Abstract
The abiotic environment can dictate the relative costs and benefits of plant-arbuscular mycorrhizal fungi (AMF) symbioses. While the effects of varying light or soil nutrient conditions are well studied, outcomes of plant-AMF interactions along soil moisture gradients are not fully understood. It is predicted that mycorrhizal associations may become parasitic in extreme soil moisture conditions. Under low soil moisture stress, costs of maintaining a mycorrhizal symbiont may outweigh benefits for the host plant, whereas under high soil moisture stress, the host plant may not need the symbiont. In a factorial growth chamber study, we investigated the effects of a plant-arbuscular mycorrhizal fungus symbiosis along a soil moisture gradient on growth, cell wall chemistry, and root architecture of a biofuel crop, Panicum virgatum (switchgrass). Regardless of soil moisture conditions, we found an increase in the number of tillers, number of leaves, root biomass, and amount of cellulose and hemicellulose in response to root colonization by the arbuscular mycorrhizal fungus. The fungus also increased aboveground biomass and changed several root architectural traits, but only under low soil moisture conditions, indicating a reduction in benefits of the mycorrhizal association under high soil moisture. Results from this study indicate that an arbuscular mycorrhizal fungus can increase some key measures of plant growth and cell wall chemistry regardless of soil moisture conditions but is most beneficial in low soil moisture conditions.
References
Alam SM (1999) Nutrient uptake by plants under stress conditions. Handbook of Plant and Crop Stress 2:285–313
Alderson J, Sharp W (1994) Grass varieties in the United States. Agricultural Handbook No. 170. Soil Conserv. Serv., USDA, Washington, DC
Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press
Anderson R, Liberta A, Dickman L (1984) Interaction of vascular plants and vesicular-arbuscular mycorrhizal fungi across a soil moisture-nutrient gradient. Oecologia 64:111–117
ANKOM200 (2016) Technical Support Fiber Analyzer A200. https://www.ankom.com/technical-support/fiber-analyzer-a200. Accessed 01/24/2020 2020
Asrar A, Abdel-Fattah G, Elhindi K (2012) Improving growth, flower yield, and water relations of snapdragon (Antirrhinum majus L.) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica 50:305–316
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958
Balestrini R, Bonfante P (2005) The interface compartment in arbuscular mycorrhizae: a special type of plant cell wall? Plant Biosystems 139:8–15
Baslam M, Garmendia I, Goicoechea N (2011) Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse-grown lettuce. J Agric Food Chemistry 59:5504–5515
Bennett AE, Grussu D, Kam J, Caul S, Halpin C (2015) Plant lignin content altered by soil microbial community. New Phytol 206:166–174
Bonfante-Fasolo P, Vian B, Perotto S, Faccio A, Knox JP (1990) Cellulose and pectin localization in roots of mycorrhizal Allium porrum: labelling continuity between host cell wall and interfacial material. Planta 180:537
Brejda JJ, Yocom D, Moser LE, Waller SS (1993) Dependence of 3 Nebraska Sandhills warm-season grasses on vesicular-arbuscular mycorrhizae. J Range Manage 46:14-20
Campbell Scientific (2020) HydroSense II Handheld Soil Moisture Sensor. https://www.campbellsci.com/hs2. Accessed 01/24/2020
Carnicer J, Coll M, Ninyerola M, Pons X, Sanchez G, Penuelas J (2011) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc Natl Academy Sci 108:1474–1478
Castellanos-Morales V, Villegas J, Wendelin S, Vierheilig H, Eder R, Cárdenas-Navarro R (2010) Root colonisation by the arbuscular mycorrhizal fungus Glomus intraradices alters the quality of strawberry fruits (Fragaria× ananassa Duch.) at different nitrogen levels. J Sci Food Agric 90:1774–1782
Chen XW, Kang Y, San So P, Ng CWW, Wong MH (2018) Arbuscular mycorrhizal fungi increase the proportion of cellulose and hemicellulose in the root stele of vetiver grass. Plant Soil 425:309–319
Clark R, Baligar V, Zobel R (2005) Response of mycorrhizal switchgrass to phosphorus fractions in acidic soil. Commun Soil Sci Plant Anal 36:1337–1359
Clark R, Zeto S, Zobel R (1999) Arbuscular mycorrhizal fungal isolate effectiveness on growth and root colonization of Panicum virgatum in acidic soil. Soil Biol Biochem 31:1757–1763
Detering S, Dettmann S, Thierfelder H, Mahna SK, Prasad B, Shamseldin AY, Werner D (2005) Glycosidase and glycosyltransferase activity increase in arbuscular mycorrhiza infected legume roots. Symbiosis 40:157–162
Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Application of in vitro methods to study carbon uptake and transport by AM fungi. Plant Soil 226:255–261
Earl HJ (2003) A precise gravimetric method for simulating drought stress in pot experiments. Crop Sci 43:1868–1873
Emery SM, Gross KL (2007) Dominant species identity, not community evenness, regulates invasion in experimental grassland plant communities. Ecology 88(4):954–964
Emery SM, Reid ML, Bell-Dereske L, Gross KL (2017) Soil mycorrhizal and nematode diversity vary in response to bioenergy crop identity and fertilization. Gcb Bioenergy 9:1644–1656
Emery SM, Rudgers JA (2012) Impact of competition and mycorrhizal fungi on growth of Centaurea stoebe, an invasive plant of sand dunes. Am Midl Nat 167(2):213–222
Fan L, Linker R, Gepstein S, Tanimoto E, Yamamoto R, Neumann PM (2006) Progressive inhibition by water deficit of cell wall extensibility and growth along the elongation zone of maize roots is related to increased lignin metabolism and progressive stelar accumulation of wall phenolics. Plant Physiol 140:603–612
Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987
Ganz T, Kailis S, Abbott L (2002) Mycorrhizal colonization and its effect on growth, phosphorus uptake and tissue phenolic content in the European olive (Olea europaea L.) Adv Horticult Sci:109–116
He C, Wolyn D (2005) Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f. sp. Asparagi. Plant Pathol 54:227-232Z
Hetrick BD, Leslie J, Wilson GT, Kitt DG (1988) Physical and topological assessment of effects of a vesicular–arbuscular mycorrhizal fungus on root architecture of big bluestem. New Phytol 110:85–96
Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187
Jayne B, Quigley M (2014) Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza 24:109–119
Johnson NC, Graham J, Smith F (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585
Jung HJG, Vogel KP (1992) Lignification of switchgrass (Panicum virgatum) and big bluestem (Andropogon gerardii) plant parts during maturation and its effect on fibre degradability. J Sci Food Agric 59:169–176
Lee BR, Muneer S, Jung WJ, Avice JC, Ourry A, Kim TH (2012) Mycorrhizal colonization alleviates drought-induced oxidative damage and lignification in the leaves of drought-stressed perennial ryegrass (Lolium perenne). Physiologia Plant 145:440–449
Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops- a meta-analysis. Soil Biol Biochem 81:147–158
Lipiec J, Doussan C, Nosalewicz A, Kondracka K (2013) Effect of drought and heat stresses on plant growth and yield: a review. International Agrophysics 27:463–477
Marulanda A, Barea J-M, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regulation 28:115–124
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol 115:495–501
Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997
Miller SP (2000) Arbuscular mycorrhizal colonization of semi-aquatic grasses along a wide hydrologic gradient. New Phytol 145:145–155
Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant 134:237–245
Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant Soil 185:241–251
Morrow WR III, Gopal A, Fitts G, Lewis S, Dale L, Masanet E (2014) Feedstock loss from drought is a major economic risk for biofuel producers. Biomass Bioenergy 69:135–143
Nilsen P, Børja I, Knutsen H, Brean R (1998) Nitrogen and drought effects on ectomycorrhizae of Norway spruce Picea abies L. (Karst.). Plant Soil 198:179–184
Oláh B, Brière C, Bécard G, Dénarié J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signaling pathway. The Plant J 44:195–207
Olsson PA, Rahm J, Aliasgharzad N (2010) Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol Ecol 72:125–131
Paracer S, Ahmadjian V (2000) Symbiosis: an introduction to biological associations. Oxford University Press on Demand
Rich MK, Schorderet M, Reinhardt D (2014) The role of the cell wall compartment in mutualistic symbioses of plants. Front Plant Sci 5:238
Rubin EM (2008) Genomics of cellulosic biofuels Nat 454:841–845
Runion G, Mitchell R, Rogers H, Prior S, Counts T (1997) Effects of nitrogen and water limitation and elevated atmospheric CO2 on ectomycorrhiza of longleaf pine. New Phytol 137:681–689
Schouteden N, Waele DD, Panis B, Vos CM (2015) Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6:1280
Schravendijk HW, Van Andel OM (1985) Interdependence of growth, water relations and abscisic acid level in Phaseolus vulgaris during waterlogging. Physiol Plant 63(2):215–220
Secilia J, Bagyaraj D (1992) Selection of efficient vesicular-arbuscular mycorrhizal fungi for wetland rice (Oryza sativa L.). Biol Fertil Soils 13:108–111
Smith FA, Smith SE (2013) How useful is the mutualism-parasitism continuum of arbuscular mycorrhizal functioning? Plant Soil 363:7–18
Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic press
Swaty RL, Gehring CA, Van Ert M, Theimer TC, Keim P, Whitham TG (1998) Temporal variation in temperature and rainfall differentially affects ectomycorrhizal colonization at two contrasting sites. New Phytol 139:733–739
Team R Core (2017) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria URL https://www.R-project.org
Thorne MA, Frank DA (2009) The effects of clipping and soil moisture on leaf and root morphology and root respiration in two temperate and two tropical grasses. Plant Ecol 200:205–215
Valdes M, Asbjornsen H, Gómez-Cárdenas M, Juarez M, Vogt K (2006) Drought effects on fine roots and ectomycorrhizal-root biomass in managed Pinus oaxacana Mirov stands in Oaxaca, Mexico. Mycorrhiza 16:117–124
Van Soest P, Robertson J (1979) Systems of analysis for evaluating fibrous feeds. In: Standardization of analytical methodology for feeds: Proc. of a Workshop IDRC, Ottawa, ON, CA
Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22:227–235
Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiologia Plant 125:393–404
Vincent C, Rowland D, Na C, Schaffer B (2017) A high-throughput method to quantify root hair area in digital images taken in situ. Plant Soil 412:61–80
Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209
Wang Y, Qiu Q, Yang Z, Hu Z, Tam NF-Y, Xin G. (2010) Arbuscular mycorrhizal fungi in two mangroves in South China. Plant Soil 331:181–191
Wirsel SG (2004) Homogenous stands of a wetland grass harbour diverse consortia of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 48:129–138
Wolf DD, Fiske DA (2009) Planting and managing switchgrass for forage, wildlife and conservation. Virginia Cooperative Extension 418:013
Wu Q-S, Xia R-X (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425
Yao Q, Wang L, Zhu H, Chen J (2009) Effect of arbuscular mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Sci Hortic 121:458–461
Zhang R-Q, Zhu H-H, Zhao H-Q, Yao Q (2013) Arbuscular mycorrhizal fungal inoculation increases phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signaling pathways. J Plant Physiol 170:74–79
Zou Y-N, Wang P, Liu C-Y, Ni Q-D, Zhang D-J, Wu Q-S (2017) Mycorrhizal trifoliate orange has greater root adaptation of morphology and phytohormones in response to drought stress. Scientific Reports 7:1–10
Zwiazek JJ (1991) Cell wall changes in white spruce (Picea glauca) needles subjected to repeated drought stress. Physiologia Plant 82:513–518
Acknowledgments
We would like to thank Heather Griffith, Aaron Sexton, Kylea Garces, and Kimberly Koenig for various assistance in the lab. We also would like to thank Dr. David Harmon from the Ruminant Nutrition Lab, University of Kentucky for providing lab space and instruments to perform fiber analyses. Finally, we would like to thank Dr. Dave Janos and two anonymous reviewers who provided constructive comments which greatly improved our manuscript.
Funding
Funding for this study was provided by the Kentucky Academy of Science.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Basyal, B., Emery, S.M. An arbuscular mycorrhizal fungus alters switchgrass growth, root architecture, and cell wall chemistry across a soil moisture gradient. Mycorrhiza 31, 251–258 (2021). https://doi.org/10.1007/s00572-020-00992-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-020-00992-6