Molecular insights of pigeonpea sterility mosaic virus mixed infections and its variability in pigeonpea

Radhakrishnan ROHINI; Vaithiyanathan SENDHILVEL; Gandhi KARTHIKEYAN; Basavaprabhu L. PATIL; Muthurajan RAVEENDRAN; Mannu JAYAKANTHAN; Maduraimuthu DJANAGUIRAMAN

doi:10.15835/nbha53114329

Authors

Radhakrishnan ROHINI Tamil Nadu Agricultural University, Department of Plant Pathology, Coimbatore, 641003 (IN)
Vaithiyanathan SENDHILVEL Tamil Nadu Agricultural University, Department of Plant Pathology, Coimbatore, 641003 (IN)
Gandhi KARTHIKEYAN Tamil Nadu Agricultural University, Department of Plant Pathology, Coimbatore, 641003 (IN)
Basavaprabhu L. PATIL ICAR-Indian Institute of Horticultural Research, Division of Basic Science, Bengaluru, 560089 (IN)
Muthurajan RAVEENDRAN Tamil Nadu Agricultural University, Department of Plant Biotechnology, Coimbatore, 641003 (IN)
Mannu JAYAKANTHAN Tamil Nadu Agricultural University, Department of Plant Molecular Biology and Bioinformatics, Coimbatore, 641003 (IN)
Maduraimuthu DJANAGUIRAMAN Tamil Nadu Agricultural University, Department of Crop Physiology, Coimbatore, 641003 (IN)

DOI:

https://doi.org/10.15835/nbha53114329

Keywords:

mixed infections, multiplex RT-PCR, pigeonpea, PPSMV-1, PPSMV-2, Sterility Mosaic Disease, Tamil Nadu

Abstract

Pigeonpea sterility mosaic virus-1 (PPSMV-1) and Pigeonpea sterility mosaic virus-2 (PPSMV-2) are the two distinct Emaraviruses causing Sterility Mosaic Disease (SMD), which is an emerging threat to the pigeonpea (Cajanus cajan L. Millspaugh) production in India. The dissemination of virus is progressing at an accelerated rate and existence of PPSMV-1 (Emaravirus cajani) and PPSMV-2 (Emaravirus toordali) exhibiting diversity across the ecosystems. A total of 34 symptomatic and healthy samples were collected from six districts covering Western, North-Eastern, Cauvery Delta Zone and North-Western agro-climatic zones of Tamil Nadu. The disease incidence ranged from 12.8% to 71.6% and the highest mean incidence of 52.67% was recorded in the North-Eastern agroclimatic zone of Tamil Nadu. The RT-PCR and multiplex RT-PCR analysis differentiated the presence of both PPSMV-1, PPSMV-2 and mixed infections. Sequence analysis of RNA1 and RNA3 segments of the virus genomes demonstrated significant genetic heterogeneity among isolates, while phylogenetic relatedness of PPSMV-1 and PPSMV-2 were grouped into distinct clusters. Intra-specific recombination events were observed in the RNA3 segments of both PPSMV-1 and PPSMV-2. There were no recombination events in RNA1 segments of the virus genomes. These results emphasise the widespread distribution and genetic diversity of PPSMV-1 and PPSMV-2 in Tamil Nadu and provide valuable insights for the development of rapid diagnostic tools for effective field management.

References

Acosta-Leal R, Duffy S, Xiong Z, Hammond RW, Elena SF (2011). Advances in plant virus evolution: translating evolutionary insights into better disease management. Phytopathology 101(10):1136-1148. https://doi.org/10.1094/phyto-01-11-0017

Baskar S, Latha TKS, Karthikeyan G, Sudha M, Patil BL (2020). Studies on the molecular variability of sterility mosaic disease of pigeonpea in Tamil Nadu State, India. International Journal of Current Microbiology and Applied Sciences 9(8):2985-2992. https://doi.org/10.20546/ijcmas.2020.908.336

Baskar S, Patil BL, Latha TKS, Karthikeyan G (2021). Variability studies on pigeonpea sterility mosaic Emaraviruses in Tamil Nadu reveals rampant mixed infections and interspecies recombination. Journal of Food Legumes 34(3):173-180.

Elbeaino T, Digiaro M, Mielke-Ehret N, Muehlbach HP, Martelli GP, ICTV Report Consortium (2018). ICTV virus taxonomy profile: Fimoviridae. Journal of General Virology 99(11):1478-1479. https://doi.org/10.1099/jgv.0.001143

Elbeaino T, Digiaro M, Uppala M, Sudini H (2015). Deep sequencing of dsRNAs recovered from mosaic-diseased pigeonpea reveals the presence of a novel emaravirus: pigeonpea sterility mosaic virus 2. Archives of Virology 160:2019-2029. https://doi.org/10.1007/s00705-015-2479-y

Elbeaino T, Digiaro M, Uppala M, Sudini H (2014). Deep sequencing of pigeonpea sterility mosaic virus discloses five RNA segments related to Emaraviruses. Virus Research 188:27-31. https://doi.org/10.1016/j.virusres.2014.03.022

Elbeaino T, Whitfield A, Sharma M, Digiaro M (2013). Emaravirus-specific degenerate PCR primers allowed the identification of partial RNA-dependent RNA polymerase sequences of Maize red stripe virus and pigeonpea sterility mosaic virus. Journal of Virological Methods 188(1-2):37-40. https://doi.org/10.1016/j.jviromet.2012.11.037

Fourth Advance Estimates of Production of Foodgrains for 2021-22 (2022). Department of Agriculture and Farmers Welfare. Directorate of Economics and Statistics. Retrieved 2022 August 17th from: https://static.pib.gov.in/WriteReadData/specificdocs/documents/2022/aug/doc202281792701.pdf

Gandhi K, Suppaiah R, Murugesan S, Krishnan N (2021). RNA interference: a novel technology for virus disease management in crop plants. Madras Agricultural Journal 108. https://doi.org/10.29321/MAJ.10.000482

Jones AT, Kumar PL, Saxena KB, Kulkarni NK, Muniyappa V, Waliya F (2004). Sterility mosaic disease—the “green plague” of pigeonpea: advances in understanding the etiology, transmission and control of a major virus disease. Plant Disease. 88(5):436-445. https://apsjournals.apsnet.org/doi/pdf/10.1094/PDIS.2004.88.5.436

Kallinen AK, Lindberg IL, Tugume AK, Valkonen JPT (2009). Detection, distribution, and genetic variability of European mountain ash ringspot-associated virus. Phytopathology 99(4):344-352. https://doi.org/10.1094/PHYTO-99-4-0344

Kannaiyan J, Nene YL, Reddy MV, Ryan JG, Raju TN (1984). Prevalence of pigeonpea diseases and associated crop losses in Asia, Africa and the Americas. International Journal of Pest Management 30(1):62-72. https://doi.org/10.1080/09670878409370853

Karthikeyan G, Rajamanickam S, Nagendran K (2023). RNA interference against RNA viruses in plants. Plant RNA Viruses 607-625 https://doi.org/10.1016/B978-0-323-95339-9.00004-1

Kormelink R, Garcia ML, Goodin M, Sasaya T (2011). Negative-strand RNA viruses: the plant-infecting counterparts. Virus Research 162(1-2):184-202. https://doi.org/10 .1016/j.virusres.2011.09.028

Kulkarni NK, Kumar PL, Muniyappa V, Jones AT, Reddy DVR (2002). Transmission of pigeon pea sterility mosaic virus by the eriophyoideriophyid mite, Acaria cajani (Acari: Arthropoda). Plant Disease 86(12):1297-1302. https://doi.org/10.1094/PDIS.2002.86.12.1297

Kumar PL, Jones AT, Waliyar F (2004). Biology, etiology and management of pigeonpea sterility mosaic disease. Annual Review of Plant Pathology 3:1-24.

Kumar S, Stecher G, Tamura K (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7):1870-1874. https://doi.org/10.1093/molbev/msw054

Kumar S, Subbarao BL, Hallan V (2017). Molecular characterization of Emaraviruses associated with pigeonpea sterility mosaic disease. Scientific Reports 7(1):11831. https://doi.org/10.1038/s41598-017-11958-8

Mediga KR, Sunkad G, Shil S, Kulkarni S, Patil B, Sharath Chandran US, Ashwini P, Sharma M (2024). Assessment of the spatial distribution and identification of potential risk areas for the sterility mosaic disease of pigeonpea (Cajanus cajan L. Huth) in Southern India. Frontiers in Sustainable Food Systems 8:1386823. https://doi.org/10.3389/fsufs.2024.1386823

Mitra M (1931) Report of the imperial mycologist. Scientific Reports of the Indian Agriculture Research Institute, pp 58-71.

Muhire BM, Varsani A, Martin DP (2014). SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PloS One 9(9) https://doi.org/10.1371/journal.pone.0108277

Nene YL, Reddy MV (1976). A new technique to screen pigeon pea for resistance to sterility mosaic. Tropical Grain Legume Bulletin 5:23. https://www.cabidigitallibrary.org/doi/full/10.5555/19770542520

Pande S, Sharma M, Avuthu N, Telangre R (2012). High throughput phenotyping of chickpea diseases: stepwise identification of host plant resistance. Information Bulletin No 92. International Crops Research Institute for Semi-Arid Tropics.

Patil BL, Dangwal M, Mishra R (2017) Variability of Emaravirus species associated with sterility mosaic disease of pigeonpea in India provides evidence of segment reassortment. Viruses 9(7):183. https://doi.org/10.3390/v9070183

Patil BL, Kumar PL (2015). Pigeonpea sterility mosaic virus: a legume‐infecting Emaravirus from South Asia. Molecular Plant Pathology 16(8):775-786 https://doi.org/10.1111/mpp.12238

Reddy MV, Raju TN, Lenne JM (1998). Diseases of pigeonpea. The Pathology of Food and Pasture Legumes 517-558.

Saxena KB, Tikka SBS, Mazumder ND (2004). Cytoplasmic genic male-sterility in pigeonpea and its utilization in hybrid breeding programme. International Crops Research Institute for the Semi-Arid Tropics132-146.

Sayiprathap BR, Patibanda AK, Kumari VP, Jayalalitha K, Rao VS, Sharma M, Sudini HK (2020). Prevalence of sterility mosaic disease (SMD) and variability in pigeonpea sterility mosaic virus (PPSMV) in southern-India. Indian Phytopathology 73:741-750. https://doi.org/10.1007/s42360-020-00246-7

Sayiprathap BR, Patibanda AK, Prasanna Kumari V, Jayalalitha K, Ramappa HK, Rajeswari E, … Sudini HK (2022). Salient findings on host range, resistance screening, and molecular studies on Sterility mosaic disease of pigeonpea induced by pigeonpea sterility mosaic viruses (PPSMV-I and PPSMV-II). Frontiers in Microbiology 13:838047 https://doi.org/10.3389/fmicb.2022.838047

Seth ML (1962). Transmission of pigeonpea sterility by an eriophyoideriophyid mite. Indian Phytopathology 15:225-227.

Sharma M, Telangre R, Ghosh R, Pande S (2015). Multi-environment field testing to identify broad, stable resistance to sterility mosaic disease of pigeonpea. Journal of General Plant Pathology 81:249-25. https://doi.org/10.1007/s10327-015-0585-z

Siril PS, Balol GB, Saabale PR, Biradar RS (2022). Prevalence of pigeonpea sterility mosaic disease in northern parts of Karnataka. Journal of Farm Sciences 35(04):452-455. https://doi.org/10.61475/jfm.v35i04.32

Walia JJ, Willemsen A, Elci E, Caglayan K, Falk BW, Rubio L (2014). Genetic variation and possible mechanisms driving the evolution of worldwide Fig mosaic virus isolates. Phytopathology 104(1):108-114

https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-05-13-0145-R

Wheeler BEJ (1969). An introduction to plant diseases. John Wiley and Sons Limited. Pp 301