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Best Linear Unbiased Prediction of Host-Range of the Facultative Parasite Colletotrichum Gloeosporioides F

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Best Linear Unbiased Prediction of Host-Range of the Facultative Parasite Colletotrichum Gloeosporioides F Biological Control 51 (2009) 158–168 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Best linear unbiased prediction of host-range of the facultative parasite Colletotrichum gloeosporioides f. sp. salsolae, a potential biological control agent of Russian thistle D.K. Berner *, W.L. Bruckart, C.A. Cavin, J.L. Michael, M.L. Carter, D.G. Luster Foreign Disease-Weed Science Research Unit, Agricultural Research Service, US Department of Agriculture, Ft. Detrick, Frederick, MD 21702, USA article info abstract Article history: Russian thistle or tumbleweed (Salsola tragus L.) is an introduced invasive weed in N. America. It is widely Received 7 March 2009 distributed in the US and is a target of biological control efforts. Accepted 10 June 2009 The fungus Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. in Penz. f. sp. salsolae (CGS) is a faculta- Available online 14 June 2009 tive parasite under evaluation for classical biological control of this weed. Host-range tests were con- ducted with CGS in quarantine to determine whether the fungus is safe to release in N. America. Keywords: Ninetytwo accessions were analyzed from 19 families: Aizoaceae, Alliaceae, Amaranthaceae, Apiaceae, Animal model Asteraceae, Brassicaceae, Cactaceae, Campanulaceae, Chenopodiaceae, Cucurbitaceae, Cupressaceae, Fab- Anthracnose aceae, Malvaceae, Nyctaginaceae, Phytolaccaceae, Poaceae, Polygonaceae, Sarcobataceae, and Solanaceae BLUP Classical biological control and 10 tribes within the Chenopodiaceae: Atripliceae, Beteae, Camphorosmeae, Chenopodieae, Corisper- Chenopodiaceae meae, Halopepideae, Polycnemeae, Salicornieae, Salsoleae, and Suaedeae. These included 62 genera and Colletotrichum gloeosporioides f. sp. salsolae 120 species. To facilitate interpretation of results, disease reaction data were combined with a relation- Deuteromycotina ship matrix derived from internal transcribed spacer DNA sequences and analyzed with mixed model Disease prediction equations to produce Best Linear Unbiased Predictors (BLUPs) for each species. Twenty-nine species GDATA (30 accessions) from seven closely-related Chenopodiaceae tribes had significant levels of disease sever- Henderson’s mixed model equations ity as indicated by BLUPs, compared to six species determined to be susceptible with least squares means Host-range testing estimates. The 29 susceptible species were: 1 from Atripliceae, 4 from Camphorosmeae, 1 from Halopepi- Invasive weeds Plant pathogens deae, 2 from Polycnemeae, 6 from Salicornieae, 8 from Salsolae, and 7 from Suaedeae. Most species in the PROC MIXED genus Salsola, which are all introduced and weedy, were very susceptible and damaged by CGS. Statistical Quartet puzzling comparisons and contrasts of BLUPs indicated that these Salsola species were significantly more suscep- Reduced animal model tible than non-target species, including 15 species from relatives in the closely-related genera Bassia Relationship matrix (=Kochia), Nitrophila, Salicornia, Sarcocornia, and Suaeda. Of the 29 susceptible species, 10 native or com- Salsola tragus mercially important species in N. America were identified as needing additional tests to determine the SAS extent of any damage caused by infection. Published by Elsevier Inc. 1. Introduction bleweed”. The tumbling habit enables rapid, long-distance dis- persal and may lead to problems with traffic or fire. Large plants Russian thistle (Salsola tragus L., Chenopodiaceae) is a major can roll across highways and dry plants may serve as a source of weed pest in the Western United States (Young, 1991). It is a suit- tinder when they lodge next to buildings. Although herbicide resis- able target for the classical biological control strategy, because it is tance has been reported in this weed (Saari et al., 1992; Stallings introduced and infests large tracts of public or low-value agricul- et al., 1994; Peterson, 1999), there are other major challenges to tural lands. Russian thistle competes with crop species (Blackshaw conventional and chemical management of this pest. Limited eco- et al., 1992; Cudney and Orloff, 1988; Young, 1988; Schillinger and nomic returns from much of the infestation preclude profitable use Young, 2004), competes for water in wheat (Schillinger and Young, of chemical herbicides and application of conventional weed con- 2000), displaces important forage plants (Crompton and Bassett, trol approaches. For these reasons, Russian thistle has been a sub- 1985), is a host of beet leafhoppers and beet curly top virus (Young, ject of research with candidate biological control agents. 1991), and some forms of the plant break off and roll with the wind A number of isolates of Colletotrichum gloeosporioides (Penz.) (Hrusa and Gaskin, 2008), hence the other common name of ‘‘Tum- Penz. & Sacc. in Penz. (Deuteromycotina, Coelomycetes; teleo- morph Glomerella cingulata [Stoneman] Spauld. & H. Schrenk) have * Corresponding author. Fax: +1 301 619 2880. been evaluated for biological control of weeds, despite the fact that E-mail address: [email protected] (D.K. Berner). C. gloeosporioides has been reported on hosts from almost 200 plant 1049-9644/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.biocontrol.2009.06.003 D.K. Berner et al. / Biological Control 51 (2009) 158–168 159 genera (Farr and Rossman, n.d.). Research on isolates of C. gloeospo- The combination of parental performance data and genetic related- rioides for biological control has shown that individual isolates are ness among parents and future progeny allow BLUPs to be gener- reasonably host specific and not damaging to non-target species ated in the absence of performance data, i.e., for future progeny. (Cartwright and Templeton, 1989; Daniel et al., 1973; Killgore In the case of host-range tests in risk assessments of candidate bio- et al., 1999; Mortensen, 1988; Mortensen and Makowski, 1997; logical control organisms, this methodology allows for prediction TeBeest, 1988; Trujillo, 2005; Trujillo et al., 1986). The isolate of of susceptibility of plant species relative to that of the target spe- C. gloeosporioides (96-067) used in this study was first described cies (Berner et al., 2009) and enables predictions of disease reac- on Salsola kali in Hungary (Schwarczinger et al., 1998). Other tion for species that cannot be tested, either because they are genetically similar isolates have been found in both Greece (Berner rare or virtually impossible to grow; a situation analogous to future et al., 2006) and Russia (Kolomiets et al., 2008), so the fungus ap- un-tested progeny. Thus the complete host-range of a pathogen, pears to be widespread in the native range of S. tragus. Isolate using both tested, i.e., inoculated, and not tested species in the 96-067 has been shown to be lethal to S. tragus, and evidence exists analysis, can be predicted. This host-range can then be used to for specificity of this isolate within the genus Salsola (Bruckart et establish if any additional non-target plant species should be al., 2004). Because of its specificity within Salsola, isolate 96-067 tested. is referred to in this paper as C. gloeosporioides f. sp. salsolae (CGS). Recently, the MME were used effectively with DNA sequences of Each isolate of C. gloeosporioides described by the aforemen- the internal transcribed spacer 1 (ITS1), 5.8S ribosomal RNA (5.8S tioned authors has been subject to a risk assessment for use as a rRNA), and internal transcribed spacer 2 (ITS2) regions, as mea- biological control agent. Central to the conduct of a risk assessment sures of genetic relationships among species, to clarify the host- is determination of host-range of the candidate agent. For the past range of the obligate parasitic rust fungus Uromyces salsolae, also 30 years, the traditional approach to developing test plant lists for being evaluated for biological control of Russian thistle (Berner et host-range determinations has been the phylogenetic testing al., 2009). Thus it was of interest to see if the same approach could method (Wapshere, 1974). Currently, this process of risk assess- be used as effectively to clarify the host-range of CGS, which is a ment is being scrutinized, and Briese (2005) has called for modern- facultative parasitic fungus, and to see how much BLUPs for disease ization of the process to better translate host-range test results, reaction to the two pathogens were dependent on genetic related- which involve small sample sizes of questionable species represen- ness of the plant species tested versus disease rating data, i.e., see tation tested under artificial conditions, into real-world expecta- how robust BLUPs were for the two pathogens. tions and outcomes. To improve the process, Briese (2005) The objectives of this study were to (1) determine whether the suggests taking into account improved knowledge of plant phylo- MME, based on ITS-5.8S rDNA sequence data and disease ratings, genetic relationships. This is particularly germane for Russian are more useful than least squares methods in delimiting the thistle. host-range of CGS; (2) determine the probable host-range of CGS Only recently has there been resolution of taxonomy and clear among related plant species; (3) determine whether CGS is suffi- identification of species commonly known as Russian thistle in ciently host specific to propose release into N. America for biolog- North America (Ryan and Ayres, 2000; Gaskin et al., 2006; Hrusa ical control or requires additional evaluation; (4) predict and Gaskin,
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