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Effect of cultivar and temperature on the synergistic interaction between panicum mosaic virus and satellite panicum mosaic virus in switchgrass

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Abstract

Panicum mosaic virus (PMV), the type member of the genus Panicovirus in the family Tombusviridae, naturally infects switchgrass (Panicum virgatum L.). PMV and its molecular partner, satellite panicum mosaic virus (SPMV), interact synergistically in coinfected millets to exacerbate the disease phenotype and increase the accumulation of PMV compared to plants infected with PMV alone. In this study, we examined the reaction of switchgrass cvs. Summer and Kanlow to PMV and PMV+SPMV infections at 24°C and 32°C. Switchgrass cv. Summer was susceptible to PMV at both temperatures. In contrast, cv. Kanlow was tolerant to PMV at 24°C, but not at 32°C, suggesting that Kanlow harbors temperature-sensitive resistance to PMV. At 24°C, PMV was readily detected in inoculated leaves, but not in upper uninoculated leaves of Kanlow, suggesting that resistance to PMV was likely mediated by abrogation of long-distance virus transport. Coinfection by PMV and SPMV at 24°C and 32°C in cv. Summer, but not in Kanlow, caused increased symptomatic systemic infection and mild disease synergism with slightly increased PMV accumulation compared to plants infected with PMV alone. These data suggest that the interaction between PMV and SPMV in switchgrass is cultivar-dependent, manifested in Summer but not in Kanlow. However, co-inoculation of cv. Kanlow with PMV+SPMV caused an enhanced asymptomatic infection, suggesting a role of SPMV in enhancement of symptomless infection in a tolerant cultivar. These data suggest that enhanced asymptomatic infections in a virus-tolerant switchgrass cultivar could serve as a source of virus spread and play an important role in panicum mosaic disease epidemiology under field conditions. Our data reveal that the cultivar, coinfection with SPMV, and temperature influence the severity of symptoms elicited by PMV in switchgrass.

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References

  1. McLaughlin SB, Kszos LA (2005) Development of switchgrass (Panicum virgatum) as a bioenergy feedstock in the United States. Biomass Bioenergy 28:515–535

    Article  Google Scholar 

  2. Vogel K, Mitchell R, Sarath G, Casler MD (2014) Registration of ‘Liberty’ switchgrass. J Plant Regist 8:242–247

    Article  Google Scholar 

  3. Schmer MR, Vogel KP, Mitchell RB, Perrin RP (2008) Net energy of cellulosic ethanol from switchgrass. Proc Natl Acad Sci USA 105:464–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bouton JH (2007) Molecular breeding of switchgrass for use as a biofuel crop. Curr Opin Genet Dev 17:553–558

    Article  CAS  PubMed  Google Scholar 

  5. Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc Natl Acad Sci USA 103:11206–11210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Casler MD, Vogel KP, Lee DK, Mitchell RB, Adler PR, Sulc RM, Johnson KD, Kallenbach RL, Boe AR, Mathison RD, Cassida KA, Min DH, Crawford J, Moore KJ (2018) 30 years of progress toward increased biomass yield of switchgrass and big bluestem. Crop Sci 58:1242–1254

    Article  Google Scholar 

  7. Edmé S, Mitchell R, Sarath G (2017) Genetic parameters and prediction of breeding values in switchgrass bred for bioenergy. Crop Sci 57:1464–1474

    Article  Google Scholar 

  8. Edmé SJ, Sarath G, Palmer N, Yuen GY, Muhle AA, Mitchell R, Tatineni S, Tobias C (2020) Genetic (co)variation and accuracy of selection for resistance to viral mosaic disease and production traits in an inter-ecotypic switchgrass breeding population. Crop Sci 61:1652–1665

    Article  CAS  Google Scholar 

  9. Alexander HM, Bruns E, Schebor H, Malmstrom CM (2017) Crop-associated virus infection in a native perennial grass: reduction in plant fitness and dynamic patterns of virus detection. J Ecol 105:1021–1031

    Article  Google Scholar 

  10. Cheng Q, Windham AS, Lamour KH, Saxton AM, Windham MT (2019) Evaluation of variation in switchgrass (Panicum virgatum L.) cultivars for rust (Puccinia emaculata) resistance1. J Environ Hortic 37:127–135

    Article  CAS  Google Scholar 

  11. Songsomboon K, Crawford R, Crawford J, Hansen J, Cummings J, Mattson N, Bergstrom G, Viands D (2019) Recurrent phenotypic selection for resistance to diseases caused by Bipolaris oryzae in switchgrass (Panicum virgatum L.). Biomass Bioenerg 125:105–113

    Article  Google Scholar 

  12. Stewart CL, Pyle JD, Jochum CC, Vogel KP, Yuen GY, Scholthof KBG (2015) Multi-year pathogen survey of biofuel switchgrass breeding plots reveals high prevalence of infections by Panicum mosaic virus and its satellite virus. Phytopathology 10:1146–1154

    Article  CAS  Google Scholar 

  13. Sykes VR, Allen FL, Mielenz JR, Stewart CN Jr, Windham MT, Hamilton CY, Rodriguez M Jr, Yee KL (2016) Reduction of ethanol yield from switchgrass infected with rust caused by Puccinia emaculata. Bioenergy Res 9:239–247

    Article  CAS  Google Scholar 

  14. VanWallendael A, Bonnette J, Juenger TE, Fritschi FB, Fay PA, Mitchell RB, Lloyd-Reilley J, Rouquette FM Jr, Bergstrom GC, Lowry DB (2020) Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum). New Phytol. https://doi.org/10.1111/nph.16555

    Article  PubMed  Google Scholar 

  15. Buzen FG, Niblett CL, Hooper GR, Hubbard J, Newman MA (1984) Further characterization of panicum mosaic virus and its associated satellite virus. Phytopathology 74:313–318

    Article  CAS  Google Scholar 

  16. Sill WH, Pickett RC (1957) A new disease of switchgrass, panicum virgatum. Plant Dis Reptr 41:241–249

    Google Scholar 

  17. Turina M, Maruoka M, Monis J, Jackson AO, Scholthof KBG (1998) Nucleotide sequence and infectivity of a full-length cDNA clone of panicum mosaic virus. Virology 241:141–155

    Article  CAS  PubMed  Google Scholar 

  18. Masuta C, Zuidema D, Hunter BG, Heaton LA, Sopher DS, Jackson AO (1987) Analysis of the genome of satellite panicum mosaic virus. Virology 159:329–338

    Article  CAS  PubMed  Google Scholar 

  19. Pyle JD, Monis J, Scholthof KBG (2017) Complete nucleotide and virion particle association of two satellite RNAs of Panicum mosaic virus. Virus Res 240:87–93

    Article  CAS  PubMed  Google Scholar 

  20. Ban N, McPherson A (1995) The structure of satellite panicum mosaic virus at 1.9 Å resolution. Nat Struct Biol 2:882–890

    Article  CAS  PubMed  Google Scholar 

  21. Qiu W, Scholthof KBG (2001) Genetic identification of multiple biological roles associated with the capsid protein of satellite panicum mosaic virus. Mol Plant Microbe Interact 14:21–30

    Article  CAS  PubMed  Google Scholar 

  22. Scholthof KBG (1999) A synergism induced by Satellite panicum mosaic virus. Mol Plant Microbe Interact 12:163–166

    Article  CAS  Google Scholar 

  23. Chowda-Reddy RV, Palmer N, Edme S, Sarath G, Kovacs F, Yuen G, Mitchell R, Tatineni S (2019) A two amino acid difference in the coat protein of Satellite panicum mosaic virus isolates is responsible for differential synergistic interaction with panicum mosaic virus. Mol Plant Microbe Interact 32:479–490

    Article  CAS  PubMed  Google Scholar 

  24. Muhle AA (2019) Rust and viral mosaic diseases in biofuel switchgrass. MS Thesis, University of Nebraska-Lincoln, p 77

  25. Ohki T, Sano M, Asano K, Nakayama T, Maoka T (2018) Effect of temperature on resistance to potato virus Y in potato cultivars carrying the resistance gene Rychc. Plant Pathol 67:1629–1635

    Article  CAS  Google Scholar 

  26. Tatineni S, Wosula SN, Bartels M, Hein GL, Graybosch RA (2016) Temperature-dependent Wsm1 and Wsm2 gene-specific blockage of viral long-distance transport provides resistance to Wheat streak mosaic virus and Triticum mosaic virus in wheat. Mol Plant Microbe Interact 29:724–738

    Article  CAS  PubMed  Google Scholar 

  27. Zhu Y, Qian W, Hua J (2010) Temperature modulates plant defense response through NB-LRR proteins. PLoS Pathog 6:e1000844

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Donze-Reiner T, Palmer NA, Scully ED, Prochaska TJ, Koch KG, HengMoss T, Bradshaw JD, Twigg P, Amundsen K, Sattler SE, Sarath G (2017) Transcriptional analysis of defense mechanisms in upland tetraploid switchgrass to green bugs. BMC Biol 17:46

    Google Scholar 

  29. Omarov RT, Qi D, Scholthof KBG (2005) The capsid protein of satellite panicum mosaic virus contributes to systemic invasion and interacts with its helper virus. J Virol 79:9756–9764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Qiu W, Scholthof KBG (2000) In vitro- and in vivo-generated defective RNAs of satellite panicum mosaic virus define cis-acting RNA elements required for replication and movement. J Virol 74:2247–2254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Qiu W, Scholthof KBG (2001) Defective interfering RNAs of a satellite virus. J Virol 75:5429–5432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. De Ronde D, Butterbach P, Kormelink R (2014) Dominant resistance against plant viruses. Front Plant Sci 5:307

    Article  PubMed  PubMed Central  Google Scholar 

  33. Fraser RSS (1990) The genetics of resistance to plant viruses. Annu Rev Phytopathol 28:179–200

    Article  Google Scholar 

  34. Bendahmane A, Kanyuka K, Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Moffett P (2009) Mechanisms of recognition in dominant R gene mediated resistance. Adv Virus Res 75:1–33

    Article  CAS  PubMed  Google Scholar 

  36. Frazier TP, Palmer NA, Xie F, Tobias CM, Donze-Reiner TJ, Bombarely A, Childs KL, Shu S, Jenkins JW, Schmutz J, Zhang B, Sarath G, Zhao B (2016) Identification, characterization, and gene expression analysis of nucleotide binding site (NB)-type resistance gene homologues in switchgrass. BMC Genom 17:892

    Article  CAS  Google Scholar 

  37. Palmer NA, Chowda-Reddy RV, Muhle AA, Tatineni S, Yuen G, Edme SJ, Mitchell RB, Sarath G (2019) Transcriptome divergence during leaf development in two contrasting switchgrass (Panicum virgatum L.) cultivars. PLoS ONE 14:e0222080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Chisholm ST, Parra MA, Anderberg RJ, Carrington JC (2001) Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of Tobacco etch virus. Plant Physiol 127:1667–1675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Decroocq V, Salvador B, Sicard O, Glasa M, Cosson P, Svanella-Dumas L, Revers F, García JA, Candresse T (2009) The determinant of potyvirus ability to overcome the RTM resistance of Arabidopsis thaliana maps to the N-terminal region of the coat protein. Mol Plant Microbe Interact 22:1302–1311

    Article  CAS  PubMed  Google Scholar 

  40. Feng X, Guzman P, Myers JR, Karasev AV (2017) Resistance to Bean common mosaic necrosis virus conferred by the bc-1 gene affects systemic spread of the virus in common bean. Phytopathology 107:893–900

    Article  CAS  PubMed  Google Scholar 

  41. Khatabi B, Fajolu OL, Wen RH, Hajimorad MR (2012) Evaluation of North American isolates of Soybean mosaic virus for gain of virulence on Rsv-genotype soybeans with special emphasis on resistance-breaking determinants on Rsv4. Mol Plant Pathol 13:1077–1088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Graybosch RA, Peterson CJ, Baenziger PS, Baltensperger DD, Nelson LA, Jin Y, Kolmer J, Seaborn B, French R, Hein G, Martin TJ, Beecher B, Schwarzacher T, Heslop-Harrison P (2009) Registration of ‘Mace’ hard red winter wheat. J Plant Regist 3:51–56

    Article  Google Scholar 

  43. Lu H, Price J, Devkota R, Rush C, Rudd J (2011) A dominant gene for resistance to wheat streak mosaic virus in winter wheat line CO960293-2. Crop Sci 51:5–12

    Article  Google Scholar 

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Acknowledgements

USDA is an equal opportunity provider and employer. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. We thank Emily Rasmussen for her technical assistance in agarose gel electrophoresis of RT-PCR products.

Funding

This research was partially funded by Department of Energy, Office of Science grant DE-SC0016108 and by USDA-ARS CRIS project 3042-21000-034-00D.

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Authors and Affiliations

  1. United States Department of Agriculture-Agricultural Research Service, University of Nebraska-Lincoln, Lincoln, USA

    Anthony A. Muhle, Nathan A. Palmer, Serge J. Edme, Gautam Sarath, Robert B. Mitchell & Satyanarayana Tatineni

  2. Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, USA

    Serge J. Edme, Gautam Sarath & Robert B. Mitchell

  3. Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA

    Anthony A. Muhle, Gary Yuen & Satyanarayana Tatineni

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  1. Anthony A. Muhle
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Contributions

ST, GS, and GY formulated and designed the experiments; AM performed the research; GS, NP, and GY supervised the research; SE and GY provided funding for the research; ST, AM, NP, and GS analyzed the data; SE and RM provided resources and analyzed the data; ST and AM wrote the manuscript; and ST, AM, NP, SE, GS, GY, and RM edited and improved the manuscript and approved the submitted version.

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Correspondence to Satyanarayana Tatineni.

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Muhle, A.A., Palmer, N.A., Edme, S.J. et al. Effect of cultivar and temperature on the synergistic interaction between panicum mosaic virus and satellite panicum mosaic virus in switchgrass. Arch Virol 167, 1247–1256 (2022). https://doi.org/10.1007/s00705-022-05412-y

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