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Pigeonpea Sterility Mosaic Emaraviruses: A Journey from a Mysterious Virus to Classic Emaraviruses

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A Century of Plant Virology in India

Abstract

Sterility mosaic disease (SMD) of pigeonpea (Cajanus cajan (L.) Millsp) first reported in 1931, is an economically most important viral disease, which is endemic to India, Nepal, Bangladesh and Myanmar. SMD was long suspected to be a viral disease, however its causal agent, pigeonpea sterility mosaic virus (PPSMV) was discovered only in 2000. In 2013, the full genome of PPSMV was sequenced and based on the genome organization the virus was assigned to the genus Emaravirus. In 2015, association of another distinct emaravirus in SMD affected pigeonpea was discovered and it was named as pigeonpea sterility mosaic virus 2. As per the latest ICTV classification, these two pigeonpea infecting emaraviruses are renamed and recognised as two different virus species, Pigeonpea sterility mosaic emaravirus 1 and Pigeonpea sterility mosaic emaravirus 2 under the family Fimoviridae of the order Bunyavirales. These two emaraviruses involved in SMD are transmitted in a semi-persistent manner by an eriophyid mite, Aceria cajani Channabassavanna (Acari: Arthropoda). These viruses and its eriophyid vector are highly specific to pigeonpea and its wild relatives. This chapter presents the review of the studies conducted on SMD of pigeonpea and PPSMVs in India.

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References

  • Bhairappanavar SB, Fakrudin B, Sambasiva Rao KRS (2014) Inheritance studies of sterility mosaic disease (SMD) resistance cross Gullyal White×BSMR736 in pigeonpea (Cajanus cajan (L.) Millsp.) Plant Gene Trait 5:27–32

    Google Scholar 

  • Boonham N, Kreuze J, Winter S, van der Vlugt R, Bergervoet J, Tomlinson J, Mumford R (2014) Methods in virus diagnostics: from ELISA to next generation sequencing. Virus Res. 186:20–31

    Article  CAS  PubMed  Google Scholar 

  • Bruenn JA (2003) A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. Nucleic Acids Res. 31:1821–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Channabasavanna GP (1981) Contributions to acarology in India. In: Channabasavanna GP, Mallik B, Ghopardé KD (eds) Proceedings of the 1st All India Symposium in Acarology, Bangalore

    Google Scholar 

  • Dharmaraj PS, Narayana YD, Kumar PL, Waliyar F, Jones AT (2004) Pigeonpea sterility mosaic disease: an emerging problem in northern Karnataka. Int. Chickpea Pigeonpea Newsl. 11:47–49

    Google Scholar 

  • Di Bello PL, Ho T, Tzanetakis IE (2015) The evolution of emaraviruses is becoming more complex: seven segments identified in the causal agent of Rose rosette disease. Virus Res. 210:241–244

    Article  PubMed  Google Scholar 

  • Di Bello PL, Laney AG, Druciarek T, Ho T, Gergerich RC, Keller KE, Martin RR, Tzanetakis IE (2016) A novel emaravirus is associated with redbud yellow ringspot disease. Virus Res. 222:41–47

    Article  PubMed  Google Scholar 

  • Divya P, Kumar PL, Rangaswamy KT, Muniyappa V (2005) Detection of pigeonpea sterility mosaic virus in floral parts and seeds. Indian J. Virol. 16:36

    Google Scholar 

  • Duijsings D, Kormelink R, Goldbach R (2001) In vivo analysis of the TSWV cap-snatching mechanism: Single base complementarity and primer length requirements. EMBO J. 20:2535–2552

    Article  Google Scholar 

  • 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. J. Virol. Methods 188:37–40

    Article  CAS  PubMed  Google Scholar 

  • Elbeaino T, Digiaro M, Uppala M, Sudini H (2014) Deep sequencing of pigeonpea sterility mosaic virus discloses five RNA segments related to emaraviruses. Virus Res. 188:27–31

    Article  CAS  PubMed  Google Scholar 

  • 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. Arch. Virol. 160:2019–2029

    Article  CAS  PubMed  Google Scholar 

  • Elliott RM, Blakqori G (2011) Molecular biology of orthobunyaviruses. In: Plyusnin A, Elliott RM (eds) The Bunyaviridae: Molecular and Cellular Biology. Horizon Scientific Press, Norwich

    Google Scholar 

  • Ganapathy KN, Byregowda M, Venkatesha SC, Rama Chandra R, Gnanesh BN, Girish G (2009) Identification of AFLP markers linked to sterility mosaic disease in pigeonpea Cajanus cajan (L.) Millsp. Int. J. Integr. Biol. 7:145–149

    CAS  Google Scholar 

  • Ganapathy KN, Gowda BM, Ajay BC, Venkatesha SC, Gnanesh BN, Gomashe SS, Prasanth BG, Girish PS, Prasad GN, Veerakumar, Pati JV (2012) Inheritance studies of sterility mosaic disease (SMD) resistance in vegetable type pigeonpea (Cajanus cajan(L.) Millsp.) Aust J Crop Sci. 6:1154–1158

    Google Scholar 

  • Ghanekar AM, Sheila VK, Beniwal SPS, Reddy MV, Nene YL (1992) Sterility mosaic of pigeonpea. In: Singh US, Mukhopadhyay AN, Kumar J, Chaube HS (eds) Plant Diseases of International Importance, Diseases of Cereals and Pulses, vol 1. Prentice Hall, New Jersey, pp 415–428

    Google Scholar 

  • Gnanesh BN, Abhishek B, Sarma M, Wesley V, Byre Gowda M, Pande S, Saxena R, Saxena KB, Varshney RK (2011) Genetic mapping and quantitative trait locus analysis of resistance to sterility mosaic disease in pigeonpea [Cajanus cajan (L) Millsp.] Field Crop Res. 123:56–61

    Article  Google Scholar 

  • Hassan M, Di Bello PL, Keller KE, Martin RR, Sabanadzovic S, Tzanetakis IE (2017) A new, widespread emaravirus discovered in blackberry. Virus Res 235:1–5. doi:10.1016/j.virusres.2017.04.006

  • Ishikawa K, Miura C, Maejima K, Komatsu K, Hashimoto M, Tomomitsu T, Fukuoka M, Yusa A, Yamaji Y, Namba S (2015) Nucleocapsid protein from Fig mosaic virus forms cytoplasmic agglomerates that are hauled by endoplasmic reticulum streaming. J. Virol. 89(1):480–491

    Article  PubMed  Google Scholar 

  • Jones AT, Kumar PL, Saxena KB, Kulkarni NK, Muniyappa V, Waliyar F (2004) Sterility mosaic disease-the “green plague” of pigeonpea: advances in understanding the etiology, transmission and control of a major virus disease. Plant Dis. 88:436–445

    Article  Google Scholar 

  • 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. Trop Pest Manag 30:62–71

    Article  Google Scholar 

  • Kaushik D, Srivastava S, Nath BC, Chauhan VB, Singh R (2013) Correlation between mite population (Aceria cajani) and environmental factors causing sterility mosaic disease of Pigeonpea. Int. J. Life Sci. 1:228–232

    Google Scholar 

  • Kikkert M, van Lent J, Storms M, Bodegom P, Kormelink R, Goldbach R (1999) Tomato spotted wilt virus particle morphogenesis in plant cells. J. Virol. 73:2288–2297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL (2011) Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res. 162:184–202

    Article  CAS  PubMed  Google Scholar 

  • Krishna G, Reddy PS, Ramteke PW, Bhattacharya PS (2010) Progress of tissue culture and genetic transformation research in pigeonpea [Cajanus cajan (L.) Millsp.] Plant Cell Rep. 29:1079–1095

    Google Scholar 

  • Kulkarni NK, Kumar PL, Muniyappa V, Jones AT, Reddy DVR (2002) Transmission of Pigeonpea sterility mosaic virus by the eriophyid mite, Aceria cajani (Acari: Arthropoda). Plant Dis. 86:1297–1302

    Article  Google Scholar 

  • Kulkarni NK, Kumar PL, Muniyappa V, Jones AT, Reddy DVR (2003a) Broad-based resistance to pigeonpea sterility mosaic disease in the accessions of Cajanus scarabaeoides. Ind. J. Plant Protect. 31:6–11

    Google Scholar 

  • Kulkarni NK, Kumar PL, Muniyappa V, Jones AT, Reddy DVR (2003b) Studies on host range of Pigeonpea sterility mosaic virus. J. Mycol. Plant Pathol. 33:141–145

    Google Scholar 

  • Kumar PL, Jones AT, Sreenivasulu P, Reddy DVR (2000) Breakthrough in the identification of the causal agent of pigeonpea sterility mosaic disease. J Mycol Plant Pathol. 30:249

    Google Scholar 

  • Kumar PL, Fenton B, Duncan G, Jones AT, Sreenivasulu P, Reddy DVR (2001) Assessment of variation in Aceria cajani (Acari: Eriophyidae) using analysis of nuclear rDNA ITS regions and scanning electron microscopy: Implications for the variability observed in host plant resistance to pigeonpea sterility mosaic disease. Ann. Appl. Biol. 139:61–73

    Article  CAS  Google Scholar 

  • Kumar PL, Jones AT, Reddy DVR (2002a) Mechanical transmission of Pigeonpea sterility mosaic virus. J. Mycol. Plant Pathol. 32:88–89

    Google Scholar 

  • Kumar PL, Duncan GH, Roberts IM, Jones AT, Reddy DVR (2002b) Cytopathology of Pigeonpea sterility mosaic virus in pigeonpea and Nicotiana benthamiana: similarities with those of eriophyid mite-borne agents of undefined aetiology. Ann. Appl. Biol. 140:87–96

    Article  Google Scholar 

  • Kumar PL, Jones AT, Reddy DVR (2003) A novel mite-transmitted virus with a divided RNA genome closely associated with pigeonpea sterility mosaic disease. Phytopathology 93:71–81

    Article  CAS  PubMed  Google Scholar 

  • Kumar PL, Latha TKS, Kulkarni NK, Raghavendra N, Saxena KB, Waliyar F, Rangaswamy KT, Muniyappa V, Doriswamy S, Jones AT (2005) Broad based resistance to pigeonpea sterility mosaic disease in wild relatives of pigeonpea (Cajanus: Phaseoleae). Ann. Appl. Biol. 146:371–379

    Article  Google Scholar 

  • Kumar PL, Jones AT, Waliyar F, Sreenivasulu P, Muniyappa V, Latha TKS, Saxena KB (2007) Pigeonpea sterility mosaic disease. In: Kumar PL, Waliyar F (eds) Diagnosis and detection of viruses infecting ICRISAT mandate crops. ICRISAT’s methods manual

    Google Scholar 

  • Kumar PL, Jones AT, Waliyar F (2008) Virus diseases of pigeonpea. In: Rao GP, Kumar PL, Holguin-Pena RJ (eds) Characterization, Diagnosis and Management of Plant Viruses, Vegetable and Pulse Crops, vol 3. Studium Press, Texas

    Google Scholar 

  • Laney AG, Keller KE, Martin RR, Tzanetakis IE (2011) A discovery 70 years in the making: characterization of the Rose rosette virus. J. Gen. Virol. 92:1727–1732

    Article  CAS  PubMed  Google Scholar 

  • Latha TKS, Doraiswamy S (2008) Detection of pigeonpea sterility mosaic virus, the causal agent of sterility mosaic disease of pigeonpea in viruliferous mite vector by DAS-ELISA and DIBA. Arch. Phytopathol. Plant Protect. 41:537–541

    Article  CAS  Google Scholar 

  • McGavin WJ, Mitchell C, Cock PJ, Wright KM, MacFarlane SA (2012) Raspberry leaf blotch virus, a putative new member of the genus Emaravirus, encodes a novel genomic RNA. J. Gen. Virol. 93:430–437

    Article  CAS  PubMed  Google Scholar 

  • Mielke N, Muehlbach HP (2007) A novel, multipartite, negative-strand RNA virus is associated with the ringspot disease of European mountain ash (Sorbus aucuparia L.) J. Gen. Virol. 88:1337–1346

    Article  CAS  PubMed  Google Scholar 

  • Mielke-Ehret N, Muhlbach HP (2012) Emaravirus: a novel genus of multipartite, negative strand RNA plant viruses. Virus 4:1515–1536

    Article  CAS  Google Scholar 

  • Mitra M (1931) Report of the imperial mycologist. Sci. Rep. Agric. Res. Inst. Pusa 19:58–71

    Google Scholar 

  • Mühlbach HP, Mielke-Ehret N (2011) Emaravirus. In: AMQ K, Adams MJ, Carstens EB, Lefkovitz EJ (eds) Virus Taxonomy. Classification and Nomenclature of Viruses, Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier, Oxford

    Google Scholar 

  • Narayana YD, Mahalinga DM, Jayalakshmi SK, Benagi VI (2000) Prevalence of SMD of pigeonpea in Northern Karnataka. Karnataka J. Agric. Sci. 13:470–472

    Google Scholar 

  • Nene YL (1995) Sterility mosaic of pigeonpea: the challenge continues. Indian J. Mycol. Plant Pathol. 25:1–11

    Google Scholar 

  • Nene YL, Reddy MV (1976a) Screening for resistance to sterility mosaic of pigeonpea. Plant Dis. Rep. 60:1034–1036

    Google Scholar 

  • Nene YL, Reddy MV (1976b) A new technique to screen pigeonpea for resistance to sterility mosaic for pigeonpea. Trop. Grain Legume Bull. 5:23–24

    Google Scholar 

  • Oldfield G, Proeseler G (1996) Eriophiod mites as vectors of plant pathogens. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid Mites-Their Biology, Natural Enemies and Control. Elsevier, Amsterdam

    Google Scholar 

  • Patil BL, Lava Kumar P (2015) Pigeonpea sterility mosaic virus: a legume-infecting Emaravirus from South Asia. Mol. Plant Pathol 16:775–786

    Google Scholar 

  • 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

    Google Scholar 

  • Patil BL, Ogwok E, Wagaba H, Mohammed IU, Yadav JS, Bagewadi B, Taylor NJ, Kreuze JF, Maruthi MN, Alicai T, Fauquet CM (2011) RNAi-mediated resistance to diverse isolates belonging to two virus species involved in Cassava brown streak disease. Mol. Plant Pathol. 12:31–41

    Article  CAS  PubMed  Google Scholar 

  • Peng JC, Chen TC, Raja JA, Yang CF, Chien WC, Lin CH, Liu FL, Wu HW, Yeh SD (2014) Broad-spectrum transgenic resistance against distinct tospovirus species at the genus level. PLoS One 9:e96073

    Article  PubMed  PubMed Central  Google Scholar 

  • Reddy MV, Nene YL (1980) Influence of sterility mosaic resistant pigeonpeas on multiplication of the mite vector. Ind Phytopathol 33:61–63

    Google Scholar 

  • Reddy MV, Raju TN, Nene YL, Ghanekar AM, Amin KS, Arjunan G, Astaputre JV, Sinha BK, Reddy SV, Gupta RP, Gangadharan K (1993) Variability in sterility mosaic pathogen in pigeonpea in India. Indian Phytopathol. 46:206–212

    Google Scholar 

  • Reddy MV, Raju TN, Lenne JM (1998) Diseases of pigeonpea. In: Allen DJ, Lenne JM (eds) The Pathology of Food and Pasture legumes. CAB International, Wallingford, pp 517–558

    Google Scholar 

  • Sharma M, Rathore A, Mangala UN, Ghosh R, Sharma S, Upadhyay H, Pande S (2012) New sources of resistance to Fusarium wilt and sterility mosaic disease in a mini-core collection of pigeonpea germplasm. Eur. J. Plant Pathol. 133:707–714

    Article  Google Scholar 

  • Singh J, Raghuraman M (2011) Emerging scenario of important mite pests in north India. Zoosymposia 6:170–179

    Google Scholar 

  • Singh AK, Rathi YPS (1997) Epidemiology of vector of pigeonpea sterility mosaic virus. Ind. J. Virol. 13:143–145

    Google Scholar 

  • Singh NK, Gupta DK, Jayaswal PK, Mahato AK, Dutta S, Singh S, Bhutani S, Dogra V, Sing BP, Kumawat G, Pal JK, Pandit A, Singh A, Rawal H, Kumar A, Rama Prashat G, Khare A, Yadav R, Raje RS, Singh MN, Datta S, Fakrudin B, Wanjari KB, Kansal R, Dash PK, Jain PK, Bhattacharya R, Gaikwad K, Mohapatra T, Srinivasan R, Sharma TR (2012) The first draft of the pigeonpea genome sequence. J. Plant Biochem. Biotechnol. 21:98–112

    Article  PubMed  Google Scholar 

  • Srinivas T, Reddy MV, Jain KC, Reddy MSS (1997) Studies on inheritance of resistance and allelic relationships for strain 2 of Pigeonpea sterility mosaic pathogen. Ann. Appl. Biol. 130:105–110

    Article  Google Scholar 

  • Tatineni S, McMechan AJ, Wosula EN, Wegulo SN, Graybosch RA, French R, Hein GL (2014) An eriophyid mite-transmitted plant virus contains eight genomic RNA segments with unusual heterogeneity in the nucleocapsid protein. J. Virol. 88:11834–11845

    Article  PubMed  PubMed Central  Google Scholar 

  • Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MT, Azam S, Fan G, Whaley AM, Farmer AD, Sheridan J, Iwata A, Tuteja R, Penmetsa RV, Wu W, Upadhyaya HD, Yang SP, Shah T, Saxena KB, Michael T, McCombie WR, Yang B, Zhang G, Yang H, Wang J, Spillane C, Cook DR, May GD, Xu X, Jackson SA (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat. Biotechnol. 30:83–89

    Article  CAS  Google Scholar 

  • Yu C, Karlin DG, Lu Y, Wright K, Chen J, MacFarlane S (2013) Experimental and bioinformatic evidence that Raspberry leaf blotch emaravirus p4 is a movement protein of the 30K superfamily. J. Gen. Virol. 94:2117–2128

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Navarro B, Wang G, Wang Y, Yang Z, Xu W, Zhu C, Wang L, Serio FD, Hong N (2017) Actinidia chlorotic ringspot-associated virus: a novel emaravirus infecting kiwifruit plants. Mol. Plant Pathol. 18(4):569–581

    Article  CAS  PubMed  Google Scholar 

  • Zote KK, Mali VR, Mayee CD, Kulkarni SV, Mote TS (1991) Outbreak of sterility mosaic of pigeonpea in Marathwada region Maharashtra. India. Int. Pigeonpea Newsl. 14:19–21

    Google Scholar 

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Acknowledgement

BLP acknowledges the financial support from ICAR-NRCPB to work on PPSMVs. Authors gratefully acknowledge research contributions of all the students, research scholars and scientists and a number of philanthropic donors for financial assistance to research work on SMD spanning over 85 years in India.

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Correspondence to Basavaprabhu L. Patil .

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Patil, B.L., Lava Kumar, P. (2017). Pigeonpea Sterility Mosaic Emaraviruses: A Journey from a Mysterious Virus to Classic Emaraviruses. In: Mandal, B., Rao, G., Baranwal, V., Jain, R. (eds) A Century of Plant Virology in India. Springer, Singapore. https://doi.org/10.1007/978-981-10-5672-7_10

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