Co-Infection Patterns and Geographic Distribution of a Complex Pathosystem Targeted by Pathogen-Resistant Plants

Ecological Applications, 22(1), 2012, pp. 35–52 Ó 2012 by the Ecological Society of America Co-infection patterns and geographic distribution of a complex pathosystem targeted by pathogen-resistant plants 1 2 1,3 J. M. BIDDLE, C. LINDE, AND R. C. GODFREE 1Black Mountain Laboratories, GPO Box 1600, Canberra, ACT 2601 Australia 2Research School of Biology, Australian National University, Building 116 Daley Road, Canberra, ACT 2601 Australia Abstract. Increasingly, pathogen-resistant (PR) plants are being developed to reduce the agricultural impacts of disease. However PR plants also have the potential to result in increased invasiveness of nontarget host populations and so pose a potential threat to nontarget ecosystems. In this paper we use a new framework to investigate geographical variation in the potential risk associated with unintended release of genetically modified alfalfa mosaic virus (AMV)-resistant Trifolium repens (white clover) into nontarget host populations containing AMV, clover yellow vein virus (ClYVV), and white clover mosaic virus (WClMV) in southeastern Australia. Surveys of 213 sites in 37 habitat types over a 300 000-km2 study region showed that T. repens is a significant weed of many high-conservation-value habitats in southeastern Australia and that AMV, ClYVV, and WClMV occur in 15–97% of nontarget host populations. However, T. repens abundance varied with site disturbance, habitat conservation value, and proximity to cropping, and all viral pathogens had distinct geographic distributions and infection patterns. Virus species frequently co-infected host plants and displayed nonindependent distributions within host populations, although co-infection patterns varied across the study region. Our results clearly illustrate the complexity of conducting environmental risk assessments that involve geographically widespread, invasive pasture species and demonstrate the general need for targeted, habitat- and pathosystem- specific studies prior to the process of tiered risk assessment. Key words: alfalfa mosaic virus; clover yellow vein virus; disease resistance; environmental risk assessment; genetically modified; invasion; nontarget ecosystem; Trifolium repens; white clover mosaic virus. INTRODUCTION challenge (Dale et al. 2002). Apart from the fact that our knowledge of the plant traits that contribute to Plant breeders and researchers are increasingly weediness in novel habitats is limited, even after decades utilizing targeted breeding or biotechnology to produce of observation on the movement of plants to new pathogen-resistant (PR) plants (Jauhar 2006, Gu et al. environments (Browne et al. 2007, Hulme 2009), the 2008) that have the potential to improve the efficiency specific role that diseases play in limiting the spatial and productivity of agricultural systems. However, some distribution and abundance of plant hosts is usually PR plants pose a potential threat to nontarget ecosys- unknown, apart from a few well-documented cases tems that lie beyond the scope of the intended involving catastrophic diseases such as Cryophonectria commercial release, since disease-resistant genotypes parasitica (Paillet 2002) and Phytophthora cinnamomi may exhibit increased weediness or invasiveness of host (Shearer et al. 2008). This is especially true of entire populations following relief from pathogen pressure, a groups of diseases, such as viruses, which have been process known as enemy release (Keane and Crawley poorly studied in non-agricultural systems (Roossinck 2002). Indeed, it has recently been shown that increased 2010). The available evidence, however, suggests that the population growth rates and niche expansion of impacts of disease on wild host populations are likely to nontarget host populations could occur following be subtle, and interact with factors such as habitat type introgression of disease resistance genes from genetically (Godfree et al. 2009b), host density (Ferrandino 2005), modified (GM) virus-resistant plants (Godfree et al. host–pathogen coevolutionary dynamics (Fargette et al. 2007, 2009a, b), with similar concerns being raised for 2006, Jones 2006), and the heritability of resistance traits other targeted pathosystems. (Conner et al. 2003). However, evaluating the risks that disease-resistant The development of PR plants that target multi- plants pose to nontarget ecosystems remains a daunting disease pathosystems by methods such as marker assisted breeding (e.g., bean cultivars resistant to anthracnose, angular leaf spot, and rust [Ragagnin et Manuscript received 27 February 2011; revised 6 June 2011; accepted 23 June 2011; final version received 23 August 2011. al. 2009]), multiple pathogen-derived transgenes (e.g., Corresponding Editor: S. K. Collinge. squash resistant to cucumber mosaic virus [CMV], 3 Corresponding author. E-mail: [email protected] watermelon mosaic virus [WMV], zucchini yellow 35 36 J. M. BIDDLE ET AL. Ecological Applications Vol. 22, No. 1 mosaic virus [ZYMV], and papaya ring spot virus quently, it has been argued that niche expansion [PRSV; Silora et al. 2006]), or RNA silencing (e.g., following release from one such pathogen (clover yellow Nicotiana benthamiana resistance to four tospovirus vein virus [Godfree et al. 2009a]) could occur if species [Bucher et al. 2006]), pose an additional resistance genes sourced from newly developed PR challenge to ecologists engaged in risk assessment. While genotypes were to enter nontarget populations, thus it is known that multi-species pathosystem complexes posing a threat to high conservation value native plant are common in nature (Raybould et al. 2002, Xu et al. communities. These results are especially significant 2008), and that spatial and temporal variation in disease because T. repens is the most important pasture legume incidence across species can be large (Garcı´ a-Arenal et in many temperate regions of the world and is currently al. 2001), the interactive effects of different diseases in one of Australia’s most widely grown pasture crops wild host-plant populations have rarely been quantified. (Bouton et al. 2005). However, it is clear that the demographic consequences Here, we develop and apply a simple new framework of multiple disease infections within host species may for assessing the risk posed by PR species that could differ from direct pairwise host–pathogen interactions potentially maintain large, geographically extensive (Murphy and Kyle 1995, Kim et al. 2010), and populations in nontarget habitats (Fig. 1). In this compensatory, synergistic, or antagonistic interactions framework, the early stages of risk assessment involve among different pathogens generate a diverse array of habitat identification, where potential habitats for possible interactions between different diseases and their further detailed study are identified, followed by field hosts (Xi et al. 2007, Latham and Wilson 2008, Alves- surveys, where information on the distribution and Ju´ nior et al. 2009). abundance of pathosystem components is collected. Risk assessments involving complex pathosystems are These data are then used to inform the development of also hindered by the fact that certain pathogens, perhaps the next stages of the tiered experimental risk assessment most notably viruses, are often difficult to identify in the (see Fig. 1 for discussion of tiered risk assessment field (Lopez et al. 2008), and can cause asymptomatic procedures, Wilkinson and Tepfer [2009] and Godfree et infection of wild host plants (Roossinck 2010). Addi- al. [2009a, b] for application). A significant element of tionally, the scale of field surveys and experiments this new framework involves critical decision-making needed to untangle disease 3 host 3 environment early in the risk assessment process, where herbarium interactions is often large, and so the few detailed records, vegetation data, and species distribution models studies to date that have investigated the risk of (Hill 1996) are used to identify potential host habitats, ecological release in pathosystems targeted by PR plants followed by determination of high-priority habitats have usually focused on single host–pathogen systems based on government policy, regulatory concerns and (e.g., Godfree et al. 2009a, b). Species that are both conservation priorities. Obviously, as the complexity of important disease hosts and have a track record of the pathosystem increases, and the geographic distribu- invasiveness (e.g., many pasture plants [Lonsdale 1994]) tion of the host species increases, the field survey present an additional challenge since their release from component of the work becomes large. suppression by disease could potentially impact on a The key aim of this study was to investigate spatial wide array of nontarget ecosystems. Some research variation in the composition and structure of a model underpinning risk assessment of pasture species has been multi-species pathosystem and to derive lessons for the undertaken (Cunlife et al. 2004, Wang et al. 2004, Kang development of risk assessment protocols targeting et al. 2009), but very few ecological risk assessments disease-resistant host plants in general. We focused on have been completed for transgenic pasture species T. repens populations infected with the viral pathogens (Sandhu et al. 2008, 2009, Bagavathiannana and Van alfalfa mosaic virus (AMV), white clover mosaic virus Ackerb 2010) and none to date that we are aware of for (WClMV), and clover yellow vein virus (ClYVV) over a a GM pasture species resistant to multiple pathogens.

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