Effects of introduced and indigenous viruses on native plants: exploring their disease causing potential at the agro-ecological interface

Abstract

The ever increasing movement of viruses around the world poses a major threat to plants growing in cultivated and natural ecosystems. Both generalist and specialist viruses move via trade in plants and plant products. Their potential to damage cultivated plants is well understood, but little attention has been given to the threat such viruses pose to plant biodiversity. To address this, we studied their impact, and that of indigenous viruses, on native plants from a global biodiversity hot spot in an isolated region where agriculture is very recent (<185 years), making it possible to distinguish between introduced and indigenous viruses readily. To establish their potential to cause severe or mild systemic symptoms in different native plant species, we used introduced generalist and specialist viruses, and indigenous viruses, to inoculate plants of 15 native species belonging to eight families. We also measured resulting losses in biomass and reproductive ability for some host-virus combinations. In addition, we sampled native plants growing over a wide area to increase knowledge of natural infection with introduced viruses. The results suggest that generalist introduced viruses and indigenous viruses from other hosts pose a greater potential threat than introduced specialist viruses to populations of native plants encountered for the first time. Some introduced generalist viruses infected plants in more families than others and so pose a greater potential threat to biodiversity. The indigenous viruses tested were often surprisingly virulent when they infected native plant species they were not adapted to. These results are relevant to managing virus disease in new encounter scenarios at the agro-ecological interface between managed and natural vegetation, and within other disturbed natural vegetation situations. They are also relevant for establishing conservation policies for endangered plant species and avoiding spread of damaging viruses to undisturbed natural vegetation beyond the agro-ecological interface.

Figure 1. South west Australian floristic region: sites where introduced generalist viruses were found infecting native plants.

Insets 1 and 2 show where natural infection with introduced generalist viruses was detected in 2001 and 2009. Inset 1 shows the overall sampling area and Inset 2 shows the urban Perth area. The red spot symbols and place names indicate positions of individual sampling sites with positive virus detections. For an explanation of which viruses were found at each site see Table 5.

Figure 2. Symptoms in native plant species inoculated with infective leaf sap containing introduced or indigenous viruses.

A, Large necrotic spot lesions caused by localised infection with an indigenous virus (Clitoria chlorosis virus) in an inoculated leaf of Kennedia coccinea; B, Large necrotic spot local lesions caused by localised infection with an introduced specialist virus (Potato virus X, PVX) in an inoculated leaf of K. coccinea; C, Large necrotic spot local lesions caused by localised infection with an introduced generalist virus (Tomato spotted wilt virus) in an inoculated leaf of Alyogyne huegelii; D, Mild bunching symptoms in young leaves in a plant of Trachymene coerulea caused by systemic infection with an introduced generalist virus (Alfalfa mosaic virus); E, Mild symptoms of necrotic streaking and necrotic leaf markings caused by systemic infection with an introduced specialist virus (PVX) in a plant of Anigozanthos manglesii; F, Mild-moderate stunting caused by systemic infection with an introduced specialist virus (Wheat streak mosaic virus) in plants of Austrostipa compressa (right) compared with more vigorous growth in a mock-inoculated plants (left).

Figure 3. Severe symptoms in native plant species inoculated with infective sap containing introduced or indigenous viruses.

A, Severe stunting caused by systemic infection with an introduced generalist virus (Cucumber mosaic virus) in two plants of Anigozanthos manglesii (left) compared with healthy vigorous growth in two mock-inoculated plants of A. manglesii (right); B, Severe plant stunting, apical shoot necrosis and leaf necrosis caused by recent infection with an introduced generalist virus (Tomato spotted wilt virus, TSWV) in three plants A. manglesii (left) compared with healthy vigorous growth in three recently mock-inoculated plants of A. manglesii (right); C, Severe plant stunting, leaf necrosis and leaf chlorosis caused by infection with TSWV in five plants of Solanum symonii (right) compared with healthy vigorous growth in five mock-inoculated plants of S. symoniii (left); D, Systemic necrosis and death caused by infection with an introduced generalist virus (Turnip mosaic virus) in two plants of Trachymene coerulea (front) compared with healthy vigorous growth in two mock-inoculated T. coerulea plants (back); E, Severe stunting caused by systemic infection with an indigenous virus (Clitoria chlorosis virus) in two plants of Kennedia coccinea (right) compared with healthy vigorous growth in two mock-inoculated plants of K. coccinea (left). F, Severe stunting caused by recent systemic infection with an indigenous virus (Passion fruit woodiness virus) in a plant of K. coccinea (right) compared with healthy vigorous growth in a recently mock-inoculated plant of K. coccinea (left).

Figure 4. Native plants growing in the South West Australian Floristic Region showing obvious virus symptoms.

For locations of site names see Fig. 1. A, Severe chlorotic mottle and leaf deformation caused by infection with an introduced generalist virus (Bean yellow mosaic virus, BYMV) in plants of Kennedia prostrata growing near Badgingarra; B, Mild mosaic caused by infection with an unidentified virus in young leaflets (right) of K. coccinea plants growing near Wooroloo; C, Bright yellow leaf mottle caused by infection with an unidentified virus in young leaves of a Bossiaea sp. plant growing at The Lakes; D, Chlorotic leaf mottle, leaf deformation and severe plant stunting (plants with arrows) caused by infection with an unidentified virus in plants of K. prostrata growing near Wooroloo compared with vigorously growing healthy K. prostrata plants (top left and right); E, Leaf mosaic caused by infection with BYMV in leaf of Caladenia paludosa growing in an orchid collection at Kings Park.