Do virus‐resistant plants pose a threat to non‐target ecosystems? I. Evidence from an Australian pathosystem based on glasshouse challenge experiments

Abstract

One key environmental risk associated with the release of novel disease-resistant plants is the potential for non-target host populations to acquire resistance genes and undergo enemy release, leading to damage to associated native plant populations in high conservation-value ecosystems. Unfortunately, the dynamics of most natural pathosystems are poorly understood, and risk assessment of disease-resistant plants remains a challenge.Here we describe the first stage of a multi-tiered risk assessment strategy aimed at quantifying potential ecological release in a model pathosystem (the weedy pasture species Trifolium repens infected with Clover yellow vein virus; ClYVV) in order to assess the level of risk posed by genetically modified and conventionally bred disease-resistant host genotypes to non-target plant communities in south-eastern Australia. Glasshouse inoculation and growth experiments using 14 ClYVV isolates and 20 wild T. repens lines collected from high conservation-value montane grassland and woodland communities show that viral infection reduces the survival and growth of host plants by on average 10-50%. However, T. repens lines exhibited variable levels of resistance and tolerance to virus infection and ClYVV isolates differed in infectivity and aggressiveness, with grassland isolates having a greater pathogenic effect on associated host plants than woodland isolates.We conclude that ClYVV potentially plays an important role in limiting the size of T. repens populations in some at-risk non-target ecosystems and that second-tier field experiments are required to adequately quantify the risk associated with the commercial release of V-R T. repens genotypes in Australia.

Co‐infection patterns and geographic distribution of a complex pathosystem targeted by pathogen‐resistant plants

“…The cause of these different distributions is difficult to explain, but could reflect the distribution of aphid vectors (both AMV and ClYVV are transmitted by aphids in a non-persistent manner (Latch andSkipp 1987, Johnstone andChu 1993), variation in disturbance (WClMV is dispersed by mechanical means and often occurs in mown areas; Johnstone and Chu 1993), differences in the specificity of aphid vectors (Wang et al 2006), transmission efficiency (Moreno et al 2005), variation in viral titer in host plants (Martı´n and Elena 2009), or perhaps in the resistance of local T. repens genotypes to extant virus genotypes (Godfree et al 2009a). Chronic drought in the southern part of the survey region (Murphy and Timbal 2008) could perhaps be important.…”

“…However, some PR plants pose a potential threat to nontarget ecosystems that lie beyond the scope of the intended commercial release, since disease-resistant genotypes may exhibit increased weediness or invasiveness of host populations following relief from pathogen pressure, a process known as enemy release (Keane and Crawley 2002). Indeed, it has recently been shown that increased population growth rates and niche expansion of nontarget host populations could occur following introgression of disease resistance genes from genetically modified (GM) virus-resistant plants (Godfree et al 2007(Godfree et al , 2009a, with similar concerns being raised for other targeted pathosystems.…”

“…In this paper, we report the first stages in the ecological risk assessment of transgenic Trifolium repens (white clover) genotypes that express resistance to a range of viral pathogens that occur in agricultural systems and nontarget host populations (Spangenberg et al 2001). T. repens is a well-studied model GM pasture species (Godfree et al 2006(Godfree et al , 2007(Godfree et al , 2009a, which meets several criteria indicative of potential risk to nontarget plant communities. In Australia, T. repens is known to become naturalized or invasive in native plant communities (Godfree et al 2004b) and is often infected by a range of viral diseases in agricultural landscapes (see (McLean 1983, McKirdy and Jones 1995, 1997, Norton and Johnstone 1998, Coutts and Jones 2002.…”

“…In Australia, T. repens is known to become naturalized or invasive in native plant communities (Godfree et al 2004b) and is often infected by a range of viral diseases in agricultural landscapes (see (McLean 1983, McKirdy and Jones 1995, 1997, Norton and Johnstone 1998, Coutts and Jones 2002. Conse-quently, it has been argued that niche expansion following release from one such pathogen (clover yellow vein virus [Godfree et al 2009a]) could occur if resistance genes sourced from newly developed PR genotypes were to enter nontarget populations, thus posing a threat to high conservation value native plant communities. These results are especially significant because T. repens is the most important pasture legume in many temperate regions of the world and is currently one of Australia's most widely grown pasture crops (Bouton et al 2005).…”

Do virus‐resistant plants pose a threat to non‐target ecosystems? II. Risk assessment of an Australian pathosystem using multi‐scale field experiments

“…1998; Kalla et al. 2001) to non‐target systems, have been described previously (see Godfree et al. 2004a, 2006, 2009); here we focus on the ecological risks associated with potential movement of genes coding for viral resistance into wild T. repens populations and their subsequent release from natural pathogen suppression.…”