The invasion biology of tomato begomoviruses in Costa Rica reveals neutral synergism that may lead to increased disease pressure and economic loss
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Maliaño Núñez, Minor Rodolfo
Rojas, María del Rosario
Macedo, Monica Alves
Barboza Vargas, Natalia María
Gilbertson, Robert L.
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Abstract
Since the late 1980s, tomato production in Costa Rica has been affected by diseases caused by whitefly-transmitted begomoviruses. The first was tomato yellow
mottle virus (ToYMoV), a locally evolved New World (NW) bipartite begomovirus associated with the tomato yellow mottle disease (ToYMoD). In the late 1990s, the
invasive NW bipartite tomato leaf curl Sinaloa virus (ToLCSiV) was detected in Costa Rica and has become established and associated with ToYMoD. Finally, the
invasive Old World (OW) monopartite tomato yellow leaf curl virus (TYLCV) was detected in Costa Rica in 2012 and has also become established and is causing
tomato yellow leaf curl disease (TYLCD). In the present study, we investigated the invasion biology of these tomato-infecting begomoviruses in Costa Rica in terms of
(i) their biological and genetic properties and (ii) disease symptoms and viral DNA accumulation in tomato plants having single and mixed infections. We first
generated infectious DNA-A and DNA-B clones and agroinoculation systems for ToYMoV and ToLCSiV isolates recovered from archival ToYMoD samples collected in
Costa Rica in 1990 and 2002, respectively. Tomato plants agroinoculated with the infectious clones of both viruses developed ToYMoD symptoms, completing Koch’s
postulates for ToYMoV, and showing that ToLCSiV also causes this disease. However, pseudorecombinants formed between the DNA components of these viruses
were not infectious, which is consistent with independent evolution in different lineages and limits genetic interactions. Furthermore, ToYMoV is well-adapted to
tomato, has a narrow host range and is mechanically transmissible. The DNA-A component has a recombination event in the hot spot area and induced a symptomless
infection in agroinoculated Nicotiana benthamiana and tomato plants. Tomato plants co-infected with two or all three viruses developed more severe symptoms
compared with plants infected with each virus alone. Symptoms induced by the NW bipartite ToYMoV and ToLCSiV appeared earlier (~7 d post-inoculation [dpi])
than those induced by TYLCV (~10 dpi), but TYLCD symptoms became predominant in single and mixed infections by 14 dpi. Viral DNA accumulation was
quantified by qPCR and generally revealed a neutral synergistic interaction in which the viruses co-existed in mixed infections. A transient reduction in accumulation
of ToYMoV and ToLCSiV was detected in mixed infections at 7 dpi, whereas TYLCV accumulation was not affected in mixed infections and was uniform among
treatments and time points. Together our results suggest that this neutral synergistic interaction will lead to increased begomovirus disease severity in Costa Rica. We
discuss this in terms of begomovirus invasion biology and disease management.
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Keywords
Costa Rica, Tomato begomoviruses, Disease symptoms
Citation
https://www.sciencedirect.com/science/article/pii/S0168170222001204?via%3Dihub