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Biology, Epidemiology, and Control of Heterobasidion Species Worldwide

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Biology, Epidemiology, and Control of Heterobasidion Species Worldwide PY51CH03-Gabelotto ARI 10 July 2013 8:2 Biology, Epidemiology, and Control of Heterobasidion Species Worldwide Matteo Garbelotto1,∗ and Paolo Gonthier2 1Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720; email: [email protected] 2Department of Agricultural, Forest, and Food Sciences, University of Torino, I-10095, Grugliasco, Italy; email: [email protected] Annu. Rev. Phytopathol. 2013. 51:39–59 Keywords First published online as a Review in Advance on biological control, forest trees, intersterility, management, root rot, May 1, 2013 speciation The Annual Review of Phytopathology is online at phyto.annualreviews.org Abstract This article’s doi: Heterobasidion annosum sensu lato is a species complex comprising five 10.1146/annurev-phyto-082712-102225 species that are widely distributed in coniferous forests of the Northern by University of California - Berkeley on 09/17/13. For personal use only. Copyright c 2013 by Annual Reviews. Hemisphere and are each characterized by a distinct host preference. All rights reserved Annu. Rev. Phytopathol. 2013.51:39-59. Downloaded from www.annualreviews.org More than 1,700 papers have been published on these fungi in the ∗ Corresponding author past four decades, making them perhaps the most widely studied forest fungi. Heterobasidion species are at different levels on the saprotroph- necrotroph gradient, and the same individual can switch from one mode to the other. This offers a unique opportunity to study how genomic structure, gene expression, and genetic trade-offs may all interact with environmental factors to determine the life mode of the organism. The abilities of Heterobasidion spp. to infect stumps as saprotrophs and to spread to neighboring trees as pathogens have resulted in significant damages to timber production in managed forests. This review focuses on the current knowledge of the biology, ecology, evolution, and man- agement of these species and is based on classical and modern studies. 39 PY51CH03-Gabelotto ARI 10 July 2013 8:2 INTRODUCTION the other. This offers a unique opportunity to study how genomic structure, gene expression, The genus Heterobasidion (Basidiomycota, and genetic trade-offs may all interact with en- Russulales, Bondarzewiaceae) included, until vironmental factors to determine the life mode recently, five taxonomic species: Heterobasidion of the organism at any given time. Milestone annosum (Fr.) Bref., Heterobasidion araucariae traditional genetic studies have been published P.K. Buchanan, Heterobasidion insulare (Murrill) (11, 12, 50, 51, 59, 60, 111, 112) that elucidate Ryvarden, Heterobasidion pahangense Corner, patterns and the heritability of genes involved and Heterobasidion rutilantiforme (Murrill) in vegetative compatibility, mating, dikaryosis, Stalpers. The number of species has increased and intersterility between species, providing because both H. annosum and H. insulare have a solid foundation for an in-depth analysis been reported to be species complexes (15, 16, using genomic and transcriptomic approaches. 84, 90). Although most Heterobasidion species Quantitative analyses of traits regulating viru- are strict saprotrophs or display uncertain lence and intersterility provide a roadmap for pathogenicity (15, 90), the H. annosum species the search of the loci that affect these important complex, hereafter referred to as H. anno- traits, and early molecular work is already avail- sum sensu lato (s.l.), comprises necrotrophic able that describes genes interacting between pathogens regarded as the most destructive host and pathogen during the early stages of disease agents of conifers. infection. Finally, the significant amount of In the past 40 years, H. annosum s.l. has been research aimed at understanding the impact the object of more than 1,700 scientific pa- that this group of organisms has on production pers, which makes it one of the most intensively forestry and, since 2004, the understanding that studied forest fungi. The complete genome se- two sister allopatric species are now sympatric quence of the fungus is now available, mak- because of a human-linked intercontinental ing H. annosum s.l. the first sequenced plant movement of one of the two provide the pathogenic homobasidiomycete (94). Further- scientific community with the opportunity to more, it is one of the few examples of a forest understand in-depth the ecological similarities pathogen that can be and has been controlled and differences among species within the in managed forests. complex. The biology, epidemiology, impact, and control of H. annosum s.l. were the objects of a book (144), whereas more recent re- TAXONOMY AND views emphasize either the biochemistry and DISTRIBUTION OF THE molecular aspects of pathogen virulence (3) or COMPLEX HETEROBASIDION ANNOSUM: BIOLOGICAL, by University of California - Berkeley on 09/17/13. For personal use only. epidemiology and disease management (46). This review attempts to present those high- PHYLOGENETIC, OR Annu. Rev. Phytopathol. 2013.51:39-59. Downloaded from www.annualreviews.org lights that make Heterobasidion an ideal model TRADITIONAL SPECIES? system to study basic and applied aspects of H. annosum s.l. is widely distributed in conif- the biology, ecology, and evolution of a forest erous forests of the Northern Hemisphere, pathogen. Not only does the complex include especially in Europe, North America, Russia, species that have diverged at different times, China, and Japan (17, 18, 68, 72, 100, 146). but the model is enriched by a combination of H. annosum was long regarded as a single species allopatric and sympatric distributions of several until mating experiments among different indi- species, allowing study of the reinforcement viduals revealed the occurrence of intersterile of speciation processes and horizontal gene groups (ISGs) (7, 10, 67). Currently, three transfer. Not only does the complex include ISGs are recognized in Eurasia and two in species that are at different levels on the North America; all are now formally described saprotroph-necrotroph gradient, but the same as species. Eurasian groups were described as individual can often switch from one mode to H. annosum sensu stricto (s.s.), Heterobasidion 40 Garbelotto · Gonthier PY51CH03-Gabelotto ARI 10 July 2013 8:2 abietinum Niemela&Korhonen,and¨ Heteroba- become invasive by spreading in Italian stone sidion parviporum Niemela¨ & Korhonen (90), pine (Pinus pinea L.) stands (45). Therefore, the whereas North American groups were named current distribution area of H. irregulare also Heterobasidion irregulare (Underw.) Garbel. & includes an area of approximately 100 km along Otrosina and Heterobasidion occidentale Otrosina the Tyrrhenian coast west of Rome (20, 45). & Garbel. (100). Although defined on the basis The evolutionary history and biogeography of partial reproductive isolation and morphol- of species within H. annosum s.l. were recently ogy, which were further supported by phy- elucidated (19, 77). Speciation within the logenetic analyses performed with a range of species complex began approximately 60 mya markers (19, 52, 77, 98), these species are also (million years ago), which is well after the characterized by a distinct host preference. radiation of host genera. The pine-associated H. annosum s.s. mostly attacks pines (Pinus H. annosum s.s. and H. irregulare are sister spp.), especially Scots pine (Pinus sylvestris taxa and appear to share a common origin L.), but can be associated with several other in a Eurasian progenitor of all species within conifers and even some broad-leaved tree the complex. The last emerging species was species. H. parviporum is strictly associated H. abietinum, which arose 14–31 mya. Although with Norway spruce [Picea abies (L.) Karst.], H. annosum s.l. species are characterized by par- and H. abietinum is commonly associated tial interfertility in laboratory experiments and with silver fir (Abies alba Mill.) and other by overlapping ranges, interspecific hybrids species of the genus Abies. In North America, have rarely been reported and only between H. irregulare generally attacks pines, junipers the sympatric North American H. irregulare (Juniperus spp.), and incense cedar [Calocedrus and H. occidentale (34, 80). Notwithstanding the decurrens (Torr.) Florin], whereas H. occidentale difficulty of identifying hybrids or genotypes shows a broader host range and can be found characterized by an admixed genome, the lack on the genera Abies, Picea, Tsuga, Pseudotsuga, of significant divergence in internal transcribed and Sequoiadendron (Table 1). spacers (ITSs) among species (19, 52) and the The distribution of H. annosum s.l. species clear evidence of horizontal gene transfer (77) reflects that of their main host species indicate the species have had the opportunity (Figure 1). H. annosum s.s. is found all over to hybridize and exchange genes. In western Europe, except in the very northern regions, North America, this opportunity has recently and its distribution area extends east to the been fostered by the presence of pine or juniper Altai region in southern Siberia (3, 17, 68). stumps colonized by both species (34, 97), but H. parviporum occurs from the most northern it may have been facilitated in the past by the parts of Europe to the southern Alps and from presence of larch (Larix spp.), a host that may by University of California - Berkeley on 09/17/13. For personal use only. western Europe to China, Japan, and southern be infected by both fungal
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