Patterns of mixed virus infections: a 3-year study of symptomatic cereal and grass hosts in Australia
Narelle Nancarrow
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Abstract
Yellow dwarf viruses (YDVs) form a complex of economically important pathogens that can significantly reduce grain yield in cereals. Mixed infections, or infection with two or more YDV species, can be particularly damaging.
We aimed to examine the proportion of single and multiple virus infections present in symptomatic cereal and grass plants in Victoria, south-eastern Australia.
Over 3 years (2020–2022), symptomatic cereal and grass plants from within and around cereal fields in Victoria, Australia were individually tested using tissue-blot immunoassay (TBIA) for barley yellow dwarf virus PAV, barley yellow dwarf virus MAV, cereal yellow dwarf virus RPV, wheat streak mosaic virus, and with a generic TBIA test that can detect multiple luteovirus and/or polerovirus species.
Across 2020–2021, 34% of virus-positive plants were infected with multiple YDV species. The proportion of mixed infections was similar in each individual year. However, higher proportions of wheat (Triticum aestivum, 47%) and wild oat (Avena fatua, 36%) plants were infected with multiple YDV species compared to barley (Hordeum vulgare, 8%) and brome grass (Bromus spp.,17%).
The proportion of virus-positive plants infected with multiple YDV species found was almost four times higher than previously reported in a similar study in Victoria, Australia in 1985. The proportion of plants infected with multiple YDV species varied more with host type than between individual years.
These findings demonstrate the complex epidemiology of these damaging viruses, and the challenges associated with developing virus-resistant cereal cultivars, while also highlighting the importance of regular surveillance over multiple years.
Keywords: aphid-transmitted viruses, barley (Hordeum vulgare), cereals, epidemiology, oats (Avena sativa), surveillance, viruses of plants, wheat (Triticum aestivum).
References
ABARES (2023) Australian Crop Report June 2023. ABARES, Canberra, Australia. Available at https://doi.org/10.25814/4xkx-8v26
Baltenberger DE, Ohm HW, Foster JE (1987) Reactions of oat, barley and wheat to infection with barley yellow dwarf virus isolates. Crop Science 27(2), 195-198.
| Crossref | Google Scholar |
Bencharki B, Mutterer J, El Yamani M, Ziegler-Graff V, Zaoui D, Jonard G (1999) Severity of infection of Moroccan barley yellow dwarf virus PAV isolates correlates with variability in their coat protein sequences. Annals of Applied Biology 134(1), 89-99.
| Crossref | Google Scholar |
Carew M, Schiffer M, Umina P, Weeks A, Hoffmann A (2009) Molecular markers indicate that the wheat curl mite, Aceria tosichella Keifer, may represent a species complex in Australia. Bulletin of Entomological Research 99(5), 479-486.
| Crossref | Google Scholar | PubMed |
Chay CA, Smith DM, Vaughan R, Gray SM (1996) Diversity among isolates within the PAV serotype of barley yellow dwarf virus. Phytopathology 86(4), 370-377.
| Crossref | Google Scholar |
Choudhury S, Al-Shammari D, Hu H, Meinke H, Westmore G, Birchall C, Larkin P, Zhou M (2018) A screening method to detect BYDV-PAV resistance in cereals under glasshouse conditions. Plant Pathology 67(9), 1987-1996.
| Crossref | Google Scholar |
Choudhury S, Hu H, Fan Y, Larkin P, Hayden M, Forrest K, Birchall C, Meinke H, Xu R, Zhu J, Zhou M (2019) Identification of new QTL contributing to barley yellow dwarf virus-PAV (BYDV-PAV) resistance in wheat. Plant Disease 103(11), 2798-2803.
| Crossref | Google Scholar | PubMed |
Coutts BA, Hammond NEB, Kehoe MA, Jones RAC (2008a) Finding Wheat streak mosaic virus in south-west Australia. Australian Journal of Agricultural Research 59(9), 836-843.
| Crossref | Google Scholar |
Coutts BA, Strickland GR, Kehoe MA, Severtson DL, Jones RAC (2008b) The epidemiology of Wheat streak mosaic virus in Australia: case histories, gradients, mite vectors, and alternative hosts. Australian Journal of Agricultural Research 59(9), 844-853.
| Crossref | Google Scholar |
Dwyer GI, Gibbs MJ, Gibbs AJ, Jones RAC (2007) Wheat streak mosaic virus in Australia: relationship to isolates from the pacific northwest of the USA and its dispersion via seed transmission. Plant Disease 91(2), 164-170.
| Crossref | Google Scholar | PubMed |
Eagling DR, Cunningham PJ, Sward RJ, Halloran GM (1989) The incidence of barley yellow dwarf virus isolates in perennial ryegrass (Lolium perenne) in south-western Victoria. Plant Pathology 38(3), 408-413.
| Crossref | Google Scholar |
Edwards MC, McMullen MP (1987) Effects of wheat streak mosaic virus infection on fifteen hard red spring wheat cultivars. Farm Research 44, 6-7.
| Google Scholar |
Ellis MH, Rebetzke GJ, Chu P (2003a) First report of Wheat streak mosaic virus in Australia. Plant Pathology 52(6), 808.
| Crossref | Google Scholar |
Ellis MH, Rebetzke GJ, Mago R, Chu P (2003b) First report of Wheat streak mosaic virus in Australia. Australasian Plant Pathology 32(4), 551-553.
| Crossref | Google Scholar |
Gill CC (1980) Assessment of losses on spring wheat naturally infected with barley yellow dwarf virus. Plant Disease 64(2), 197-203.
| Crossref | Google Scholar |
Guy PL, Johnstone GR, Duffus JE (1986) Occurrence and identity of barley yellow dwarf viruses in Tasmanian pasture grasses. Australian Journal of Agricultural Research 37(1), 43-53.
| Crossref | Google Scholar |
Guy PL, Johnstone GR, Morris DI (1987) Barley yellow dwarf viruses in, and aphids on, grasses (including cereals) in Tasmania. Australian Journal of Agricultural Research 38(1), 139-152.
| Crossref | Google Scholar |
Hall GS, Little DP (2013) Within-host competition between barley yellow dwarf-PAV and -PAS. Virus Research 174(1), 148-151.
| Crossref | Google Scholar |
Halliday RB, Knihinicki DK (2004) The occurrence of Aceria tulipae (Keifer) and Aceria tosichella Keifer in Australia (Acari: Eriophyidae). International Journal of Acarology 30(2), 113-118.
| Crossref | Google Scholar |
Hawkes JR, Jones RAC (2005) Incidence and distribution of barley yellow dwarf virus and cereal yellow dwarf virus in over-summering grasses in a Mediterranean-type environment. Australian Journal of Agricultural Research 56(3), 257-270.
| Crossref | Google Scholar |
Henry M, Francki RIB, Wallwork H (1992) Occurrence of barley yellow dwarf virus in cereals and grasses of the low-rainfall wheatbelt of South Australia. Plant Pathology 41(6), 713-721.
| Crossref | Google Scholar |
Hodge BA, Paul PA, Stewart LR (2020) Occurrence and high-throughput sequencing of viruses in Ohio wheat. Plant Disease 104(6), 1789-1800.
| Crossref | Google Scholar | PubMed |
Hu H, Choudhury S, Shabala S, Gupta S, Zhou M (2019) Genomic regions on chromosome 5H containing a novel QTL conferring barley yellow dwarf virus-PAV (BYDV-PAV) tolerance in barley. Scientific Reports 9(1), 11298.
| Crossref | Google Scholar | PubMed |
Jarošová J, Chrpová J, Šíp V, Kundu JK (2013) A comparative study of the Barley yellow dwarf virus species PAV and PAS: distribution, accumulation and host resistance. Plant Pathology 62(2), 436-443.
| Crossref | Google Scholar |
Jo Y, Bae J-Y, Kim S-M, Choi H, Lee BC, Cho WK (2018) Barley RNA viromes in six different geographical regions in Korea. Scientific Reports 8(1), 13237.
| Crossref | Google Scholar | PubMed |
Jones RAC, Burges N (2006) Wheat streak mosaic virus: keeping a new enemy in check. Australian Grain 15, 4-8.
| Google Scholar |
Jones RAC, McKirdy SJ, Shivas RG (1990) Occurrence of barley yellow dwarf viruses in over-summering grasses and cereal crops in Western Australia. Australasian Plant Pathology 19(3), 90-96.
| Crossref | Google Scholar |
Jones RAC, Coutts BA, Mackie AE, Dwyer GI (2005) Seed transmission of Wheat streak mosaic virus shown unequivocally in wheat. Plant Disease 89(10), 1048-1050.
| Crossref | Google Scholar | PubMed |
Kundu JK (2008) First report of Barley yellow dwarf virus-PAS in wheat and barley grown in the Czech Republic. Plant disease 92(11), 1587.
| Crossref | Google Scholar | PubMed |
Kundu JK, Jarošová J, Gadiou S, Cervená G (2009) Discrimination of three BYDV species by one-step RT-PCR-RFLP and sequence based methods in cereal plants from the Czech Republic. Cereal Research Communications 37(4), 541-550.
| Crossref | Google Scholar |
Lacroix C, Seabloom EW, Borer ET (2014) Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses. New Phytologist 204(2), 424-433.
| Crossref | Google Scholar | PubMed |
Leclercq-Le Quillec F, Plantegenest M, Riault G, Dedryver CA (2000) Analyzing and modeling temporal disease progress of Barley yellow dwarf virus serotypes in barley fields. Phytopathology 90(8), 860-866.
| Crossref | Google Scholar | PubMed |
Malmstrom CM, Bigelow P, Trębicki P, Busch AK, Friel C, Cole E, Abdel-Azim H, Phillippo C, Alexander HM (2017) Crop-associated virus reduces the rooting depth of non-crop perennial native grass more than non-crop-associated virus with known viral suppressor of RNA silencing (VSR). Virus Research 241, 172-184.
| Crossref | Google Scholar | PubMed |
McKirdy SJ, Jones RAC (1993) Occurrence of barley yellow dwarf virus serotypes MAV and RMV in over-summering grasses. Australian Journal of Agricultural Research 44(6), 1195-1209.
| Crossref | Google Scholar |
McKirdy SJ, Jones RAC (1996) Use of imidacloprid and newer generation synthetic pyrethroids to control the spread of barley yellow dwarf luteovirus in cereals. Plant Disease 80(8), 895-901.
| Crossref | Google Scholar |
McKirdy SJ, Jones RAC, Nutter FW, Jr (2002) Quantification of yield losses caused by barley yellow dwarf virus in wheat and oats. Plant Disease 86, 769-773.
| Crossref | Google Scholar | PubMed |
Milgate A, Adorada D, Chambers G, Terras MA (2016) Occurrence of winter cereal viruses in New South Wales, Australia, 2006 to 2014. Plant Disease 100(2), 313-317.
| Crossref | Google Scholar | PubMed |
Nancarrow N, Aftab M, Freeman A, Rodoni B, Hollaway G, Trębicki P (2018) Prevalence and incidence of yellow dwarf viruses across a climatic gradient: a four-year field study in south eastern Australia. Plant Disease 102, 2465-2472.
| Crossref | Google Scholar | PubMed |
Nancarrow N, Aftab M, Zheng L, Maina S, Freeman A, Rodoni B, Spackman M, Trębicki P (2019) First report of barley virus G in Australia. Plant Disease Notes 103(7), 1799.
| Crossref | Google Scholar |
Nancarrow N, Aftab M, Hollaway G, Rodoni B, Trębicki P (2021) Yield losses caused by Barley Yellow Dwarf Virus-PAV infection in wheat and barley: a three-year field study in South-Eastern Australia. Microorganisms 9(3), 645.
| Crossref | Google Scholar | PubMed |
Nancarrow N, Kinoti WM, Lam SK, Rodoni B, Trębicki P (2023) First report of cereal yellow dwarf virus RPS infecting wheat in Australia. Plant Disease 107(10), 3325.
| Crossref | Google Scholar |
Nancarrow N, Kinoti WM, Rodoni B, Lam SK, Trebicki P (2024) First report of barley yellow dwarf virus PAS (Luteovirus pashordei) in oat in Australia. Plant Disease 108(4), 1123.
| Crossref | Google Scholar |
Oswald JW, Houston BR (1951) A new virus disease of cereals, transmissible by aphids. Plant Disease Reporter 35(11), 471-475.
| Google Scholar |
Pereira AMN (1993) Epidemiology of barley yellow dwarf viruses in Portugal. Phytopathologia Mediterranea 32(3), 211-222.
| Google Scholar |
Robertson NL, French R (2007) Genetic structure in natural populations of barley/cereal yellow dwarf virus isolates from Alaska. Archives of Virology 152(5), 891-902.
| Crossref | Google Scholar | PubMed |
Shahwan I, Hill J (1984) Identification and occurrence of wheat streak mosaic virus in winter wheat in Colorado and its effects on several wheat cultivars. Plant Disease 68(7), 579-581.
| Crossref | Google Scholar |
Singh K, Wegulo SN, Skoracka A, Kundu JK (2018) Wheat streak mosaic virus: a century old virus with rising importance worldwide. Molecular Plant Pathology 19(9), 2193-2206.
| Crossref | Google Scholar | PubMed |
Slykhuis JT (1955) Aceria tulipae Keifer (Acarina: Eriophyidae) in relation to the spread of wheat streak mosaic. Phytopathology 45(3), 116-128.
| Google Scholar |
Smith HC (1957) Cereal yellow dwarf virus seen in Australia. Commonwealth Phytopathological News 3, 10-11.
| Google Scholar |
Smith PR, Sward RJ (1982) Crop loss assessment studies on the effects of barley yellow dwarf virus in wheat in Victoria. Australian Journal of Agricultural Research 33(2), 179-185.
| Crossref | Google Scholar |
Sõmera M, Fargette D, Hébrard E, Sarmiento C, ICTV Report Consortium (2021a) ICTV Virus Taxonomy Profile: Solemoviridae 2021. Journal of General Virology 102(12), 001707.
| Crossref | Google Scholar |
Sõmera M, Massart S, Tamisier L, Sooväli P, Sathees K, Kvarnheden A (2021b) A survey using high-throughput sequencing suggests that the diversity of cereal and barley yellow dwarf viruses is underestimated. Frontiers in Microbiology 12, 673218.
| Crossref | Google Scholar | PubMed |
Sward RJ, Lister RM (1987) The incidence of barley yellow dwarf viruses in wheat in Victoria. Australian Journal of Agricultural Research 38(5), 821-828.
| Crossref | Google Scholar |
Sward RJ, Lister RM (1988) The identity of barley yellow dwarf virus isolates in cereals and grasses from mainland Australia. Australian Journal of Agricultural Research 39(3), 375-384.
| Crossref | Google Scholar |
Thackray DJ, Ward LT, Thomas-Carroll ML, Jones RAC (2005) Role of winter-active aphids spreading Barley yellow dwarf virus in decreasing wheat yields in a Mediterranean-type environment. Australian Journal of Agricultural Research 56, 1089-1099.
| Crossref | Google Scholar |
Trębicki P, Nancarrow N, Bosque-Pérez NA, Rodoni B, Aftab M, Freeman A, Yen A, Fitzgerald G (2017) Virus incidence in wheat increases under elevated CO2: a 4-year field study of yellow dwarf viruses from a free air carbon dioxide facility. Virus Research 241, 137-144.
| Crossref | Google Scholar | PubMed |
Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Alfenas-Zerbini P, Davison AJ, Dempsey DM, Dutilh BE, García ML, Harrach B, Harrison RL, Hendrickson RC, Junglen S, Knowles NJ, Krupovic M, Kuhn JH, Lambert AJ, Łobocka M, Nibert ML, Oksanen HM, Orton RJ, Robertson DL, Rubino L, Sabanadzovic S, Simmonds P, Smith DB, Suzuki N, Van Dooerslaer K, Vandamme A-M, Varsani A, Zerbini FM (2021) Changes to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021). Archives of Virology 166(9), 2633-2648.
| Crossref | Google Scholar | PubMed |
Waterhouse PM, Helms K (1985) Metopolophium dirhodum (Walker): a newly arrived vector of barley yellow dwarf virus in Australia. Australasian Plant Pathology 14(4), 64-66.
| Crossref | Google Scholar |
Watson MA, Mulligan TE (1960) Comparison of two barley yellow-dwarf viruses in glasshouse and field experiments. Annals of Applied Biology 48(3), 559-574.
| Crossref | Google Scholar |
Welgemoed T, Pierneef R, Read DA, Schulze SE, Pietersen G, Berger DK (2020) Next generation sequencing reveals past and current widespread occurrence of maize yellow mosaic virus in South Africa. European Journal of Plant Pathology 158(1), 237-249.
| Crossref | Google Scholar |
Wen F, Lister RM, Fattouh FA (1991) Cross-protection among strains of barley yellow dwarf virus. Journal of General Virology 72(4), 791-799.
| Crossref | Google Scholar |
Zhou M, Larkin P, Schwinghamer M, Coutts B, Birchall C, Johnson P, Westmore G, Davey B (2015) Studies on barley yellow dwarf virus (BYDV) in wheat. In ‘Proceedings of 17th Australian Society of Agronomy Conference’, 20–24 September 2015, Hobart, Australia. pp. 1–4. Available at http://www.agronomyaustraliaproceedings.org/images/sampledata/2015_Conference/pdf/agronomy2015final00295.pdf