Origins and inheritance of chromosome-length polymorphisms in the barley covered smut fungus, Ustilago hordei

Abstract

Numerous chromomsome-length polymorphisms (CLPs) associated with chromosome IV were detected in an inbred line of race 8 of Ustilago hordei (teliospore line 1279). Polymorphisms for chromosome IV were observed in the 1600-1900-kb range in approximately 8% of the haploid sporidia originating from this teliospore collection. A monosporidial strain, 1279Ca2, exhibited a new 1620-kb chromosome band and a concurrent loss of the 1950-kb chromosome IV. A ribosomal DNA probe from Armillaria mellea specifically hybridized to both the variant 1620-kb chromosome and to the 1950-kb rDNA chromosome IV in parental strains. Following digestion of chromosome IV with HinfI, the telomere fragments of the 1620-kb chromosome were similar to those of the 1950-kb chromosome IV, indicating that the 1620-kb chromosome arose following a deletion of approximately 330 kb from chromosome IV. The Hinf1 digest of chromosome IV, when probed with the rDNA probe, revealed that much of the rDNA of chromosome IV was lost in the 1279Ca2 line. rDNA sequences were coincidentally recorded in chromosomes I and II in the sister sporidial line, 1279Ca4. When the 1279Ca2 line was mated to other members within the same tetrad and inoculated onto susceptible barley, karyotypes of tetrads and random sporidia originating from the F1 progeny possessed variant chromosomes ranging in size from 1536 to 2110 kb. Among sporidia in 5 of the 12 ordered tetrads sampled, a 1:1 ratio of the 1950-kb parental chromosome IV to the variant chromosome was observed. Within these tetrads, the two polymorphic chromosomes were identical in size and larger than that of the original variant 1620-kb chromosome suggesting that a chromosome expansion, averaging 150 kb, had occurred. In 5 of the 12 tetrads, a 1:1:1:1 ratio representing the two original parents and two recombinant chromosomes was observed, suggesting that normal or unequal recombination had occurred during meiosis. In 2 of the 12 F1 progeny tetrads, the 1950-kb chromosome IVs were apparently eliminated. In karyotypes of these sporidial lines, we observed rDNA sequences in chromosomes I and III that were translocated from chromosome IV. Among 78 random sporidia in the F1 generation, duplication of the variant chromosome IV was observed in three strains. These results suggest that polymorphisms in the rDNA chromosome IV, which consist of chromosome expansion, translocation, and chromosome elimination or duplication, are common in the 1279 strain of U. hordei and its progeny, and that this variability appears to be associated with the tandem-repeat nature of the rDNA sequences.

Electrophoretic karyotype and gene mapping of the vascular wilt fungus Verticillium dahliae

“…The pol polyprotein probe, which appears to be part of an LTR retrotransposon (it displayed high sequence similarity with the Cg ret retrotransposon of Colletotrichum gloeosporioides [44]), was present on all chromosomes and possibly at multiple copies, since its hybridization intensity signal was comparable only to the signal produced by the nuclear rDNA gene complex. The latter, located exclusively onto chromosome VII can, therefore, be excluded from being an agent of chromosome polymorphism, due to its tandem‐repeat nature, as it has been suggested in fungi where copies of the repeat where found onto different chromosomes [45]. On the contrary, the LTR retrotransposon and its multi‐copy distribution throughout the genome of V. dahliae , may be an additional factor for karyotype polymorphism, since such elements are known to lead to chromosome expansion, translocation, elimination and duplication in other fungi [19,45].…”

“…The latter, located exclusively onto chromosome VII can, therefore, be excluded from being an agent of chromosome polymorphism, due to its tandem‐repeat nature, as it has been suggested in fungi where copies of the repeat where found onto different chromosomes [45]. On the contrary, the LTR retrotransposon and its multi‐copy distribution throughout the genome of V. dahliae , may be an additional factor for karyotype polymorphism, since such elements are known to lead to chromosome expansion, translocation, elimination and duplication in other fungi [19,45]. It would, therefore, be interesting to correlate the presence of this transposon with recombination events during the parasexual cycle or even with the karyotypic variation among isolates of the phylogenetically closely related phytopathogenic Verticillium species.…”

Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals

“…Previous characterization of the genome by electrophoretic karyotyping identiWed 15-19 chromosome-sized bands and a haploid genome size of approximately 20 Mb (McCluskey and Mills, 1990;Abdennadher and Mills, 2000). Chromosome IV was the most variable between strains and the variation (size range 1.6-1.9 Mb) was proposed to result from rearrangements within the rDNA cluster (Gaudet and Kiesling, 1991;McCluskey et al, 1994;Gaudet et al, 1998). The physical map described here represents an important resource for characterization of genomic features such as chromosome length polymorphism and for eventual completion of the genomic sequence.…”

The Ustilaginales as Plant Pests and Model Systems

“…Attempts to differentiate strains belonging to the different races by use of molecular techniques such as isozyme analysis (Hellmann and Christ, 1991) and electrophoretic karyotyping (McCluskey and Mills, 1990;McCluskey et al, 1994) have generated inconclusive results. Variability in rDNA among strains of U. hordei have been detected (Gaudet et al, 1998). More recently, the use of telomere-associated restriction fragment length polymorphism (RFLP) analysis in association with chromosomelength polymorphism detection has produced good results in identifying strains that form a direct lineage (Abdennadher et al, 2000).…”

“…Research on other members of the Ustilaginales has steadily increased, concentrating mostly on taxonomy, genetic variability, cultivar resistance, and PCR detection (Smith et al, 1996;Bonde et al, 1997;Gaudet et al, 1998;Akhter and Antonovics, 1999;McDonald et al, 1999;Willits and Sherwood, 1999;Xu et al, 1999;Abdennadher and Mills, 2000;Bakkeren et al, 2000;Laroche et al, 2000). However, the most studied member of the Ustilaginales is U. maydis.…”