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United States Department of Agriculture

Agricultural Research Service

Research Project: SUSTAINABLE VINEYARD PRODUCTION SYSTEMS

Location: Crops Pathology and Genetics Research

Title: Evidence of natural hybridization among homothallic members of the basidiomycete Armillaria mellea

Authors
item Baumgartner, Kendra
item Baker, Bethany -
item Korhonen, Kari -
item Zhao, Jun -
item Hughes, Karen -
item Bruhn, Johann -
item Bowman, Tiffany -
item Bergemann, Sarah -

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: March 30, 2012
Publication Date: April 11, 2012
Repository URL: http://www.sciencedirect.com/science/article/pii/S1878614612000669
Citation: Baumgartner, K., Baker, B.R., Korhonen, K., Zhao, J., Hughes, K., Bruhn, J., Bowman, T.S., Bergemann, S.E. 2012. Evidence of natural hybridization among homothallic members of the basidiomycete Armillaria mellea. Fungal Genetics and Biology. 116:677-691.

Interpretive Summary: The root-pathogenic fungus Armillaria mellea has a typical, sexual reproductive mode (‘heterothallism’) across much of its geographic range. In three disjunct locales (Africa, China, Japan) populations are found to exhibit a different reproductive mode (‘homothallism’). A spore from the mushroom of a heterothallic strain must mate with another spore, in order to reproduce (i.e., to form a mushroom). In contrast, the spores of a homothallic strain do not need to mate in order to reproduce, and this characteristic could allow homothallic strains to spread more easily among crop plants. In order to determine the origins of homothallism in A. mellea, we constructed gene trees and mutational networks for partial sequences of protein-coding genes [nuclear genes: actin (ACTIN), elongation factor subunit 1-alpha (EFA), glyceraldehyde 3-phosphate dehydrogenase (GPD), second largest subunit of RNA polymerase (RPB2); mitochondrial gene: ATP synthase subunit 6 (ATP6) ], from a collection of 47 heterothallic isolates from China, Europe, and North America, and 14 homothallic isolates from Africa, China, and Japan. The genetic relatedness of CBS G and heterothallic isolates from China suggests that there is a common ancestor in China for these populations. Homothallic isolates shared ancestry with heterothallic isolates from China, Europe, or both, depending on the gene analyzed. Therefore, it appears that homothallic populations are hybrids of heterothallic populations from Europe and China.

Technical Abstract: Populations of Armillaria mellea (Basidiomycota, Agaricales, Physalacriaceae) across much of its geographic range are heterothallic; homothallic populations are reported only from Africa (A. mellea ssp. africana), China [China Biological Species (CBS) G], and Japan (A. mellea ssp. nipponica). Monosporous isolates of heterothallic A. mellea are haploid, and their mating behavior is consistent with that of two different alleles at two mating-type loci (heteroallelism) for a successful mating. In contrast, monosporous isolates of homothallic A. mellea, which are the equivalent of diploid zygotes, bypass the haploid mycelial phase by undergoing karyogamy in the basidium and then packaging diploid nuclei into single spores (homoheteromixis). In order to determine the origins of homothallism in A. mellea, we constructed gene trees and mutational networks for partial sequences of protein-coding genes [nuclear genes: actin (ACTIN), elongation factor subunit 1-alpha (EFA), glyceraldehyde 3-phosphate dehydrogenase (GPD), second largest subunit of RNA polymerase (RPB2); mitochondrial gene: ATP synthase subunit 6 (ATP6) ], from a collection of 47 heterothallic isolates from China, Europe, and North America, and 14 homothallic isolates from Africa, China, and Japan. The clustering of nuclear and mitochondrial haplotypes representing CBS G and heterothallic isolates from China suggests that there is a common ancestor in China for these A. mellea populations, although it is not possible to determine which reproductive mode is ancestral. Introgression of the European haplotype into all three homothallic populations was a pattern unique to phylogenetic analysis of ATP6. In phylogenetic analyses of the nuclear genes, A. mellea ssp. africana and A. mellea ssp. nipponica grouped with heterothallic isolates from Europe and/or Chinese isolates (both CBS G and heterothallic isolates). Such discordance between ATP6 and the nuclear genes, coupled with reticulate patterns in the mutational networks of the nuclear genes, suggest that intra-lineage hybridization explains this intraspecific genetic variation in homothallic A. mellea.

Last Modified: 8/1/2014
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