The differential genotype, ICC 4991 showed grades ranging from 6-9 against all isolates of the pathogen and regarded as the most susceptible differential in both the experiments. Whereas the most resistant differential was observed in the genotype H00 108 because barring a susceptible responseto AR25 isolate, showed resistant and moderately resistant reactions against the remaining isolates (Table 2). Five isolates of A. rabiei namely AR1, AR2, AR7, AR8 and AR9 caused only one susceptible reaction on the differential genotype, ICC 4991 and form the least virulent category. Only one isolate namely AR25 produced susceptible reactions to all the ten differential genotypes. The remaining isolates have variation in the disease reactions on the differentials (Table 3).
Based on the differential reactions of the genotypes seven races of A. rabiei were identified (Table 4). Race 1 was found in Delhi, Himachal Pradesh and Jammu and Kashmir (Fig.1). Two genotypes ICC 1467 and GL 26054 showed resistant reaction and identified as differential for race 1. Race 2 was detected from Haryana, Himachal Pradesh and Punjab and its identification was based on the combination of resistant/moderately resistant and susceptible reactions on ICC 1467 and GPF2, respectively. Race 3 was found only in Himachal Pradesh. Its identification was based on the moderately resistant reaction on the genotype GPF 2 and susceptible reaction on ICC 1903. Race 4 was found only in Jammu and Kashmir and its identification was based on the moderately resistant reaction on GL 26054 and susceptible reaction on ICC 11879. Race 5 was found in Punjab and Rajasthan. Its identification was based on the moderately resistant reaction on ICC 1467 and susceptible reaction on ICC 15978. Race 6 was found in Uttarakhand. Its identification was based on the moderately resistant reaction on ICC 15978 and susceptible reaction on ICC 1467. The race 7 was found in Uttar Pradesh and it was differentiated by the susceptible reactions on all the differential genotypes.  
Discussion
Based on morphological characteristics of the mycelium, pycnidia and conidia the isolated fungus was identified as A. rabiei. Understanding the pathogenic variability is an important for development of resistant varieties. In the present study, the isolates of A. rabiei collected from Northern states of India were analysed for their variability. The reason being these areas are favouring frequent ascochyta blight outbreak and hotspot for the disease. The isolates of A. rabiei proved pathogenic on the susceptible cultivar. All the isolates were virulent showing susceptible reaction.  However, isolate AR2 was comparatively less virulent on the susceptible cultivar, which might be due to presence of less virulence gene in the isolates.   Earlier to this, nine isolates were tested for pathogenicity and identified three groups based on their virulence as weakly, intermediate and highly virulent15. In present study all the isolates were proved to be virulent. 
The differential genotypes exhibited variable reactions against different isolates of the pathogen, which forms the basis for the establishment of their race identity. The genotype ICC 4991 was found to be the susceptible against large number of the isolates followed by the genotypes, ICC 1527, ICC 1903 and GPF 2. The genotype H00 108 followed by ICC 3996 and ICC 15978 proved to be resistant against majority of the isolates. The remaining differentials were variable in their reactions profile. These differences might be due to different levels of susceptibility and resistance among the genotypes selected for pathogenic variability, which later would be able to distinguish the isolates and classified them into groups. 
The isolates of A. rabiei were grouped into seven categories and each category was considered as a race of the pathogen. The differential genotypes for each race were identified. The order of race begins with the least virulent ones beginning with race 1 and ending withrace 7 which was the most virulent because it caused susceptibility in all the genotypes followed by race 6 and race 5. Race 1 showed resistant reactions against most of the genotypes and present in Delhi, Himachal Pradesh and Jammu and Kashmir and race 2 which was found in Haryana, Himachal Pradesh and Punjab, were considered the most scattered races. The present results are supported by the findings of Kumar et al., 200916 who reported 7 distinct pathotypes of A. rabiei based on their reactions but they have used only nine isolates and seven differential genotypes of chickpea. Earlier to his study, variable number of races (2-12) of A. rabiei reported worldwide using different differentials. The present findings did not match with earlier reports in respect of number of races and differentials used might be due to differences in cultivars and virulence in the isolates. One of the earliest reports indicated prevalence of 2 races of A. rabiei reported in India17. Subsequently, 3 pathotypes of A. rabiei detected using 11 chickpea lines in North western Algeria18 and Pakistan19 Likewise, 4 races/pathotypes of A. rabiei were described in Algeria20 and in Syria21 while six races of Didymella rabiei were reported from Turkey using 7 chickpea cultivars22. In contrast to present study, the isolates of A. rabiei�could not be categorised�into pathotypes or races from the Western province of Iran23. The number of isolates used in the present study represents eight north Indian states where the disease is of regular occurrence due to favourable climatic conditions. A set of differentials designed in the present study is based on the variable reactions of the common genotypes used by earlier worker worldwide. 
The present finding provides important and up-to-date information about the race pattern of Ascochyta rabiei prevalent in India along with their differential genotypes. The ten differential genotypes of chickpea can be used for virulence analysis of A. rabiei isolates worldwide. The information on pathogenic variability will be useful for the plant pathologists to adopt a suitable management approach against the prevailing races and be more vigilant in areas where the virulent race is predominant. The information is also useful to the plant breeders in improving/developing chickpea varieties resistant to a particular race of A. rabiei. Mechanisms of disease resistance in chickpea against A. rabiei and disease epidemiology have to be investigated to enhance the disease management strategies. 

Acknowledgements
The first author is grateful to ICAR- Indian Agricultural Research Institute, New Delhi for providing the research facilities and authors are also thankful to Dr. Ashwini Kumar, Dr. Mamta Sharma, Dr. S.K. Singh and Dr. Livinder Kaur for providing disease specimen/fungal cultures. Special thanks to National Phytotron Facility, IARI, New Delhi for providing the plant growth chamber and ICRISAT, Hyderabad for providing the chickpea seeds.
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Atik O, Seid A, Abang MM, Imtiaz M, Hamwieh A, et al. (2013) Pathogenic and genetic diversity of Didymella rabiei affecting chickpea in Syria. Crop Protection 46: 70 79.
Turkkan M, Dolar FS (2009) Determination of pathogenic variability of Didymella rabiei, the agent of ascochyta blight of chickpea in Turkey. Turkish Journal of Agriculture and Forestry 33: 585 591.
Vafaei SH, Rezaee S, Moghadam A, Zamanizadeh HR (2015) Virulence diversity of Ascochyta rabiei the causal agent of Ascochyta blight of chickpea in the western provinces of Iran. Archives of Phytopathology and Plant Protection 48: 17�20.

Figure caption
Fig.1. Distribution pattern of races of Ascochyta rabiei in different parts of India.
Table captions
Table 1. Pathogenicity test of Ascochyta rabiei isolates on chickpea cultivar, JG-62 at 15 days of inoculation
Table 2. ����`�b�d�l�n���ؽ��2�<�@�B�H�J�~�Ծ��d���ʻʻʻ��ʜʻ��scP<P'hu7OhvT6�CJOJQJaJnH	tH	$hu7OhvTCJOJQJaJnH	tH	hvTCJOJQJaJnH	tH	$hNvjhvTCJOJQJaJnH	tH	+hvThvTCJOJPJQJ\�aJnH	tH	h7ihvTCJOJQJaJhNvjhvT6�CJOJQJaJhNvjhvTCJOJQJaJhvTCJOJQJaJ$h�<�hvTCJOJQJaJnH	tH	,h�QahvTCJOJQJaJmH	nH	sH	tH	d���¿ĿԿֿ� �!�9�I�����������������÷���������ڨzdJ=hNvjh�TPJnH	tH	2hNvjh�T5�CJOJQJ]�aJmH	nH	sH	tH	+hNvjhvT5�CJOJPJQJaJnH	tH	h�<�hvTCJOJQJaJh7ihvTCJOJQJaJhNvjhvT6�CJOJQJaJhNvjhvTCJOJQJaJhvTCJOJQJaJh�<�hvThvTCJOJQJaJnH	tH	$hu7OhvTCJOJQJaJnH	tH	$hW�hvTCJOJQJaJnH	tH	������ �<�=�>�M�S�T�U�V�h�i�l�|�����ƺ����|maRCaC3hNvjh�]I6�CJOJQJaJhNvjh�]ICJOJQJaJhNvjh�E�CJOJQJaJhQ�CJOJQJaJhNvjh�CJOJQJaJhNvjh�TCJOJQJaJ+hNvjh�T5�CJOJPJQJaJnH	tH	hNvjh�ThNvjh�]QKHhNvjh�KHhNvjh�T6�KH]�hNvjh�TKHhNvjh�E�PJnH	tH	hamPJnH	tH	hNvjh�PJnH	tH	hNvjh�*PJnH	tH	|�}�������������N�^�z����������������	�
��������Ǹ���������|m]m���|N�NhNvjhQPcCJOJQJaJhNvjhY�6�CJOJQJaJhNvjhY�CJOJQJaJhNvjh�E�CJOJQJaJhNvjh�T6�CJOJQJaJUh?P�CJOJQJaJhNvjh�CJOJQJaJhNvjh�TCJOJQJaJhNvjh�]I5�CJOJQJaJhQ�CJOJQJaJhNvjh�]ICJOJQJaJhQ�6�CJOJQJaJDisease grading on differential genotypes of chickpea against the isolates of Ascochyta rabiei at 15 days post inoculation
Table 3. Disease reactions on differential genotypes of chickpea against the isolates of Ascochyta rabiei at 15 days post inoculation
Table 4. Details of races of Ascochyta rabiei in different parts of India








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