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Diversity, Pathogenicity, and Management of Verticillium Species

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Diversity, Pathogenicity, and Management of Verticillium Species UC Davis UC Davis Previously Published Works Title Diversity, Pathogenicity, and Management of Verticillium Species Permalink https://escholarship.org/uc/item/4xr5g80x Journal Annual Review of Phytopathology, 47 Author Subbarao, Krishna V Publication Date 2009-04-12 Peer reviewed eScholarship.org Powered by the California Digital Library University of California ANRV384-PY47-03 ARI 12 April 2009 14:58 V I E E W R S Review in Advance first posted online on April 22, 2009. (Minor changes may still occur before final publication I E online and in print.) N C N A D V A Diversity, Pathogenicity, and Management of Verticillium Species Steven J. Klosterman,1,∗ Zahi K. Atallah,2,∗ Gary E. Vallad,3 and Krishna V. Subbarao2 1USDA-ARS, Salinas, California 93905, 2Department of Plant Pathology, University of California, Davis, California 95616, and 3University of Florida, Wimauma, Florida 33598; email: [email protected] Annu. Rev. Phytopathol. 2009. 47:39–62 Key Words The Annual Review of Phytopathology is online at taxonomy, species concept, host range expansion, host colonization, phyto.annualreviews.org seed transmission, host resistance This article’s doi: 10.1146/annurev-phyto-080508-081748 Abstract Copyright c 2009 by Annual Reviews. The genus Verticillium encompasses phytopathogenic species that cause All rights reserved vascular wilts of plants. In this review, we focus on Verticillium dahliae, by University of California - Davis on 06/22/09. For personal use only. 0066-4286/09/0908/0039$20.00 placing emphasis on the controversy surrounding the elevation of a ∗Steven J. Klosterman and Zahi K. Atallah long-spored variant as a new species, recent advances in the analysis Annu. Rev. Phytopathol. 2009.47. Downloaded from arjournals.annualreviews.org contributed equally to this review and are to be of compatible and incompatible interactions, highlighted by the use of considered joint senior authors. strains expressing fluorescent proteins, and the genetic diversity among Verticillium spp. A synthesis of the approaches to explore genetic diver- sity, gene flow, and the potential for cryptic recombination is provided. Control of Verticillium wilt has relied on a panoply of chemical and nonchemical strategies, but is beset with environmental or site-specific efficacy problems. Host resistance remains the most logical choice, but is unavailable in most crops. The genetic basis of resistance to Verticillium wilt is unknown in most crops, as are the subcellular signaling mech- anisms associated with Ve-mediated, race-specific resistance. Increased understanding in each of these areas promises to facilitate management of Verticillium wilts across a broad range of crops. 39 ANRV384-PY47-03 ARI 12 April 2009 14:58 INTRODUCTION genus. Verticillium spp. have no described sexual stage. The genus Verticillium encompasses a cos- Of the four remaining species in the genus, mopolitan group of ascomycete fungi, includ- is the suggested type species of the ing several phytopathogenic species that cause V. dahliae genus (56) and also the more ubiquitous mem- vascular wilts of plants. The two most notorious ber of the genus. It is the primary causal agent species are V. dahliae and V. albo-atrum, which of Verticillium wilt in temperate and subtrop- cause billions of dollars in annual crop losses ical climates (17, 69, 109) and is the focus of worldwide (109). Yield losses in potato crops this review. has great genetic plasticity may reach 50%, but are more commonly in V.dahliae and is able to infect more than 200 plant species the range of 10–15% (114, 124, 125), whereas (1), including high-value annual and perennial in lettuce, losses can easily reach 100% (150). crop plants, as well as landscape, fruit, and or- The soil habitat of these species, the ability namental trees and shrubs (17, 109). The list of their survival structures to persist for years, of the hosts infected by is continually and their capacity to infect a bewildering V. dahliae expanding as disease outbreaks on new hosts array of hosts make them chronic economic are identified (16, 43). One example of host problems in crop production. Four other range expansion occurred in lettuce in coastal plant-pathogenic species historically associated California where entire crops have been lost with the genus Verticillium are V. tricorpus, to Verticillium wilt (150, 161). The population V. nigrescens, V. nubilum, and V. theobromae biology of V. dahliae remains the least under- (13). The recent assignment of V. nigrescens stood aspect of this ubiquitous phytopathogen. and V. theobromae to the genera Gibellulopsis Whereas strains of V. albo-atrum were divided and Musicillium, respectively (170), reduced into two groups based on their virulence and the number of plant pathogenic species in the aggressiveness to lucerne (a.k.a. alfalfa, Med- genus Verticillium to four. In addition, both the icago sativa), V. dahliae is divided based on veg- entomopathogenic V. lecanii and V. fungicola, etative compatibility into six groups (16, 71). a pathogen of agaric basidiomycetes, were Nevertheless, vegetative compatibility groups assigned to the genus Lecanillium (169). (VCGs) do not describe the overall genetic di- A variant of V. dahliae from horseradish, versity among strains, gene flow, or the poten- first described by Stark (13) produces mi- tial for recombination. They will, however, aid crosclerotia like V. dahliae but also conidia in the deployment of resistant cultivars, pre- significantly longer than the typical V. dahliae venting pathogen introductions and exploring strains, and thus was named V. dahliae var. the evolution of an agronomically important longisporum. This morphological difference and by University of California - Davis on 06/22/09. For personal use only. group of phytopathogens. other characteristics were considered sufficient The availability of cultivars tolerant to Ver- Annu. Rev. Phytopathol. 2009.47. Downloaded from arjournals.annualreviews.org to elevate such strains into a new species, ticillium wilt has reduced the disease to a minor V. longisporum (76). Erecting this new species nuisance in some crops such as cotton. When has been controversial and much effort over this type of resistance is compromised, Verti- the past decade has focused on resolving the cillium wilt is likely to re-emerge as a signif- taxonomic, phylogenetic, and evolutionary icant production problem for such crops. Sev- status of the long-spored crucifer strains. This eral potato cultivars with improved resistance to is the subject of the first part of this review. In are available, in addition to wild and the context of this review, the taxonomic status V. dahliae cultivated accessions of Solanum tuberosum and of Verticillium spp. is discussed relative to the hybrids of spp. (32, 70). On tomato, morphological and phylogenetic species con- Solanum resistance to race 1 was overcome within a few cepts, as described in numerous reviews (11, 86, years after its introduction (109). Race 2 steadily 153, 154), and does not include the biological supplanted race 1 in various regions of the world species concept because it does not apply to this because of the extensive use of race 1-resistant 40 Klosterman et al. ANRV384-PY47-03 ARI 12 April 2009 14:58 cultivars (41). Two races were also described in by V. dahliae, in contrast to V. albo-atrum, lettuce (65, 162), and germplasm with resistance which produces melanized hyphae but no mi- to race 1 was identified (65). However, there re- crosclerotia (13, 69, 109, 120), and (b) although mains no source of resistance to race 2 in either V. albo-atrum fails to grow in culture or wilt ◦ tomato or lettuce. More importantly, resistance plants at 30 C, V. dahliae grows and infects un- in most crops is either scarce or unavailable, hindered at 30◦C (69, 109, 120). Even though making Verticillium wilt a significant chronic this information existed in the literature, the problem in the production of these crops. Sub- taxonomic debate relative to the distinctive- stantial economic losses caused by Verticillium ness of these two species continued until the wilt are expected in the absence of fumigation late 1970s when V. dahliae was universally ac- for high-value crops such as strawberry, potato, cepted as a species separate from V. albo-atrum cotton, tomato, and ornamentals (44, 125). For (53, 109). Subsequent phylogenetic studies have the few crops in which resistance exists, the na- clearly identified V. albo-atrum and V. dahliae as ture of resistance has received little scrutiny. In distinct taxa (9, 13, 26, 117). this review, we also cover studies exploring the Based on host specificity, two clear subspe- V.dahliae-lettuce interaction at the microscopic cific groups in V. albo-atrum are recognized. level, providing a unique description of the in- Strains from alfalfa that cause severe symp- fection process from seedling to crop maturity. toms on this host and also on numerous other We further define host resistance in a new light hosts, and strains from hosts other than alfalfa based on studies using a fluorescently tagged that do not infect alfalfa or do so poorly (13, strain (163). 31). This grouping is strongly supported both by molecular markers (13) and VCG data (31, 61). A number of strains morphologically de- VERTICILLIUM TAXONOMY scribed as V.albo-atrum cluster separately based Nees von Essenbeck erected the genus Verti- on the internal transcribed spacer region (ITS) cillium in 1816 (69, 109) based on its unique, rDNA regions (99, 119), and thus were desig- branched conidiophores, which form whorls nated as V. albo-atrum Grp2. All other strains capped with flask-shaped and pointed phialides of V. albo-atrum are referred to as Grp1 (13). carrying terminal conidia. Although a few The resting structures and molecular mark- species of the genus Verticillium have been as- ers such as random amplification of polymor- sociated with ascomycetous teleomorphs (109, phic DNA (RAPDs) and ITS sequences all dis- 170), V.
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