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Chapter 20 : Dikaryons, Diploids, and Evolution

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Abstract:

The majority of the genetic inferences about dikaryons, diploids, and their interactions reviewed by John Raper in in 1966 remain essentially unchanged to the present. This review examines the immediate and long-term consequences of dikaryosis, with comparison to diploidy. In keeping with the theme of Raper’s book , it focuses on fungi with prolonged dikaryotic phases, mainly the Hymenomycetes. The four interrelated conclusions of this review are that (i) the known dynamics of nuclear migration and dikaryon formation suggest that mating in nature is asymmetric for male and female function, (ii) the transmissions of nuclear and mitochondrial genomes follow different rules, (iii) dikaryons produce recombinant genotypes without fruiting, and (iv) dikaryons and diploids carry different expectations for evolution. In addition to the genetic differences between diploids and dikaryons their different phenotypic responses may confer advantages or disadvantages depending on conditions. With an enhanced range of phenotypes, dikaryons might be more adept than diploids in coping with heterogeneous environments. It may be possible to make fair comparisons of dikaryotic cell populations with and without opportunities for nuclear-mitochondrial genomic conflict, somatic recombination, and diploidy and to compare the evolutionary outcomes.

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
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Figures

Image of Figure 20.1
Figure 20.1

Mating of haploid strains of . Two mates were inoculated alone on either side; the pairing appears in the middle. The dotted line indicates the region of initial contact between mycelia, where fusion of hyphae from the different mates occurs. Nuclear migration proceeded bidirectionally, with each mate functioning both as donor (male) and recipient of nuclei (female). While the nuclei migrate rapidly (i.e., on the order of 10-fold faster than the mycelial growth rate), the mitochondria do not and the final mated colony is mosaic for parental mtDNA types. Heteroplasmy for mtDNA is restricted to those cells resulting from fusion of hyphae of the two mates near the center (dashed line). The rhizomorphs (arrow) carry the mtDNA type from the area of the mated colony from which they arose. In , the initial dikaryon is established after nuclear migration becomes diploid, but the dynamics of nuclear migration and mitochondrial inheritance are otherwise typical of Homobasidiomycetes. Note that the colony morphology of the diploid is different from that of the mates; it has less aerial mycelium.

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
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Image of Figure 20.2
Figure 20.2

Unpublished spatial map of genetic individuals of in a mixed hardwood forest of Michigan. The rectangle (130 m in length) in the middle is a clear-cut site that was replanted with red pine and was the subject of intensive sampling of in individuals (75–77). The dots represent collection points, and the lines encircle collections with identical multilocus genotypes. Each individual has a unique mtDNA type, such that the samples of each individual have only a single mtDNA. No mosaicism for mtDNA that may have been present in the initial mating has been detected in these or any other individuals of from which multiple collections were made ( ).

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
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Image of Figure 20.3
Figure 20.3

Somatic recombination in an incompatible di-mon mating of , shown as a graphic representation of the data of Ellingboe ( ). The dikaryon genotype is at the top. The homokaryon is below the dikaryon. The two haploid genomes of the dikaryon are marked as light/dark gray. Linkage between markers is indicated by a solid line; breaks in lines indicate that markers are not linked. The nuclei fertilizing the monokaryon were genotyped by the method of Papazian. Recombinants include numerous examples of unlinked and linked loci, as would be expected in meiosis. Interestingly, specific-factor transfer was not observed in this di-mon mating; recombination was exclusively meiotic-like.

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
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Figure 20.4

Reciprocal and nonreciprocal genetic exchange between nuclei during long-term growth. Two of 25 SNP markers were detected by Southern hybridization of amplified DNA of marker loci with allele-specific oligonucleotide probes ( ). The original paired haploid nuclei carried different alleles for each of the 25 marker loci. Asterisks show reciprocal genetic exchange; circles show a nonreciprocal exchange.

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
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Image of Figure 20.5
Figure 20.5

Generalized basidiomycete life cycles. Diploid nuclei are in black; haploid nuclei are in gray. (a) Typical life cycle of most homobasidiomycetes with dikaryotic vegetative phases. (b) Typical life cycle of . No dikaryotic stage has been observed, and matings produce only diploids, which carry through the vegetative phase and into the basidia. (c) Typical life cycle of most species including , , and . A dikaryon forms in matings, but the duration of the dikaryon phase is variable. The nuclei fuse, leading to a persistent diploid. During fruiting there is a premeiotic reduction with dikaryons appearing in the prebasidial cells. Finally, the nuclei of the dikaryon fuse to form a diploid that immediately undergoes meiosis. – strains of form dikaryons that become diploid as in panel c; the events during fruiting and up to meiosis have not been characterized for – strains. Modified with the permission of Kari Korhonen, who created the original version (see reference ).

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
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Image of Figure 20.6
Figure 20.6

Genetic exchange in diploids and dikaryons affecting two loci of unknown linkage relationship. Both reciprocal and nonreciprocal exchanges produce new combinations of alleles within the nuclei of the dikaryon, but not in the diploid.

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
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Tables

Generic image for table
Table 20.1

Classification of di-mon matings

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
Generic image for table
Table 20.2

Genotyping nuclei in incompatible di-mon matings of the form ( + ) × ; Quintinilha’s test ( )

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20
Generic image for table
Table 20.3

Genotyping nuclei in incompatible di-mon matings of the form ( + ) × ; Papazian’s test ( )

Citation: Anderson J, Kohn L. 2007. Dikaryons, Diploids, and Evolution, p 333-348. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch20

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