Indian Journal of Agricultural Research

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Relationship between Whiteflies, Yellow Mosaic Severity, Weather and Crop Age in Soybean

Sunil Kumar1, Pawan K. Amrate2,*, M.K. Shrivastava2, R. S. Marabi3, Shivani Jawarkar2, Sanjay Kharte1, Kailash Chaukikar3, Akash Barela2
1Department of Plant Pathology, Jawaharlal Nehru Krishi Vishwa Vidyalaya, Jabalpur-482 004, Madhya Pradesh, India.
2Department of Plant Breeding and Genetics, Jawaharlal Nehru Krishi Vishwa Vidyalaya, Jabalpur-482 004, Madhya Pradesh, India.
3Department of Entomology, Jawaharlal Nehru Krishi Vishwa Vidyalaya, Jabalpur-482 004, Madhya Pradesh, India.

Background: Yellow mosaic disease (YMD), caused by the Mungbean yellow mosaic India virus (MYMIV), seriously affects soybean production in the central and northern regions of India.

Methods: The present investigation was conducted to reveal the relation among the fluctuating population of whiteflies, YMD progression, meteorological parameters and crop age in four varieties, i.e. 335, JS 20-34, NRC 86 and MACS 1520, at J.N.K.V.V., Jabalpur, during kharif 2021 (June to September). The whitefly population, by visual and cage and YMD severity were recorded at weekly intervals. 

Result: Whiteflies first appeared 13 days after sowing (27th SMW) and reached a peak of 7.73 per plant (cage) and 3.29 per trifoliate (visual) at 29th SMW (July, 16-22). During this maximum and minimum temperature, morning and evening RH were 33.4 and 25.4°C, 84.10 and 70.0 %, respectively. Whiteflies on JS 335 (0.639* and 0.635*) and MACS 1520 (0.672* and 0.639*) significantly positively correlated with maximum temperature in visual and cage counts. Wind speed exhibited a significant negative relation with a whitefly count of JS 335 (-0.753*) and MACS 1520 (-0.764*). YMD initiated (28th SMW) at high temperature (max 33.3°C and min 25.1°C), low rainfall (33.2 mm), less humid conditions (evening 58.3-morning 85.1 %) and presence of whitefly. In contrast, at the time of maximum disease progression (32nd SMW), comparative low temperature (max 28.5 and min 24.2°C) and high humid conditions (evening 79.0-morning 90.0) prevailed. Among the four varieties, maximum disease severity was recorded in JS 20-34 (48.16%). The corresponding week’s maximum temp (0.771**) and sunshine hours (0.792**) were negatively significant and evening RH (0.717*) and wind speed (0.708*) had a positively significant relation with mean YMD progression. A similar significant association was also obtained between the previous week¢s parameters and disease. YMD and whitefly exhibited a negative, non-significant association. Crop age also linked non-significantly with YMD progression. The present findings could be utilized to predict vector and YMD and to formulate appropriate management strategies for both.

Soybean [Glycine max (L.) Merrill] (2n=40) regarded as “wonder crop”, “golden bean”, “Miracle bean”, “protein hope of the future”, “Super legume” and “Golden Nugget” is the richest, cheapest and most accessible source of best quality proteins, fats and fibres (Liu, 2000; Upadhyay et al., 2020; Barela et al., 2022; Ramlal et al., 2023; Jawarkar et al., 2023). It is one of the richest vegetarian sources of total proteins (36.1-42.8%); additionally, it contains considerable edible oil (16.8-20.2%) and several vitamins, minerals, essential fatty acids, omega-3 fatty acids and antioxidants, thereby utilizing for several purposes, like food and feed for human and animals, pharmaceutical and industrial etc (Kumar et al., 2020; Uikey et al., 2022; Banerjee et al., 2023; Amrate et al., 2024). Its consumption reduces the risk of developing cancer, heart attack and cholesterol and triglyceride levels in the human body (Parle et al., 2014; Banerjee et al., 2022). In India, it is grown over an area of 12.7 Mh with production of 10.45 MT and productivity of 0.82 tons per hectare as per the data of 2020-21 (USDA, 2022). However, India is among the top five nations regarding soybean cultivation in the world, but production, productivity and area has fluctuated since 2012-13 (Sagarika et al., 2023; Amrate et al., 2024).
       
Soybean is the preferred host for most kinds of fungi, bacteria, nematodes and viruses and about 135 pathogens have been observed infecting soybean throughout the world (Hartman and Hill, 2010). Among these,>50 viruses have been observed affecting soybean crops (Nyvall, 1989). In India, soybean crop is grown in the kharif season under rainfed conditions wherein severe attacks of many diseases have been reported (Rajput et al., 2021; Amrate et al., 2023a; Amrate et al., 2023b; Amrate et al., 2024).
       
There are fourteen disease which infect soybean crop at different growth stage in central Indian conditions (Amrate et al., 2021; Amrate, 2024).  Among all the diseases, yellow mosaic is a major one distributed in India, Srilanka, Bangladesh, Pakistan and Thailand (Kumar et al., 2022). During the early 1970s, YMD was observed in the northern plains of India. It gradually started appearing in central India and has become a common disease of soybean, mungbean and urdbean (Amrate et al., 2023a). In Central India, yellow mosaic disease in soybean is caused by Mungbean yellow mosaic India virus (MYMIV) and exclusively transmitted by whitefly (Bemisia tabaci Genn.) in a persistent manner (Talukdar et al., 2013; Kumar et al., 2014; Amrate et al., 2023a). Yellow mosaic is a common disease that infects soybean varieties and many genotypes yearly in central and northern Indian conditions (Amrate et al., 2018; Singh and Aravind, 2019; Kumar et al., 2022; Amrate et al., 2023a). Its vector, the whitefly, sucks the phloem sap from the lower surface of leaves and requires a temperature higher than 26°C and 60% relative humidity for optimum development (Nene, 1972; Butler et al., 1983). A single viruliferous whitefly can able to transmit virus (Swathi et al., 2023). Mungbean yellow mosaic virus-affected plant exhibits irregular and varying size contrast yellow-green patterns (mottels) on leaves (Silodia et al., 2018; Amrate et al., 2020a; Kumar et al., 2022). YMD quickly spreads during the early stage of soybean growth, resulting in the alteration of biochemical and yield-attributing traits and severe yield reduction of up to 85.7% in soybeans (Amrate et al., 2020b; Kumar et al., 2022). In India, annual yield losses caused by YMD in soybean, black gram and green gram have been recorded at about 300 million USD per year (Varma and Malathi, 2013). It has been noticed that disease incidence and severity of YMD in soybean varied year to year depending upon vector population and weather conditions. Considering the significance of yellow mosaic disease in soybean cultivation, the present investigations were undertaken to establish a relation between the development of yellow mosaic of soybean with vector and meteorological parameters.
Experimental details
 
A field experiment was undertaken to record the influence of prevailing weather and vector (Whitefly) on yellow mosaic disease severity in soybean during kharif, June to September 2021, at the experimental field of AICRP on Soybean at J.N.K.V.V., Jabalpur (latitude 23°12’42"N and longitude 79°56’53"E).  Four yellow mosaic susceptible varieties, i.e. JS 20-34, JS 335, NRC 86 and MACS 1520, were sown on 25th June 2021 in three replications. Sowing was done in a well-drained sandy, loamy soil. Each variety had been maintained in a plot size of 3.0×1.2 m2 (3 rows of 3 m length). Initially, seeds were treated with thiophenate methyl 45%+pyraclostrobin 5% @ 1.5 ml/kg seed and sprayed with tebuconazole 25.9 EC @ 1.25 ml/litre at 45 days to avoid the attack of fungal disease in the experimental plot. Proper thinning was done ten days after sowing to maintain the plant-to-plant distance (7-8 cm) and the row-to-row distance was kept at 40cm. All packages and practices were applied to care for the crop except insecticides. 
 
Recording of meteorological parameters
 
Meteorological variables at the experimental location during the cropping season, viz., maximum and minimum temperature, morning and evening relative humidity, wind speed, sunshine hours, rainy days and rainfall, were collected from the Meteorological Observatory, Department of Physics and Agro-meteorology, College of Agricultural Engineering, J.N.K.V.V., Jabalpur (M.P) (Fig 1). 
 

Fig 1: Weekly weather variables, Whitefly (WF) and progression of YMD (PDI) in soybean varieties during Kharif 2021 at Jabalpur.


 
Monitoring of vector
 
Whitefly populations on all four varieties were monitored at weekly intervals by visual and cage methods. 
 
By visual
 
Whitefly present on upper two trifoliate leaves were counted during morning hours (before 8:00 AM) by twisting of leaves (Bisht et al., 2017; Amrate et al., 2023a) (Fig 2). Population of adult fly was recorded from five randomly selected plants.
 

Fig 2: Counting of adult whitefly by visual (A+B) and Cage Method (C+D).


 
By cage
 
The cage was designed with plastic cylinders of different heights and diameters (20×15, 40×25 and 60×45 cm). The inner wall of the cage was coated with black paint to induce darkness and one end was left open while the other was closed with transparent polythene. The cage was fixed so that no space was left to escape the adult whitefly from inside the cage. The adult whitefly population was recorded on five randomly selected plants with the help of a cage. To record the number of adult whitefly populations, the cage was carefully placed on an individual plant without disturbing it. The adult whitefly congregated on the inner surface of the polyethene due to its phototactic behaviour, which enabled it to count them easily (Fig 2). In the early stage of crop growth, narrow-diameter cages were used, while in the later stages, cages with broader diameters with more height and sufficient space to cover an individual plant were used for recording the observations (Marabi et al., 2017a).
 
Recording of YMD intensity
 
Plants were observed critically for yellow mosaic development throughout the cropping season. Disease severity was recorded weekly per standard meteorological weeks from the vegetative stage (V1) to the reproductive stage (R6). The severity of the yellow mosaic was recorded on 20 randomly selected plants. From each plant, four leaves (two upper and two middle) were observed and each was rated on a 0-9 grade disease rating scale (Anonymous, 2019) (Table 1). Per cent disease index (PDI) for yellow mosaic using the above severity grade was calculated as per the formula suggested by Wheeler (1969).

 
 

Table 1: Scoring of yellow mosaic disease by using 0-9 disease rating scale.


       
Calculation of correlation matrix
 
Pearson’s correlation coefficient was calculated based on the current and previous week’s weather, increasing whitefly count and YMD severity at the experimental site for each variety and varietal average. Online statistical tools and MS Excel were used for the calculation. Significance was determined at the 1 (p=0.01) and 5 (p=0.05) per cent levels of error.
Whitefly and weather
 
The first occurrence of whitefly on soybean was detected 13 days after sowing, on the 27th SMW (standard meteorological week), which was July 8th, 2021 (Table 2). The Whitefly population was varied in four varieties (Table 2). The highest whitefly counts, 3.87 per trifoliate (visual) and 8.53 pe plant (cage), were recorded in NRC 86 at 29th SMW (July 16-22). Simultaneously, the highest whitefly counts, 2.80 per plant (visual) and 7.00 per plant (cage) were recorded in JS 335 at 29th SMW. The mean initial whitefly population was 1.80 per trifoliate (visual) and 3.50 per plant (cage) at 27th SMW, i.e. July 8th. After that, a sudden increase in the whitefly population was observed and attained its peak at 29th SMW (July 16-22), which was 3.29 per trifoliate (by visual) and 7.73 per plant (by cage). At the time of the peak of the whitefly, maximum and minimum temperatures were 33.4 and 25.4°C respectively, whereas sunshine, wind speed, rainfall, morning Rh and evening Rh were 5.5 hrs, 3.9 km/hr., 35.4 mm, 84.10 and 70.0, respectively (Fig 1). Whitefly remained active till the crop’s maturity, but a sudden decline in the whitefly population was seen at the time of maturity. The dynamics of the whitefly were nearly uniform in all varieties. Present findings corroborate the findings of Raghuvanshi et al., (2014), Ahirwar et al., (2015) and Marabi et al., (2017a), as they also reported that the first appearance of whitefly on soybean ranged from 14-30 DAS (28th-33rd SMW) to till maturity. Previous workers also reported similar weather parameters during the peak of white flies in the present investigation (Raghuvanshi et al., 2014). 

Table 2: Population dynamics of whitefly on different varieties growing during Kharif 2021.


       
In Pearson correlation, maximum and minimum temperature and sunshine hours exhibited positive relation [r= 0.535, 0.497 and 0.582 (visual) and 0.541, 0.426 and 0.659* (cage), respectively] with mean whitefly population (Table 3). Among varieties, whitefly counts in JS 335 (0.639* and 0.635*) and MACS 1520 (0.672* and 0.639*) significantly correlated with maximum temperature in both visual and cage counts. A similar significant positive relation was exhibited between white flies and sunshine hours. While rainfall, morning and evening humidity, rainy days, wind speed and crop age exhibited negative non-significant correlation with the mean white fly count in a cage of both methods. However, Wind speed exhibited a significant negative relation with the white fly count in a cage of JS 335 (-0.753*) and MACS 1520 (-0.764*). Present findings conform with the findings of many researchers (Kalkal et al., 2015; Marabi et al., 2017a; Marabi et al., 2017b; Amrate et al., 2023a) about white fly, maximum temperature and sunshine hours. However, researchers also reported that max temp had a negative impact on the whitefly population (Sharma and Kumar, 2014). Rainfall negatively correlated with the whitefly population (Marabi et al., 2017a; Amrate et al., 2023a). 
 

Table 3: Relation of weather parameters with whitefly population.


 
Progression of YMD
 
Yellow mosaic disease (YMD) appeared on the 28th SMW (Fig 1). At initiation, yellow mosaic disease severity was very low (Fig 1).  During this period, high temperature (max 33.3°C and min 25.1°C), low rainfall (33.2 mm), less humid (evening 58.3-morning 85.1 %) and high whitefly population [2.65 per trifoliate (visual) and 5.78 per plant (cage)] prevailed. After that, there was a sharp increase in the disease severity between the 30th and the 33rd SMW. Maximum weekly disease progression was noticed in 32th SMW (06/08/2021 to 12/08/2021). At the time of maximum disease progression, max temp and minimum temperature were 28.5 and 24.2°C, respectively, whereas sunshine hours, rainfall, morning RH and evening RH were 0.5 hrs, 11.1 mm, 90.0 and 79.0%, respectively.  While the whitefly population was 1.70 per plant (visual) and 3.04 per plant observed (cage) and the mean whitefly population was 2.37 per plant (Table 2). After that, disease progression was slow and maximum mean severity (36.71%) was recorded at 36th SMW on 76 DAS. Among four varieties, maximum disease severity was recorded in JS 20-34 (48.16%), followed by MACS 1520 (38.86%), JS 335 (30.91%) and NRC 86 (28.92%) (Fig 1, Fig 3). Previous workers have also reported similar weather conditions for the development and progression of YMD (Singh et al., 2009; Silodia et al., 2018; Amrate et al., 2023a). Amrate et al., (2023a) indicated that low mean temp and high rainfall in July (cool) lead to low white fly and low YMD and conversely, high mean temperature and low rainfall in July (hot) lead to high white fly and high diseases in the overall season.
 

Fig 3: Experimental view exhibiting appearance of yellow mosaic during last week of July (V-3 to R-1 crop stage).


 
Relation of YMD, weather, crop age and whitefly  
 
Pearson correlation matrix between corresponding week’s weather parameters, crop age and vector population with YMD severity revealed that max temp and sunshine hours (r = -0.771**and -0.792**, respectively) were significant negatively and evening RH and wind speed (r = 0.717* and 0.708*, respectively) were significant positively correlated with mean YMD progression (Table 4). A similar significant relation was exhibited in the case of all four varieties for a max temperature, sunshine hour, evening RH and wind speed. While rainfall, Morning RH, rainy days and crop age (r = 0.315, 0.597, 0.522 and 0.024, respectively) had a positive, non-significant relation with YMD progress. Meanwhile, in JS 20-34, crop age showed a negative correlation (r = -0.055) with disease progression. Meanwhile, minimum temp and mean vector population (r = -0.613 and -0.341, respectively) were negatively correlated with YMD progression. 
 

Table 4: Pearson correlation matrix between weekly YMD increase in soybean varieties and corresponding current and previous week weather, whitefly and crop age.


       
Relation between disease progression and previous week parameters (viz., weather parameters, crop age and vector population) revealed that evening RH, rainy days and wind speed (r = 0.831**, 0.806** and 0.713*, respectively) had a significant positive correlation with disease severity (Table 4). Similar to the current week’s pattern, max temp and sunshine hours (r = -0.763* and -0.714*, respectively) were negatively correlated with the progression of disease severity. While rainfall, morning RH and crop age had a positive and minimum temp, the mean vector population had a negative, non-significant relation with the disease. A similar pattern, as revealed with the current week’s relation, was exhibited except on rainy days wherein disease progression in all the varieties and their mean were positively significantly related. Previously, Marabi et al., (2017b) reported that maximum temp and sunshine hours significantly positively impacted YMD incidence. Researchers also supported our findings regarding the negative association of YMD with rainfall and other parameters in blackgram and soybean (Marabi et al., 2017b; Srivastava et al., 2021). Amrate et al., (2023a) reported that the coefficient of infection of YMD was significantly correlated with the whitefly population. 
It is concluded that the whitefly population was comparatively  higher in the early stage of the plant during July. Among varieties, JS 20-34 (48.16%) was highly affected by yellow mosaic disease, followed by MACS 1520, JS 335 and NRC 86. At the time of YMD initiation or early stage of disease spread, high temperature (min 25.0°C to max 33.5°C), low rainfall, comparatively less humid conditions (60.0-85.0%) coupled with a high whitefly population may lead to the severe spread of disease in the field in an upcoming fortnight. Whitefly had significant positive and negative relations with maximum temperature and wind speed. Similarly, maximum temp and sunshine hours had a negative significance and evening RH and wind speed had a positive significant relation with YMD progression.
The authors sincerely thank the Head of the Department of Plant Breeding and Genetics, the Head of Plant Pathology and other field staff for their support and guidance during the investigation. They also express their gratitude to the university’s In-charge meteorological observatory for providing weather data for analysis.
The authors declare that they have no conflict of interest.

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