Virus complexes in strawberry: What are they and how do we manage them?

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1 Virus complexes in strawberry: What are they and how do we manage them? William M. Wintermantel USDA-ARS Salinas, CA Ph: Robert R. Martin USDA-ARS HCRL Corvallis, OR Ph:

2 History of Pallidosis Related Decline (PRD) in California 1999 Bob Martin (ARS-Corvallis) carried out survey of strawberry viruses in Maryland with S.C. Hokanson and found pallidosis to be the most common virus disease there A crinivirus, Strawberry pallidosis associated virus (SPaV), was found associated with pallidosis disease We identified a second crinivirus, Beet pseudo yellows virus (BPYV) in some strawberries with pallidosis disease from Watsonville.

3 History of PRD (cont) 2003 Surveys found these two viruses most common among viruses in declining plants in California and beyond Found aphid and nematode transmitted viruses along with either SPaV or BPYV in strawberry with PRD symptoms.

4 Strawberry Decline in CA Ventana (Watsonville)

5 Strawberry Decline in CA Camarosa (Watsonville) Others had looked for causes of this since it did not look like a virus disease, foliar nematodes and cyclamen mite were absent. Declining plants were Infected with multiple viruses.

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9 Note brittle root symptoms

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11 Some plants may exhibit recovery after dieback

12 Strawberry DECLINE in Totem

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14 Double-stranded RNA from strawberry exhibiting decline symptoms * The pattern at left suggested the plants contained a crinivirus

15 Detection of Criniviruses in strawberry by RT-PCR Polymerase Chain Reaction (PCR) Actually RT-PCR

16 Detection of Crinivirus infection and SPaV by degenerate and specific RT-PCR CRINI Pol primers SPaV CP primers DNA Ladder H. Strawberry Str 1 Str 2 Str 3 Str 4 Str 5 DNA Ladder H. Strawberry Str 1 Str 2 Str 3 Str 4 Str nt product 750 nt product

17 Detection of BPYV in strawberry by RT-PCR Strawberry 1 Strawberry 2 Strawberry 3 H. Strawberry DNA Ladder Primers detect portion of BPYV CPm gene (approx 350 nts)

18 Nearly all strawberry plants exhibiting virus related decline symptoms were infected with one or both of two whitefly-transmitted viruses: Strawberry pallidosis associated virus (SPaV) Beet pseudo-yellows virus (BPYV)

19 Beet pseudo yellows virus (BPYV) First characterized in 1965 by J.E. Duffus, USDA- ARS-Salinas, CA Transmitted exclusively by the greenhouse whitefly (T. vaporariorum) after feeding on infected sources for several hours to a few days BPYV has a very large host range infecting large number of species from at least 20 taxonomic families

20 Detection of BPYV in Monterey County crops and weeds by RT-PCR (Fall 2003) Malva Malva Radish Strawberry Hemlock Malva Jimsonweed Radish Artichoke Jimsonweed Malva DNA Ladder Pumpkin Pumpkin Strawberry Pumpkin Artichoke N. Benthamiana (GH) H. Strawberry (GH) H. Malva (GH) BPYV CPm Primers

21 Strawberry pallidosis associated virus (SPaV) Discovered in 1969 by Frazier and Stubbs (Plant Dis. Rept. 53: Vector: Greenhouse whitefly (T. vaporariorum). Host range: appears limited to strawberry (Fragaria species) and a few weed hosts.

22 Limited knowledge of SPaV host range Susceptible host species: Fragaria ananassa F. chiloensis F. vesca F. virginiana Diagnostic species: Nicotiana benthamiana N. clevelandii Physalis wrightii Urtica californica Sibbaldia procumbens Malva parviflora Fragaria ananassa, F. vesca - symptomless. Fragaria virginiana - leaf deformation, chlorosis and dwarfing. Ref: Tzanetakis et al., 2006 Plant Disease 90:

23 Transmission of SPaV and BPYV by the greenhouse whitefly* Virus Plant Species Fragaria x ananassa Nicotiana benthamiana BPYV 8/21 (38%) 16/20 (80%) SPaV 3/21 (14%) 3/20 (15%) No transmission by either banded wing whitefly (T. abutilonea) or sweet potato whitefly (B. tabaci) Ref: Tzanetakis et al., 2006 Plant Disease 90:

24 Most strawberry plants exhibiting virus related decline symptoms were also infected with one of several non-whitefly transmitted viruses (previous studies): Virus (Vector) Strawberry mild yellow edge virus (APHID) Strawberry crinkle virus (APHID) Strawberry mottle virus (APHID) Strawberry latent ringspot virus (NEMATODES) Fragaria chiloensis latent virus (APHID) Strawberry necrotic shock virus (THRIPS, POLLEN)

25 Fast Forward to 2013: Strawberry Decline in Guadalupe Massive populations of greenhouse whitefly infested Guadalupe area Fields in fall PRD-like symptoms appeared in Spring 2013.

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31 Multiple collections of symptomatic plants were collected from Guadalupe area Symptoms similar to those of PRD in , but some variation among varieties Samples sent to USDA-ARS in Salinas and Corvallis to determine which viruses were present

32 Results confirmed classic PRD combination of a crinivirus (SPaV or BPYV) with up to three other viruses. Predominant whitefly-transmitted virus was SPaV, but also substantial BPYV Also identified Strawberry mild yellow edge virus; aphid transmitted Strawberry mottle virus; aphid transmitted Strawberry necrotic shock virus; thrips and pollen transmitted

33 Where did these viruses come from? SPaV likely came from strawberry, possibly from older infected plants, and distributed by large whitefly populations in Fall 2012 BPYV could have come from strawberry or from a wide array of weed hosts common in coastal regions Aphid and thrips viruses likely came from strawberry

34 Many fields were mowed and began to regrow in mid-summer. Does this help???

35 Mowing does not remove the virus, but: Plants begin to grow again as SPaV levels decline in late summer and early fall. Recovery peaks mid fall, then plants begin to decline again as virus levels increase in late fall and early winter. Growers will need to decide if this is really cost-effective; it does not eliminate virus.

36 Nurseries Nurseries are working agressively to eliminate and certify seedlings Strawberry nurseries have supplied samples to USDA-ARS-Corvallis for virus monitoring Results take time In the meantime, use effective disease management

37 Management Start with certified clean nursery stock If plants are already in the ground and must be kept, aggressive whitefly management is critical to limit spread to new fields Remove diseased fields prior to planting new fields (maintain regional virus-free period) Use effective weed management to avoid movement of virus from weed hosts. Be alert that unaffected areas in 2013 may be vulnerable to transmission if growers do not use aggressive whitefly suppression; it s not easy to bring an epidemic under control! Cooperate with and talk to your neighbors about it!