Nuclear and Genome Dynamics in Multinucleate Ascomycete Fungi

Roper, Marcus; Ellison, Chris; Taylor, John W.; Glass, N. Louise

doi:10.1016/j.cub.2011.06.042

Cited by 120 publications

(98 citation statements)

References 86 publications

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“…These observations explain the observed high frequency of nuclear bypassing for daughter nuclei (Alberti-Segui et al, 2001;Gladfelter et al, 2006). An efficient mechanism for nuclear bypassing is of advantage in multinucleated hyphae because it allows nuclear mixing (Roper et al, 2011). Without nuclear mixing a detrimental mutation for example in the leading nucleus of a hypha, will be inherited to all daughter nuclei in this region thereby impairing future growth.…”

Section: Discussionmentioning

confidence: 99%

“…In multinucleated filamentous fungi the cMT cytoskeleton has evolved into a complex system with the remarkable ability to control the migration and distribution of multiple nuclei in the same cell. The biological advantage of multinuclearity and nuclear dynamics in fungi is well known (Roper et al, 2011). However, the underlying mechanism to control the movements of multiple nuclei in fungal hyphae is not well understood.…”

Section: Introductionmentioning

confidence: 99%

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Electron tomography of the microtubule cytoskeleton in multinucleated hyphae of Ashbya gossypii

Gibeaux

Lang

Politi

et al. 2012

Journal of Cell Science

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SummaryWe report the mechanistic basis guiding the migration pattern of multiple nuclei in hyphae of Ashbya gossypii. Using electron tomography, we reconstructed the cytoplasmic microtubule (cMT) cytoskeleton in three tip regions with a total of 13 nuclei and also the spindle microtubules of four mitotic nuclei. Each spindle pole body (SPB) nucleates three cMTs and most cMTs above a certain length grow according to their plus-end structure. Long cMTs closely align for several microns along the cortex, presumably marking regions where dynein generates pulling forces on nuclei. Close proximity between cMTs emanating from adjacent nuclei was not observed. The majority of nuclei carry duplicated side-by-side SPBs, which together emanate an average of six cMTs, in most cases in opposite orientation with respect to the hyphal growth axis. Such cMT arrays explain why many nuclei undergo short-range back and forth movements. Only occasionally do all six cMTs orient in one direction, a precondition for long-range nuclear bypassing. Following mitosis, daughter nuclei carry a single SPB with three cMTs. The increased probability that all three cMTs orient in one direction explains the high rate of nuclear bypassing observed in these nuclei. The A. gossypii mitotic spindle was found to be structurally similar to that of Saccharomyces cerevisiae in terms of nuclear microtubule (nMT) number, length distribution and three-dimensional organization even though the two organisms differ significantly in chromosome number. Our results suggest that two nMTs attach to each kinetochore in A. gossypii and not only one nMT like in S. cerevisiae.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Electron tomography of the microtubule cytoskeleton in multinucleated hyphae of Ashbya gossypii

Gibeaux

Lang

Politi

et al. 2012

Journal of Cell Science

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“…Nucleotypes created by mutation or mitotic recombination are likely to have lower fitness as homokarya, but sharing cytoplasm with wildtype nuclei may shield them from fitness defects (35). Nonetheless, selective forces must also act on novel nucleotypes, both for the evolution of new strains and to purify colonies (12). Experiments with heterokarya in which one nucleotype has, e.g., antibiotic resistance will open a new window on the nuclear ecology of syncytia in which nuclei can interact either antagonistically or cooperatively (4).…”

Section: Discussionmentioning

confidence: 99%

“…Fusion between different fungal individuals is limited by somatic (heterokaryon) compatibility barriers (8), and most internal genetic diversity results from mutations within a single, initially homokaryotic individual (4). However, somatic compatibility barriers are not absolute (9), and exchange of nuclei between heterospecific individuals is now believed to be a motor for fungal diversification (10)(11)(12).…”

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confidence: 99%

Nuclear dynamics in a fungal chimera

Roper

Simonin

Hickey

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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100

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A fungal colony is a syncytium composed of a branched and interconnected network of cells. Chimerism endows colonies with increased virulence and ability to exploit nutritionally complex substrates. Moreover, chimera formation may be a driver for diversification at the species level by allowing lateral gene transfer between strains that are too distantly related to hybridize sexually. However, the processes by which genomic diversity develops and is maintained within a single colony are little understood. In particular, both theory and experiments show that genetically diverse colonies may be unstable and spontaneously segregate into genetically homogenous sectors. By directly measuring patterns of nuclear movement in the model ascomycete fungus Neurospora crassa, we show that genetic diversity is maintained by complex mixing flows of nuclei at all length scales within the hyphal network. Mathematical modeling and experiments in a morphological mutant reveal some of the exquisite hydraulic engineering necessary to create the mixing flows. In addition to illuminating multinucleate and multigenomic lifestyles, the adaptation of a hyphal network for mixing nuclear material provides a previously unexamined organizing principle for understanding morphological diversity in the more-thana-million species of filamentous fungi.heterokaryon | hydrodynamics | biological networks G enetic diversity between individuals is important to the resilience of species (1) and ecosystems (2). However, physical and genetic barriers constrain internal genetic diversity within single organisms: Cell walls limit nuclear movement between cells, whereas separation of germ and somatic cell lines means that diversity created by somatic mutations is not transmitted intergenerationally. However, in syncytial organisms, including filamentous fungi and plasmodial slime molds (3), populations of genetically different and mobile nuclei may share a common cytoplasm ( Fig. 1A and Movie S1). Internal diversity may be acquired by accumulation of mutations as the organism grows or by somatic fusion followed by genetic transfer between individuals. For filamentous fungi, intraorganismic diversity is ubiquitous (4, 5). Shifting nuclear ratios to suit changing or heterogeneous environments enhances growth on complex substrates such as plant cell walls (6) and increases fungal virulence (7). Fusion between different fungal individuals is limited by somatic (heterokaryon) compatibility barriers (8), and most internal genetic diversity results from mutations within a single, initially homokaryotic individual (4). However, somatic compatibility barriers are not absolute (9), and exchange of nuclei between heterospecific individuals is now believed to be a motor for fungal diversification (10-12).A fungal chimera must maintain its genetic richness during growth. Maintenance of richness is challenging because fungal mycelia, which are made up of a network of filamentous cells (hyphae), grow by extension of hyphal tips. A continual tipward flow of vesicles and n...

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“…In networked organisms, such as filamentous fungi, cytoplasmic continuity facilitates long-distance transport of resources at speeds much faster than those with diffusion alone through cytoplasmic streaming (26,50,73) or mass flow (14) without the elaboration of a separate vascular system (32). These data suggest that the architecture of a colony can have an important influence on the physiological state, organelle distribution, and nutrient translocation within the mycelium (64).…”

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confidence: 80%

Physiological Significance of Network Organization in Fungi

et al. 2012

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bThe evolution of multicellularity has occurred in diverse lineages and in multiple ways among eukaryotic species. For plants and fungi, multicellular forms are derived from ancestors that failed to separate following cell division, thus retaining cytoplasmic continuity between the daughter cells. In networked organisms, such as filamentous fungi, cytoplasmic continuity facilitates the long-distance transport of resources without the elaboration of a separate vascular system. Nutrient translocation in fungi is essential for nutrient cycling in ecosystems, mycorrhizal symbioses, virulence, and substrate utilization. It has been proposed that an interconnected mycelial network influences resource translocation, but the theory has not been empirically tested. Here we show, by using mutants that disrupt network formation in Neurospora crassa (⌬so mutant, no fusion; ⌬Prm-1 mutant, ϳ50% fusion), that the translocation of labeled nutrients is adversely affected in homogeneous environments and is even more severely impacted in heterogeneous environments. We also show that the ability to share resources and genetic exchange between colonies (via hyphal fusion) is very limited in mature colonies, in contrast to in young colonies and germlings that readily share nutrients and genetic resources. The differences in genetic/resource sharing between young and mature colonies were associated with variations in colony architecture (hyphal differentiation/diameters, branching patterns, and angles). Thus, the ability to share resources and genetic material between colonies is developmentally regulated and is a function of the age of a colony. This study highlights the necessity of hyphal fusion for efficient nutrient translocation within an N. crassa colony but also shows that established N. crassa colonies do not share resources in a significant manner.T he transition from unicellular to multicellular organisms has occurred on multiple occasions in diverse lineages over considerable evolutionary time (28,38,68). While an initial adaptive advantage may have accrued simply from being larger, multicellular organisms subsequently developed increased differentiation and specialization, leading to a more efficient division of labor (8). Multicellularity may have arisen by either the aggregation of individual cells to form a colony or by the failure of daughter cells to separate following division. Comparisons of unicellular animals and their multicellular relatives support the view that multicellularity is associated with expansion of the genetic families involved in cell adhesion, cell-cell signaling, and cell differentiation (63). In contrast, multicellular plants and fungi are derived from ancestors that failed to separate following cell division, providing an opportunity to retain cytoplasmic continuity between daughter cells (75). Thus, plant cells are linked by tissue-specific patterns of plasmodesmata (41, 47), while fungi are either coenocytic or have perforated septa that allow intercompartmental exchange (40).In ascomycete an...

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Nuclear and Genome Dynamics in Multinucleate Ascomycete Fungi

Cited by 120 publications

References 86 publications

Electron tomography of the microtubule cytoskeleton in multinucleated hyphae of Ashbya gossypii

Electron tomography of the microtubule cytoskeleton in multinucleated hyphae of Ashbya gossypii

Nuclear dynamics in a fungal chimera

Physiological Significance of Network Organization in Fungi

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