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. 2005 Mar;169(3):1311-27.
doi: 10.1534/genetics.104.033167. Epub 2005 Jan 16.

Chromosome loss followed by duplication is the major mechanism of spontaneous mating-type locus homozygosis in Candida albicans

Wei Wu  1 , Claude Pujol, Shawn R Lockhart, David R Soll
Affiliations

Chromosome loss followed by duplication is the major mechanism of spontaneous mating-type locus homozygosis in Candida albicans

Wei Wu et al. Genetics. 2005 Mar.

Abstract

Candida albicans, which is diploid, possesses a single mating-type (MTL) locus on chromosome 5, which is normally heterozygous (a/alpha). To mate, C. albicans must undergo MTL homozygosis to a/a or alpha/alpha. Three possible mechanisms may be used in this process, mitotic recombination, gene conversion, or loss of one chromosome 5 homolog, followed by duplication of the retained homolog. To distinguish among these mechanisms, 16 spontaneous a/a and alpha/alpha derivatives were cloned from four natural a/alpha strains, P37037, P37039, P75063, and P34048, grown on nutrient agar. Eighteen polymorphic (heterozygous) markers were identified on chromosome 5, 6 to the left and 12 to the right of the MTL locus. These markers were then analyzed in MTL-homozygous derivatives of the four natural a/alpha strains to distinguish among the three mechanisms of homozygosis. An analysis of polymorphisms on chromosomes 1, 2, and R excluded meiosis as a mechanism of MTL homozygosis. The results demonstrate that while mitotic recombination was the mechanism for homozygosis in one offspring, loss of one chromosome 5 homolog followed by duplication of the retained homolog was the mechanism in the remaining 15 offspring, indicating that the latter mechanism is the most common in the spontaneous generation of MTL homozygotes in natural strains of C. albicans in culture.

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Figures

F<sc>igure</sc> 1.—
Figure 1.—
Models for the three possible mechanisms of mating-type locus (MTL) homozygosis in Candida albicans, mitotic recombination (A), gene conversion (B), and deletion of one homolog of chromosome 5 followed by duplication of the retained homolog (C). Hypothetical polymorphic alleles on the chromosome 5 homolog harboring MTLa (a) are represented as solid boxes and those on the chromosome 5 homolog harboring MTLα (α) are represented as open boxes. The centromere is represented as a solid ellipsoid. Dashed boxes represent outcome of homozygosis for each possible mechanism. The step in the line between the a and α homologs in A is the position of a crossover. The small curved arrow from α to a in B represents a gene conversion. The a homolog is deleted and the α homolog duplicates in C.
F<sc>igure</sc> 2.—
Figure 2.—
Development of a partial contig map for chromosome 5 and placement of the polymorphic genes and intergenic sequences used in this study in their respective contigs. (A) the placements of contigs with associated genes along chromosome 5 were interpreted from data obtained from the Stanford Genome Technology Center C. albicans sequencing project database (http://www-sequence.stanford.edu/group/candida/), the partial physical map posted by P. T. Magee and colleagues (http://alces.med.umn.edu/Candida.html; Forche et al. 2004) and Whiteway and colleagues (http://cbr-rbc.nrc-cnrc.gc.ca/biovis/candida/). An explanation of the logic behind the map is presented in results. The 5′-3′ orientations of the contigs are indicated by arrow direction. The positions of the putative centromere (Sanyal et al. 2004), the RPS locus, and the CARE2 locus are noted. (B) Tentative ordering of polymorphic genes and intergenic sequences along chromosome 5. Note that the orientation of the markers 1990C and 1990A could be either on the right or left of the centromere, but have been arbitrarily ordered as in the sequence of contig 19-10170 for simplicity. A change in orientation changes none of the interpretations or conclusions in this article. The distances between markers are arbitrary.
F<sc>igure</sc> 3.—
Figure 3.—
Southern blot analysis of MTLa1 and MTLα2 for three of the MTL-heterozygous strains and one MTL-homozygous derivative from each. Note that the intensity of MTLa1 and MTLα2 bands in the MTL-heterozygous strains is roughly half that of the derivative MTL-homozygous strain. Similar results were obtained for the remaining MTL-heterozygous strain and additional MTL-homozygous derivatives not shown.
F<sc>igure</sc> 4.—
Figure 4.—
MTL homozygosis in the a/α strain P37037 generating six MTL-homozygous derivatives occurred by either mitotic recombination along chromosome 5 in one case or by loss of one chromosome 5 homolog followed by duplication of the retained homolog in five cases. (A) Diagram of polymorphic sites along the homologs of chromosome 5 in the original a/α strain. The solid and open boxes represent gene and intergenic sequence polymorphisms. Diagrams of sites along the homologs of chromosome 5 are presented for the α/α-1 derivative (B); the α/α-2, α/α-3, α/α-4, and α/α-5 derivatives (C); and the a/a-1 derivative (D). The interpretive mechanisms of MTL homozygosis for the derivatives are mitotic recombination for α/α-1 and loss of one chromosome 5 homolog followed by duplication of the retained homolog for α/α-2, α/α-3, α/α-4, α/α-5, and a/a-1.
F<sc>igure</sc> 5.—
Figure 5.—
Southern blot hybridization analysis of four polymorphic genes positioned within a 30-kb region harboring the mating-type locus (MTL). The relative positions of the genes are shown in the schematic above the Southern blots. Restriction enzymes used to show the polymorphism for each gene are indicated to the right. The primers used to generate the open reading frame of each gene are presented in Table 1.
F<sc>igure</sc> 6.—
Figure 6.—
MTL homozygosis in the a/α strain P37039 generating an MTL-homozygous derivative occurred by loss of one chromosome 5 homolog followed by duplication of the retained homolog. (A) Diagram of polymorphic sites along the homologs of chromosome 5 in the original a/α strain. The solid and open boxes represent the gene and intergenic sequence polymorphisms. (B) Diagram of sites is presented for the α/α-1 derivative.
F<sc>igure</sc> 7.—
Figure 7.—
MTL homozygosis in the a/α strain P75063 generating two independent MTL-homozygous derivatives occurred by loss of one chromosome 5 homolog followed by duplication of the retained homolog. (A) Diagram of the polymorphic sites along the homologs of chromosome 5 in the original a/α strain. The solid and open boxes represent the gene and intergenic sequence polymorphisms. (B) Diagrams of the tested sites along the homologs of chromosome 5 are presented for the P75063 derivatives a/a-1 and a/a-2.
F<sc>igure</sc> 8.—
Figure 8.—
MTL homozygosis in the a/α strain P34048 generating seven MTL-homozygous derivatives occurred by loss of one chromosome 5 homolog followed by duplication of the retained homolog in all cases. (A) Diagram of polymorphic sites along the homologs of chromosome 5 in the original a/α strain. The solid and open boxes represent gene and intergenic sequence polymorphisms. Diagrams of sites along the homologs of chromosome 5 are presented for the α/α-1, α/α-2, α/α-3, α/α-4, α/α-5, and α/α-6 derivatives (B) and the a/a-1 derivative (C).
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