Role of life-history strategies of arbuscular mycorrhizal fungi in partner selection by a juvenile C4 grass under low-light conditions

doi:10.21203/rs.3.rs-4708467/v1

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Role of life-history strategies of arbuscular mycorrhizal fungi in partner selection by a juvenile C4 grass under low-light conditions

https://doi.org/10.21203/rs.3.rs-4708467/v1

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Background and Aims

In coastal grasslands carbon cost of arbuscular mycorrhizal (AM) fungi is a crucial factor for the successful establishment of juvenile plants grown under the canopy of large plants that restricts their photosynthesis. Network competitor (NC) fungi that colonize via hyphal networks may be less costlythan soil-propagule-mediated colonizer (SP) fungibecause C cost for colonization could be covered by the donor plant of the networks.

Methods

Intact root-soil-core samples (NC inocula) and root-zone-soil samples (sieved before inoculation, SP inocula) were collected from a coastal grassland, and seedlings of Miscanthus sinensis were grown with both inocula and either with the NC or SP inocula with or without shading. DNA was extracted from the root, and fungal LSU rDNA was amplified and sequenced to assign to AM fungal operational taxonomic units (OTUs). All AM fungi that occurred with the SP inocula were defined as SP fungi, whereas those that occurred uniquely with the NC inocula were defined as NC fungi.

Results

Shading increased the genus richness of SP fungi, but not that of NC fungi, without changing OTU richness, which was due to the replacement of several Glomerales SP fungi with those that belong to diverse genera in non-Glomerales under the shaded conditions.

Conclusion

These observations suggest that cost of SP fungi is comparable to that of NC fungi and, further, that Glomerales fungi are generally less competitive under which photosynthesis of the host is restricted, providing new insight into the selection of AM fungal partners by plants.

arbuscular mycorrhizal fungi

coastal grassland

juvenile plants

shading

soil disturbance

In coastal sand dune ecosystems, soil is constantly disturbed by wind and tide, and vegetation often distributes zonally along coastlines due to steep gradients of soil disturbance and salinity from the seaward to landward slopes of dunes (Wilson and Sykes 1999; Moreno-Casasola 1986). The seaward slopes are severely disturbed, in which only limited plant species that are specifically adapted to the environment inhabit, whereas severity of disturbance is lower in the landward slopes where species-rich coastal grassland develops (e.g., Kawahara and Ezawa 2013). Frequent disturbance acts as selection pressure not only for plants but also for arbuscular mycorrhizal (AM) fungi. AM fungi form symbiotic associations with most land plants, deliver mineral nutrients to the host (Smith and Read 2008) and play a significant role in the establishment and maintenance of vegetation in harsh environments (Corkidi and Rincón 1997; Fujiyoshi et al. 2006; Maki et al. 2008). Life-history strategies of AM fungi have recently been characterized along a disturbance gradient in Ishikari coastal sand dunes, Japan (Cahyaningtyas and Ezawa 2024), according to the C-S-R (competitor, stress-tolerator, and ruderal) framework applied to AM fungi (Chagnon et al. 2013). In the seaward slopes typical "ruderal fungi" that are capable of regenerating from soil propagules (i.e., spores and hyphal fragments) and colonized roots rapidly after disturbance were enriched, and a majority of this type of fungi belong to the order Glomerales and Gigasporales (Cahyaningtyas and Ezawa 2024). Whereas in the landward slopes not only ruderal fungi but also disturbance-sensitive "competitor fungi" that explore new a host mainly through hyphal networks in the soil, namely network competitor (NC) fungi in this study, coexist. Many of the competitor fungi belong to the Entrophosporales, Diversiporales, and Archaeosporales (Cahyaningtyas and Ezawa 2024).

In coastal grasslands it is likely that not only disturbance severity but also carbon (C) cost of AM fungi are crucial factors for the successful establishment of juvenile plants, particularly under the canopy of adult plants that shade the juvenile plants and thus their photosynthetic activity. Light availability has a significant impact on mycorrhizal benefits (Konvalinková and Jansa 2016). Phosphorus uptake through the mycorrhizal pathway rapidly declines by short-term shading without apparent decreases in fungal colonization, and long-term shading often results in negative host growth response to mycorrhiza (Konvalinková et al. 2015), implying that C cost for mycorrhizal colonization exceeds the benefits under the shade. Selection of low-cost AM fungal partners, therefore, is likely a critical issue for the juvenile plants, but information about the impact of light availability on the selection of AM fungal partners is limited.

C cost of AM fungi may differ among those that have different life-history strategies. NC fungi are likely advantageous for the juvenile plants because C cost for constructing intraradical hyphae in a new host, at least at the initial stage of colonization, could be covered by the original (adult) host (e.g., Nakano-Hylander and Olsson 2007). Furthermore, the association with NC fungi may enable the new host to share the hyphal networks constructed by the original host through which the plants can readily take up nutrients. In contrast, ruderal fungi that colonize new hosts mainly via soil propagules, namely soil-propagule-mediated colonizer (SP) fungi in this study, may cost more than NC fungi. This is because SP fungi have limited C storage in their spores, and thus the new host should cover most of the cost for the establishment of intraradical and extraradical hyphal networks.

The landward slopes of the primary dunes in Ishikari coastal dunes are dominated by the C₄ perennial grass Miscanthus sinensis that grows over 2 m height (Kawahara and Ezawa 2013). M. sinensis juvenile plants (seedlings), therefore, should survive and establish under the canopy of the plants. In this study, we aimed to assess the significance of the life-history strategies of AM fungi in the partner selection of the juvenile plants under low-light availability, addressing the following hypotheses; 1) M. sinensis seedlings preferentially associate with NC fungi under low-light conditions, which is accompanied by 2) decreases in the occurrence of the SP fungi in the orders Glomerales and Gigasporales and increases in that of the NC fungi in the orders Entrophosporales, Diversisporales, and Archaeosporales. To test these hypotheses, we conducted a greenhouse experiment with or without shading to mimic the growth conditions of M. sinensis juvenile plants in the field, employing the nylon-mesh-separated compartment culture to identify NC and SP strategist fungi.

Sampling site and soil sampling

In June 2022, soil sampling was conducted in the landward slopes of Ishikari coastal dunes, Hokkaido, Japan (43˚14'N, 141˚20'E), of which vegetation was described in Kawahara and Ezawa (2013) and Cahyaningtyas and Ezawa (2024). Three sampling squares of 1-m-quadrat were designated at 100 m intervals along the coastal line, and six pairs of a root-soil-core sample with or without an aboveground part of M. sinensis plant were collected from each of them by stainless-steel core samplers [5 × 5 cm (diam/ height), 100 mL in vol]. The aboveground part was cut at 5 cm above the ground level before collecting by the sampler, which were designated as NC inocula. Whereas the samples without a living plant were sieved on a 2-mm-stainless mesh to destruct AM fungal hyphal networks before trap culture and termed as SP inocula. Twenty kilograms of sand was also collected from the seaward slope of the dunes where no vegetation was present and autoclaved for 2 h as a base medium for trap culture.

Soil trap cultures

As a main experiment, the NC inoculum was transferred to a cylinder-shaped 37-µm-nylon mesh bag [5 × 5 cm (diam/ height)] inserted in a 400-mL plastic pot, and then the pot was filled with a mixture of the SP inoculum (100 mL) and base medium (200 mL) (Fig. 1). The nylon mesh allows AM fungal hyphae, but not plant roots, to pass through. As a supporting experiment, two treatments were set up to assign either of the two life-history strategies NC and SP to the fungi detected in the main experiment as follows. As a NC treatment, the NC inoculum was transferred to the mesh bag, and the pot was filled with a mixture of an autoclaved SP inoculum and the base medium, whereas as a SP treatment, four-week-old M. sinensis seedling was transplanted in an autoclaved NC inoculum (the living plant was removed prior to autoclaving) in the mesh bag, and the pot was filled with a mixture of the intact SP inoculum and base medium. Then M. sinensis seeds (Snow Brand Seed Co., Ltd., Sapporo) were sown outside the mesh bag as test plants, covered with a thin layer of autoclaved sand, and grown in a greenhouse either under natural light or under a plastic net that reduces natural light by 80% at day/ night temperatures of 26/ 20 ̊C (n = 3). The seedlings were grown with tap water for the first month and with liquid fertilizer made of Peters Professional 25-5-20 (ICL, St. Louis, MO) at 50 µM phosphate once a week thereafter.

After two months, the roots of the test plants were collected, washed with pressured tap water, cut into 1-cm segments, randomized in water, blotted on a paper towel, immersed in RNAlater (Thermo Fisher Scientific, Tokyo) for more than 48 h at room temperature to fix nucleic acid, blotted on a paper towel to remove excess RNAlater, transferred to a 3-mL tube with an O-ring sealed cap (Yasui Kikai, Osaka), and stored at -80°C until DNA extraction.

Molecular identification and strategy assignment

The frozen roots in the 3-mL tube were ground with a metal cone in the presence of liquid nitrogen at 2,500 rpm for 2 × 5 s using Multi-Beads Shocker (Yasui Kikai, Osaka), and DNA was extracted and purified from approx. 100 mg of ground sample by Maxwell RSC Instrument (Promega, Madison, WI) using Maxwell RSC PureFood GMO and Authentication Kit (Promega) according to the manufacturer's instructions, stored at -30˚C, and used as template for PCR amplification. The divergent domain 2 of large-subunit ribosomal RNA gene (LSU rDNA) was amplified in a 25-µL reaction mixture of Expand High-Fidelity PCR System (Roche Diagnostics, Tokyo), 0.5 nmol µL^− 1 each of FLd3 (forward) and FLR2 (reverse) primers that were linked to TruSeq-type forward- and reverse-adapter sequences (Illumina, Tokyo), respectively, at the 5'-end (Niwa et al. 2018), and 0.2–2 µL template DNA using C1000 TouchTM Thermal Cycler (BIO-RAD, Tokyo) with the following program: initial denaturation at 94˚C for 2 min, followed by 30 cycles of denaturation at 94˚C for 15 s, annealing at 48˚C for 40 s, polymerization at 72˚C for 1 min, and final elongation at 72˚C for 10 min. The PCR products were sequenced on the Illumina MiSeq platform (2 × 300 bp), and high-quality paired end reads (read 1 and read 2) were merged with a minimum overlap length of 10 nt using FLASH (http://ccb.jhu.edu/software/FLASH/) at Bioengineering Lab (Sagamihara, Kanagawa, Japan). The merged reads were subjected to blastn searches against the fungal LSU rDNA database consisted of 82,769 operational taxonomic units (OTUs) of fungi, including 687 OTUs of AM fungi (http://amfungi.kazusa.or.jp/) and assigned to the OTUs at ≥ 95% similarities over 250-bp alignment with an E-value cut-off of 1e-30. Details of the phylogenetic positions of the 687 OTUs are indicated in the maximum likelihood tree of am03 release (ML-tree of am03) at http://amfungi.kazusa.or.jp/.

The life-history strategies of the AM fungal OTUs detected in the main experiment were assigned with reference to the supporting experiment and previous studies as follows. All the OTUs that occurred in the SP treatment in the supporting experiment, those that were categorized as SP or SP/RD fungi in Cahyaningtyas and Ezawa (2024), and those that occurred in the trap cultures in Kawahara and Ezawa (2013) were assigned to SP strategists, irrespective of the occurrence in the NC treatment. Only the OTUs that occurred "uniquely" in the NC treatment and those that were categorized as SL fungi in Cahyaningtyas and Ezawa (2024) were assigned to NC strategists. The OTUs that occurred only in the main experiment, but neither in the supporting experiment nor in the previous studies were left unassigned. The sequences obtained by Cahyaningtyas and Ezawa (2024) and Kawahara and Ezawa (2013) were subjected to blastn searches and re-assigned to the latest AM fungal OTUs in the recently renewed database (http://amfungi.kazusa.or.jp/) by applying the same criteria prior to the strategy assignment.

Statistical analysis

All read count data were transformed to presence-absence data prior to analysis, and numbers of the sample in which the OTUs occurred were designated as abundance data for abundance-based analyses. Welch's t-test and two-way ANOVA followed by Tukey's post hoc test were performed on the R 4.3.1 platform (R Core Team 2023). Scatter plots were drawn with the dabestr package on the R platform (Ho et al. 2019). Similarity-difference-replacement (SDR) simplex analysis for abundance data was performed to explore OTU distribution patterns between the light and shaded conditions using SDR-abunSimplex program (Podani et al. 2013) (http://podani.web.elte.hu/SYN2000.html). Light-shade preference index of the M. sinensis seedlings (test plants) for the OTUs were defined by the following equation:

Light-shade preference index = OC_shade - OC_light

where OC_shade and OC_light represent the occurrence of OTU, that is, the numbers of samples in which the OTU occurred, under the shaded and light conditions, respectively. Positive and negative values of the index imply that the plants associate with the OTU more preferentially under the shaded and light conditions, respectively.

Assignment of OTU and life-history strategy

Sequencing of the PCR products generated 23,334–38,802 reads per sample (29,396 reads on average). Among them, 6.2% − 98.6% (75.4% on average) were assigned to 92 AM fungal OTUs (Supplementary material table S1). In the main experiment 50 and 44 OTUs were detected in the light and shaded conditions, respectively, in which 21 OTUs are shared between them. In the supporting experiment 23 and 28 OTUs were detected in the NC and SP treatments, respectively, under the light conditions, whereas 34 and 27 OTUs were detected in the NC and SP treatments, respectively, under the shaded conditions. Based on the occurrence of the OTUs in the supporting experiment and the previous studies (Supplementary material table S1), 64 and 18 OTUs could be assigned to SP and NC strategists, respectively, but 10 OTUs were left unassigned.

Impact of shading on plant preference for AM fungal life-history strategy

In the main experiment a majority of the OTUs associated with the plants were SP strategists (Fig. 2a). OTU richness of the whole communities (i.e., all strategists), NC fungi, SP fungi, and strategy-unassigned fungi was not different between the light and shaded conditions. Relative abundances of the NC, SP, and unassigned fungal OTUs, that is, their percentages in the total OTU numbers in each sample, were also not different between the light and shaded conditions (Supplementary material Fig. 1). Genus richness, however, was significantly higher in the whole communities under the shaded conditions, which was due to the higher genus richness of the SP fungi under the conditions (P < 0.01) (Fig. 2b).

SDR-simplex analysis at the OTU level showed that richness agreement (sum of similarity and replacement) accounted for 98.0% of the OTU distribution pattern in which replacement consisted of 73.1%, implying that many of OTUs were replaced between the light and shaded conditions without changing richness (Table 1). In contrast, the genus level analysis indicated that replacement explained only 19.3% of the distribution pattern, but instead, nestedness (sum of similarity and difference) accounted for 80.7%, implying that the genus-poor communities (i.e., those under the light conditions) were a subset of the genus-rich communities (i.e., those under the shaded conditions). The same analysis was performed on the combined dataset of the main and supporting experiments, in which similar trends were observed; richness agreement accounted for 95.7% in which replacement consisted of 55.5% at the OTU level, whereas, at the genus level, nestedness accounted for 82.9% of the pattern (Supplementary material table S2).

Table 1

SDR-simplex analysis on the OTU and genus distribution patterns between the light and shaded conditions in the main experiment.
	2D Simplex (%)			1D Simplex (%)
Taxon level	Similarity (S)	Difference (D)	Replacement (R)	Beta diversity (R + D)	Agreement (S + R)	Nestedness (S + D)
OTU	25.0	1.9	73.1	75.0	98.1	26.9
Genus	35.5	45.2	19.3	64.5	54.8	80.7

Phylogenetic distribution of the life-history strategies with respect to light-shade preference index

The OTU replacement, which was accompanied by the increases in the genus richness of SP strategists, led us to analyze phylogenetic distribution of the life-history strategies of the OTUs with respect to the light-shade preference index. At the genus level, the index of the OTUs belong to the genera Nanoglomus and Paraglomus (most are SP strategists), as well as those belong to Rhizophagus and Acaulospora (both SP and NC fungi), varied from negative to positive values (Fig. 3). Most of the OTUs in Microdominikia and Racocetra (mainly SP fungi) showed negative index values, while all OTUs in Glomus (SP fungi), Complexispora (both SP and NC fungi), and Entrophospora (both SP and NC fungi) showed positive values. Genus-level-averages of the index values of the OTUs that occurred in three or more samples are: Microdominikia, -2.00; Racocetra, -0.89; Rhizophagus, -0.55; Acaulospora, 0; Nanoglomus, 0.20; Glomus, 1.00; Complexispora, 1.00; Paraglomus, 1.25; Entrophospora, 1.50; Dominikia, 2.00; Scutellospora, 2.00 (Supplementary material fig. S2). At the order level, the average index value of the members of Glomerales was negative (-0.19), which was mainly due to the negative average values of the Rhizophagus OTUs that consist of 57% of all Glomerales OTUs (Fig. 3). Whereas all average values in the other orders were positive: Gigasporales, 0.67; Entrophosporales, 1.50; Diversisporales, 0.11; Paraglomerales, 1.25. As expected, the average index value of the non-Glomerales OTUs (0.57) was significantly higher than that of the Glomerales OTUs (Supplementary material fig. S3). The average values of the Glomerales SP, NC, and unassigned fungi were negative, whereas those of the non-Glomerales fungi were positive (Fig. 4a). Among them, the average of the Glomerales SP fungi was statistically lower than that of the non-Glomerales SP fungi. This is likely due to the fact that the most Rhizophagus SP fungi (i.e., 10 out of the 14 OTUs) showed negative values (Fig. 3 and Supplementary material table S1). The percentages of non-Glomerales OTUs were positively correlated with the index values (R² = 0.702, P < 0.01) (Fig. 4b), implying that the plants preferentially associated with non-Glomerales fungi under shaded conditions.

The present study demonstrated that SP strategist fungi play a significant role in partner selection by juvenile plants under different light availability. Unexpectedly, the impact of shading was evident only on SP fungi, but not on NC fungi, which is contrary to our first hypothesis. Shading increased the genus diversity of SP fungi without changing OTU richness, leading to nested structure at the genus level. Although the plant preferences for fungal partners generally varied at the OTU level, irrespective of their strategies, consistent preferences for particular genera were also observed; e.g., the members of Glomus, Coplexispora, and Entrophospora were preferred under the shaded conditions, whereas those of Microdominikia and Racocetra were preferred under the light conditions. In general, the plants associated more with Glomerales fungi under the light conditions, but their occurrences were decreased under the shaded conditions with increasing the occurrences of non-Glomerales SP fungi, which partially supports our second hypothesis.

Shading did not affect the OTU richness of any of the strategists but increased the genus diversity of SP strategists by replacing with the OTUs from diverse genera, indicating that the plants selected fungal partners in response to light availability. So far, minimum information about the influence of shading on AM fungal community is available, in which shading had only limited impact not only on AM fungal richness but also on the community compositions (Koorem et al. 2017; Liu et al. 2014; Neuenkamp et al. 2021). For example, Liu et al. (2014) observed no apparent changes in richness by shading neither at the OTU (virtual taxon) level nor at higher taxonomic levels. These previous studies were conducted in meadows (Koorem et al. 2017; Liu et al. 2014) and forest understories (Neuenkamp et al. 2021) where soil disturbance is likely minimum. In such stable ecosystems AM fungal community in which a small number of competitive fungi, e.g., NC strategists, may occupy the niche is likely robust thus less sensitive to host C deprivation by shading. In contrast, the coastal sand dune ecosystem employed in this study is frequently disturbed by wind and tide, and high-potential diversity of AM fungi is maintained, particularly in the landward slopes (Cahyaningtyas and Ezawa 2024; Kawahara and Ezawa 2013) where the inocula were collected. It is likely, therefore, that this high-potential diversity, as well as the empty niche of the newly growing seedlings (test plants), allowed the plants to fine-tune the selection of the symbiotic partners.

There were no differences in the richness and relative abundance of SP and NC fungi between the light and shaded conditions. These results suggest that C cost of NC fungi is not necessarily lower than that of SP fungi for juvenile plants, or that C cost for the early stage of colonization, probably before forming arbuscules where nutrient exchange between the symbionts occurs (Lanfranco et al. 2018), is mostly covered by the fungi. The main propagule of SP fungi is likely to be spores (Cahyaningtyas and Ezawa 2024), and about 20% of spore biomass consists of neutral lipid (Olsson and Johansen 2000) that is consumed during germination (Gaspar et al. 1994) and probably also during the early stage of colonization. It is likely that this energy source in spores provides competitiveness of SP fungi, comparable to that of NC fungi.

OTU selection by the juvenile plants in response to light availability was evident in the SP fungal communities, but not in the NC fungal communities, suggesting that cost among SP fungi is more variable than that among NC fungi. The higher OTU richness of SP fungi in the roots suggests that potential diversity was much higher in the SP fungal communities than in the NC fungal communities in the ecosystem, as supported by the previous study (Cahyaningtyas and Ezawa 2024), and this would provide greater opportunities for exploring lower-cost SP fungi. Therefore, replacing high-cost SP fungi with lower-cost ones is likely more efficient than seeking lower-cost NC fungi for maintaining the symbiotic function at lower cost. One might assume that C deficiency occurred in the NC fungi due to the restriction of photosynthesis in the donor plants under the shaded conditions and thus reduced inoculum potential of their extraradical hyphae. For example, C availability directly affects the growth of extraradical hyphae (Olsson et al. 2014). We consider, however, that this possibility is unlikely because apparent decreases in the OTU richness and relative abundance by shading was not observed in the NC communities, implying that the inoculum potential of NC fungi was comparable to that of SP fungi, irrespective of light availability. But this issue should be addressed in future studies for confirmation.

The plants generally preferred the non-Glomerales SP fungi under the shaded conditions, although there were some exceptions. This was typically characterized by the replacement of several Rhizophagus OTUs and all Microdominikia OTUs with those in the rather minor genera, e.g., Entrophospora (Entrophosporales), Scutellospora and Cetraspora (Gigasporales), and Archaeospora (Archaeosporales), leading to higher genus diversity. These observations suggest not only that C cost varies within the major genus Rhizophagus, even among those that have the same life-history strategies, but also that C cost of the fungi in those minor taxa is lower than that of Glomerales fungi. Glomerales fungi have been characterized as those that grow rapidly and allocate more biomass to intraradical mycelia, compared to Gigasporales fungi that grow slowly and allocate more biomass to extraradical mycelia in the soil (Hart and Reader 2002a). Glomerales fungi promote host growth greater than Gigasporales and Acaulosporales fungi in general, although significant intra-species, -genus, and -family variations in host growth response were also observed (Hart and Reader 2002b). Similarly, Koch et al. (2017) observed highly variable host growth responses to different families, genera, species, and even isolates of the same species of the fungi, although fungal morphology, that is, biomass allocation to intra- and extra-radical mycelia, was conserved at the family level. These previous studies imply that the biomass allocation patterns of AM fungi are not correlated with host growth responses. Although information about the morphology and host growth responses of such minor taxa is limited, we propose the following two mechanisms underlying the replacement of SP fungi in response to light availability; i) the Glomerales fungi are more sensitive to C availability and thus more competitive, that is, capable of colonizing more rapidly, under C-rich conditions than those in the minor taxa, but less competitive under C-deprived conditions, and/or ii) cost-benefit ratios of the fungi in the minor taxa are lower than those of the Glomerales fungi, even though their absolute benefits are smaller. Further comparative characterization of the colonization strategy and host growth responses of such minor taxa, together with the well-characterized generalist fungi Rhizophagus spp., is necessary.

We demonstrated that SP strategist AM fungi play a major role in the establishment of M. sinensis juvenile plants in the coastal dune ecosystem, providing taxonomic/functional diversity from which the plants are able to select better partners that meet their demands in given environments. Glomerales fungi, in particular Rhizophagus spp., are prevalent in the dunes, but the juvenile plants preferred non-Glomerales fungi under shaded conditions. This suggests differentiation in cost-benefit ratios, e.g., C-use efficiency for nutrient delivery, between the Glomerales and non-Glomerales, although also the genus Rhizophagus, are comprise.

Acknowledgement

We acknowledge Ministry of Education, Culture, Sports, Science and Technology, Japan for the scholarship to AC.

Competing interests

The authors have no relevant financial or non-financial interests to disclose.

Author contributions

All authors contributed to the study conception, design, and writing the manuscript.

Data availability

The sequence reads have been deposited in the Sequence Read Archive of National Center for Biotechnology Information under the accession number xxxxx (in progress).

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Role of life-history strategies of arbuscular mycorrhizal fungi in partner selection by a juvenile C4 grass under low-light conditions

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