Country-wide distribution map of YMD-causing viruses

Overview

The distribution map aims to understand the national spread of Begomoviruses responsible for Yellow Mosaic Disease (YMD) in legumes. By mapping these viruses across India, we can idenjpgy patterns based on location and crop type. This map provides insights into the geographical distribution and prevalence of YMD-causing begomoviruses, aiding in the development of targeted management strategies.

Yellow mosaic disease in pulse crops

YMD, caused by begomoviruses, is a significant threat to legume crops, particularly in Asia and Southeast Asia. It affects vital food crops like mungbean, urdbean, cowpea, and soybean, leading to substantial yield losses. Other affected legumes include horsegram, mothbean, common bean, Dolichos, Kudzu, Velvet bean, Rhynchosia, Cajanus scarabaeoides, and pigeonpea.

Symptomatology and diagnostics

YMD-affected legume plants exhibit similar yellowing symptoms, making visual idenjpgication of the specific causing virus challenging. Accurate diagnosis is crucial for effective disease management. To address this, we have developed PCR-based diagnostic tools for precise idenjpgication of begomoviruses associated with YMD in various legume crops and weed hosts. Our patented Multiplex-PCR kit allows for the simultaneous detection of four viruses based on amplicon size.

YMD transmission

YMD in leguminous crops is primarily transmitted by whiteflies. These tiny, sap-sucking insects are vectors for the begomoviruses that cause YMD. When a whitefly feeds on an infected plant, it acquires the virus particles. Subsequently, when it feeds on a healthy plant, it can transmit the virus, initiating a new infection cycle. Several species of whiteflies, including Bemisia tabaci, are known to efficiently transmit YMD. Effective whitefly management is crucial for controlling the spread of YMD in legume crops.

Viruses involved in causing yellow mosaic disease

YMD is caused by a group of begomoviruses named Legume Yellow Mosaic Viruses (LYMVs) or legumoviruses. Notable legumoviruses include:

• mungbean yellow mosaic India virus (MYMIV) or Begomovirus vignaradiataindiaense
• mungbean yellow mosaic virus (MYMV) or Begomovirus vignaradiatae
• horsegram yellow mosaic virus (HgYMV) or Begomovirus loniceramusivi
• dolichos yellow mosaic virus (DoYMV) or Begomovirus dolichoris
• Rhynchosia yellow mosaic virus (RhYMV) or Begomovirus rhynchosiaflavi
• Rhynchosia yellow mosaic India virus (RhYMIV) or Begomovirus rhynchosiaindiaense
• velvet bean severe mosaic virus (VbSMV) or Begomovirus mucunae
• kudzu mosaic virus (KuMV) or Begomovirus puerariae
• soybean mild mottle virus (SbMMV) or Begomovirus glycinevariati
• soybean chlorotic blotch virus (SbCBV) or Begomovirus glycinepallidi
• Desmodium mottle virus (DeMV) or Begomovirus desmodii
• Cajanus scarabaeoides yellow mosaic virus (CsYMV)

Genome organization of legume yellow mosaic viruses (LYMVs)

LYMVs have two circular single-stranded DNA molecules: DNA-A and DNA-B. DNA-A is essential for viral replication and coat protein formation, while DNA-B is crucial for successful infection. Both DNA-A and DNA-B are approximately 2.6 to 2.7 kilobase pairs in length, separated by an intergenic region (IR) containing a highly conserved common region (CR).

DNA-A contains six to seven open reading frames (ORFs):

• Virion-sense ORFs: AV1 (coat protein) and AV2 (pre-coat protein).
• Complementary-sense ORFs: AC1, AC2, AC3, AC4 and AC5, involved in replication, transcription, and host defence suppression.

DNA-B has two ORFs:

• BV1 ORF: Encodes the nuclear shuttle protein.
• BC1 ORF: Encodes the movement protein.

Disease cycle

YMD presents a complex epidemiological scenario characterized by a muljpgaceted disease cycle. The perpetuation of YMD is contingent upon a combination of factors, including a diverse host range, a polyphagous vector, and the influence of agro-climatic conditions. A wide spectrum of cultivated legumes and weed species serve as hosts for YMD, ensuring a continuous source of inoculum throughout the year. The population dynamics of the whitefly vector, the primary mode of virus transmission, are significantly influenced by prevailing weather conditions. India’s diverse agro-climatic zones, characterized by distinct weather patterns, support the cultivation of a variety of pulse crops. This crop diversity, coupled with the adaptability of certain legumes to different climatic conditions, results in year-round availability of susceptible hosts.

For instance, in the northern regions of India, the cultivation of mungbean, urdbean, cowpea, and pigeonpea is predominantly practiced during the spring-summer (Rabi) and rainy (Kharif) seasons. The extended duration of certain pigeonpea cultivars until April provides a critical source of primary inoculum for subsequent crops. Additionally, winter-season common beans can contribute to the initial establishment of the disease.

Once introduced into a crop, the virus rapidly disseminates through whitefly-mediated transmission, leading to sustained disease prevalence. This intricate interplay of host plants, vector populations, and environmental factors underscores the challenges associated with YMD management.

Development of the distribution map

To understand the spread of YMD-causing viruses, we processed a total of 259 symptomatic leaf samples from six pulse crops: mungbean (n=148), urdbean (n=69), cowpea (n=26), horsegram (n=5), and mothbean (n=10), as well as the wild relative Vigna stipulacea (n=1). These samples were collected from 38 different locations representing five agro-climatic zones for legume crops in India: the Central Zone (CZ), South Zone (SZ), North East Plain Zone (NEPZ), North West Plain Zone (NWPZ), and North Hill Zone (NHZ).

Using PCR-based detection methods, we idenjpgied the presence of MYMIV, MYMV, or HgYMV in these samples. Detailed methodologies for PCR-based detection can be found in our previous publications (Naimuddin et al., 2011a,b,c; Akram et. al., 2020; Akram et al., 2022; Kumar et al., 2024). Additional samples tested included Rhynchosia minima (n=15) (Akram et.al., 2024), dolichos (n=10) (Akram et al., 2015), mungbean (n=9), urdbean (n=6), cowpea (n=26), rajma or French bean (n=21), and weeds (n=9), all collected from the IIPR main campus. These additional tests revealed the presence of MYMIV, MYMV, RhYMV, and DoYMV in the samples. Positively tested samples underwent sequencing of the PCR products to validate the causal viral agent, resulting in the generation and characterization of molecular sequencing data for DNA-A (full-length and partial) and DNA-B (full-length) components of the five viruses. Specifically, we obtained 119 full-length and 72 partial sequences of the DNA-A component, and 106 full-length sequences of the DNA-B component for MYMIV, MYMV, HgYMV, DoYMV, and RhYMV.

To explore the current distribution of 12 legumoviruses, we gathered previously reported information on their isolates, including locations and hosts, from the public database NCBI. This data encompassed reports from 171 locations across 16 countries. Including the data on DNA-A and DNA-B components characterised by us, there were 581 DNA-A and 287 DNA-B sequences (full-length and partial) from India represented 119 locations for eight legumoviruses: CsYMV, DoYMV, HgYMV, MYMIV, MYMV, RhYMV, RhYMIV, and VbSMV. So far, CsYMV, RhYMIV, and VbSMV are reported from single locations in Raipur (CZ), Thiruvananthapuram (SZ), and Lucknow (NEPZ), infecting Cajanus scarabaeoides, R. minima, and Mucuna pruriens (velvet bean), respectively.

RhYMV was reported from four different locations in the CZ and NEPZ, while HgYMV had a distribution restricted to the SZ with 60 reports from 30 locations. DoYMV and MYMV were found in all zones except the NHZ, with 43 reports from 12 locations and 146 reports from 40 locations, respectively. MYMIV was the most widespread, observed throughout five agro-climatic zones with 324 reports from 75 locations. Our efforts highlight the predominant existence of MYMIV, MYMV, and HgYMV in the SZ, with evidence of mixed infections involving any combination of these three species, as well as simultaneous infections of all three.

The 581 reports for eight legumoviruses from 119 locations can be categorized into 53 hosts, consisting of 22 species of crops (both legume and non-legume) and 31 species of weeds. These “weeds” are either ornamental flowering plants used for gardening or plants naturally occurring near legume crop fields. Among legume crops, MYMIV and MYMV were most frequently detected in mungbean, followed by urdbean and soybean. They were also found in cowpea and French bean to a lesser extent. Other legume crops, such as lentil, clusterbean, pigeonpea, mothbean, dolichos, and horsegram, were reported as hosts for MYMIV, MYMV, or both. DoYMV was predominantly reported in dolichos, followed by cowpea and French bean, with only two reports in mungbean, and none in urdbean. HgYMV was mainly found in French bean, followed by horsegram and pigeonpea, and was also reported in mungbean, urdbean, soybean, limabean, cowpea, and mothbean. Non-legume crops such as Cucurbita maxima, Solanum lycopersicum (Agnihotri et.al., 2019), Annona squamosa, and Solanum melongena were reported to carry MYMIV, whereas DoYMV was found in Capsicum annum. In total, there were 45 reports documenting infections in 31 distinct weed hosts in India, with MYMIV accounting for nine reports, MYMV for 19, DoYMV for five, HgYMV for 11, and RhYMIV for one, representing 17 locations.

The distribution map, currently operational at https://www.icar-iipr.org.in/new-map-location provides a comprehensive visual representation of the prevalence and spread of key legumoviruses across India. As new data becomes available, the map can be updated to reflect the most current information.

Global presence of legumoviruses

Legumovirus incidences have been documented across a diverse range of countries beyond India, reflecting a widespread global distribution. Reports of YMD-causing viruses have been observed in neighbouring nations such as Nepal, Pakistan, Bangladesh, and Sri Lanka. The presence of these viruses extends to East Asia, with incidences reported in Vietnam, Thailand, Indonesia, Cambodia, and China, as well as reaching Oman in Southwest Asia. Additionally, African countries such as Benin, Togo, Cameroon, Nigeria, and Uganda have also reported these viruses.

MYMIV has been reported in Bangladesh, India, Indonesia, Nepal, Oman, and Pakistan. MYMV incidences have been documented in Cambodia, India, Pakistan, Thailand, and Vietnam. HgYMV and DoYMV are reported in Sri Lanka and Bangladesh, respectively, aside from India. DeMV and SbMMV have been reported exclusively in Uganda and Nigeria, respectively. SbCBV has been found in several West African countries, including Benin, Togo, Cameroon, and Nigeria. KuMV has been reported in China and Vietnam, while RhYMV reports are limited to Pakistan and India.

However, it is important to note that the existing reports from these countries are insufficient to fully infer the distribution patterns of these viruses. More comprehensive data and further research are needed to accurately understand the global spread and impact of YMD-causing viruses.

Prevalence

The analysis of YMD-causing viruses across India reveals notable regional variations in prevalence and dominance. Across 119 locations and total available reports, MYMIV is the most abundant (55.9 % and 45.7 %, respectively) and dominant (0.56 and 0.46, respectively), followed by MYMV, HgYMV and others. Whereas, MYMV was observed to have a wider host range followed by MYMIV. Zone-wise reports highlights that HgYMV and MYMV are significant in the SZ, MYMIV dominates in the CZ, and MYMIV and MYMV are key in the NEPZ. The diversity indices indicate that the NEPZ has the highest overall diversity, whereas the SZ shows considerable species evenness. These findings underscore the need for region-specific strategies to manage and monitor YMD-causing viruses effectively across different zones.

Significance of the map

The All India Coordinated Research Project (AICRP) on pulses is pivotal in evaluating new pulse and legume varieties, alongside their associated production and protection technologies, across multiple locations. A key component of this project involves the exchange of advanced breeding materials and genotypes. However, assessing these materials against all species and strains of YMD-causing viruses at each location poses a significant challenge, complicating the development of effective YMD-resistant cultivars.

To address this issue, it is essential to compile detailed information on the prevalence of various YMD-causing virus species across different agro-climatic zones. Crops such as mungbean, urdbean, cowpea, soybean, horsegram, and mothbean show variations in YMD development both temporally and spatially. These variations are influenced by overlapping cropping patterns, local weather conditions, fluctuations in vector populations, and the presence of diverse virus species in different regions.

Previously, knowledge was limited to the regional distribution of MYMV and HgYMV in southern India and MYMIV in northern and central regions. This map now provides researchers and plant breeders with crucial, centralized information on the presence of various legumovirus species causing YMD, including both single and mixed infections. By consolidating this information, the map streamlines the process of understanding virus distribution and reduces the need for additional detection methods. Such comprehensive insights are invaluable for the development of zone-specific YMD-resistant cultivars, enhancing the resilience and productivity of legume crops across diverse agro-climatic conditions.

Further readings

1. Akram, M., Kamaal, N., Kumar, D., Datta, D., and Agnihotri, A. K. (2024). Characterization, phylogeny and recombination of Rhynchosia yellow mosaic virus infecting Rhynchosia minima, a wild relative of pigeonpea (Cajanus cajan) from India. Virus Genes 61, 110–120.
2. Kumar, D., Akram, M., and Kamaal, N. (2024). Low-cost water boiling method successfully employed to extract DNA from a single whitefly to detect yellow mosaic disease-causing viruses in PCR. Archives of Phytopathology and Plant Protection, 1–17.
3. Akram, M., Kamaal, N., Pratap, A., Muin, A., Agnihotri, A. K., Rathore, U. S., et al. (2022). Species diversity, phylogeny and evidence of recombination in begomoviruses associated with yellow mosaic disease of moth bean (Vigna aconijpgolia) in South India. Journal of Phytopathology 170, 300–314. doi: 10.1111/jph.13079
4. Akram, M., Kamaal, N., Pratap, A., Muin, A., Ahmad, S., Agnihotri, A. K., et al. (2020). Molecular characterization of begomoviruses causing yellow mosaic disease in Vigna stipulacea and evidence of recombination. Journal of Food Legumes 33, 232–244.
5. Agnihotri, A. K., Mishra, S. P., Ansar, M., Tripathi, R. C., Singh, R., and Akram, M. (2019). Molecular characterization of Mungbean yellow mosaic India virus infecting tomato (Solanum lycopersicum L.). Australasian Plant Pathology 48, 159–165. doi: 10.1007/s13313-018-0611-7
6. Akram, M., Naimuddin, Agnihotri, A. K., Gupta, S., and Singh, N. P. (2015). Characterisation of full genome of Dolichos yellow mosaic virus based on sequence comparison, genetic recombination and phylogenetic relationship. Annals of Applied Biology 167, 354–363. doi: 10.1111/aab.12231
7. Naimuddin, Akram, M., and Gupta, S. (2011a). Idenjpgication of Mungbean yellow mosaic India virus infecting Vigna mungo var. silvestris L. Phytopathologia mediterranea 50, 94–100.
8. Naimuddin, Akram, M., and Pratap, A. (2011b). First report of natural infection of Mungbean yellow mosaic India virus in two wild species of Vigna. New Disease Reports 23, 21–21. doi: 10.5197/j.2044-0588.2011.023.021
9. Naimuddin, Akram, M., Pratap, A., Chaubey, B. K., and John, J. K. (2011c). PCR based idenjpgication of the virus causing yellow mosaic disease in wild Vigna accessions. Journal of Food Legumes 24, 14–17.