- Email: [email protected]
Arbuscular mycorrhizal fungal diversity increases growth and phosphorus uptake in C3 and C4 crop plants
Soil Biology and Biochemistry 135 (2019) 248–250
Contents lists available at ScienceDirect
Soil Biology and Biochemistry journal homepage: www.elsevier.com/locate/soilbio
Short Communication
Arbuscular mycorrhizal fungal diversity increases growth and phosphorus uptake in C3 and C4 crop plants
T
Adam Frewa,b,c,∗ a
School of Agricultural and Wine Sciences, Charles Sturt University, Wagga Wagga, New South Wales, Australia Institute for Land, Water and Society, Charles Sturt University, Albury, New South Wales, Australia c Graham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, New South Wales, Australia b
A R T I C LE I N FO
A B S T R A C T
Keywords: Arbuscular mycorrhizal fungi Microbial diversity Microbial inoculant Phosphorus nutrition Plant functional group
Most plants associate with arbuscular mycorrhizal (AM) fungi which can enhance their growth and nutrient uptake. Outcomes of the AM symbiosis can be highly variable, depending on soil fertility, plant functional group (C3, C4) and AM fungal diversity. This study assessed the growth and nutrient (C, N, P) responses of two C3 (Triticum aestivum and Hordeum vulgare) and two C4 (Sorghum bicolor and Zea mays) plants to different AM fungal inocula (no AM fungi, single AM fungal species, and four AM fungal species) under high and low P conditions. Higher AM fungal diversity resulted in greater P concentration and aboveground biomass of H. vulgare and S. bicolor. Triticum aestivum did not respond to AM fungi, while Z. mays responded positively but a similar positive response of Z. mays growth and nutrition occured when it was colonised with single or multiple AM fungal species. These findings suggest that, although C3 crop plants are less responsive to AM fungi than C4, some C3 and C4 species can benefit from higher AM fungal diversity in the soil.
The vast majority of terrestrial plants form associations with coevolved soil-dwelling fungi of the Glomeromycota known as arbuscular mycorrhizal (AM) fungi. These fungi colonise plant roots and provide their hosts with access to soil resources (phosphorus (P), nitrogen (N) and water) while plants provide the fungi with carbon (C) in the form of sugars and lipids (Keymer and Gutjahr, 2018; Smith and Smith, 2011). As such, the AM symbiosis is a key component of ecosystems, maintaining plant productivity and ecosystem stability (Powell and Rillig, 2018; Rillig, 2004). However, the outcomes of the AM symbiosis for plants can be highly variable (Hoeksema et al., 2010), and are known to be strongly driven by soil nutrient (P and N) availability (Johnson, 2010). When P is limiting in the environment, plants often benefit from the AM symbiosis, conversely when P is abundant there can be little benefit or even negative outcomes for plants (Johnson and Graham, 2013). Outcomes for host plants can depend on plant and fungal identities. For example, C4 plants often benefit more from AM fungal associations than C3 plants, partly due to their higher photosynthetic efficiency and greater nutrient demands (Hoeksema et al., 2010). Meanwhile the ability of AM fungi to provide a growth, nutrient or defence benefit to their host can also vary between fungal taxa. For example, some taxa may be more associated with enhanced plant growth and nutrient uptake, with others are more associated with enhanced plant defence
∗
against herbivory (Bennett and Bever, 2007; Sikes et al., 2009). There has been a long-held interest in employing the mycorrhizal symbiosis in sustainable plant production, but the efficacy and variability in responses remains a significant challenge (Hart et al., 2018; Rillig et al., 2019). Our understanding of the variation in plant growth and nutritional responses between C3 and C4 species to AM fungal diversity remains ambiguous. Yet, it is a key step towards effectively using the AM symbiosis in agriculture. Using a factorial pot experiment, I assessed differences in the growth, nutrient status and AM fungal colonisation of two economically significant C3 species (Triticum aestivum L., Hordeum vulgare L.) and two C4 species (Sorghum bicolor L. Moench, Zea mays L.) grown for eight weeks without AM fungi, with a single AM fungal species (Rhizophagus irregularis (Błaszk., Wubet, Renker & Buscot) C. Walker & A. Schüßler), or with a community of four AM fungal species (Claroideoglomus etunicatum (W. N. Becker & Gerd.) C. Walker & A. Schüßler, Funneliformis coronatum (Giovann.) C. Walker & A. Schüßler, F. mosseae (T. H. Nicolson & Gerd.) C. Walker & A. Schüßler, and Rhizophagus irregularis), under low (13 mg kg-1 plant available P) or high P soil (addition of 80mL 32µg g-1 soluble P) (Weremijewicz and Seto, 2016). Plants were harvested from their pots, aboveground biomass recorded, foliar and root samples were taken for nutrient analysis and mycorrhizal colonisation assessment, respectively (for methodological details see
Charles Sturt University, Building 286, Wagga Wagga, New South Wales, 2678, Australia. E-mail address: [email protected].
https://doi.org/10.1016/j.soilbio.2019.05.015 Received 23 March 2019; Received in revised form 11 May 2019; Accepted 16 May 2019 Available online 17 May 2019 0038-0717/ © 2019 Elsevier Ltd. All rights reserved.
Soil Biology and Biochemistry 135 (2019) 248–250
A. Frew
fungal species but were greatest in response to four mycorrhizal species. For example, under low P, a single AM fungal species increased biomass by 10.2%, which increased by 16.3% when inoculated with four AM fungal species (Fig. 1a). A similar step-wise response was observed in P concentrations and in foliar C: P and N: P ratios to increasing AM fungal diversity (Fig. 1b; Figs. S1a and b; Table S1). Mycorrhizal root colonisation of S. bicolor reflected these responses, with more colonisation in plants inoculated with four AM fungal species than plants inoculated with a single species (Fig. 1c and d; Table S2). Single plant species are known to increase productivity in response to increasing AM fungal diversity, and different mycorrhizal fungi are known to provide different growth and nutritional outcomes for their hosts (Bennett and Bever, 2007; Jansa et al., 2008; Maherali and Klironomos, 2007). Here, it is likely that higher AM fungal diversity increased the opportunities for plants to associate with effective fungal partners. Indeed, functional complementarity between AM fungal species has also been shown where simultaneous associations with multiple species can synergistically enhance P uptake and plant growth (Jansa et al., 2008). In contrast to S. bicolor, there was no additional benefit from increasing AM fungal diversity (four AM fungal species treatment) to Z. mays, although the plants responded positively to AM fungi overall (Fig. 1a and b). Mycorrhizal colonisation of Z. mays was similar under the single and multiple AM fungal species treatments (Fig. 1c and d; Table S2). Thus, for Z. mays, the single AM fungal species (R. irregularis) may be the most efficient partner, and increasing the pool of potential symbiotic partners provided no added benefit. Indeed, mycorrhizal priority effects have previously been shown, where early colonising fungi can effectively suppress subsequent colonisers (Werner and Kiers, 2015). Therefore here, early colonisation by R. irregularis, which can be a fast coloniser, may have prevented other fungi from forming associations (Werner and Kiers, 2015). Of the two C3 plants, only H. vulgare showed significant responses to AM fungi where, in a low P environment, the combination of four mycorrhizal species increased foliar P concentrations by 22.8%, compared to the non-mycorrhizal plants (Fig. 1b; Table S1). Interestingly, arbuscular colonisation (presence of AM fungal arbuscular structures) by the four AM fungal species was greater than the single species (Fig. 1d). Furthermore, although AM fungal effects were not significant (P = 0.08), the aboveground biomass of H. vulgare in low P was increasing in response to four AM fungal species (Fig. 1a). The responsiveness of H. vulgare, a C3 crop, to higher diversity may also be attributed to greater opportunity for plants to find an effective mycorrhizal partner. Contrastingly, T. aestivum did not exhibit significant biomass or nutrient responses to AM fungi, regardless of the diversity (Fig. 1a and b; Fig. S1); although, there were strong positive responses to the P addition. C3 plants are typically less responsive to AM fungi, and negative outcomes (growth depression and defence reduction) have been reported in both T. aesitvum and H. vulgare (Elsen et al., 2008; Frew et al., 2018; Grace et al., 2009; Ryan and Kirkegaard, 2012). The results from this study suggest that increasing AM fungal diversity can provide growth and nutritional benefits to both C3 and C4 host plants, however the identity of the host plant is an important determinant. Among the C3 plants, H. vulgare had a clear benefit from high AM fungal diversity (four AM fungal species), but was unaffected by inoculation with R. irregularis alone. Meanwhile, T. aestivum did not respond to any AM fungal treatment. Although both C4 plants responded positively to AM fungi, S. bicolor benefitted from increasing AM fungal diversity and had higher colonisation rates, while Z. mays did not. Given these results, assessment of the individual effects of each AM fungal species used here, along with a variety of species combinations, may determine the AM fungal species-specific and community composition-specific effects on C3 and C4 hosts. Research to date has made considerable progress in our understanding of the importance of AM fungal diversity to plant productivity and community structure (van der Heijden et al., 1998). Although the
Fig. 1. Effects of phosphorus treatments on the (a) aboveground biomass (g) and (b) foliar phosphorus concentrations (mg g−1) of two C3 plant species Triticum aestivum and Hordeum vulgare and two C4 plant species Sorghum bicolor and Zea mays, grown with no arbuscular mycorrhizal (AM) fungi, with a single AM fungal species or with four AM fungal species. Effects of phosphorus treatments on the (c) total root colonisation (%) and (d) arbuscular root colonisation (%) of plants with a single AM fungal species or with four AM fungal species.
Supplementary data). The responses of the C3 and C4 plants to the AM fungal treatments were distinct (Fig. 1). C4 species exhibited positive responses to AM fungi, even under the high P environment (Fig. 1a and b). Biomass and foliar P concentrations increased in S. bicolor in response to a single AM 249
Soil Biology and Biochemistry 135 (2019) 248–250
A. Frew
need to consider AM fungal abundance and diversity to maximise crop yield is debated (Ryan and Graham, 2018), there are clear benefits towards enhancing agricultural sustainability (Rillig et al., 2019). Despite variable responses, the results from this study suggest that increasing AM fungal diversity can potentially augment C3 and C4 plant growth and nutrient uptake. However, increasing AM fungal diversity in the soil is not uniformly advantageous to all plants.
genes. New Phytologist 181, 938–949. Hart, M.M., Antunes, P.M., Chaudhary, V.B., Abbott, L.K., 2018. Fungal inoculants in the field: is the reward greater than the risk? Functional Ecology 32, 126–135. Hoeksema, J.D., Chaudhary, V.B., Gehring, C.A., Johnson, N.C., Karst, J., Koide, R.T., Pringle, A., Zabinski, C., Bever, J.D., Moore, J.C., Wilson, G.W.T., Klironomos, J.N., Umbanhowar, J., 2010. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13, 394–407. Jansa, J., Smith, F.A., Smith, S.E., 2008. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytologist 177, 779–789. Johnson, N.C., 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185, 631–647. Johnson, N.C., Graham, J.H., 2013. The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant and Soil 363, 411–419. Keymer, A., Gutjahr, C., 2018. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Current Opinion in Plant Biology, Biotic Interactions 44, 137–144. Maherali, H., Klironomos, J.N., 2007. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316, 1746–1748. Powell, J.R., Rillig, M.C., 2018. Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytologist 220, 1059–1075. Rillig, M.C., 2004. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7, 740–754. Rillig, M.C., Aguilar-Trigueros, C.A., Camenzind, T., Cavagnaro, T.R., Degrune, F., Hohmann, P., Lammel, D.R., Mansour, I., Roy, J., van der Heijden, M.G.A., Yang, G., 2019. Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytologist. https://doi.org/10.1111/nph.15602. Ryan, M.H., Graham, J.H., 2018. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytologist 220, 1092–1107. Ryan, M.H., Kirkegaard, J.A., 2012. The agronomic relevance of arbuscular mycorrhizas in the fertility of Australian extensive cropping systems. Agriculture, Ecosystems & Environment 163, 37–53. Sikes, B.A., Cottenie, K., Klironomos, J.N., 2009. Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. Journal of Ecology 97, 1274–1280. Smith, S.E., Smith, F.A., 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62, 227–250. van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., Sanders, I.R., 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72. Weremijewicz, J., Seto, K., 2016. Mycorrhizas influence functional traits of two tallgrass prairie species. Ecology and Evolution 6, 3977–3990. Werner, G.D.A., Kiers, E.T., 2015. Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytologist 205, 1515–1524.
Data statement Raw data from this study are available upon reasonable request. Acknowledgements This work was supported by a Charles Sturt University Faculty of Science Postdoctoral Research Fellowship awarded to AF. The author would like to thank the technical team at Charles Sturt University for technical support, the three anonymous reviewers and the handling editor for their helpful comments. There are no conflicts of interest to declare. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.soilbio.2019.05.015. References Bennett, A.E., Bever, J.D., 2007. Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88, 210–218. Elsen, A., Gervacio, D., Swennen, R., Waele, D.D., 2008. AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18, 251–256. Frew, A., Powell, J.R., Glauser, G., Bennett, A.E., Johnson, S.N., 2018. Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations. Soil Biology and Biochemistry 126, 123–132. Grace, E.J., Cotsaftis, O., Tester, M., Smith, F.A., Smith, S.E., 2009. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter
250
Contents lists available at ScienceDirect
Soil Biology and Biochemistry journal homepage: www.elsevier.com/locate/soilbio
Short Communication
Arbuscular mycorrhizal fungal diversity increases growth and phosphorus uptake in C3 and C4 crop plants
T
Adam Frewa,b,c,∗ a
School of Agricultural and Wine Sciences, Charles Sturt University, Wagga Wagga, New South Wales, Australia Institute for Land, Water and Society, Charles Sturt University, Albury, New South Wales, Australia c Graham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, New South Wales, Australia b
A R T I C LE I N FO
A B S T R A C T
Keywords: Arbuscular mycorrhizal fungi Microbial diversity Microbial inoculant Phosphorus nutrition Plant functional group
Most plants associate with arbuscular mycorrhizal (AM) fungi which can enhance their growth and nutrient uptake. Outcomes of the AM symbiosis can be highly variable, depending on soil fertility, plant functional group (C3, C4) and AM fungal diversity. This study assessed the growth and nutrient (C, N, P) responses of two C3 (Triticum aestivum and Hordeum vulgare) and two C4 (Sorghum bicolor and Zea mays) plants to different AM fungal inocula (no AM fungi, single AM fungal species, and four AM fungal species) under high and low P conditions. Higher AM fungal diversity resulted in greater P concentration and aboveground biomass of H. vulgare and S. bicolor. Triticum aestivum did not respond to AM fungi, while Z. mays responded positively but a similar positive response of Z. mays growth and nutrition occured when it was colonised with single or multiple AM fungal species. These findings suggest that, although C3 crop plants are less responsive to AM fungi than C4, some C3 and C4 species can benefit from higher AM fungal diversity in the soil.
The vast majority of terrestrial plants form associations with coevolved soil-dwelling fungi of the Glomeromycota known as arbuscular mycorrhizal (AM) fungi. These fungi colonise plant roots and provide their hosts with access to soil resources (phosphorus (P), nitrogen (N) and water) while plants provide the fungi with carbon (C) in the form of sugars and lipids (Keymer and Gutjahr, 2018; Smith and Smith, 2011). As such, the AM symbiosis is a key component of ecosystems, maintaining plant productivity and ecosystem stability (Powell and Rillig, 2018; Rillig, 2004). However, the outcomes of the AM symbiosis for plants can be highly variable (Hoeksema et al., 2010), and are known to be strongly driven by soil nutrient (P and N) availability (Johnson, 2010). When P is limiting in the environment, plants often benefit from the AM symbiosis, conversely when P is abundant there can be little benefit or even negative outcomes for plants (Johnson and Graham, 2013). Outcomes for host plants can depend on plant and fungal identities. For example, C4 plants often benefit more from AM fungal associations than C3 plants, partly due to their higher photosynthetic efficiency and greater nutrient demands (Hoeksema et al., 2010). Meanwhile the ability of AM fungi to provide a growth, nutrient or defence benefit to their host can also vary between fungal taxa. For example, some taxa may be more associated with enhanced plant growth and nutrient uptake, with others are more associated with enhanced plant defence
∗
against herbivory (Bennett and Bever, 2007; Sikes et al., 2009). There has been a long-held interest in employing the mycorrhizal symbiosis in sustainable plant production, but the efficacy and variability in responses remains a significant challenge (Hart et al., 2018; Rillig et al., 2019). Our understanding of the variation in plant growth and nutritional responses between C3 and C4 species to AM fungal diversity remains ambiguous. Yet, it is a key step towards effectively using the AM symbiosis in agriculture. Using a factorial pot experiment, I assessed differences in the growth, nutrient status and AM fungal colonisation of two economically significant C3 species (Triticum aestivum L., Hordeum vulgare L.) and two C4 species (Sorghum bicolor L. Moench, Zea mays L.) grown for eight weeks without AM fungi, with a single AM fungal species (Rhizophagus irregularis (Błaszk., Wubet, Renker & Buscot) C. Walker & A. Schüßler), or with a community of four AM fungal species (Claroideoglomus etunicatum (W. N. Becker & Gerd.) C. Walker & A. Schüßler, Funneliformis coronatum (Giovann.) C. Walker & A. Schüßler, F. mosseae (T. H. Nicolson & Gerd.) C. Walker & A. Schüßler, and Rhizophagus irregularis), under low (13 mg kg-1 plant available P) or high P soil (addition of 80mL 32µg g-1 soluble P) (Weremijewicz and Seto, 2016). Plants were harvested from their pots, aboveground biomass recorded, foliar and root samples were taken for nutrient analysis and mycorrhizal colonisation assessment, respectively (for methodological details see
Charles Sturt University, Building 286, Wagga Wagga, New South Wales, 2678, Australia. E-mail address: [email protected].
https://doi.org/10.1016/j.soilbio.2019.05.015 Received 23 March 2019; Received in revised form 11 May 2019; Accepted 16 May 2019 Available online 17 May 2019 0038-0717/ © 2019 Elsevier Ltd. All rights reserved.
Soil Biology and Biochemistry 135 (2019) 248–250
A. Frew
fungal species but were greatest in response to four mycorrhizal species. For example, under low P, a single AM fungal species increased biomass by 10.2%, which increased by 16.3% when inoculated with four AM fungal species (Fig. 1a). A similar step-wise response was observed in P concentrations and in foliar C: P and N: P ratios to increasing AM fungal diversity (Fig. 1b; Figs. S1a and b; Table S1). Mycorrhizal root colonisation of S. bicolor reflected these responses, with more colonisation in plants inoculated with four AM fungal species than plants inoculated with a single species (Fig. 1c and d; Table S2). Single plant species are known to increase productivity in response to increasing AM fungal diversity, and different mycorrhizal fungi are known to provide different growth and nutritional outcomes for their hosts (Bennett and Bever, 2007; Jansa et al., 2008; Maherali and Klironomos, 2007). Here, it is likely that higher AM fungal diversity increased the opportunities for plants to associate with effective fungal partners. Indeed, functional complementarity between AM fungal species has also been shown where simultaneous associations with multiple species can synergistically enhance P uptake and plant growth (Jansa et al., 2008). In contrast to S. bicolor, there was no additional benefit from increasing AM fungal diversity (four AM fungal species treatment) to Z. mays, although the plants responded positively to AM fungi overall (Fig. 1a and b). Mycorrhizal colonisation of Z. mays was similar under the single and multiple AM fungal species treatments (Fig. 1c and d; Table S2). Thus, for Z. mays, the single AM fungal species (R. irregularis) may be the most efficient partner, and increasing the pool of potential symbiotic partners provided no added benefit. Indeed, mycorrhizal priority effects have previously been shown, where early colonising fungi can effectively suppress subsequent colonisers (Werner and Kiers, 2015). Therefore here, early colonisation by R. irregularis, which can be a fast coloniser, may have prevented other fungi from forming associations (Werner and Kiers, 2015). Of the two C3 plants, only H. vulgare showed significant responses to AM fungi where, in a low P environment, the combination of four mycorrhizal species increased foliar P concentrations by 22.8%, compared to the non-mycorrhizal plants (Fig. 1b; Table S1). Interestingly, arbuscular colonisation (presence of AM fungal arbuscular structures) by the four AM fungal species was greater than the single species (Fig. 1d). Furthermore, although AM fungal effects were not significant (P = 0.08), the aboveground biomass of H. vulgare in low P was increasing in response to four AM fungal species (Fig. 1a). The responsiveness of H. vulgare, a C3 crop, to higher diversity may also be attributed to greater opportunity for plants to find an effective mycorrhizal partner. Contrastingly, T. aestivum did not exhibit significant biomass or nutrient responses to AM fungi, regardless of the diversity (Fig. 1a and b; Fig. S1); although, there were strong positive responses to the P addition. C3 plants are typically less responsive to AM fungi, and negative outcomes (growth depression and defence reduction) have been reported in both T. aesitvum and H. vulgare (Elsen et al., 2008; Frew et al., 2018; Grace et al., 2009; Ryan and Kirkegaard, 2012). The results from this study suggest that increasing AM fungal diversity can provide growth and nutritional benefits to both C3 and C4 host plants, however the identity of the host plant is an important determinant. Among the C3 plants, H. vulgare had a clear benefit from high AM fungal diversity (four AM fungal species), but was unaffected by inoculation with R. irregularis alone. Meanwhile, T. aestivum did not respond to any AM fungal treatment. Although both C4 plants responded positively to AM fungi, S. bicolor benefitted from increasing AM fungal diversity and had higher colonisation rates, while Z. mays did not. Given these results, assessment of the individual effects of each AM fungal species used here, along with a variety of species combinations, may determine the AM fungal species-specific and community composition-specific effects on C3 and C4 hosts. Research to date has made considerable progress in our understanding of the importance of AM fungal diversity to plant productivity and community structure (van der Heijden et al., 1998). Although the
Fig. 1. Effects of phosphorus treatments on the (a) aboveground biomass (g) and (b) foliar phosphorus concentrations (mg g−1) of two C3 plant species Triticum aestivum and Hordeum vulgare and two C4 plant species Sorghum bicolor and Zea mays, grown with no arbuscular mycorrhizal (AM) fungi, with a single AM fungal species or with four AM fungal species. Effects of phosphorus treatments on the (c) total root colonisation (%) and (d) arbuscular root colonisation (%) of plants with a single AM fungal species or with four AM fungal species.
Supplementary data). The responses of the C3 and C4 plants to the AM fungal treatments were distinct (Fig. 1). C4 species exhibited positive responses to AM fungi, even under the high P environment (Fig. 1a and b). Biomass and foliar P concentrations increased in S. bicolor in response to a single AM 249
Soil Biology and Biochemistry 135 (2019) 248–250
A. Frew
need to consider AM fungal abundance and diversity to maximise crop yield is debated (Ryan and Graham, 2018), there are clear benefits towards enhancing agricultural sustainability (Rillig et al., 2019). Despite variable responses, the results from this study suggest that increasing AM fungal diversity can potentially augment C3 and C4 plant growth and nutrient uptake. However, increasing AM fungal diversity in the soil is not uniformly advantageous to all plants.
genes. New Phytologist 181, 938–949. Hart, M.M., Antunes, P.M., Chaudhary, V.B., Abbott, L.K., 2018. Fungal inoculants in the field: is the reward greater than the risk? Functional Ecology 32, 126–135. Hoeksema, J.D., Chaudhary, V.B., Gehring, C.A., Johnson, N.C., Karst, J., Koide, R.T., Pringle, A., Zabinski, C., Bever, J.D., Moore, J.C., Wilson, G.W.T., Klironomos, J.N., Umbanhowar, J., 2010. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13, 394–407. Jansa, J., Smith, F.A., Smith, S.E., 2008. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytologist 177, 779–789. Johnson, N.C., 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185, 631–647. Johnson, N.C., Graham, J.H., 2013. The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant and Soil 363, 411–419. Keymer, A., Gutjahr, C., 2018. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Current Opinion in Plant Biology, Biotic Interactions 44, 137–144. Maherali, H., Klironomos, J.N., 2007. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316, 1746–1748. Powell, J.R., Rillig, M.C., 2018. Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytologist 220, 1059–1075. Rillig, M.C., 2004. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7, 740–754. Rillig, M.C., Aguilar-Trigueros, C.A., Camenzind, T., Cavagnaro, T.R., Degrune, F., Hohmann, P., Lammel, D.R., Mansour, I., Roy, J., van der Heijden, M.G.A., Yang, G., 2019. Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytologist. https://doi.org/10.1111/nph.15602. Ryan, M.H., Graham, J.H., 2018. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytologist 220, 1092–1107. Ryan, M.H., Kirkegaard, J.A., 2012. The agronomic relevance of arbuscular mycorrhizas in the fertility of Australian extensive cropping systems. Agriculture, Ecosystems & Environment 163, 37–53. Sikes, B.A., Cottenie, K., Klironomos, J.N., 2009. Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. Journal of Ecology 97, 1274–1280. Smith, S.E., Smith, F.A., 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62, 227–250. van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., Sanders, I.R., 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72. Weremijewicz, J., Seto, K., 2016. Mycorrhizas influence functional traits of two tallgrass prairie species. Ecology and Evolution 6, 3977–3990. Werner, G.D.A., Kiers, E.T., 2015. Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytologist 205, 1515–1524.
Data statement Raw data from this study are available upon reasonable request. Acknowledgements This work was supported by a Charles Sturt University Faculty of Science Postdoctoral Research Fellowship awarded to AF. The author would like to thank the technical team at Charles Sturt University for technical support, the three anonymous reviewers and the handling editor for their helpful comments. There are no conflicts of interest to declare. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.soilbio.2019.05.015. References Bennett, A.E., Bever, J.D., 2007. Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88, 210–218. Elsen, A., Gervacio, D., Swennen, R., Waele, D.D., 2008. AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18, 251–256. Frew, A., Powell, J.R., Glauser, G., Bennett, A.E., Johnson, S.N., 2018. Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations. Soil Biology and Biochemistry 126, 123–132. Grace, E.J., Cotsaftis, O., Tester, M., Smith, F.A., Smith, S.E., 2009. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter
250