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The Nuclear Reproductive Cycle in the Myxomycetes: a Review

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The Nuclear Reproductive Cycle in the Myxomycetes: a Review Mycosphere Doi 10.5943/mycosphere/4/2/6 The nuclear reproductive cycle in the myxomycetes: a review Clark J1 and Haskins EF2 1Department of Biology, University of Kentucky, Lexington, Kentucky 40506 – [email protected] 2Department of Biology, University of Washington, Seattle, Washington 98195 – [email protected] Clark J, Haskins EF 2013 – The nuclear reproductive cycle in the myxomycetes: a review. Mycosphere 4(2), 233–248, Doi 10.5943/mycosphere/4/2/6 Our understanding of the taxonomy, ecology and population biology of myxomycetes has been enhanced by investigations of the nuclear reproductive cycle of taxa in this group. These studies have involved light microscopy, electron microscopy, DNA cytophotometric reports and genetic investigations. Heterothallism with its associated life cycle events of syngamy and meiosis is extensively reviewed as revealed by light microscopy, genetics and DNA spectrophotometric analysis of nuclear ploidy levels. Non-heterothallism, i.e., homothallism and apogamy, specifically automixis and its genetical and evolutionary significance is discussed. Nuclear division, chromosomal number and polyploidy in the myxomycetes is also detailed. Key words – apogamy – automixis – heterothallism – homothallism – myxomycetes – nuclear- cycle – polyploidy Article Information Received 11 January 2013 Accepted 30 January 2013 Published online 25 March 2013 Corresponding author: Jim Clark – [email protected] Introduction and can form large populations; these An understanding of the nuclear amoeboflagellates then form multi-nucleate reproductive cycle, and its variations, can aid vegetative plasmodia which give rise to and inform our understanding of the taxonomy, sporangia to complete the cycle by producing ecology and population biology of myxo- spores. However, while the sequence of stages mycetes. Thus considerable effort has been in the reproductive cycle is consistent from one expended in the study of the occurrence and species and isolate to the next, the nuclear location of these nuclear cycle events. While cycle can display considerable variability; that several excellent reviews (Gray & Alexopoulos can be divided into two major categories: 1968, Collins 1979, 1981) have covered parts heterothallism and non-heterothallism (see of this area, they are somewhat limited in review by Clark & Haskins 2010). In the availability and enough new information has heterothallic group, the amoeboflagellates accumulated to warrant an updated review. possess mating types and have a haploid- In the myxomycetes, the reproductive diploid sexual reproductive cycle, whereas the pattern set out by de Bary (1858) is followed non-heterothallic group is not known to by all known species: small generally wind- possess mating types and thus may be either borne spores germinate to release uninucleate sexual (homothallic) or nonsexual (apogamic). amoeboflagellate cells, which are vegetative While a nonsexual organism would not have a 233 Mycosphere Doi 10.5943/mycosphere/4/2/6 nuclear cycle since there would be no change Clastoderma debaryanum: plasmogamy of in ploidy during the reproductive cycle, the paired swarm cells (McManus 1961). occurrence of a haploid/diploid nuclear cycle in Comatricha nigra: a single pre-cleavage a non-heterothallic isolate would indicate that division (Lister 1893); meiosis I & II in it is homothallic. spores (von Stosch 1937). A list of reproductive nuclear cycle Comatricha typhoides: syngamy of paired reports is given in Table I. This list is divided swarm cells (Ross 1957); pre-cleavage into three groups: group A studies where the meiosis I & II (Wilson & Ross 1955). heterothallic/non-heterothallic nature of the Diachea leucopodia: syngamy of paired material was unknown; group B studies where swarm cells (Ross 1957). the isolates were known heterothallics; and Dictydiaethalium plumbeum: syngamy of group C studies where the isolates were known paired swarm cells (Ross 1957). non-heterothallics. The A group, which consist Dictydium cancellatum: no sporangial division mainly of earlier studies, displays rather (Jahn 1901); syngamy of paired swarm variable results and is probably of limited value cells and pre-cleavage meiosis I & II since the lack of background information (Ross 1961). makes it difficult to evaluate the validity and Didymium clavus: meiosis I & II in spores meaning of these results. (Dangeard 1947). Didymium difforme: plasmogamy of multiple Table 1 Reproductive nuclear cycle reports myxamoebae (Cienkowski 1863a, b); plasmogamy of multiple myxamoebae All names according to Martin & Alexopoulos and karyogamy in plasmodium just (1968) prior to sporulation (Skupienski 1926a, b); plasmogamy of paired A. Studies where only cytological swarm cells (Cayley 1929). information was available Didymium iridis (includes all D. nigripes): Arcyria cinerea: karyogamy in plasmodium, syngamy of paired myxamoebae with and nuclear fusion with meiosis I & II pre-cleavage meiosis I & II (Cadman in spores Kranzlin (1907); synapti- 1931); plasmogamy of paired nemal complexes in young spores myxamoebae and karyogamy in (Aldrich & Mims 1970). plasmodium just prior to sporulation Arcyria incarnata: a single pre-cleavage (Schünemann 1930). division (Lister 1893); synaptinemal Didymium melanospermum: a single pre- complexes in young spores (Aldrich & cleavage division (Harper 1914). Mims 1970). Didymium squamulosum: syngamy of paired Badhamia utricularis: a single pre-cleavage myxamoebae (Ross 1957). division (Lister 1893); a single meiotic Enteridium rozeanum: syngamy of paired pre-cleavage division (Jahn 1933). swarm cells (Ross 1957). Ceratiomyxa fruiticulosa: plasmogamy of Enteridium sp. (Reticularia): a single pre- swarm cells and karogamy in plasmodia cleavage division (Harper 1914). with a single meiotic pre-cleavage Fuligo septica: a single pre-cleavage division division (Jahn 1908); multiple swarm (Harper 1914, Rosen 1893); syngamy cell plasmogamy and plasmodial of paired swarm cells with pre-cleavage karyogamy with meiosis I & II in meiosis I & II (Ross 1961). spores (Gilbert 1935); meiosis I & II in Hemitrichia stipitata: synaptinemal complexes spores (Olive 1907); plasmogamy of in young spores (Aldrich & Mims paired swarm cells (McManus 1958); 1970). meiosis I & II in spores (Wilson & Lamproderma arcyriodes: syngamy of paired Ross 1955); syngamy of swarm cells swarm cells with pre-cleavage meiosis I with meiosis I & II in spores (Sansome & II (Ross 1960). & Sansome 1961, Sansome & Dixon Lamproderma arcyrionema: pre-cleavage 1965). meiosis I & II (Wilson & Ross 1955). 234 Mycosphere Doi 10.5943/mycosphere/4/2/6 Lycogala epidendrum: syngamy of paired Stemonitis flavogenita: plasmogamy of swarm cells (Ross 1957); a single pre- myxamoebae and or swarm cells cleavage division (Harper 1914); pre- (Koevenig 1961, 1964). cleavage meiosis I & II (Wilson & Ross Stemonitis fusca: plasmogamy between a 1955). myxamoeba and a swarm cell Lycogala exiguum: a single pre-cleavage (McManus 1961, Benedict 1962); a division (Conrad 1910). single pre-cleavage division (Bisby Metatrichia vesparium (Hemitrichia 1914); pre-cleavage meiosis I & II vesparium): syngamy of paired swarm (Koevenig 1964); syngamy of paired cells (Ross 1957); pre-cleavage swarm cells (Ross 1957). meiosis I & II (Wilson & Ross 1955). Stemonitis herbatica: syngamy of paired Mucilago crustacean: pre-cleavage meiosis I & swarm cells (Ross 1957); synaptinemal II (Schure 1949). complexes in young spores (Aldrich & Perichaena vermicularis: pre-cleavage meiosis Mims 1970). I & II or in spores depending upon Stemonitis pallida: pre-cleavage meiosis I & II sporulation conditions (Ross 1967b). (Wilson & Ross 1955). Physarella oblonga: a single pre-cleavage Stemonitis nigrescens: syngamy of paired division (Bisby 1914); syngamy of swarm cells (Ross 1957). paired myxamoebae with pre-cleavage Trichia botrytis (fragilis): a single pre-cleavage meiosis I & II (Ross 1961). division (Lister 1893). Physarum bogoriense: synaptinemal com- Trichia persimilis: nuclear fusion in plexes in young spores (Aldrich & sporangium with meiosis I & II at spore Mims 1970). germination (Kranzlin 1907); syngamy Physarum cinereum: synaptinemal complexes of paired swarm cells (Ross 1957); pre- in young spores (Aldrich & Mims cleavage meiosis I & II (Wilson & Ross 1970). 1955). Physarum didermoides: syngamy of paired Trichia decipiens (fallax): a single pre- myxamoebae with one possible pre- cleavage division (Strasburger 1884); cleavage meiotic division (Jahn 1911); nuclear fusion in sporangium with one pre-cleavage division (Schure meiosis I & II at spore germination 1949). (Kranzlin 1907); a single pre cleavage Physarum gyrosum: syngamy of myxamoebae division (Lister 1893). and or swarm cells with pre-cleavage Trichia varia: a single pre-cleavage division division figures (Koevenig 1964). (Jahn 1933). Physarum leucophaeum: a single pre-cleavage Tubifera ferruginosa: synaptinemal complexes division (Lister 1893). in young spores (Aldrich & Mims Physarum oblatum: syngamy of paired 1970). myxamoebae cells (Ross 1957). Tubifera microsperma: pre-cleavage meiosis I Physarum polycephalum: syngamy of swarm & II (Ross 1961). cells with a single pre-cleavage division (Howard 1931); a single pre- B. Studies involving known heterothallic cleavage division (Dalleux 1940); isolates syngamy of swarm cells with pre- Didymium iridis (including all D. nigripes): cleavage meiosis I & II (Ross 1961). syngamy of paired swarm cells with Physarum psittacinum: karyogamy in meiosis I & II
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