BMC Evolutionary Biology | |
The scope for nuclear selection within Termitomyces fungi associated with fungus-growing termites is limited | |
Duur K Aanen2  Anton SM Sonnenberg1  Johan JP Baars1  Bertha Koopmanschap2  Tania Nobre3  | |
[1] Plant Research International – Mushrooms, Wageningen University and Research Centre, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands;Laboratory of Genetics, Wageningen University and Research Center, Droevendaalsesteeg 1, Radix West, Building 107, 6708 PB Wageningen, The Netherlands;Currently: ICAAM, University of Évora, Pólo da Mitra Apartado 94, 7002-554 Évora, Portugal | |
关键词: Mating system; Fungi; Mutualism; Social evolution; Levels of selection; Polyploid; Ploidy; Termitomyces; | |
Others : 855422 DOI : 10.1186/1471-2148-14-121 |
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received in 2014-03-04, accepted in 2014-05-29, 发布年份 2014 | |
【 摘 要 】
Background
We investigate the scope for selection at the level of nuclei within fungal individuals (mycelia) of the mutualistic Termitomyces cultivated by fungus-growing termites. Whereas in most basidiomycete fungi the number and kind of nuclei is strictly regulated to be two per cell, in Termitomyces mycelia the number of nuclei per cell is highly variable. We hypothesised that natural selection on these fungi not only occurs between mycelia, but also at the level of nuclei within the mycelium. We test this hypothesis using in vitro tests with five nuclear haplotypes of a Termitomyces species.
Results
First, we studied the transition from a mixture of five homokaryons (mycelia with identical nuclei) each with a different nuclear haplotype to heterokaryons (mycelia with genetically different nuclei). In vitro cultivation of this mixture for multiple asexual transfers led to the formation of multiple heterokaryotic mycelia, and a reduction of mycelial diversity over time. All heterokaryotic mycelia contained exactly two types of nucleus. The success of a heterokaryon during in vitro cultivation was mainly determined by spore production and to a lesser extent by mycelial growth rate. Second, heterokaryons invariably produced more spores than homokaryons implying that homokaryons will be outcompeted. Third, no homokaryotic ‘escapes’ from a heterokaryon via the formation of homokaryotic spores were found, despite extensive spore genotyping. Fourth, in contrast to most studied basidiomycete fungi, in Termitomyces sp. no nuclear migration occurs during mating, limiting the scope for nuclear competition within the mycelium.
Conclusions
Our experiments demonstrate that in this species of Termitomyces the scope for selection at the level of the nucleus within an established mycelium is limited. Although ‘mate choice’ of a particular nuclear haplotype is possible during mating, we infer that selection primarily occurs between mycelia with two types of nucleus (heterokaryons).
【 授权许可】
2014 Nobre et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Maynard SJ: Szathmary E: The Major Transitions in Evolution. Oxford: W.H. Freeman; 1995.
- [2]Taylor DR, Zeyl C, Cooke E: Conflicting levels of selection in the accumulation of mitochondrial defects in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2002, 99:3690-3694.
- [3]Aanen DK, Kuyper TW, Debets AJM, Hoekstra RF: The evolution of non-reciprocal nuclear exchange in mushrooms as a consequence of genomic conflict. P Roy Soc B - Biol Sci 2004, 271(1545):1235-1242.
- [4]Johnson RA, Thomas RJ, Wood TG, Swift MJ: The inoculation of the fungus comb in newly founded colonies of some species of the Macrotermitinae (Isoptera) from Nigeria. J Nat Hist 1981, 15:751-756.
- [5]Korb J, Aanen DK: The evolution of uniparental transmission of fungal symbionts in fungus-growing termites (Macrotermitinae). Behav Ecol Sociobiol 2003, 53:65-71.
- [6]Nobre T, Rouland Lefèvre C, Aanen DK: Comparative Biology of Fungus Cultivation in Termites and Ants. In Biology of Termites: a Modern Synthesis. Edited by Bignell DE, Roisin Y, Lo N. Netherlands: Springer; 2011:193-210.
- [7]Darlington J: Nutrition and evolution in fungus-growing termites. In Nourishment and evolution in insect societies. Edited by Hunt JH. Nalepa CA: Boulder, Westview Press; 1994:105-130.
- [8]Koné N, Dosso K, Konaté S, Kouadio J, Linsenmair K: Environmental and biological determinants of Termitomyces species seasonal fructification in central and southern Côte d’Ivoire. Insect Soc 2011, 58:371-382.
- [9]Aanen DK, de Fine Licht HH, Debets AJM, Kerstes NAG, Hoekstra RF, Boomsma JJ: High symbiont relatedness stabilizes mutualistic cooperation in fungus-growing termites. Science 2009, 326:1103-1106.
- [10]Leuthold RH, Badertscher S, Imboden H: The inoculation of newly formed fungus comb with Termitomyces in Macrotermes colonies (Isoptera, Macrotermitinae). Insect Soc 1989, 36:328-338.
- [11]Aanen DK, Boomsma JJ: Social-insect fungus farming. Curr Biol 2006, 16:R1014-R1016.
- [12]De Fine Licht HH, Boomsma JJ, Aanen DK: Presumptive horizontal symbiont transmission in the fungus-growing termite Macrotermes natalensis. Mol Ecol 2006, 15:3131-3138.
- [13]Roper M, Ellison C, Taylor JW, Glass NL: Nuclear and genome dynamics in multinucleate ascomycete fungi. Curr Biol 2011, 21:R786-R793.
- [14]James TY, Stenlid J, Olson A, Johannesson H: Evolutionary significance of imbalanced nuclear ratios within heterokaryons of the basidiomycete fungus Heterobasidion parviporum. Evolution 2008, 62:2279-2296.
- [15]De Fine Licht HH, Andersen A, Aanen DK: Termitomyces sp associated with the termite Macrotermes natalensis has a heterothallic mating system and multinucleate cells. Mycol Res 2005, 109:314-318.
- [16]Casselton LA, Olesnicky NS: Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol R 1998, 62:55-70.
- [17]Pittenger TH, Brawner TG: Genetic control of nuclear selection in Neurospora heterokaryons. Genetics 1961, 46:1645-1663.
- [18]Davis RH: Adaptation in pantothenate-requiring Neurospora. II. Nuclear competition during adaptation. Am J Bot 1960, 47:648-654.
- [19]Snider PJ: Genetic evidence for nuclear migration in basidiomycetes. Genetics 1962, 48:47-55.
- [20]Nieuwenhuis BPS, Aanen DK: Sexual selection in fungi. J Evol Biol 2012, 25:2397-2411.
- [21]Nieuwenhuis BPS, Debets AJM, Aanen DK: Sexual selection in mushroom-forming basidiomycetes. P Roy Soc B - Biol Sci 2011, 278:152-157.
- [22]Aanen DK, Ros V, De Fine Licht H, Mitchell J, De Beer ZW, Slippers B, Rouland LeFevre C, Boomsma JJ: Patterns of interaction specificity of fungus-growing termites and Termitomyces symbionts in South Africa. BMC Evol Biol 2007, 7:115-123.
- [23]Casselton LA, Challen M, Kües U, Fischer R: The Mating Type Genes of the Basidiomycetes. In Growth, Differentiation and Sexuality. Edited by Esser K. Berlin Heidelberg: Springer; 2006:357-374.
- [24]Aanen DK: As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi. Biol Lett 2006, 13:209-212.
- [25]Buller AHR: The biological significance of conjugate nuclei in Coprinus lagopus and other hymenomycetes. Nature 1931, 126:686-689.
- [26]Raper C, Raper J, Miller R: Genetic analysis of the life cycle of Agaricus bisporus. Mycologia 1972, 64:1088-1117.
- [27]Miller R: Evidence of sexuality in the cultivated mushroom, Agaricus bisporus. Mycologia 1971, 63:630-634.
- [28]James TY, Johansson SBK, Johannesson H: Trikaryon formation and nuclear selection in pairings between heterokaryons and homokaryons of the root rot pathogen Heterobasidion parviporum. Mycol Res 2009, 113:583-590.
- [29]Nobre T, Fernandes C, Boomsma JJ, Korb J, Aanen DK: Farming termites determine the genetic population structure of Termitomyces fungal symbionts. Mol Ecol 2011, 20:2023-2033.
- [30]Simchen G, Jinks JL: The determination of dikaryotic growth gate in the basidiomycete Schizophyllum commune: a biometrical analysis. Heredity 1964, 19:629-649.
- [31]Clark T, Anderson JB: Dikaryons of the basidiomycete fungus Schizophyllum commune: evolution in long-term culture. Genetics 2004, 167:1663-1675.
- [32]Hiscox J, Baldrian P, Rogers HJ, Boddy L: Changes in oxidative enzyme activity during interspecific mycelial interactions involving the white-rot fungus Trametes versicolor. Fungal Genet Biol 2010, 47:562-571.
- [33]Martin MM, Martin JS: Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: the role of acquired digestive enzymes. Science 1978, 199:1453-1455.
- [34]Nobre T, Aanen DK: Fungiculture or Termite Husbandry? (Special issue on Symbiosis: A Source of Evolutionary Innovation in Insects.). Insects 2012, 3:307-323.
- [35]Hansen EM, Stenlid J, Johansson M: Somatic incompatibility and nuclear reassortment in Heterobasidion annosum. Mycol Res 1993, 97:1223-1228.
- [36]Ramsdale M, Rayner ADM: Imbalanced nuclear ratios, postgermination mortality and phenotype-genotype relationships in allopatrically-derived heterokaryons of Heterobasidion annosum. New Phytol 1996, 133:303-319.
- [37]Hui C, Yamamoto H, Ohta T, Takeo K, Kitamoto Y: Nuclear selection in monokaryotic oidium formation from dikaryotic mycelia in a basidiomycete, Pholiota nameko. Mycoscience 1999, 40:199-203.
- [38]Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Froslev T, Rosendahl S, Boomsma JJ: The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci U S A 2002, 99:14887-14892.
- [39]Scott JJ, Kweskin M, Cooper M, Mueller UG: Polymorphic microsatellite markers for the symbiotic fungi cultivated by leafcutter ants (Attini, Formicidae). Mol Ecol Resour 2009, 9:1391-1394.
- [40]Pawlowska T, Taylor J: Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 2004, 427:733-737.
- [41]Hijri M, Sanders I: Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 2005, 433:160-163.
- [42]Lin K, Limpens E, Zhang Z, Ivanov S, Saunders DGO, Mu D, Pang E, Cao H, Cha H, Lin T, Zhou Q, Shang Y, Li Y, Sharma T, van Velzen R, de Ruijter R, Aanen DK, Win J, Kamoun S, Bisseling T, Geurts R, Huang S: Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet 2014, 10(1):e1004078.
- [43]Bendich AJ: Why do chloroplasts and mitochondria contain so many copies of their genome? Bioessays 1987, 6:279-282.
- [44]Bretagnolle F, Thompson J: Gametes with the stomatic chromosome number: mechanisms of their formation and role in the evolution of autopolypoid plants. New Phytol 1995, 129:1-22.
- [45]Sonnenberg AS, Wessels JG, van Griensven LJ: An efficient protoplasting/regeneration system for Agaricus bisporus and Agaricus bitorquis. Curr Microbiol 1988, 17:285-291.
- [46]Meixner B, Bresinsky A: Cytofluorometric determination of relative DNA content in nuclei of Coniophoraceae (Boletales) using DAPI. T Brit Mycol Soc 1988, 90:175-180.
- [47]Butt TM, Hoch HC, Staples RC, St. Leger RJ: Use of fluorochromes in the study of fungal cytology and differentiation. Exp Mycol 1989, 13:303-320.
- [48]Nobre T, Koopmanschap B, Baars JP, Sonnenberg ASM, Aanen D: Data from: The scope for nuclear selection within Termitomyces fungi associated with fungus-growing termites is limited. Dryad Digital Repositoryhttp://datadryad.org: webcite Dryad doi:10.5061/dryad.b28k2