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Conditions Promoting Mycorrhizal Parasitism Are of Minor Importance for Competitive Interactions in Two Differentially Mycotrophic Species

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ABSTRACT

Interactions of plants with arbuscular mycorrhizal fungi (AMF) may range along a broad continuum from strong mutualism to parasitism, with mycorrhizal benefits received by the plant being determined by climatic and edaphic conditions affecting the balance between carbon costs vs. nutritional benefits. Thus, environmental conditions promoting either parasitism or mutualism can influence the mycorrhizal growth dependency (MGD) of a plant and in consequence may play an important role in plant-plant interactions. In a multifactorial field experiment we aimed at disentangling the effects of environmental and edaphic conditions, namely the availability of light, phosphorus and nitrogen, and the implications for competitive interactions between Hieracium pilosella and Corynephorus canescens for the outcome of the AMF symbiosis. Both species were planted in single, intraspecific and interspecific combinations using a target-neighbor approach with six treatments distributed along a gradient simulating conditions for the interaction between plants and AMF ranking from mutualistic to parasitic. Across all treatments we found mycorrhizal association of H. pilosella being consistently mutualistic, while pronounced parasitism was observed in C. canescens, indicating that environmental and edaphic conditions did not markedly affect the cost:benefit ratio of the mycorrhizal symbiosis in both species. Competitive interactions between both species were strongly affected by AMF, with the impact of AMF on competition being modulated by colonization. Biomass in both species was lowest when grown in interspecific competition, with colonization being increased in the less mycotrophic C. canescens, while decreased in the obligate mycotrophic H. pilosella. Although parasitism-promoting conditions negatively affected MGD in C. canescens, these effects were small as compared to growth decreases related to increased colonization levels in this species. Thus, the lack of plant control over mycorrhizal colonization was identified as a possible key factor for the outcome of competition, while environmental and edaphic conditions affecting the mutualism-parasitism continuum appeared to be of minor importance.

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Biplots showing Y-scores and X- and Y-loadings of the first two components of Partial Least Squares (PLS) regression models for mycorrhizal (A) and non-mycorrhizal (B) plants of Corynephorus canescens and mycorrhizal (C) and non-mycorrhizal (D) plants of Hieracium pilosella. Symbols of sample scores are colored depending on assumed ranks of a theoretical scale of mycorrhizal parasitism potential, with blue to red indicating treatments with low to high parasitism potential. Symbol types refer to competition treatments, with dots indicating plants grown alone and triangles and squares indicating intra- and interspecific competition, respectively. Scaled X-loadings are represented by gray labeled arrows. Scaled Y-loadings are depicted by crosses with black letters in larger fond. For explained variance in Y please see Table 2. AM, mycorrhizal plants; NM, non-mycorrhizal plants. Independent variables (X): inter, intra, and single = interspecific, intraspecific competition and plants grown alone; shade = shade treatment; N, P, nF = nitrogen and phosphorus fertilization and no fertilization, respectively. Dependent variables (Y): MGD = mycorrhizal growth dependency; B = total biomass; Co = colonization; P = plant phosphorus content, N = plant nitrogen content.
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Figure 1: Biplots showing Y-scores and X- and Y-loadings of the first two components of Partial Least Squares (PLS) regression models for mycorrhizal (A) and non-mycorrhizal (B) plants of Corynephorus canescens and mycorrhizal (C) and non-mycorrhizal (D) plants of Hieracium pilosella. Symbols of sample scores are colored depending on assumed ranks of a theoretical scale of mycorrhizal parasitism potential, with blue to red indicating treatments with low to high parasitism potential. Symbol types refer to competition treatments, with dots indicating plants grown alone and triangles and squares indicating intra- and interspecific competition, respectively. Scaled X-loadings are represented by gray labeled arrows. Scaled Y-loadings are depicted by crosses with black letters in larger fond. For explained variance in Y please see Table 2. AM, mycorrhizal plants; NM, non-mycorrhizal plants. Independent variables (X): inter, intra, and single = interspecific, intraspecific competition and plants grown alone; shade = shade treatment; N, P, nF = nitrogen and phosphorus fertilization and no fertilization, respectively. Dependent variables (Y): MGD = mycorrhizal growth dependency; B = total biomass; Co = colonization; P = plant phosphorus content, N = plant nitrogen content.

Mentions: Increasing intensity of conditions promoting parasitism resulted in lower biomass in the AM treatment in C. canescens. Here, single plants produced ~4 times less biomass under P fertilization and shade (high expected parasitism) than under N fertilization and light (high expected mutualism; Supplementary Table S1). In accordance, in the biplot of the first two components of the PLS model, X-loadings of P fertilization and shade, with high parasitism potential, were located opposite to Y-loadings of biomass, which indicates that biomass was negatively related to these treatments (Figure 1A). The distribution of the sample scores of the first two components also indicated the negative relation between biomass and parasitism potential. Scores of samples in treatments with high parasitism potential (red end of color scale) had higher values on component 1 and where thus located opposite to the loadings of biomass, plant N, and plant P, while the location of samples with low parasitism potential (blue end of color scale) indicated higher values of these responses (Figure 1A). Further, P fertilization and shade treatments were identified as significant predictors for biomass, plant N, and plant P of AM C. canescens (Table 1). N fertilization treatment was also a significant predictor for biomass and plant N, while the factor “no fertilization” was not important for the prediction of these parameters (Table 1). However, the negative effects of parasitism promoting conditions were not related to mycorrhization, as the NM treatments of C. canescens showed similar dependence structure and score distribution with blue colored scores next to biomass, plant N, and plant P loadings (Figure 1B). On component 1, the loadings for shade and P fertilization were located opposite to biomass, plant N and plant P, which were explained by the first component with 48.1, 46.3, and 37.7%, respectively (Table 2). Both AM and NM C. canescens tended to have least biomass with P fertilization (~0.73 and ~3.50 g, respectively) and highest biomass with N fertilization (~2.13 and ~5.99 g, respectively; Supplementary Table S1), as reflected in the location of fertilization loadings as compared to biomass loadings on components 1 and 2 (Figures 1A,B). MGD in C. canescens single plants was markedly negative in all treatments with an average value of −59% (Supplementary Table S1), showing that AM C. canescens were smaller (~1.79 g) than the corresponding NM plants (~4.51 g), which was significant for AM plants with P fertilization (~0.73 g, p < 0.05; Supplementary Table S1). PLS indicated a negative relation between MGD and the X-loadings shade and P fertilization by the opposite position along component 2 (Figure 1A), with P fertilization being a significant predictor for MGD (Table 1).


Conditions Promoting Mycorrhizal Parasitism Are of Minor Importance for Competitive Interactions in Two Differentially Mycotrophic Species
Biplots showing Y-scores and X- and Y-loadings of the first two components of Partial Least Squares (PLS) regression models for mycorrhizal (A) and non-mycorrhizal (B) plants of Corynephorus canescens and mycorrhizal (C) and non-mycorrhizal (D) plants of Hieracium pilosella. Symbols of sample scores are colored depending on assumed ranks of a theoretical scale of mycorrhizal parasitism potential, with blue to red indicating treatments with low to high parasitism potential. Symbol types refer to competition treatments, with dots indicating plants grown alone and triangles and squares indicating intra- and interspecific competition, respectively. Scaled X-loadings are represented by gray labeled arrows. Scaled Y-loadings are depicted by crosses with black letters in larger fond. For explained variance in Y please see Table 2. AM, mycorrhizal plants; NM, non-mycorrhizal plants. Independent variables (X): inter, intra, and single = interspecific, intraspecific competition and plants grown alone; shade = shade treatment; N, P, nF = nitrogen and phosphorus fertilization and no fertilization, respectively. Dependent variables (Y): MGD = mycorrhizal growth dependency; B = total biomass; Co = colonization; P = plant phosphorus content, N = plant nitrogen content.
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Figure 1: Biplots showing Y-scores and X- and Y-loadings of the first two components of Partial Least Squares (PLS) regression models for mycorrhizal (A) and non-mycorrhizal (B) plants of Corynephorus canescens and mycorrhizal (C) and non-mycorrhizal (D) plants of Hieracium pilosella. Symbols of sample scores are colored depending on assumed ranks of a theoretical scale of mycorrhizal parasitism potential, with blue to red indicating treatments with low to high parasitism potential. Symbol types refer to competition treatments, with dots indicating plants grown alone and triangles and squares indicating intra- and interspecific competition, respectively. Scaled X-loadings are represented by gray labeled arrows. Scaled Y-loadings are depicted by crosses with black letters in larger fond. For explained variance in Y please see Table 2. AM, mycorrhizal plants; NM, non-mycorrhizal plants. Independent variables (X): inter, intra, and single = interspecific, intraspecific competition and plants grown alone; shade = shade treatment; N, P, nF = nitrogen and phosphorus fertilization and no fertilization, respectively. Dependent variables (Y): MGD = mycorrhizal growth dependency; B = total biomass; Co = colonization; P = plant phosphorus content, N = plant nitrogen content.
Mentions: Increasing intensity of conditions promoting parasitism resulted in lower biomass in the AM treatment in C. canescens. Here, single plants produced ~4 times less biomass under P fertilization and shade (high expected parasitism) than under N fertilization and light (high expected mutualism; Supplementary Table S1). In accordance, in the biplot of the first two components of the PLS model, X-loadings of P fertilization and shade, with high parasitism potential, were located opposite to Y-loadings of biomass, which indicates that biomass was negatively related to these treatments (Figure 1A). The distribution of the sample scores of the first two components also indicated the negative relation between biomass and parasitism potential. Scores of samples in treatments with high parasitism potential (red end of color scale) had higher values on component 1 and where thus located opposite to the loadings of biomass, plant N, and plant P, while the location of samples with low parasitism potential (blue end of color scale) indicated higher values of these responses (Figure 1A). Further, P fertilization and shade treatments were identified as significant predictors for biomass, plant N, and plant P of AM C. canescens (Table 1). N fertilization treatment was also a significant predictor for biomass and plant N, while the factor “no fertilization” was not important for the prediction of these parameters (Table 1). However, the negative effects of parasitism promoting conditions were not related to mycorrhization, as the NM treatments of C. canescens showed similar dependence structure and score distribution with blue colored scores next to biomass, plant N, and plant P loadings (Figure 1B). On component 1, the loadings for shade and P fertilization were located opposite to biomass, plant N and plant P, which were explained by the first component with 48.1, 46.3, and 37.7%, respectively (Table 2). Both AM and NM C. canescens tended to have least biomass with P fertilization (~0.73 and ~3.50 g, respectively) and highest biomass with N fertilization (~2.13 and ~5.99 g, respectively; Supplementary Table S1), as reflected in the location of fertilization loadings as compared to biomass loadings on components 1 and 2 (Figures 1A,B). MGD in C. canescens single plants was markedly negative in all treatments with an average value of −59% (Supplementary Table S1), showing that AM C. canescens were smaller (~1.79 g) than the corresponding NM plants (~4.51 g), which was significant for AM plants with P fertilization (~0.73 g, p < 0.05; Supplementary Table S1). PLS indicated a negative relation between MGD and the X-loadings shade and P fertilization by the opposite position along component 2 (Figure 1A), with P fertilization being a significant predictor for MGD (Table 1).

View Article: PubMed Central - PubMed

ABSTRACT

Interactions of plants with arbuscular mycorrhizal fungi (AMF) may range along a broad continuum from strong mutualism to parasitism, with mycorrhizal benefits received by the plant being determined by climatic and edaphic conditions affecting the balance between carbon costs vs. nutritional benefits. Thus, environmental conditions promoting either parasitism or mutualism can influence the mycorrhizal growth dependency (MGD) of a plant and in consequence may play an important role in plant-plant interactions. In a multifactorial field experiment we aimed at disentangling the effects of environmental and edaphic conditions, namely the availability of light, phosphorus and nitrogen, and the implications for competitive interactions between Hieracium pilosella and Corynephorus canescens for the outcome of the AMF symbiosis. Both species were planted in single, intraspecific and interspecific combinations using a target-neighbor approach with six treatments distributed along a gradient simulating conditions for the interaction between plants and AMF ranking from mutualistic to parasitic. Across all treatments we found mycorrhizal association of H. pilosella being consistently mutualistic, while pronounced parasitism was observed in C. canescens, indicating that environmental and edaphic conditions did not markedly affect the cost:benefit ratio of the mycorrhizal symbiosis in both species. Competitive interactions between both species were strongly affected by AMF, with the impact of AMF on competition being modulated by colonization. Biomass in both species was lowest when grown in interspecific competition, with colonization being increased in the less mycotrophic C. canescens, while decreased in the obligate mycotrophic H. pilosella. Although parasitism-promoting conditions negatively affected MGD in C. canescens, these effects were small as compared to growth decreases related to increased colonization levels in this species. Thus, the lack of plant control over mycorrhizal colonization was identified as a possible key factor for the outcome of competition, while environmental and edaphic conditions affecting the mutualism-parasitism continuum appeared to be of minor importance.

No MeSH data available.


Related in: MedlinePlus