Parasexual cycle

The parasexual cycle, a process restricted to fungi and single-celled organisms, is a nonsexual mechanism of parasexuality for transferring genetic material without meiosis or the development of sexual structures.^[1] It was first described by Italian geneticist Guido Pontecorvo in 1956 during studies on Aspergillus nidulans (also called Emericella nidulans when referring to its sexual form, or teleomorph). A parasexual cycle is initiated by the fusion of hyphae (anastomosis) during which nuclei and other cytoplasmic components occupy the same cell (heterokaryosis and plasmogamy). Fusion of the unlike nuclei in the cell of the heterokaryon results in formation of a diploid nucleus (karyogamy), which is believed to be unstable and can produce segregants by recombination involving mitotic crossing-over and haploidization. Mitotic crossing-over can lead to the exchange of genes on chromosomes; while haploidization probably involves mitotic nondisjunctions which randomly reassort the chromosomes and result in the production of aneuploid and haploid cells. Like a sexual cycle, parasexuality gives the species the opportunity to recombine the genome and produce new genotypes in their offspring. Unlike a sexual cycle, the process lacks coordination and is exclusively mitotic.

The parasexual cycle resembles sexual reproduction. In both cases, unlike hyphae (or modifications thereof) may fuse (plasmogamy) and their nuclei will occupy the same cell. The unlike nuclei fuse (karyogamy) to form a diploid (zygote) nucleus. In contrast to the sexual cycle, in the parasexual cycle recombination takes place during mitosis followed by haploidization (but without meiosis). The recombined haploid nuclei appear among vegetative cells, which differ genetically from those of the parent mycelium.

Both heterokaryosis and the parasexual cycle are very important for those fungi that have no sexual reproduction. Those cycles provide for somatic variation in the vegetative phase of their life cycles. This is also true for fungi where the sexual phase is present, although in this case, additional and significant variation is incorporated through the sexual reproduction.

Stages

Diploidization

Occasionally, two haploid nuclei fuse to form a diploid nucleus—with two homologous copies of each chromosome. The mechanism is largely unknown, and it seems to be a relatively rare event, but once a diploid nucleus has been formed it can be very stable and divide to form further diploid nuclei, along with the normal haploid nuclei. Thus the heterokaryon consists of a mixture of the two original haploid nuclear types as well as diploid fusion nuclei.^[2]

Mitotic chiasma formation

Chiasma formation is common in meiosis, where two homologous chromosomes break and rejoin, leading to chromosomes that are hybrids of the parental types. It can also occur during mitosis but at a much lower frequency because the chromosomes do not pair in a regular arrangement. Nevertheless, the result will be the same when it does occur—the recombination of genes.^[2]

Haploidization

Occasionally, nondisjunction of chromosomes occurs during division of a diploid nucleus, so that one of the daughter nuclei has one chromosome too many (2n+1) and the other has one chromosome too few (2n–1). Such nuclei with incomplete multiples of the haploid number are termed aneuploid, as they do not have even chromosome number sets such as n or 2n. They tend to be unstable and to lose further chromosomes during subsequent mitotic divisions, until the 2n+1 and 2n-1 nuclei progressively revert to n. Consistent with this, in E. nidulans (where normally, n=8) nuclei have been found with 17 (2n+1), 16 (2n), 15 (2n–1), 12, 11, 10, and 9 chromosomes.^[2]

Each of these events is relatively rare, and they do not constitute a regular cycle like the sexual cycle. But the outcome would be similar. Once a diploid nucleus has formed by fusion of two haploid nuclei from different parents, the parental genes can potentially recombine. And, the chromosomes that are lost from an aneuploid nucleus during its reversion to a euploid could be a mixture of those in the parental strain.^[2]

Organisms

The potential to undergo a parasexual cycle under laboratory conditions has been demonstrated in many species of filamentous fungi, including Fusarium monoliforme,^[3] Penicillium roqueforti^[4] (used in making blue cheeses^[5]), Verticillium dahliae,^[6][7] Verticillium alboatrum,^[8] Pseudocercosporella herpotrichoides,^[9] Ustilago scabiosae,^[10] Magnaporthe grisea,^[11] Cladosporium fulvum,^[12][13] and the human pathogens Candida albicans^[14] and Candida tropicalis.^[15]

Candida species

A study of the evolution of sexual reproduction in six Candida species concluded that there were recent losses in components of the major meiotic crossover-formation pathway, but retention of a minor pathway.^[16] It was suggested that if Candida species undergo meiosis it is with reduced machinery, or different machinery, and also that unrecognized meiotic cycles may exist in many species.^[16]

Significance

Parasexuality has become a useful tool for industrial mycologists to produce strains with desired combinations of properties. Its significance in nature is largely unknown and will depend on the frequency of heterokaryosis, determined by cytoplasmic incompatibility barriers and it is also useful in rDNA technology.^[2]

References

1. Alexopolous (1996), et al., pp. 196–97.
2. Deacon J. (2005). Fungal Biology. Cambridge, MA: Blackwell Publishers. pp. 167–68. ISBN 1-4051-3066-0.
3. Sidhu GS. (1983). "Sexual and parasexual variability in soil fungi with special reference to Fusarium moniliforme". Phytopathology. 73 (6): 952–55. doi:10.1094/phyto-73-952.
4. Durand N, Reymond P, Fevre M (1992). "Transmission and modification of transformation markers during an induced parasexual cycle in Penicillium roqueforti". Current Genetics. 21 (4–5): 377–83. doi:10.1007/bf00351698. S2CID 30871714.
5. Alexopolous (1996), et al., p. 12.
6. Pulhalla JE, Mayfield JE (1974). "The mechanism of heterokaryotic growth in Verticillium dahliae". Genetics. 76 (3): 411–422. PMC 1213075. PMID 17248647.
7. O'Garro LW, Clarkson JM (1992). "Variation for pathogenicity on tomato among parasexual recombinants of Verticillium dahliae". Plant Pathology. 41 (2): 141–47. doi:10.1111/j.1365-3059.1992.tb02331.x.
8. Hastie AC. (1964). "The parasexual cycle in Verticillium albo-atrum". Genetics Research. 5 (2): 305–15. doi:10.1017/s0016672300001245.
9. Hocart MJ, Lucas JA, and Peberdy JF. "Parasexual recombination between W and R pathotypes of Pseudocercosporella herpotrichoides through protoplast fusion." Mycological Research. 1993 August;97(8):977-983.
10. Garber ED, Ruddat M (1992). "The parasexual cycle in Ustilago scabiosae (Ustilaginales)". International Journal of Plant Sciences. 153: 98–101. doi:10.1086/297010.
11. Zeigler RS, Scott RP, Leung H, Bordeos AA, Kumar J, Nelson RJ (1997). "Evidence of parasexual exchange of DNA in the rice blast fungus challenges its exclusive clonality". Phytopathology. 87 (3): 284–94. doi:10.1094/phyto.1997.87.3.284. PMID 18945171.
12. Higgins VJ, Miao V, Hollands J (1987). "The use of benomyl and cycloheximide resistance markers in studies of race development by the leaf mold pathogen Cladosporium fulvum". Canadian Journal of Plant Pathology. 9: 14–19. doi:10.1080/07060668709501905.
13. Arnaru J, Oliver RP (1993). "Inheritance and alteration of transformed DNA during an induced parasexual cycle in the imperfect fungus Cladosporium fulvum". Current Genetics. 23 (5–6): 508–11. doi:10.1007/bf00312643. PMID 8319310. S2CID 25780981.
14. Bennett RJ and Johnson AD. "Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains." EMBO J. 2003 May 15;22(10):2505-15.
15. Seervai RNH, Knox SKJ, Hirakawa MK, Porman AM, and Bennett RJ. "Parasexuality and Ploidy Change in Candida tropicalis." Eukaryotic Cell. 2013 Dec; 12(12): 1629–1640.
16. Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA, et al. (June 2009). “Evolution of pathogenicity and sexual reproduction in eight Candida genomes”. Nature. 459 (7247): 657–662. Bibcode:2009Natur.459..657B. doi:10.1038/nature08064. PMC 2834264. PMID 19465905

Cited text

• Alexopoulos CJ, Mims CW, Blackwell M (1996). Introductory Mycology. John Wiley and Sons. pp. 196–97. ISBN 0-471-52229-5.