Abstract
Aims
Arbuscular mycorrhizal (AM) fungi have been found to increase plant biomass, cellulose content, and the associated root biomechanical properties, but little is known about how AM fungi affect the in situ root decay process in terms of the changes in the chemical and biomechanical properties.
Methods
In this study, we inoculated AM fungi to Bermuda grass (Cynodon dactylon L.) and measured the biomass, the contents of cellulose and lignin, and the biomechanical properties, including tensile strength and Young’s modulus of the grass roots as they grew for 180 days and then decayed for 360 days after burning or for 60 days after the herbicide application.
Results
Results show that the AM fungi accelerated the accumulation of grass biomass and root cellulose content compared with non-mycorrhizal grass during the growth period. This effect of AM fungi made mycorrhizal grass generally maintained more biomass and cellulose content than non-mycorrhizal grass at every decaying stage. Inoculation of the AM fungi did not significantly change the root tensile strength or Young’s modulus, but it altered the correlations between tensile strength and root diameter, and Young’s modulus and root diameter. Mycorrhizal effects during the root decaying process appeared to diminish under herbicide treatment, compared with normal growth and burning treatments.
Conclusion
Our study highlights the important role of AM fungi in maintaining in situ root biomass (a proxy for carbon content) from decaying or decomposing.
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References
Apriyono A, Yuliana, Kamchoom V (2022) Serviceability of cut slope and embankmentunder seasonal climate variations. Acta Geophysica 1-13. https://doi.org/10.1007/s11600-022-00953-x
Augé RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97. https://doi.org/10.1023/A:1004891210871
Basyal B, Emery SM (2021) An arbuscular mycorrhizal fungus alters switchgrass growth, root architecture, and cell wall chemistry across a soil moisture gradient. Mycorrhiza 31:251–258. https://doi.org/10.1007/s00572-020-00992-6
Beidler KV, Pritchard SG (2017) Maintaining connectivity: understanding the role of root order and mycelial networks in fine root decomposition of woody plants. Plant Soil 420:19–36. https://doi.org/10.1007/s11104-017-3393-8
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. https://doi.org/10.1038/ncomms1046
Burgert I (2006) Exploring the micromechanical design of plant cell walls. Am J Bot 93:1391–1401. https://doi.org/10.3732/ajb.93.10.1391
Burylo M, Rey F, Bochet E, Dutoit T (2012) Plant functional traits and species ability for sediment retention during concentrated flow erosion. Plant and Soil 353:135–144
Chen XW, Kang Y, So PS et al (2018) Arbuscular mycorrhizal fungi increase the proportion of cellulose and hemicellulose in the root stele of vetiver grass. Plant Soil 425:309–319. https://doi.org/10.1007/s11104-018-3583-z
Chen XW, Wu L, Luo N et al (2019) Arbuscular mycorrhizal fungi and the associated bacterial community influence the uptake of cadmium in rice. Geoderma 337:749–757. https://doi.org/10.1016/j.geoderma.2018.10.029
Chen XW, Wong JTF, Wang JJ et al (2021) Effects of mycorrhizal Bermuda grass on low-range soil matric suction. J Soils Sediments 21:990–1000. https://doi.org/10.1007/s11368-020-02839-1
Cobb AH, Reade JPH (2010) Herbicides and Plant Physiology, 2nd edn. Wiley-Blackwell, Chichester, West Sussex; Ames, Iowa
Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328:307–317. https://doi.org/10.1016/S0022-2836(03)00307-3
De Baets S, Poesen J, Reubens B, Wemans K, De Baerdemaeker J, Muys B (2008) Root tensile strength and root distribution of typical Mediterranean plant species and their contribution to soil shear strength. Plant and soil 305:207–226
Detering S, Dettmann S, Thierfelder H et al (2005) Glycosidase and glycosyltransferase activity increase in arbuscular mycorrhiza infected legume roots. Symbiosis 40:157–162
Dumlao MR, Ramananarivo S, Goyal V et al (2015) The role of root development of Avena fatua in conferring soil strength. Am J Bot 102:1050–1060. https://doi.org/10.3732/ajb.1500028
Emmett BD, Lévesque-Tremblay V, Harrison MJ (2021) Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME J 15:2276–2288. https://doi.org/10.1038/s41396-021-00920-2
Faucette LB, Risse LM, Jordan CF, Cabrera ML, Coleman DC, West LT (2006) Vegetation and soil quality effects from hydroseed and compost blankets used for erosion control in construction activities. J Soil Water Conserv 61(6):355–362
Fedtke C (2011) Biochemistry and Physiology of Herbicide Action. Softcover reprint of the original 1st ed. 1982 edition. Springer
Fiorilli V, Catoni M, Miozzi L et al (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987. https://doi.org/10.1111/j.1469-8137.2009.03031.x
Genet M, Stokes A, Salin F et al (2005) The influence of cellulose content on tensile strength in tree roots. Plant Soil 278:1–9. https://doi.org/10.1007/s11104-005-8768-6
Giovannetti M, Mosse B (1980) An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots. New Phytologist 84(3):489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Greenwood JR, Norris JE, Wint J (2004) Assessing the contribution of vegetation to slope stability. Proc Institution Civil Engr - Geotech Eng 157(4):199–207. https://doi.org/10.1680/geng.2004.157.4.199
Guether M, Balestrini R, Hannah M et al (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182:200–212. https://doi.org/10.1111/j.1469-8137.2008.02725.x
Gutjahr C, Sawers RJH, Marti G et al (2015) Transcriptome diversity among rice root types during asymbiosis and interaction with arbuscular mycorrhizal fungi. Proc Natl Acad Sci U S A 112:6754–6759. https://doi.org/10.1073/pnas.1504142112
Harrier LA, Watson CA (2004) The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest Manag Sci: Formerly Pesticide Sci 60(2):149–157
Hathaway RL, Penny D (1975) Root Strength in Some Populus and Salix Clones. New Zealand J Botany 13(3):333–344. https://doi.org/10.1080/0028825X.1975.10430330
Higuera PE, Shuman BN, Wolf KD (2021) Rocky Mountain subalpine forests now burning more than any time in recent millennia. Proc Natl Acad Sci 118:e2103135118. https://doi.org/10.1073/pnas.2103135118
Hoagland RE, Norsworthy JK, Carey F, Talbert RE (2004) Metabolically based resistance to the herbicide propanil in Echinochloa species. Weed Sci 52:475–486. https://doi.org/10.1614/WS-03-039R
Hoeksema JD, Chaudhary VB, Gehring CA et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x
Hooker JE, Black KE, Perry RL, Atkinson D (1995) Arbuscular mycorrhizal fungi induced alteration to root longevity of poplar. Plant and Soil 172(2):327–329
Jiang Y, Wang W, **e Q et al (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–1175. https://doi.org/10.1126/science.aam9970
Jiang L, Wang H, Li S et al (2021) Mycorrhizal and environmental controls over root trait–decomposition linkage of woody trees. New Phytol 229:284–295. https://doi.org/10.1111/nph.16844
Kamchoom V, Jotisankasa A (2019) Effect of root growth on slope hydrology and stability during early plant establishment. 16th Asian Regional Conference on Soil Mechanics and Geotecnical Engineering,Taipei, Taiwan
Kamchoom V, Leung AK (2018) Hydro-mechanical reinforcements of live poles to slope stability. Soils Foundations 58(6):1423–1434. https://doi.org/10.1016/j.sandf.2018.08.003
Kamchoom V, Boldrin D, Leung AK, Sookkrajang C, Likitlersuang S (2021) Biomechanical properties of the growing and decaying roots of Cynodon dactylon. Plant and Soil 471:193–210. https://doi.org/10.1007/s11104-021-05207-1
Kamchoom V, Leung AK, Boldrin D, Sakolpanya T, Wu Z, Likitlersuang S (2022) Shearing behaviour of vegetated soils with growing and decaying roots. Can Geotech J. https://doi.org/10.1139/cgj-2021-0695
Kong D, Wang J, Yang F, Shao P (2018) Rhizosheaths stimulate short-term root decomposition in a semiarid grassland. Sci Total Environ 640–641:1297–1301. https://doi.org/10.1016/j.scitotenv.2018.05.398
Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84:2302–2312. https://doi.org/10.1890/02-0282
Langley JA, Chapman SK, Hungate BA (2006) Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecol Lett 9:955–959. https://doi.org/10.1111/j.1461-0248.2006.00948.x
Leavitt SW, Danzer SR (1993) Method for Batch Processing Small Wood Samples to Holocellulose for Stable-Carbon Isotope Analysis. Anal Chem 65:87–89. https://doi.org/10.1021/ac00049a017
Leifheit EF, Veresoglou SD, Lehmann A et al (2013) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil 347:523–537. https://doi.org/10.1007/s11104-013-1899-2
Leung HM, Ye ZH, Wong MH (2007) Survival strategies of plants associated with arbuscular mycorrhizal fungi on toxic mine tailings. Chemosphere 66:905–915. https://doi.org/10.1016/j.chemosphere.2006.06.037
Leys BA, Marlon JR, Umbanhowar C, Vannière B (2018) Global fire history of grassland biomes. Ecol Evol 8:8831–8852. https://doi.org/10.1002/ece3.4394
Liu J, Blaylock LA, Endre G et al (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123. https://doi.org/10.1105/tpc.014183
Loades KW, Bengough AG, Bransby MF, Hallett PD (2013) Biomechanics of nodal, seminal and lateral roots of barley: effects of diameter, waterlogging and mechanical impedance. Plant Soil 370(1–2):407–418. https://doi.org/10.1007/s11104-013-1643-y
Loades KW, Bengough AG, Bransby MF, Hallett PD (2015) Effect of root age on the biomechanics of seminal and nodal roots of barley (Hordeum vulgare L.) in contrasting soil environments. Plant Soil 395:253–261. https://doi.org/10.1007/s11104-015-2560-z
Mamy L, Barriuso E, Gabrielle B (2016) Glyphosate fate in soils when arriving in plant residues. Chemosphere 154:425–433. https://doi.org/10.1016/j.chemosphere.2016.03.104
Mickovski SB, Ennos AR (2003) The effect of unidirectional stem flexing on shoot and root morphology and architecture in young Pinus sylvestris trees. Can J Forest Res 33(11):2202–2209. https://doi.org/10.1139/x03-139
Mickovski SB, Bengough AG, Bransby MF, Davies MCR, Hallett PD, Sonnenberg R (2007) Material stiffness, branching pattern and soil matric potential affect the pullout resistance of model root systems. Eur J Soil Sci 58(6):1471–1481. https://doi.org/10.1111/j.1365-2389.2007.00953.x
Moran LA, Horton RA, Scrimgeour G, Perry M (2011) Principles of Biochemistry, 5th edn. Prentice Hall, Boston
Niklas KJ (1992) Plant Biomechanics : An Engineering Approach to Plant Form and Function. University of Chicago Press, Chicago
Page DH, El-Hosseiny F, Winkler K (1971) Behaviour of single wood fibres under axial tensile strain. Nature 229:252. https://doi.org/10.1038/229252a0
Pauly M, Gille S, Liu L et al (2013) Hemicellulose biosynthesis. Planta 238:627–642. https://doi.org/10.1007/s00425-013-1921-1
Phan TN, Likitlersuang S, Kamchoom V, Leung AK (2021) Root biomechanical properties of Chrysopogon zizanioides and Chrysopogon nemoralis for soil reinforcement and slope stabilisation. Land Degrad Dev 32(16):4624–4636. https://doi.org/10.1002/ldr.4063
Phan TN, Leung AK, Kamchoom V, Likitlersuang S (2022) Reinforcement losses in soil stabilisation due to decomposing roots of Chrysopogon zizanioides and Chrysopogon nemoralis. Land Degrad Dev. https://doi.org/10.1002/ldr.4517
Pregitzer KS (2002) Fine roots of trees – a new perspective. New Phytologist 154(2):267–270. https://doi.org/10.1046/j.1469-8137.2002.00413_1.x
Ripley B, Visser V, Christin PA et al (2015) Fire ecology of C3 and C4 grasses depends on evolutionary history and frequency of burning but not photosynthetic type. Ecology 96:2679–2691. https://doi.org/10.1890/14-1495.1
Schwarz M, Cohen D, Or D (2011) Pullout tests of root analogs and natural root bundles in soil: Experiments and modeling. J Geophys Res: Earth Surface 116(F2). https://doi.org/10.1029/2010JF001753
See CR, Luke McCormack M, Hobbie SE et al (2019) Global patterns in fine root decomposition: climate, chemistry, mycorrhizal association and woodiness. Ecol Lett 22:946–953. https://doi.org/10.1111/ele.13248
Siciliano V, Genre A, Balestrini R et al (2007) Pre-penetration apparatus formation during AM infection is associated with a specific transcriptome response in epidermal cells. Plant Signal Behav 2:533–535. https://doi.org/10.4161/psb.2.6.4745
Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419. https://doi.org/10.1007/s004420100740
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London
Solly EF, Schöning I, Boch S et al (2014) Factors controlling decomposition rates of fine root litter in temperate forests and grasslands. Plant Soil 382:203–218. https://doi.org/10.1007/s11104-014-2151-4
Stokes A, Douglas GB, Fourcaud T et al (2014) Ecological mitigation of hillslope instability: Ten key issues facing researchers and practitioners. Plant Soil 377:1–23. https://doi.org/10.1007/s11104-014-2044-6
Taiz L, Zeiger E, Møller IM, Murphy A (2014) Plant Physiology & Development, 6th edn. Sinauer Associates, Inc, Sunderland
Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytol 178:239–252. https://doi.org/10.1111/j.1469-8137.2008.02385.x
Vangelisti A, Natali L, Bernardi R et al (2018) Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (Helianthus annuus L.) roots. Sci Rep 8:4. https://doi.org/10.1038/s41598-017-18445-0
Vergani C, Chiaradia EA, Bassanelli C, Bischetti GB (2014) Root strength and density decay after felling in a Silver Fir-Norway Spruce stand in the Italian Alps. Plant Soil 377:63–81. https://doi.org/10.1007/s11104-013-1860-4
Vergani C, Schwarz M, Soldati M et al (2016) Root reinforcement dynamics in subalpine spruce forests following timber harvest: A case study in Canton Schwyz, Switzerland. Catena 143:275–288. https://doi.org/10.1016/j.catena.2016.03.038
Watson A, Marden M, Rowan D (1997) Root-wood strength deterioration in kanuka after clearfelling. New Zealand J Forestry Sci 27(2):205–215
Watson A, Phillips C, Marden M (1999) Root strength, growth, and rates of decay: root reinforcement changes of two tree species and their contribution to slope stability. Plant Soil 217(1):39–47
Weng JK, Li X, Bonawitz ND, Chapple C (2008) Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. Curr Opin Biotechnol 19:166–172. https://doi.org/10.1016/j.copbio.2008.02.014
Wu TH, McKinnell WP III, Swanston DN (1979) Strength of tree roots and landslides on Prince of Wales Island, Alaska. Can Geotech J 16(1):19–33. https://doi.org/10.1139/t79-003
Wu Z, Leung AK, Boldin D, Ganesan SP (2021) Variability in root biomechanics of Chrysopogon zizanioides for soil eco-engineering solutions. Sci Total Environ 145943. https://doi.org/10.1016/j.scitotenv.2021.145943
Zhang X, Wang W (2015) The decomposition of fine and coarse roots: their global patterns and controlling factors. Sci Rep 5:9940. https://doi.org/10.1038/srep09940
Zhang CB, Chen LH, Jiang J (2014) Why fine tree roots are stronger than thicker roots: The role of cellulose and lignin in relation to slope stability. Geomorphology 206:196–202. https://doi.org/10.1016/j.geomorph.2013.09.024
Zhu J, Wang Y, Wang Y, Mao Z, Langendoen EJ (2020) How does root biodegradation after plant felling change root reinforcement to soil? Plant Soil 446(1–2):211–227. https://doi.org/10.1007/s11104-019-04345-x
Acknowledgements
V.K. would like to acknowledge the grant (FRB66065/0258-RE-KRIS/FF66/53) from King Mongkut's Institute of Technology Ladkrabang (KMITL) and National Science, Research and Innovation Fund (NSRF), the grant (N10A650844) under Climate Change and Climate Variability Research in Monsoon Asia (CMON3) from the National Research Council of Thailand (NRCT) and the National Natural Science Foundation of China (NSFC). X.W.C. gratefully acknowledges the grants provided by the NSFC (42077298) and the Hong Kong Research Grant Council (16207521). A.K.L. gratefully acknowledges the Hong Kong Research Grant Council funding (GRF/16202720, CRF/C6006-20G) and the NSFC grant (51922112).
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V.K. analysed the data, drafted and revised the manuscript. X.W.C. analyzed the data, plotted the graphs, drafted and revised the manuscript. A.K.L. commented and edited the manuscript. T.K. and C.S. conducted the experiments and acquired the data. V.K. conceived the idea, designed the experiments, and supervised the project. V.K., X.W.C., and A.K.L. acquired the funding.
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Kamchoom, V., Chen, X.W., Leung, A.K. et al. Dynamic changes in cellulose content and biomechanical properties of mycorrhizal roots during growth and decay. Plant Soil 490, 573–589 (2023). https://doi.org/10.1007/s11104-023-06103-6
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DOI: https://doi.org/10.1007/s11104-023-06103-6