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Biology Department, Stonehill College, Easton, Massachusetts 02357
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Vegetative mycelial cells of Armillaria are expected to have diploid nuclei. Cells from a single mycelium therefore would not be expected to differ from one another for ecologically relevant quantitative traits. We isolated two sets of basidiome cell lines (from spores and stipe cells) and one set of vegetative cell lines (from an attached rhizomorph) from a single contiguous Armillaria gallica mycelium. We isolated a second set of vegetative cell lines from the soil 20 cm from the above basidiomerhizomorph complex. In all four sets of cell lines in situ DAPI-DNA measurements showed cells are haploid and quantitative-trait analyses of cell lines grown at different water potentials revealed high levels of among-cell-line genetic variation for both growth and phenotypic plasticity. Haploidy and the existence of ecologically relevant genetic variation within vegetative individuals are unexpected and mean that a process similar to evolutionary adaptation could take place within the soma of a genetic individual. We believe this is a key to understanding how large A. gallica mycelia survive exposure to variation in ecological conditions during lives that potentially span several tree (host) generations.
Key words: basidiomycete, genetic mosaicism, indeterminate fungal growth, long-lived species, natural selection, phenotypic plasticity
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The discovery that single A. gallica individuals colonize habitats larger than 15 hectares and remain genetically stable for lives that span several centuries (Smith et al 1992, Hodnett and Anderson 2000) raises the question of how these individuals can tolerate exposure to potentially broad ranges of ecological conditions.
In arborescent plants and clonal organisms, genetic mosaicism produced by high rates of somatic mutation has been proposed as a mechanism that might explain how long-lived individuals keep up with short-term fluctuations in pest populations and environmental conditions (Gill 1986, Gill et al 1995). Estimated mutation rates in natural populations of A. gallica (Hodnett and Anderson 2000) are much too low for a mutation-based model of mosaicism to explain longevity in this species, however. A different model that has the potential to work for A. gallica has been proposed by Peabody et al (2000, FIG. 1). In this model genetic mosaicism is produced by Armillaria’s two-diploidization-two-haploidization life cycle (Korhonen 1980, Grillo et al 2000, Peabody et al 2000) and the model does not require high rates of somatic mutation. Instead the model relies on alleles that first were brought together when compatible spores mated during the life cycle’s first diploidization and later recombined during the life cycle’s first (cryptic) haploidization (FIG. 1).
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, Peabody et al 2000) were based on cells isolated from short-lived basidiomes. Basidiomes presumably are less likely to encounter broad ranges of environmental conditions than are long-lived vegetative mycelia that potentially last for centuries (Smith et al 1992, Hodnett and Anderson 2000). And, while basidiome spore production may be important for long-range dispersal (Kile et al 1991), vegetative stages of the life cycle appear to be more important in colonizing new food sources (Guillaumin and Legrand 2001, Ferguson et al 2003). If the evolutionary significance of mosaicism in indeterminate growth of long-lived fungal individuals is to be understood, vegetative stages of the life cycle clearly should be studied.
We studied quantitative traits because these continuously variable traits often are related directly to an organism’s biological fitness (de Meester 1996, Freeman and Herron 2004). Growth, in particular, was selected because it is one of the most widely accepted components of fitness in fungi (Brasier 1999) that access resources primarily by growing indeterminately through their environment. Water potential was chosen as an environmental variable because soil moisture is considered to be one of the most important factors affecting the establishment and survival of genetic individuals in nature (Anderson et al 1979, Kile 1986, Worrall 1994, Ferguson et al 2003). Our particular values of water potential represent wet (–1.0 MPa) through dry (–4.5 MPa) forest soils that have been reported to affect A. gallica growth in nature (Whiting and Rizzo 1999). Spore cell lines and stipe cell lines were chosen for study because an earlier study analyzed their growth patterns when exposed to variation in pH, temperature and host species (Peabody et al 2003). It also was important to study spores because they provide a baseline for the amount of variation to be expected in a haploid, genetically variable life-cycle stage that has undergone meiosis. Rhizomorph cell lines and soil mycelium cell lines represent potentially long-lived vegetative stages of the life cycle and are therefore of key importance to our hypothesis (i.e. vegetative cell lines within single A. gallica individuals are characterized by ecologically-relevant quantitative-trait variation that affects growth in response to variation in water potential).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Peabody et al 2003) to isolate 40 cells that produced 40 cell lines (10 spore cell lines, 10 stipe cell lines, 10 rhizomorph cell lines, 10 soil mycelium cell lines). Spores, stipe cells and rhizomorph cells were collected from a single, contiguous mycelium (a basidiome attached to a rhizomorph) growing 1 m from the base of a white ash tree (Fraxinus americana) at 493 Leonard Street, Raynham, Massachusetts, (41°55'02''N, 071°00'18''W, ~13 m elevation) on 31 Oct 2001. Because of the physical connection of the source of these three cell lines, it is likely that they are part of a single genetic individual. The 10 soil mycelium cells were isolated from a strawberry plant acting as bait and growing in the soil 20 cm from that same basidiome. At this point it is not possible to say whether the 30 cell lines isolated from the basidiomerhizomorph structure (i.e. spore cell lines, stipe cell lines, rhizomorph cell lines) and the 10 cell lines isolated from the strawberry plant (i.e. soil mycelium cell lines) all are isolates of a single genetic individual or isolates of two closely spaced but separate genetic individuals.
Spores represent cells that have completed the first and second diploidization-haploidization events in the life cycle; stipe cells represent short-lived, basidiome cells that have completed the first diploidization-haploidization event but not the second. Rhizomorph cells and soil mycelium cells represent potentially long-lived, vegetative stages of the life cycle that have completed the first diploidization-haploidization event of the life cycle but not the second (FIG. 1
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In situ nuclear DAPI-DNA measurements.— –
Established methods of DAPI-DNA staining and microspectrophotometry (Peabody and Peabody 1985, 1987) were used to quantify relative amounts of nuclear DNA in ethanol-preserved samples for all 40 cell lines (10 measurements were made for each of the 40 cell lines). To provide a basis for comparison to cells that are known to be haploid, we also measured nuclei from 30 ethanol-preserved spores from the same basidiome that produced spore and stipe cell lines. To provide a basis for comparison to cells that are known to be diploid with replicated DNA (i.e. 4C) (Peabody and Peabody 1985), we measured 30 nuclei of ethanol-preserved prophase I basidia taken from the same basidiome.
Quantitative trait analyses: growth of cell lines.— – After isolation from nature, each cell was transferred to its own 1.5% malt-extract agar (MEA) plate and allowed to grow and establish its own cell line. All 40 cell lines were transferred to fresh 1.5% MEA plates and grown 25 d in randomized positions in the dark at 23 C. These plates served as sources of inocula for inoculum plates (i.e. plates used later as sources of inoculum for experimental plates in the growth study).
Quantitative trait analyses: control for environmental history of inocula.— – Many factors other than experimental treatments can affect the growth of mycelia during growth experiments. Factors known to affect growth include variables such as age of inocula, variation in water/nutrient content of media, degree of injury to mycelia in inoculum plugs and relative positions of inoculum plugs within parent mycelia. Many unknown factors also might affect the growth of mycelia during an experiment. Precautions were taken at each step to control for all known variables that affect growth, and our experimental design (see below) helped to control for unknown variables.
After 25 d in the dark at 23 C, each of 10 uniform inoculum plugs (mycelium-agar cylinders, ht = 6 mm, d = 6 mm) of each of the 40 cell lines was transferred from the actively growing margin of the colony to a separate, fresh 1.5% MEA plate and grown in a randomized position 23 d in the dark at 23 C. This created a grid of 100 separate inoculum plates for each cell set (spore cell lines, stipe cell lines, rhizomorph cell lines and soil mycelium cell lines). Whenever we refer to a 100 plate (10 x 10) grid, either a "100 plate inoculum grid" (as in this section) or a "100 plate experimental treatment grid" (as in the next section), we are referring to 10 separate, independent replicate plates for each of the 10 different cell lines. This procedure controls for variations in environmental history among inoculum plugs and produces experimental treatment grids of 100 independent plates (see next section) suitable for analysis by ANOVA.
Quantitative trait analyses: experimental design of growth studies.— –
The 100 plate (10 x 10) experimental treatment grids used to compare levels of ecologically relevant, quantitative-trait genetic variation in all four sets of cell lines were set up as follows: uniform inoculum plugs from the growing edge of colonies in the 100 independent inoculum plates were used to inoculate 100 experimental plates (containing 1% malt-extract agar modified with KCl [Whiting and Rizzo 1999] to produce the desired water potential). There was a one-to-one correspondence between the 100 inoculum plates and the 100 experimental plates in each grid. This procedure was repeated for all four sets of cell lines. This produced four different grids of 100 plates each, or a total of 400 plates. One set of 400 plates was grown in media at each of these four water potentials: –1.0, –1.5, –2.5 and –4.5 MPa (see next section) to produce a total of 1600 experimental plates. Because all 100 plates within an experimental treatment grid are independent, unknown variations peculiar to any particular plate in the grid are taken into account by ANOVA.
Mycelial areas were measured by image analysis (Peabody et al 2003) after 18 d in the dark at 23 C. During this time the smallest mycelia had begun to show measurable growth but the largest mycelia had not begun to show reduced growth due to depletion of nutrients. Two-way mixed model ANOVA (cell line = random factor, water potential treatment = fixed factor) was used to test for: (i) cell effect, which tests for among-cell-line genetic variation in growth; (ii) treatment effect, which tests for phenotypic plasticity (or the effect of different water potentials); and (iii) cell x treatment effect, which tests for among-cell-line genetic variation in phenotypic plasticity or gene-environment interaction. All statistical computations in this study were carried out by StatView 5.0.1.
Quantitative trait analyses: preparation of growth media with different water potentials.— –
The four water potentials used were –1.0, –1.5, –2.5 and –4.5 MPa. One percent malt-extract agar contributes 0.48 MPa to growth media (Whiting and Rizzo 1999). To reach water potentials of –1.0, –1.5, –2.5 and –4.5 MPa respectively, 8.43 g, 16.78 g, 33.78 g and 67.40 g of KCl were added per L of water (Robinson and Stokes 1955, Whiting and Rizzo 1999). In other studies water potentials have been adjusted with KCl, NaCl or sucrose and empirical results suggest that all three osmotica have similar effects on fungal growth (Whiting and Rizzo 1999).
Quantitative trait analyses: reliability of growth studies.— – In our lab we found the results of Armillaria growth studies to be consistent and repeatable. To demonstrate this we randomly selected six cell lines and asked four different pairs of individuals to independently conduct four replicates of the same growth study (different from the water potential study reported in this paper). In each study one set of six replicate plates for each of the six cell lines was exposed to one treatment (treatment 1) while another set of six replicate plates for the same six cell lines was exposed to a different treatment (treatment 2). With the exception of expected chance variation, the four studies produced identical results for cell effects, treatment effects and cell x treatment effects. Relative growth for all six cell lines was identical in the first three studies and in five out of six cell lines in the fourth study. When mean values for growth of cell lines were ranked the differences among rankings in the four different studies were not significant. (Spearman’s coefficient of rank correlation for cell line vs. rank produced P values of P = 0.4993 and P = 0.7426 for treatments 1 and 2, respectively; Kendall’s coefficient of rank correlation for cell line vs. rank produced P values of P = 0.4719 and P = 0.7284 for treatments 1 and 2, respectively).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, FIG. 2).
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), they establish the 4C value at 219.0 arbitrary units (a.u.), by inference the 2C value at 109.5 a.u. and the 1C value at 54.7 a.u. Diploid nuclei therefore should fall within the 2–4C (109.5–219.0 a.u.) range depending on the stage of DNA synthesis and haploid nuclei should fall within the 1–2C (54.7–109.5 a.u.) range depending on the stage of DNA synthesis. To check this assertion, we collected and measured 30 preserved spores (different from the spores used to establish spore cell lines) from the above basidiome. These spores had a mean DAPI-DNA content of 86.8 a.u. with a 95% confidence interval (CI) of 78.9–94.7 a.u., which falls within the 1–2C range expected for haploid nuclei.
Of the 20 potentially long-lived, vegetative cell lines (i.e. soil mycelium cell lines m1–m12 and rhizomorph cell lines r1–r11), 19 have 95% CIs that fall primarily within the 1–2C range (TABLE I, FIG. 2). One soil mycelium cell line, m3, has a 95% CI (109.8–139.0 a.u.) that falls just outside the 1–2C range (54.7–109.5 a.u.). It statistically is not unexpected that 1 out of 20 95% CIs would fall outside the expected range. None of the 20 vegetative cell lines (including soil mycelium cell line m3) has a 95% CI that even approaches the 2C–4C (i.e. diploid) midpoint of 164.2 a.u. or the 4C (i.e. diploid, replicated) value of 219.0 a.u. When the 30 preserved spores (mean = 86.8 a.u., SD = 22.0, n = 30) are compared to lumped data for vegetative cell lines by one-way ANOVA, they do not differ from either rhizomorph cell lines (overall mean for 10 rhizomorph cell lines = 80.4 a.u., SD = 29.3, N = 100 total measurements, P = 0.2677) or soil mycelium cell lines (overall mean for 10 soil mycelium cell lines = 91.3 a.u., SD = 29.8, N = 100 total measurements, P = 0.4311). DAPI-DNA data therefore are consistent with the interpretation that all 20 vegetative cell lines used in this study are haploid.
Of the 20 cell lines isolated from a basidiome, all 10 stipe cell lines (i.e. t2–t11) and six of 10 spore cell lines (i.e. s4, s5, s6, s8, s11 and s12) have 95% CIs that fall within the 1–2C range that would be expected for haploid cells (TABLE I, FIG. 2). Four spore cell lines have 95% CIs that fall below the 1–2C range (i.e. s3, s9, s10 and s14). Although this is more than would be expected statistically, it is possible that spore-cell-line nuclei all happened to be haploid and unreplicated when they were measured. This interpretation is supported by the facts that: (i) 100 spore-cell-line measurements had a mean of 51.3 a.u., which is close to the inferred 1C value of 54.7 a.u.; and (ii) the standard deviation for these same 100 measurements (spore-cell-line SD = 19.9 a.u.) is smaller than the standard deviations for the three sets of cell lines that overlapped more closely with the 1–2C range and therefore are likely to represent mixtures of unreplicated and replicated nuclei (i.e. stipe-cell-line SD = 31.6 a.u., rhizomorph-cell-line SD = 29.3 a.u., and soil-mycelium-cell-line SD = 29.8 a.u.). DAPI-DNA data therefore are consistent with the interpretation that spore cell lines and stipe cell lines in this study are haploid.
Quantitative trait analyses.— –
Cell effects, treatment effects and cell treatment effects were significant for all four sets of cell lines (P values ranged from P < 0.0001 to P < 0.0005, TABLE II). This means that: (i) all four sets of cell lines possess among-cell-line, quantitative-trait genetic differences for loci affecting growth (note that both sets of vegetative cell lines are just as variable as spore cell lines and stipe cell lines, i.e. all cell-effect P values are < 0.0001); (ii) all four sets of cell lines are phenotypically plastic (i.e. their growth is affected by water potential); and (iii) all four sets of cell lines possess among-cell-line, quantitative-trait genetic differences for loci affecting phenotypic plasticity (i.e. the effect of water potential on growth differs from cell line to cell line).
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and 4) are helpful for visualizing patterns of phenotypic variation. Significant cell effects are reflected by differences in the vertical position of reaction norm lines (FIG. 3A–D). Note for example, on the rhizomorph graphs (FIGS. 3C and 4), that cell line r2 grew significantly more than r11 at all water potentials, and more than r3 at water potentials of –2.5, –1.5 and –1.0 MPa (Fisher’s Protected Least Significant Difference [PLSD] P values are provided below, nine lines down). Significant treatment effects are reflected by the positive slope of all reaction norm lines; for example, on the rhizomorph graph (FIG. 3C), growth is greater at higher water potentials than it is at lower water potentials for all possible comparisons of different water potential pairs (PLSD, P < 0.0001). Significant cell treatment effects are reflected by the fact that reaction norm lines do not all show similar changes in growth as water potentials change from dry (–4.5 MPa) to wet (–1.0 MPa) (FIG. 3A–D). For example, on the rhizomorph graph (FIG. 4), notice that r2 grew more than r3 at the three wetter water potentials (i.e. –1.0 MPa, P < 0.0001 [all probabilities are from PLSD]; –1.5 MPa, P = 0.0348; and –2.5 MPa, P = 0.0078) but not at the driest water potential (i.e. –4.5 MPa, P = 0.5752). Conversely, r3 grew more than r11 at the two drier water potentials (–4.5 MPa, P = 0.0003; and –2.5 MPa, P = 0.0230) but not at the two wetter water potentials (i.e. –1.5 MPa, P = 0.0985; and –1.0 MPa, P = 0.1329). This indicates that an increase in water potential above –4.5 MPa causes more of an increase in the growth of cell line r2 than it does in the growth of r3 or r11.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Franklin et al 1983, Korhonen 1983, Kim et al 2000), in situ nuclear DAPI-DNA measurements demonstrated that all 40 cell lines (including the 20 vegetative cell lines) were haploid (TABLE I).
Quantitative-trait variation.— –
Life span estimates for mycelia analyzed in this study could not be made because agricultural activity limits growth in soils surrounding the collection site. Nevertheless, if they are old, these individuals are likely to have been exposed to a wide range of conditions during the past two centuries because the collection site was a mixed pine-hardwood forest until the mid-1800s, farmland from the mid-1800s until 1977 and has been a residential lot since then. Investigators addressing the ability of long-lived species to survive exposure to changing environmental conditions have considered the possible significance of somatic-mutation-based mosaicism in clonal organisms and plants (Gill 1985, Gill et al 1995); recombination-based mosaicism in fungi (Peabody et al 2000, Peabody et al 2003); and phenotypic plasticity in a wide range of organisms (Andrews 1992, de Meester 1996, Schlichting and Pigliucci 1998, Peabody et al 2003). Armillaria gallica has been shown to be both genetically mosaic (Peabody et al 2000) and phenotypically plastic (Pearce and Malajczuk 1990, Schwarze et al 2000, Baumgartner and Rizzo 2001, Peabody et al 2003).
In most organisms populations adapt over time as fit individuals contribute disproportionate numbers of genes to future generations. In long-lived species of plants and fungi capable of indeterminate growth, however, this view of the individual and of individual fitness may be too narrow (Gill 1985, Gill et al 1995, Rayner et al 1995, Davidson et al 1996, Rayner 1997, Rayner et al 1999). In the case of fungal individuals in particular, it might be more accurate to think of individuals as "continuous, indeterminately growing . . . interactive trajectories . . .(that), purely by responding to local circumstances, and without any central administration" (Rayner 1997) are able to re-configure themselves during their lives in ways that let them adapt to changing conditions.
This view describes A. gallica individuals almost perfectly, with genetic mosaicism serving as the proximate mechanism that provides dynamic mycelial boundaries with the potential for differential cell-line growth within different parts of a single mycelium. For loci affecting growth and phenotypic plasticity, mosaicism may cause alleles to be grouped together in different combinations within different mycelial cell lines. Consider rhizomorph cell lines r2, r3 and r11 (FIG. 4), for example. In conditions approximating dry forest soil (i.e. –4.5 MPa) the growth of cell line r3 is similar to that of r2 and exceeds that of r11. In contrast, in conditions approximating wet forest soil (i.e. –1.0 MPa) the growth of cell line r3 is now similar to that of r11 and less than that of r2. If a large, mosaic mycelium were bounded by dry soil on one side and wet soil on the other, the contribution of cell line r3 to the overall indeterminate growth of the entire mycelium would be variable. On the dry side, r3 would undergo mitosis as rapidly as r2 and these two cell lines would have the potential to contribute more cells than r11 to the future mycelium on that side. On the wet side, r3 would undergo mitosis more slowly than r2 and would have the potential to contribute fewer cells than r2 and the same number of cells as r11 to the future mycelium on that side.
Armillaria gallica has been shown to possess among-cell-line genetic variation for response to variation in several environmental variables (i.e. pH, temperature, host species [Peabody et al 2003]; water potential [this study]). Given differences in cell-line genotypes and in values of environmental variables, some cell lines might grow and reproduce more effectively in one portion of a mycelium while other cell lines might grow and reproduce more effectively in another. Differential cell-line growth has the potential to change allele frequencies locally within an individual and let dynamic mycelial boundaries re-configure themselves in response to local conditions. In this scenario genetic mosaicism in conjunction with selection among cell lines might produce genetically different sectors within an individual. However, because bulk flow takes place within basidiomycetes (Moore 1998), successful cell lines within the mycelium might support one another’s growth as well as the growth of cell lines that are less well suited to current conditions. In this scenario, genetic mosaicism in concert with bulk flow might be expected to maintain the level of genetic uniformity within individuals that has been reported by Smith et al (1992) and Hodnett and Anderson (2000). Using either of these models, we think genetic mosaicism has the potential to explain how A. gallica individuals tolerate extensive spatial and temporal variation in ecological conditions during their lives.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: rpeabody{at}stonehill.edu
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LITERATURE CITED |
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