Skip to main content

Advertisement

SpringerLink
Log in

Arbuscular mycorrhizal fungi increase the proportion of cellulose and hemicellulose in the root stele of vetiver grass

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Arabidopsis thaliana is the model plant that is mainly used in studying cellulose and hemicellulose (CH) biosynthesis. Unfortunately, A. thaliana does not associate with mycorrhiza and as a result there are only rare reports on the role of arbuscular mycorrhiza (AM) fungi on CH biosynthesis. This study aims to investigate the effects of AM fungi on changing the CH content in mycorrhizal plant.

Methods

Three AM fungi, Glomus aggregatum, Rhizophagus intraradices and Funneliformis mosseae, were inoculated to vetiver grass (Chrysopogon zizanioides) and grown for 12 months. Roots were harvested, and the proportions of CH, lignin, lipids and hydrosoluble content were analysed. The corresponding root tensile strength (positively correlated with the proportion of CH) was measured to counter check the CH content.

Results

Plants inoculated with AM showed a higher proportion of CH (P < 0.05) compared with uninoculated ones. This increase was coupled to a 40–60% enhancement in tensile strength. Potential mechanisms for this phenomenon are discussed.

Conclusions

This is the first study showing that the proportion of CH and tensile strength of plant root could be significantly affected by AM symbiosis. It is thus desirable that future research on CH biosynthesis uses mycorrhizal-associating plants, such as medic (Medicago truncatula) and rice (Oryza sativa).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amor Y, Haigler CH, Johnson S et al (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci U S A 92:9353–9357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arioli T, Peng L, Betzner AS et al (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720

    Article  CAS  PubMed  Google Scholar 

  • ASTM (2007) Test Methods for Laboratory Compaction Characteristics of Soil Using Standard Effort (12 400 ft-lbf/ft3 (600 kN-m/m3)). ASTM standard D698. American Society for Testing and Materials, West Conshohocken

  • Baets SD, Poesen J, Reubens B et al (2008) Root tensile strength and root distribution of typical Mediterranean plant species and their contribution to soil shear strength. Plant Soil 305:207–226

    Article  CAS  Google Scholar 

  • Balestrini R, Bonfante P (2005) The interface compartment in arbuscular mycorrhizae: A special type of plant cell wall? Plant Biosyst Int J Deal Asp Plant Biol 139:8–15

    Google Scholar 

  • Balestrini R, Bonfante P (2014) Cell wall remodeling in mycorrhizal symbiosis: A way towards biotrophism. Front Plant Sci 5:1–10

    Article  Google Scholar 

  • Balestrini R, Romera C, Puigdomenech P, Bonfante P (1994) Location of a cell-wall hydroxyproline-rich glycoprotein, cellulose and β-1,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195:201–209

    Article  CAS  Google Scholar 

  • Balestrini R, Cosgrove DJ, Bonfante P (2005) Differential location of α-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta 220:889–899

    Article  CAS  PubMed  Google Scholar 

  • Bashline L, Li S, Gu Y (2014) The trafficking of the cellulose synthase complex in higher plants. Ann Bot 114:1059–1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bencherif K, Boutekrabt A, Dalpé Y, Lounès-Hadj Sahraoui A (2016) Soil and seasons affect arbuscular mycorrhizal fungi associated with Tamarix rhizosphere in arid and semi-arid steppes. Appl Soil Ecol 107:182–190

    Article  Google Scholar 

  • Bidhendi AJ, Geitmann A (2016) Relating the mechanics of the primary plant cell wall to morphogenesis. J Exp Bot 67:449–461

    Article  CAS  PubMed  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546

    Article  CAS  PubMed  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48

    Article  PubMed  Google Scholar 

  • Bonfante P, Vian B, Perotto S et al (1990) Cellulose and pectin localization in roots of mycorrhizal Allium porrum: labelling continuity between host cell wall and interfacial material. Planta 180:537

    Article  Google Scholar 

  • Chen XW, Wong JTF, Ng CWW, Wong MH (2016) Feasibility of biochar application on a landfill final cover—a review on balancing ecology and shallow slope stability. Environ Sci Pollut Res 23:7111–7125

    Article  CAS  Google Scholar 

  • Cheng L, Booker FL, Tu C et al (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087

    Article  CAS  PubMed  Google Scholar 

  • Coleman HD, Yan J, Mansfield SD (2009) Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc Natl Acad Sci U S A 106:13118–13123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328:307–317

    Article  CAS  PubMed  Google Scholar 

  • Detering S, Dettmann S, Thierfelder H et al (2005) Glycosidase and glycosyltransferase activity increase in arbuscular mycorrhiza infected legume roots. Symbiosis 40:157–162

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • GEO (Geotechnical Engineering Office, Civil Engineering and Development Department of the Government of the Hong Kong SAR, China) (2000) Guide to Rock and Soil Descriptions. http://www.cedd.gov.hk/eng/publications/geo/doc/eg3.pdf

  • GEO (Geotechnical Engineering Office, Civil Engineering and Development Department of the Government of the Hong Kong SAR, China) (2011) GEO Publication No. 1/2011. Technical Guidelines on Landscape Treatment for Slopes. http://www.cedd.gov.hk/eng/publications/geo/geo_p111.html. Accessed 21 Aug 2017

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289–292

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–32

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Holland N, Holland D, Helentjaris T et al (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu W-J, Harding SA, Lung J et al (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotechnol 17:808–812

    Article  CAS  PubMed  Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N et al (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104:1720–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi CP, Mansfield SD (2007) The cellulose paradox — simple molecule, complex biosynthesis. Curr Opin Plant Biol 10:220–226

    Article  CAS  PubMed  Google Scholar 

  • Kalia S, Kaith BS, Kaur I (eds) (2011) Cellulose Fibers: Bio- and Nano-Polymer Composites: Green Chemistry and Technology, 2011 edition. Heidelberg, Springer

    Google Scholar 

  • Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    Article  CAS  PubMed  Google Scholar 

  • Klute A, Weaver RW, Mickelson SH et al (1994) Methods of Soil Analysis: Part 4, Physical Methods. Soil Science Society of America, Madison

    Google Scholar 

  • Leavitt SW, Danzer SR (1993) Method for batch processing small wood samples to holocellulose for stable-carbon isotope analysis. Anal Chem 65:87–89

    Article  CAS  Google Scholar 

  • Li X, Weng J-K, Chapple C (2008) Improvement of biomass through lignin modification. Plant J 54:569–581

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr R, Godoy R (1990) Seasonal patterns in vesicular-arbuscular mycorrhiza in Melic-Beech Forest. Agric Ecosyst Environ 29:281–288

    Article  Google Scholar 

  • Moran LA, Horton RA, Scrimgeour G, Perry M (2011) Principles of Biochemistry, 5th edn. Prentice Hall, Boston

    Google Scholar 

  • Nadian H, Smith SE, Alston AM, Murray RS (1996) The effect of soil compaction on growth and P uptake by Trifolium subterraneum: interactions with mycorrhizal colonisation. Plant Soil 182:39–49

    Article  CAS  Google Scholar 

  • Nadian H, Smith SE, Alston AM et al (1998) Effects of soil compaction on phosphorus uptake and growth of Trifolium subterraneum colonized by four species of vesicular–arbuscular mycorrhizal fungi. New Phytol 140:155–165

    Article  Google Scholar 

  • Ng CWW, Leung AK, Woon KX (2013) Effects of soil density on grass-induced suction distributions in compacted soil subjected to rainfall. Can Geotech J 51:311–321

    Article  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 99:13324–13329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pauly M, Gille S, Liu L et al (2013) Hemicellulose biosynthesis. Planta 238:627–642

    Article  CAS  PubMed  Google Scholar 

  • Pollen N, Simon A (2005) Estimating the mechanical effects of riparian vegetation on stream bank stability using a fiber bundle model. Water Resour Res 41:W07025

    Article  Google Scholar 

  • Reddy N, Yang Y (2005) Biofibers from agricultural byproducts for industrial applications. Trends Biotechnol 23:22–27

    Article  CAS  PubMed  Google Scholar 

  • Rich MK, Schorderet M, Reinhardt D (2014) The role of the cell wall compartment in mutualistic symbioses of plants. Front Plant Sci 5:238

    Article  PubMed  PubMed Central  Google Scholar 

  • Ross P, Mayer R, Benziman M (1991) Cellulose biosynthesis and function in bacteria. Microbiol Rev 55:35–58

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rowell RM (ed) (1984) The Chemistry of Solid Wood, 1st edn. American Chemical Society, Washington, D.C

    Google Scholar 

  • Saxena IM, Brown RM (2005) Cellulose biosynthesis: current views and evolving concepts. Ann Bot 96:9–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London

    Google Scholar 

  • Solaiman ZM (2014) Contribution of Arbuscular Mycorrhizal Fungi to Soil Carbon Sequestration. In: Solaiman ZM, Abbott LK, Varma A (eds) Mycorrhizal Fungi: Use in Sustainable Agriculture and Land Restoration. Springer, Berlin, pp 287–296

    Google Scholar 

  • Sparks DL, Page AL, Dalton PA et al (1996) Methods of Soil Analysis: Part 3, Chemical Methods. Soil Science Society of America, American Society of Agronomy, Madison

    Google Scholar 

  • Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytol 178:239–252

    Article  CAS  PubMed  Google Scholar 

  • Tosi M (2007) Root tensile strength relationships and their slope stability implications of three shrub species in the Northern Apennines (Italy). Geomorphology 87:268–283

    Article  Google Scholar 

  • Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200

    Article  CAS  Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M et al (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Veiga RSL, Faccio A, Genre A et al (2013) Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant Cell Environ 36:1926–1937

    PubMed  Google Scholar 

  • Watanabe Y, Meents MJ, McDonnell LM et al (2015) Visualization of cellulose synthases in Arabidopsis secondary cell walls. Science 350:198–203

    Article  CAS  PubMed  Google Scholar 

  • Weng J-K, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285

    Article  CAS  PubMed  Google Scholar 

  • Weng J-K, Li X, Bonawitz ND, Chapple C (2008) Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. Curr Opin Biotechnol 19:166–172

    Article  CAS  PubMed  Google Scholar 

  • Wightman R, Turner S (2010) Trafficking of the plant cellulose synthase complex. Plant Physiol 153:427–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong CC, Wu SC, Kuek C et al (2007) The role of mycorrhizae associated with vetiver grown in Pb-/Zn-contaminated soils: Greenhouse study. Restor Ecol 15:60–67

    Article  Google Scholar 

  • Wu TH (2013) Root reinforcement of soil: Review of analytical models, test results, and applications to design. Can Geotech J 50:259–274

    Article  Google Scholar 

  • Wu TH, McKinnell WP III, Swanston DN (1979) Strength of tree roots and landslides on Prince of Wales Island, Alaska. Can Geotech J 16:19–33

    Article  Google Scholar 

  • Wu Q-S, Liu C-Y, Zhang D-J et al (2016) Mycorrhiza alters the profile of root hairs in trifoliate orange. Mycorrhiza 26:237–247

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Zhou Q, Shan B (2010) Design and construction of modern bamboo bridges. J Bridg Eng 15:533–541

    Article  Google Scholar 

  • Xiao C, Zhang T, Zheng Y et al (2016) Xyloglucan deficiency disrupts microtubule stability and cellulose biosynthesis in Arabidopsis, altering cell growth and morphogenesis. Plant Physiol 170:234–249

    Article  CAS  PubMed  Google Scholar 

  • Youssefian S, Rahbar N (2015) Molecular origin of strength and stiffness in bamboo fibrils. Sci Rep 5:11116

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng W, Jiang N, Nadella R et al (2010) A glucurono(arabino)xylan synthase complex from wheat contains members of the GT43, GT47, and GT75 families and functions cooperatively. Plant Physiol 154:78–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S-Y, Fei B-H, Yu Y et al (2013) Effect of the amount of lignin on tensile properties of single wood fibers. For Sci Pract 15:56–60

    Google Scholar 

  • Zhang C-B, Chen L-H, 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

    Article  Google Scholar 

  • Zhang Y, Nikolovski N, Sorieul M et al (2016) Golgi-localized STELLO proteins regulate the assembly and trafficking of cellulose synthase complexes in Arabidopsis. Nat Commun 7:11656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Anderson S, Zhang Y, Garavito RM (2011) The structure of sucrose synthase-1 from Arabidopsis thaliana and its functional implications. J Biol Chem 286:36108–36118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The financial support from the Collaborative Research Fund of the Research Grants Council, Hong Kong SAR (HKUST6/CRF/12R) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, SAR, China

    Xun Wen Chen, Pui San So, Charles Wang Wai Ng & Ming Hung Wong

  2. School of Chemistry & Environment, Higher Education Mega Center, South China Normal University, Guangzhou, 510006, China

    Yuan Kang

  3. Consortium on Health, Environment, Education and Research (CHEER), and Department of Science and Environmental Studies, The Education University of Hong Kong, Tai Po, Hong Kong, SAR, China

    Ming Hung Wong

  4. School of Environment, Jinan University, Guangzhou, China

    Ming Hung Wong

Authors
  1. Xun Wen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuan Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pui San So
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charles Wang Wai Ng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ming Hung Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Charles Wang Wai Ng or Ming Hung Wong.

Additional information

Responsible Editor: Tatsuhiro Ezawa

Electronic supplementary material

ESM 1

(DOC 150 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, X.W., Kang, Y., So, P.S. et al. Arbuscular mycorrhizal fungi increase the proportion of cellulose and hemicellulose in the root stele of vetiver grass. Plant Soil 425, 309–319 (2018). https://doi.org/10.1007/s11104-018-3583-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3583-z

Keywords

Search

Navigation