Biography: A.L.N. Rao, UC-Riverside

BIOGRAPHY

A. Professional Preparation

Name: A. L.N. Rao

Institution Major Degree Year A.P. Agricultural University, India Agriculture B.Sc(Ag) 1972 Indian Agricultural Research Institute Plant Pathology M.Sc 1976 University of Adelaide, South Australia Plant Pathology Ph.D 1982

B. Appointments

2004- present Professor, Dept. Plant Pathology & Microbiology, University of California, Riverside, 1997-2004 Associate Professor, Dept. Plant Pathology & Microbiology, University of California, Riverside, 1993-1997 Assistant Professor, Dept. of Plant Pathology, University of California, Riverside, CA. 1986-1993 Research Associate, Texas A & M University, College Station, Texas. 1982-1986 Postdoctoral Fellow, University of Alberta, Edmonton, Alberta, Canada.

C. Research Interests

A fundamental question in virology is how package their into stable virions. The major focus of research in my laboratory is to understand the replication and mechanism of packaging in RNA viruses of plants and insects with divided genomes. To this end, we are using Brome mosaic (BMV), a tripartite plant infecting RNA virus as a model system for analyzing various molecular interactions between coat protein and RNA leading to assembly of mature infectious virions. In addition, we are also applying molecular and proteomics approaches for dissecting the mechanism regulating the nuclear localization and replication of a satellite RNA of Cucumber mosaic virus and replication of Satellite tobacco mosaic virus (STMV). More recently, we initiated a projected to initiate the assembly of virus like particles of Human Immuno deficiency Virus (HIV) and Ebola Virus (EBV) in plants with an eventual aim of developing novel strategies of vaccine development.

D. Synergistic activities

2015- Member, NSF, GRFP Grant Review Panel 2013- Editorial Board, Virology 2013- Academic Editor, PLoS ONE 2006-2009 Senior Editor (Virology), Phytopathology 2006 Ad Hoc reviewer, NIH Study Section, Membrane Biology & Protein Processing 2002 Chairman and Organizer Plant Virology Satellite Symposium at ASV 2003 Chairman and Organizer Plant Virology Satellite Symposium at ASV

1 Biography: A.L.N. Rao, UC-Riverside

2004 Chairman and Organizer Plant Virology Satellite Symposium at ASV 2005 Chairman and Organizer Plant Virology Satellite Symposium at ASV

E. Journal articles (JA) (Referred)

1. Sonali Chaturvedi and A. L. N. Rao (2017). Molecular and biological factors regulating the genome packaging in single-strand positive-sense tripartite RNA plant viruses. Current Opinion in Virology (In Press).

2. Sonali Chaturvedi and A. L. N. Rao (2017). Riboproteomics: A versatile approach for the identification of host protein interaction network in plant pathogenic noncoding . PLoS ONE 12(10) https://doi.org/10.1371/journal.pone.0186703. 3. Venkatesh Sivanandam, Deborah Mathews, Rees Garmann, Gonca Erdemci- Tandogan, Roya Zandi and A. L. N. Rao (2016). Functional analysis of the N- terminal basic motif of a eukaryotic satellite RNA virus protein in replication and packaging. Scientific Reports. 6, 26328.

4. Sonali Chaturvedi., Jang-Kyun Seo and A. L. N. Rao (2016). Functionality of host proteins in Cucumber mosaic virus replication: GAPDH is obligatory to promote interaction between replication-associated proteins. Virology 494: 47-55.

5. Sonali Chaturvedi and A. L. N. Rao (2016). A shift in plant proteome profile for a Bromodomain containing RNA binding Protein (BRP1) in plants infected with cucumber mosaic virus and its satellite RNA. Journal of Proteomics 131: 1-7. 6. Sivanandam, V., Mathews, D and A.L.N. Rao (2015) Properties of Satellite tobacco mosaic virus phenotypes expressed in the presence and absence of helper virus. Virology 483: 163-173. 7. Venkatesh Sivanandam, Erika Varady and A. L. N. Rao (2015) Heterologous replicase driven 3' end repair of Cucumber mosaic virus satellite RNA. Virology: 478: 18-26. 8. Dong Gui, Sharad Gupta, Jun Xu, Roya Zandi, Sarjeet Gill, I-Chueh Huang, A.L.N. Rao and Umar Mohideen (2014). A novel minimal in vitro system for analyzing HIV-1 Gag mediated budding. J. Biological Physics. 41(2) 135-149. 9. Gopal, A.J., Egecioglu, D., Yoffe, A, Ben-Shaul. A., Rao, A., Knobler, C., and Gelbart, W (2014). Viral RNAs are unusually Compact. PLOS ONE 9 (9) e105875. 10. Sonali Chaturvedi and A.L.N. Rao (2014) Live Cell Imaging of Interactions Between Replicase and Capsid Protein of Brome Mosaic Virus using Bimolecular Fluorescence Complementation: Implications for Replication and Genome Packaging. Virology 464-465: 67-75. 11. Sonali Chaturvedi, Kriton Kalantidis and A. L. N. Rao (2014). A bromodomain containing host protein mediates the nuclear import of a satellite RNA of cucumber mosaic virus. Journal of Virology 88(4) 1890-1896.

2 Biography: A.L.N. Rao, UC-Riverside

12. Sun-Jung Kwon, Sonali Chaturvedi and A. L. N. Rao (2014). Repair of the 3' proximal and internal deletions of a satellite RNA associated with Cucumber mosaic virus is directed toward restoring structural integrity. Virology 450-451: 222-232. 13. Bamunusinghe, D., Sonali Chaturvedi, Jang-Kyun Seo and A. L. N. Rao (2013). Mutations in the Capsid Protein of Brome Mosaic Virus Affecting Encapsidation Eliminate Vesicle Induction in planta: Implications for Virus Cell-to-Cell Spread. Journal of Virology 87:8982-892. 14. Sharad Gupta, Muhammad R. Chatni , Ayala L. N. Rao , Valentine I. Vullev , Lihong V. Wang and Bahman Anvari (2013). Virus-mimicking nano- constructs as a contrast agent for near infrared photoacoustic imaging. Nanoscale 5: 1772-1776. 15. Jang-Kyun Seo, Sun-Jung Kwon, Sonali Chaturvedi and A.L.N. Rao (2013). Functional significance of a hepta nucleotide motif present at the junction of cucumber mosaic virus satellite RNA multimers in helper-virus-dependent replication. Virology 435: 214-219. 16. Mauricio Comas-Garcia, Ruben D. Cadena-Nava, A. L. N. Rao, Charles M. Knobler, and William M. Gelbart (2012) In Vitro Quantification of the Relative Packaging Efficiencies of Single-Stranded RNA Molecules by Viral Capsid Protein. J. Virol. 86: 12271-12282. 17. Jang-Kyun Seo, Sun-Jung Kwon and A.L.N. Rao (2012). Molecular dissection of Flock house virus protein B2 reveals that electrostatic interactions between N- terminal domains of B2 monomers are critical for dimerization. Virology 432: 296- 305. 18. Jang-Kyun Seo, Sun-Jung Kwon and A.L.N. Rao (2012). A physical interaction between viral replicase and capsid protein is required for genome packaging specificity in an RNA virus. Journal of Virology 86(11): 6210-6221. 19. Soon Ho Choi, Jang-Kyun Seo, Sun-Jung Kwon and A. L. N. Rao (2012). Helper virus independent transcription and multimerization of a satellite RNA associated with cucumber mosaic virus. Journal of Virology 86(9): 4823-4832. 20. Sun-Jung Kwon and A. L.N. Rao (2012). Emergence of distinct brome mosaic virus recombinants is determined by the polarity of the inoculum RNA. Journal of Virology 86(9): 5204-5220. 21. Cadena-Nava, R., Mauricio Comas-Garcia., Rees Garmann., A.L.N. Rao., Charles Knobler and William Gelbart (2012). Self-assembly of viral capsid protein and RNA molecules of different sizes: requirement for a specific high protein/RNA mass ratio. Journal of Virology 86(6): 3318-3326. 22. Chaturvedi, S., S. Gupta, B. Jung., B. Anvari and A. L. N. Rao (2012). A simple and robust in vivo and in vitro approach for studying assembly in RNA viruses. Journal of Visualization Experiment. March 2012, vol 61:e3645. 23. Jung, B., A. L. N. Rao and Bahman Anvari (2011). Optical nano constructs composed of genome depleted brome mosaic virus doped with a near infrared chromophore for potential biomedical applications. ACS Nano 5(2) 1243-1252. (Featured as cover article).

3 Biography: A.L.N. Rao, UC-Riverside

24. Bamunusinghe, D., Jang-Kyun Seo and A. L. N. Rao (2011). Subcellular localization and rearrangement of endoplasmic reticulum by brome mosaic virus capid protein. Journal of Virology 85(6) 2953-2963. 25. de Wispelaere, M and A. L. N. Rao. (2011). Packaging and structural phenotype of brome mosaic virus capsid protein with altered N-terminal β-hexamer structure. Virology 419: 17-23. 26. de Wispelaere, M and A. L. N. Rao. (2009). Production of cucumber mosaic virus RNA5 and its role in recombination. Virology 384: 179-191. 27. Annamalai, P. Fady Rofail, D.A. Demason and A.L.N. Rao, 2008. Replication coupled packaging mechanism in positive-strand RNA viruses; Synchronized co- expression of functional multigenome components of an animal and plant virus in Nicotiana benthamiana cells by agroinfiltration. Journal of Virology 82: 1484- 1495. This paper was selected as “Articles of Significant Interest (Spot light)” by the Journal of Virology Editorial Board. 28. Calhoun, S.L. and A. L.N. Rao. 2008. Functional analysis of brome mosaic virus coat protein-RNA interacting domains. Archives of Virology 153: 231-245. 29. Annamalai Padmanaban and A.L.N. Rao. 2007. In vivo packaging of brome mosaic virus RNA3, but not RNAs 1 and 2, is dependent on a cis-acting 3’ tRNA- like structure. Journal of Virology 81: 173-181. 30. Calhoun, S.L., Speir, J.A., A. L. N. Rao. 2007. In vivo polymorphism results from deletion of a N-terminal peptide molecular switch in brome mosaic virus capsid protein. Virology 364: 407-421. 31. Annamalai Padmanaban and A.L.N. Rao. 2006. Packaging of brome mosaic virus subgenomic RNA is functionally coupled to replication-dependent transcription and translation of coat protein. Journal of Virology 80:10096-10108. This paper was selected as “Articles of Significant Interest (Spot light)” by the Journal of Virology Editorial Board. 32. Rao, A.L.N. 2006. Sensitivity of brome mosaic virus replication to 3’ mutations in RNA1 implies a requirement for sustained synthesis of 1a replicase protein. Arch. Virol. 151: 721-733. 33. Rao, A.L.N. and Bret Cooper. 2006. Capsid protein gene and the type of host plant differentially modulate cell-to-cell movement of cowpea chlorotic mottle virus. 2005. Virus Genes. 32: 219-227. 34. Annamalai Padmanaban and A.L.N. Rao. 2005. Replication-Independent Expression of genome components and capsid protein of brome mosaic virus in planta: a functional role for viral replicase in RNA packaging. Virology 338: 96- 111. 35. Annamalai Padmanaban and A.L.N. Rao. 2005. Dispensability of 3’ tRNA-like sequence for packaging of cowpea chlorotic mottle virus genomic RNAs. Virology 332: 650-658. 36. Annamalai Padmanban, Swapna Apte, Stephan Wilkens and A.L.N. Rao. 2004. Deletion of highly conserved arginine rich RNA binding motif in cowpea chlorotic mottle virus capsid protein results in virion structural alterations and RNA packaging constraints. Journal of Virology 79: 3277-3288. 37. Choi, Y.G. and A.L.N. Rao. 2003. Packaging of brome mosaic virus RNA3 is mediated through a bipartite signal. Journal of Virology 77: 9750-9757.

4 Biography: A.L.N. Rao, UC-Riverside

38. Choi, Y. G., T.W. Dreher and A.L.N. Rao. 2002. tRNA elements mediate the assembly of an icosahedral RNA virus. Proceedings of National Academy of Sciences, USA 99: 655-660. 39. Choi, Y.G. and A.L.N. Rao. 2000. Packaging of tobacco mosaic virus subgenomic RNAs by brome mosaic virus coat protein exhibits RNA controlled polymorphism. Virology 275:249-257. 40. Choi, Y.G. and A.L.N. Rao. 2000. Molecular studies on bromovirus capsid protein. VII. Selective packaging of BMV RNA4 by specific N-terminal arginine residues. Virology 275: 207-217. 41. Choi, Y.G., G.L. Grantham, and A.L.N. Rao. 2000. Molecular studies on bromovirus capsid protein. VI. Contributions of the N-terminal arginine rich motif of BMV capsid protein to virion stability and RNA packaging. Virology 270:377- 385. 42. Osman, F., I. Schmitz, and A.L.N. Rao. 1999. Effect of C-terminal deletions in the movement protein of cowpea chlorotic mottle virus on cell-to-cell and long distance movement. J. Gen. Virol. 80:1357-1365. 43. Chapman, M.R., A.L.N. Rao, and C.C. Kao. 1998. Sequences of 5' of the conserved tRNA-like promoter modulate the initiation of minus-strand synthesis by the brome mosaic virus RNA-dependent RNA polymerase. Virology 252:458- 467. 44. Osman, F., Y. Choi, G.L. Grantham, and A.L.N. Rao. 1998. Molecular studies on bromovirus capsid protein. V. Evidence for the specificity of brome mosaic virus encapsidation using RNA3 chimera of brome mosaic and cucumber mosaic viruses expressing heterologous coat proteins. Virology 251:438-448. 45. Schmitz, I. and A.L.N. Rao. 1998. Deletions in the highly conserved amino- terminal basic arm of cucumber mosaic virus coat protein disrupt virion assembly but do not abolish infectivity and cell-to-cell movement. Virology 248:323-331. 46. Rao, A.L.N., B. Cooper, and C.M. Deom. 1998. Defective movement of viruses in the family Bromoviridae is differently complemented in Nicotiana benthamiana expressing tobamovirus or dianthovirus movement proteins. Phytopathology 88:666-672. 47. Osman, F., G.L. Grantham, and A.L.N. Rao. 1997. Molecular studies on bromovirus capsid protein. IV. Coat protein exchanges between brome mosaic and cowpea chlorotic mottle viruses exhibit neutral effects in heterologous hosts. Virology 238:452-459. 48. Routh, G., M.N.A. Yassi, A.L.N. Rao, T.R. Mirkov, and J.A. Dodds. 1997. Replication of wild-type and mutant clones of satellite tobacco mosaic virus in nicotiana benthamiana protoplasts. Journal of General Virology 78:1271-1275. 49. Rao, A.L.N. 1997. Molecular studies on bromovirus capsid protein. III. Analysis of cell-to-cell movement competence of coat protein defective variants of Cowpea Chlorotic Mottle Virus. Virology 232:385-395. 50. He, X.-H, A.L.N. Rao, and R. Creamer. 1996. Characterization of beet yellows closterovirus specific RNAs in infected plants and protoplasts. Phytopathology 87:347-352.

5 Biography: A.L.N. Rao, UC-Riverside

51. Rao, A.L.N. and G.L. Grantham. 1996. Molecular studies on bromovirus capsid protein. II. Functional analysis of the amino terminal arginine rich motif and its role in encapsidation, movement and pathology. Virology 226:294-306. 52. Schmitz, I. and A.L.N. Rao. 1996. Molecular studies on bromovirus capsid protein. I. Characterization of cell-to-cell movement defective RNA3 variants of brome mosaic virus. Virology 226:281-293. 53. Cooper, B., I. Schmitz, I., A.L.N. Rao, R.N. Beachy, and J.A. Dodds. 1996. Cell- to-cell transport of movement-defective cucumber mosaic and tobacco mosaic viruses in transgenic plants expressing heterologous movement protein genes. Virology 216:208-213. 54. Rao, A.L.N. and G.L. Grantham. 1995. Biological significance of the seven amino-terminal basic residues of brome mosaic virus coat protein. Virology 211:42-52. 55. Rao, A.L.N. and G.L. Grantham. 1995. A spontaneous mutation in the movement protein gene of brome mosaic virus modulates symptom phenotype in Nicotiana benthamiana. Journal of Virology 69:2689-2691. 56. Rao, A.L.N. and G.L. Grantham. 1994. Amplification in vivo of brome mosaic virus RNAs bearing 3' noncoding region from cucumber mosaic virus. Virology 204:478-481. 57. Rao, A.L.N. and T.C. Hall. 1993. Recombination and polymerase error facilitate restoration of infectivity in brome mosaic virus. J. Virology 67:969-979. 58. Duggal, R., A.L.N. Rao, and T.C. Hall. 1992. Unique nucleotide differences in the conserved 3' termini of brome mosaic virus RNAs are maintained through their optimization of genome replication. Virology 187:261-270 59. Rao, A.L.N. and T.C. Hall. 1991. Interference in trans with brome mosaic virus replication by RNA-2 bearing aminoacylation-deficient mutants. Virology 180:16- 22. 60. Rao, A.L.N., C.C. Huntley, L.E. Marsh, and T.C. Hall. 1990. Analysis of RNA stability and - strand content in viral infections using biotinylated RNA probes. Journal of Virological Methods 30:239-250. 61. Rao, A.L.N., B.P. Sullivan and T.C. Hall. 1990. Use of Chenopodium hybridum facilitates isolation of brome mosaic virus RNA recombinants. Journal of General Virology 71:1403-1407. 62. Rao, A.L.N. and T.C. Hall. 1990. Requirement for a viral trans-acting factor encoded by brome mosaic virus RNA-2 provides strong selection in vivo for functional recombinants. Journal of Virology 64:2437-2441. 63. Rao, A.L.N., T.W. Dreher, L.E. Marsh, and T.C. Hall. 1989. Telomeric function of the tRNA-like structure of brome mosaic virus RNA. Proceedings of National Academy of Science, U.S.A, 86:5335-5339. 64. Dreher, T.W., A.L.N. Rao, and T.C. Hall. 1989. Replication in vivo of mutant brome mosaic virus RNAs defective in aminoacylation. Journal of Molecular Biology 206:425-438. 65. Rao, A.L.N., D.K. Lakshman, S.T. Ohki, and C. Hiruki. 1987. Identification of a new serotype and antigenic relationships among six strains of red clover necrotic mosaic virus. Phytopathology 77:995-999.

6 Biography: A.L.N. Rao, UC-Riverside

66. Rao, A.L.N. and C. Hiruki. 1987. Unilateral compatibility of genome segments from two distinct strains of red clover necrotic mosaic virus. Journal of General Virology 68:191-194. 67. Rao, A.L.N. and C. Hiruki. 1985. Clover primary leaf necrosis virus, a strain of red clover necrotic mosaic virus. Plant Disease 69: 959-961. 68. Rao, A.L.N. and C. Hiruki. 1985. Occurrence and identification of lucerne transient streak virus in Alberta, Canada. Plant Disease 69:610-612. 69. Hiruki, C., A.L.N. Rao, Y. Furuya, G. Figueiredo. 1984. Serological studies of dianthoviruses using monoclonal and polyclonal antibodies. Journal of General Virology 65:2273-2275. 70. Rao, A.L.N. and A. Verma. 1984. Transmission studies with cucumber green mottle mosaic virus. Phytopathlogische Zeitschrift. 109: 325-331. 71. Rao, A.L.N. and R.I.B. Francki. 1982. Distribution of determinants for symptom production and host range on the three RNA components of cucumber mosaic virus. Journal of General Virology 61:197-205. 72. Tien, P., Rao, A. L. N. and Francki, R. I .B. 1982. Cucumber mosaic virus from corn flower in China. Plant Disease. 66: 337-339. 73. Rao, A.L.N., T. Hatta, and R.I.B. Francki. 1982. Comparative studies on tomato aspermy and cucumber mosaic viruses. VII. Serological relationships reinvestigated. Virology 116:318-326. 74. Rao, A.L.N. and R.I.B. Francki. 1981. Comparative studies on tomato aspermy and cucumber mosaic viruses. VI. Partial compatibility of genome segments from the two viruses. Virology 114:573-575.

Book chapters:

1. Sun-Jung Kwon, Jang-Kyun Seo, and A.L.N. Rao (2012): Detection and quantification of viral and satellite RNAs in plants hosts. Hailin Jn and Walter Gassmann (eds). RNA Abundance Analysis; Methods and Protocols, Methods in Molecular Biology, Vol 883:131-141, Humana Press. 2. Rao, A.L.N. and Annamalai, P. 2007. RNA encapsidation assay. In “ Plant Virology Protocols”. Vol 451: 251-264; Edited by Garry Foster and Peter Nagy. Humana Press, Totowa, NJ. 3. Rao, A.L.N. 2007. Preparation and inoculation of mesophyll protoplasts from monocotyledonous and dicotyledenous hosts. Current Protocols in Microbiology, John Willey & Sons, p 16D.2.1-2.8. 4. Annamalai, P and Rao, A.L.N. 2006. Delivery and expression of functional viral genomes in plants by agroinfiltration. Current Protocols in Microbiology, John Willey & Sons, p 16B.2.1-2.15. 5. Rao, A.L.N. 2006. Genome packaging in spherical plant RNA viruses. Annual Review of Phytopathology. 44: 61-87. 6. Rao, A.L.N. and V. Reddy (2006). Composition and Architecture of Plant viruses. In “Hand book of Plant Virology; Eds. J. A. Khan and J. Dijkstra; Haworth Press, New York, USA.

7 Biography: A.L.N. Rao, UC-Riverside

7. Rao, A.L.N. 2006. Preparation and inoculation of mesophyll protoplasts from monocotyledonous and dicotyledonous hosts. Current Protocols in Microbiology, John Willey & Sons, (In press). 8. Annamalai, P and A.L.N. Rao. 2006. RNA Encapsidation Assay. Plant Virology Protocols: Methods in Molecular Biology, Eds. G. Foster and Peter Nagy, Human Press (In press). 9. Rao, A.L.N. 2003 Plant viruses: Structure and assembly. Encyclopedia of Plant and Crop Sciences, Marcel Decker Inc, NY. Pp. 155-158. 10. Rao, A.L.N. and Y.G. Choi. 2001. Molecular Biology of plant virus movement. In: Plant viruses as molecular pathogens, Ed. J.A. Khan and J. Dijkstra. pp. 127- 144. The Haworth Press, Inc. NY. 11. Rao, A.L.N. 2000. Bromoviruses. In: Encyclopedia of Plant Pathology. eds. Maloy, O. C & Murray, T. D, John Wiley & Sons, Canada, pp. 155-158. 12. Rao, A.L.N. 1999. Molecular Basis of Symptomatology. In: Molecular Biology of Plant Viruses. Ed. C.L. Mundahar, Kluwer Academic Publishers, pp 201-210. 13. Rao, A.L.N., R. Duggal, F. Lahser, and T.C. Hall. 1994. Analysis of RNA replication in plant viruses. “Methods in Molecular Genetics: Molecular Virology Techniques”. K.W. Adolph (ed.). Vol. 4, Academic Press, Orlando, FL. pp. 216- 236. 14. Hall, T.C., A.L.N. Rao, G.P. Pogue, C.C. Huntley, and L. Marsh. 1990. Replication, repair and recombination of brome mosaic virus RNA. In: New Aspects of Positive Strand RNA Viruses, Ed. M. Brinton, F.X. Heinz. pp. 47-54. ASM Press, Washington, D. C.

Review articles:

15. Katsarou, K., Rao, A.L.N., Tsagris, M and Kalantidis, K. (2015). Infectious long non- coding RNAs. Biochimie 117: 37-47. 16. Rao, A.L.N. and Kriton Kalantidis (2015) Virus-Associated Small Satellite RNAs and Viroids Display Similarities in their Replication Strategies. Virology 479-480C: 627-636. 17. Rao, A.L.N and Kao, C.C (2015) The Brome Mosaic Virus 3' Untranslated Sequence Regulates RNA Replication, Recombination, and Virion Assembly. Virus Research 206:46-52 18. Rao, A.L.N., Sonali Chaturvedi and Rees Garmann (2014). Integration of replication and assembly of infectious virions in plant RNA viruses. Curr. opin. virol. 9: 61- 66. 19. Rao, A.L.N. 2006. Genome packaging by spherical plant RNA viruses. Annual Review of Phytopathology 44:61-87. 20. Dreher, T. W. and Rao, A.L.N. (2003). Plant Viruses do their thing. Virology 317: 187-189.

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