Advertisement

Response of Arbuscular Mycorrhizal Fungi to Global Climate Change and Their Role in Terrestrial Ecosystem C and N Cycling

  • Bhoopander GiriEmail author
  • Bhawna Saxena
Chapter

Abstract

The global climate change presents a serious threat to nature and has been predicted to largely impact the life of human beings in the twenty-first century. The Intergovernmental Panel on Climate Change predicted that human-induced climate change is a major threat and also emphasized to develop global plans for mitigation and adaptation to climate change. Taking into consideration the existing feedbacks between carbon cycle and climate change, understanding whether terrestrial ecosystems will respond to elevated atmospheric carbon dioxide concentration (eCO2) or up to what extent is of utmost significance. In the global ecosystems, CO2 is largely used by plants in the process of photosynthesis (net primary production). On the other hand, microbes contribute directly, to a great extent, to net carbon exchange through decomposition and respiration and indirectly by developing symbiotic associations with plants. One of the most common symbiotic associations established between plants and fungi is known as arbuscular mycorrhizal fungi (AMF). This association facilitates the host plants for the better acquisition of water and nutrients and seems to sequester soil organic carbon. AMF could play a vital role in the global carbon cycle, as they can utilize a large proportion of the carbon fixed by the plants, deposit slow-cycling organic compounds (glomalin), and protect organic matter from microbial attack by promoting soil aggregation. In view of the importance of AM symbiosis in the terrestrial ecosystems, this chapter highlights whether the arbuscular mycorrhizal fungi contribute to soil carbon sequestration or influence soil carbon decomposition.

Keywords

Soil Organic Carbon Arbuscular Mycorrhizal Fungus Arbuscular Mycorrhiza Soil Carbon Sequestration Extraradical Hypha 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Authors duly acknowledge the technical support provided by Mr Harsh Sharma, computer analyst, Institute of Life Long Learning, University of Delhi, Delhi, India.

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Al-Karaki GN, Clark RB (1999) Varied rates of mycorrhizal inoculum on growth and nutrient acquisition by barley grown with drought stress. J Plant Nutr 22:1775–1784CrossRefGoogle Scholar
  3. Antibus RK, Lauber C, Sinsabaugh RL, Zak DR (2006) Responses of Bradford-reactive soil protein to experimental nitrogen addition in three forest communities in northern lower Michigan. Plant Soil 288:173–187CrossRefGoogle Scholar
  4. Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437:349–355PubMedCrossRefGoogle Scholar
  5. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  6. Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bai C, He X, Tang H, Shan B, Zhao L (2009) Spatial distribution of arbuscular mycorrhizal fungi, glomalin and soil enzymes under the canopy of Astragalus adsurgens Pall. in the Mu US sandland, China. Soil Biol Biochem 41:941–947CrossRefGoogle Scholar
  8. Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contribution to climate change through carbon cycle feedbacks. ISME J 2:805–814PubMedCrossRefGoogle Scholar
  9. Bonfante P, Anca I (2010) Plants, mycorrhizal fungi and bacteria: a network of interaction. Annu Rev Microbiol 63:363–383CrossRefGoogle Scholar
  10. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. doi: 10.1038/ncomms1046 PubMedCrossRefGoogle Scholar
  11. Bonfante P, Requena N (2011) Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 14:1–7CrossRefGoogle Scholar
  12. Caesar J, Lowe JA (2012) Comaparing the impacts of mitigation verses non-intervention scenarios on future temperature and precipitation extremes in the HadGE2 climate model. J Geophys Res 117:1–14CrossRefGoogle Scholar
  13. Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Barker DG, Bonfante P (2011) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and non legume root epidermis. New Phytol 189:347–355PubMedCrossRefGoogle Scholar
  14. Cheng W, Kuzyakov Y (2005) Root effects on soil organic matter decomposition. Agronomy 48:119–140Google Scholar
  15. Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087PubMedCrossRefGoogle Scholar
  16. Cheng W, Parton WJ, Gonzalez-meler MA, Phillips R, Asao S, Mcnickle GG, Brzostek E, Jastrow JD (2013) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201:31–44PubMedCrossRefGoogle Scholar
  17. Clemmensen KE (2013) Roots and associated fungi drive long-term carbon sequestration in Boreal Forest. Science 339:1615–1618PubMedCrossRefGoogle Scholar
  18. Del Giorgio PA, Duarte CM (2002) Respiration in the open ocean. Nature 420:379–384PubMedCrossRefGoogle Scholar
  19. Drigo B, Kowalchuk G, van Veen J (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679CrossRefGoogle Scholar
  20. Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci USA 107:10939–10942CrossRefGoogle Scholar
  21. Driver JD, Holben WE, Rillig MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37:101–106CrossRefGoogle Scholar
  22. Elliott ET, Coleman DC (1988) Let the soil work for us. Ecol Bull 39:23–32Google Scholar
  23. Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Toby Kiers E, Bücking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 109:72666–72671CrossRefGoogle Scholar
  24. Frank AB (1885) Über die auf Würzelsymbiose beruhende Ehrnährung gewisser Bäum durch unterirdische Pilze. Berichte der Deutschen Botanischen Gesellschaft (in German) 3:128–145Google Scholar
  25. Gerdemann JW, Trappe JM (1974) Endogonaceae in the Pacific North West. Mycol Mem 5:1–76Google Scholar
  26. Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:2989–3005PubMedPubMedCentralCrossRefGoogle Scholar
  27. Hansen J, Sato M, Kharecha P, Beerling D, Berner R, Masson-Delmotte V, Pagani M, Raymo M, Royer DL, Zaches JC (2008) Target atmospheric CO2: where should humanity aim? Open Atmos Sci J 2:217–231CrossRefGoogle Scholar
  28. Hartge KH, Stewart BA (1995) Soil structure. Its development and function. Advances in soil science. CRC Lewis, Boca Raton, FL, pp 424. isbn: 1–56670–173-2Google Scholar
  29. Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107:13754–13759PubMedPubMedCentralCrossRefGoogle Scholar
  30. Hooker JE, Black KE (1995) Arbuscular mycorrhizal fungi as components of sustainable soil-plant systems. Crit Rev Biotechnol 15:210–212CrossRefGoogle Scholar
  31. Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83CrossRefGoogle Scholar
  32. Jastrow JD, Miller RM (1997) Soil aggregate stabilization and carbon sequestration: feedbacks through organomineral associations. In: Lal R, Kimble JM, Follet RF, Stewart BA (eds) Soil processes and the carbon cycle. CRC Press, Boca Raton, FL, pp 207–223Google Scholar
  33. Jastrow JD, Miller RM, Lussenhop J (1998) Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol Biochem 7:905–916CrossRefGoogle Scholar
  34. Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ (CO2)-C-13 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334CrossRefGoogle Scholar
  35. Kasischke ES, Turetsky MR (2006) Recent changes in the fire regime across the North American boreal region—spatial and temporal patterns of burning across Canada and Alaska. Geophys Res Lett 33:1–5Google Scholar
  36. King GM (2011) Enhancing soil carbon storage for carbon remediation: potential contributions and constraints by microbes. Trends Microbiol 19:75–84PubMedCrossRefGoogle Scholar
  37. Kosuta S, Chabaud M, Lougnon G, Gough C, Denarie J, Barker DG, Becard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962PubMedPubMedCentralCrossRefGoogle Scholar
  38. Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627PubMedCrossRefGoogle Scholar
  39. Lal R (2012) Climate change mitigation by managing the terrestrial biosphere. In: Lal R, Klaus L, Reinhard FH, Bernd US, von Joachim B (eds) Recarbonization of the biosphere. Springer, Dordrecht, pp 17–39CrossRefGoogle Scholar
  40. Leifheit EF, Veresoglou SD, Lehmann A, Morris EK, Rillig MC (2014) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil 374:523–537CrossRefGoogle Scholar
  41. Leifheit EF, Verbruggen E, Rillig MC (2015) Arbuscular mycorrhizal fungi reduce decomposition of woody plant litter while increasing soil aggregation. Soil Biol Biochem 81:323–328CrossRefGoogle Scholar
  42. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207PubMedCrossRefGoogle Scholar
  43. Loboda T (2012) Understanding origins and impacts of drought. Eos 93:417. doi: 10.1029/2012EO420007 CrossRefGoogle Scholar
  44. Lovelock CE, Wright SF, Nichols KA (2004a) Using glomalin as an indicator for arbuscular mycorrhizal hyphal growth: an example from a tropical rainforest soil. Soil Biol Biochem 36:1009–1012CrossRefGoogle Scholar
  45. Lovelock CE, Wright SF, Clark DA, Ruess RW (2004b) Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape. J Ecol 92:278–287CrossRefGoogle Scholar
  46. Maracchi G, Sirotenko O, Bindi M (2005) Impacts of present and future climate variability on agriculture and forestry in the temperate region Europe. Clim Chang 70:117–135CrossRefGoogle Scholar
  47. Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: molecular biology and physiology. Kluwer Academic, Dordrecht, pp 3–18CrossRefGoogle Scholar
  48. Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103:17–23PubMedCrossRefGoogle Scholar
  49. Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon 37:471–491Google Scholar
  50. Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673–681PubMedPubMedCentralCrossRefGoogle Scholar
  51. Nichols KA, Wright SF (2004) Contributions of soil fungi to organic matter in agricultural soils. In: Magdoff F, Weil R (eds) Functions and management of soil organic matter in agroecosystems. CRC Press, Boca Raton, FL, pp 179–198Google Scholar
  52. Nichols K, Wright SF, Dzantor EK (2002) Glomalin: hiding place for a third of the world’s stored soil carbon. Agri Res Mag 50:4–7. www.ars.usda.gov/is/AR/archive/sep02/soil0902.htm
  53. Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337CrossRefGoogle Scholar
  54. Oehl F, de Souza FA, Sieverding E (2008) Revision of Scutellospora and description of five new genera and three new families in the arbuscular-forming Glomeromycetes. Mycotaxon 106:311–360Google Scholar
  55. Oehl F, da Silva GA, Sánchez-Castro I, Goto BT, Maia LC, Evangelista Vieira HEE, Barea JM, Sieverding E, Palenzuela J (2011) Revision of Glomeromycetes with entrophosporoid and glomoid spore formation with three new genera. Mycotaxon 117:297–316CrossRefGoogle Scholar
  56. Orwin KH, Kirschbaum MUF, St John MG, Dickie IA (2011) Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol Lett 14:493–502PubMedCrossRefGoogle Scholar
  57. Pachauri RK, Reisinger A (2007) Climate change 2007: synthesis report. Contribution of working groups I, II and III to the fourth assessment report of the Intergovernmental Panel on Climate Change. IPCC. Cambridge University Press, CambridgeGoogle Scholar
  58. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional tradeoffs in arbuscular mycorrhizal fungi. Proc R Soc Lond B Biol Sci 276:4237–4245CrossRefGoogle Scholar
  59. Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101:133–149CrossRefGoogle Scholar
  60. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–396CrossRefGoogle Scholar
  61. Redecker D, Raab P (2006) Phylogeny of the Glomeromycota (arbuscular mycorrhizal fungi): recent developments and new gene markers. Mycologia 98:885–895PubMedCrossRefGoogle Scholar
  62. Redecker D, Schüssler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531PubMedCrossRefGoogle Scholar
  63. Rillig MC (2004a) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol lett 7:740–754CrossRefGoogle Scholar
  64. Rillig MC (2004b) Arbuscular mycorrhizae, glomalin and soil quality. Can J Soil Sci 84:355–363CrossRefGoogle Scholar
  65. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53PubMedCrossRefGoogle Scholar
  66. Rillig MC, Steinberg PD (2002) Glomalin production by an arbuscular mycorrhizal fungus: a mechanism of habitat modification? Soil Biol Biochem 34:1371–1374CrossRefGoogle Scholar
  67. Rillig MC, Wright SF, Kimball BA, Pinter PJ, Wall GW, Ottman MJ, Leavitt SW (2001a) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field: a possible role for arbuscular mycorrhizal fungi. Glob Chang Biol 7:333–337CrossRefGoogle Scholar
  68. Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001b) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233:167–177CrossRefGoogle Scholar
  69. Rillig MC, Wright SF, Eviner VT (2002) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant Soil 238:325–333CrossRefGoogle Scholar
  70. Rillig MC, Ramsey PW, Morris S, Paul EA (2003) Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant Soil 253:293–299CrossRefGoogle Scholar
  71. Rojas O, Vrieling A, Rembold F (2011) Assessing drought probability for agricultural areas in Africa with coarse resolution remote sensing imagery. Remote Sens Environ 115:343–352CrossRefGoogle Scholar
  72. Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178:253–266PubMedCrossRefGoogle Scholar
  73. Rosewarne GM, Barker SJ, Smith SE (1997) Production of near-synchronous fungal colonization in tomato for development and molecular analyses of mycorrhiza. Mycol Res 101:966–970CrossRefGoogle Scholar
  74. Rosier CL, Hoye AT, Rillig MC (2006) Glomalin-related soil protein: assessment of current detection and quantification tools. Soil Biol Biochem 38:2205–2211CrossRefGoogle Scholar
  75. Ruiz-Lozano JM, Azcon R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478CrossRefGoogle Scholar
  76. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  77. Schopf JW, Packer BM (1987) Early Archean (3.3-billion to 3.5-billionyearold) microfossils from Warrawoona Group, Australia. Science 237:70–73PubMedCrossRefGoogle Scholar
  78. Schüßler A, Walker C (2010) The Glomeromycota. A species list with new families and new Genera (Libraries at the Royal Botanic Garden Edinburgh, Edinburgh; The Royal Botanic Garden Kew, Kew; Botanische Staatssammlung Munich, Munich; and Oregon State University, Corvallis, OR). pp 1–56Google Scholar
  79. Schüβler A, Walker C (2011) Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota. In: Poggeler S, Wostemeyer J (eds) Evolution of fungi and fungal-like organisms. Springer, Berlin, pp 163–185CrossRefGoogle Scholar
  80. Schüβler A, Mollenhauer D, Schnepf E, Kluge M (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  81. Schüβler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936CrossRefGoogle Scholar
  82. Schwarzott D, Walker C, Schüβler A (2001) Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is non monophyletic. Mol Phylogenet Evol 21:190–197PubMedCrossRefGoogle Scholar
  83. Selsted MB, van der Linden L, Ibrom A, Michelsen A, Larsen KS, Pedersen JK, Mikkelsen TN, Pilegaard K, Beier C, Ambus P (2012) Soil respiration is stimulated by elevated CO2 and reduced by summer drought: three years of measurements in a multifactor ecosystem manipulation experiment in a temperate heathland (CLIMATE). Glob Chang Biol 18:1216–1230CrossRefGoogle Scholar
  84. Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790PubMedCrossRefGoogle Scholar
  85. Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31CrossRefGoogle Scholar
  86. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego, CAGoogle Scholar
  87. Smith SE, Read D (2008) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego, CAGoogle Scholar
  88. Smith FA, Smith SE (1997) Structural diversity in vesicular-arbuscular mycorrhizal symbioses. New Phytol 137:373–388CrossRefGoogle Scholar
  89. Srivastava D, Kapoor R, Srivastava SK, Mukerji KG (1996) Vesicular arbuscular mycorrhiza-an overview. In: Mukerji KG (ed) Concepts in mycorrhizal research. Kluwer Academic Press, Dordrecht, pp 1–39CrossRefGoogle Scholar
  90. Talbot JM, Treseder KK (2011) Dishing the dirt on carbon cycling. Nat Clim Chang 1:144–146CrossRefGoogle Scholar
  91. Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, OxfordGoogle Scholar
  92. Tisdall JM, Oades JM (1982) Organic matter and water stable aggregates in soils. J Soil Sci 33:141–163CrossRefGoogle Scholar
  93. Torres-Cortes G, Ghignone S, Bonfante P, Schüßler A (2015) Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: transkingdom gene transfer in an ancient mycoplasma-fungus association. Proc Natl Acad Sci USA 112:7785–7790PubMedPubMedCentralCrossRefGoogle Scholar
  94. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355CrossRefGoogle Scholar
  95. Treseder KK (2016) Model behavior of arbuscular mycorrhizal fungi: predicting soil carbon dynamics under climate change. Botany 94:417–423CrossRefGoogle Scholar
  96. Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200CrossRefGoogle Scholar
  97. Treseder KK, Holden SR (2013) Fungal carbon sequestration. Science 339:1528–1529PubMedCrossRefGoogle Scholar
  98. Treseder KK, Turner KM (2007) Glomalin in ecosystems. Soil Sci Soc Am J 71:1257–1266CrossRefGoogle Scholar
  99. van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752PubMedCrossRefGoogle Scholar
  100. Van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310PubMedCrossRefGoogle Scholar
  101. Verbruggen E, Veresoglou SD, Anderson IC, Caruso T, Hammer EC, Kohler J (2013) Arbuscular mycorrhizal fungi—short-term liability but long-term benefits for soil carbon storage? New Phytol 197:366–368PubMedCrossRefGoogle Scholar
  102. Verbruggen E, Jansa J, Hammer EC, Rillig MC (2016) Do arbuscular mycorrhizal fungi stabilize litter derived carbon in soil? J Ecol 104:261–269CrossRefGoogle Scholar
  103. Walker C (1992) Systematics and taxonomy of the arbuscular endomycorrhizal fungi (Glomales)—a possible way forward. Agronomie 12:887–897CrossRefGoogle Scholar
  104. Wayman RL (1991) Global climate change and life on earth. Chapman and Hall, New York, p 282Google Scholar
  105. Wilson GWT, Rice CW, Rillig MC, Springer A, Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–461PubMedCrossRefGoogle Scholar
  106. Wright SF (2000) A fluorescent antibody assay for hyphae and glomalin from arbuscular mycorrhizal fungi. Plant Soil 226:171–177CrossRefGoogle Scholar
  107. Wright SF, Anderson RL (2000) Aggregate stability and glomalin in alternative crop rotations for the central Great Plains. Biol Fertil Soils 31:249–253CrossRefGoogle Scholar
  108. Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161:575–585CrossRefGoogle Scholar
  109. Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoproteins produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107CrossRefGoogle Scholar
  110. Wright SF, Upadhyaya A (1999) Quantification of arbuscular mycorrhizal activity by the glomalin concentration on hyphae. Mycorrhiza 8:283–285CrossRefGoogle Scholar
  111. Wright SF, Franke-Snyder M, Morton JB, Upadhyaya A (1996) Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant Soil 181:193–203CrossRefGoogle Scholar
  112. Wright SF, Starr JL, Paltineanu IC (1999) Changes in aggregate stability and concentration of glomalin during tillage management transition. Soil Sci Soc Am J 63:1825–1829CrossRefGoogle Scholar
  113. Wright SF, Nichols KA, Schmidt WF (2006) Comparison of efficacy of three extractants to solubilize glomalin on hyphae and in soil. Chemosphere 64:1219–1224PubMedCrossRefGoogle Scholar
  114. Wright SF, Green VS, Cavigelli MA (2007) Glomalin in aggregate size classes from three different farming systems. Soil Tillage Res 94:546–549CrossRefGoogle Scholar
  115. Wu QS, Cao MQ, ZouYN HXH (2014) Direct and indirect effects of glomalin, mycorrhizal hyphae, and roots on aggregate stability in rhizosphere of trifoliate orange. Sci Rep 4:5823. doi: 10.1038/srep05823 PubMedPubMedCentralCrossRefGoogle Scholar
  116. Zhang B, Li S, Chen S, Ren T, Yang Z, Zhao H, Liang Y, Han X (2016) Arbuscular mycorrhizal fungi regulate soil respiration and its response to precipitation change in a semiarid steppe. Sci Rep 6:19990. doi: 10.1038/srep19990 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Botany, Swami Shraddhanand CollegeUniversity of DelhiDelhiIndia

Personalised recommendations