Skip to main content
SpringerLink
Log in

Morphological and Physiological Aspects of Symbiotic Plant–Microbe Interactions and Their Significance

  • Chapter
  • First Online:
Root Biology

Part of the book series: Soil Biology ((SOILBIOL,volume 52))

Abstract

All living organisms seem to have a large number of interactions among themselves, but mutualism is of special interest ecologically and evolutionarily. Mutualism is a general term in which two organisms interact where either one (commensalism) or both are benefitted (symbiosis). Plants in nature always grow among soil microorganisms, and some of these become closely associated with plants to form mutualistic symbioses. Examples of such symbiotic microorganisms include N2-fixing prokaryotes (Rhizobium) and mycorrhizal fungi of various types. These associations affect fitness and survival of plants. It is particularly true for mycorrhiza which promotes better absorption of nutrients, while Rhizobium itself is involved in fulfilling nitrogen requirements of the plant. Such interactions involve a large number of cross talks by means of surface chemistry and release of chemicals. Host–symbiont specificity is the key feature in symbiotic interactions. Besides providing nutritional benefits to their hosts, mycorrhizal fungi also contribute toward ecological significance such as decreased susceptibility to biotic diseases; improved tolerance to abiotic stresses such as heavy metals, drought, and salinity; resistance to invasion by weeds; and synergistic interaction with other useful soil microbes. Interestingly Rhizobium is able to fix nitrogen for the host crop plants even in highly arid conditions and improve productivity in such unfavorable conditions. In view of their importance in plant growth and development, this chapter highlights the morphology, systematics, and ecological significance of the most important plant–microbe symbionts–Rhizobium, mycorrhizae, and a growth-promoting endophyte, Piriformospora indica.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdelaziz ME, Kim D, Ali S, Fedoroff NV, Al-Babili S (2017) The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na+/K+ homeostasis under salt stress conditions. Plant Sci 263:107–115

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesqueterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • Akkermans ADL, Abdulkadir S, Trinick MJ (1978) N2-fixing root nodules in Ulmaceae: Parasponia or (and) Trema spp. Plant Soil 49:711–715

    Article  CAS  Google Scholar 

  • Alazard D (1985) Stem and root nodulation in Aeschynomene spp. Appl Environ Microbiol 50:732–734

    CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Karaki MG, Zak B (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269

    Article  PubMed  Google Scholar 

  • Anderson IC, Cairney JWG (2007) Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol Rev 31:388–406

    Article  CAS  PubMed  Google Scholar 

  • Ansari MW, Bains G, Shukla A, Pant RC, Tuteja N (2013) Low temperature stress ethylene and not Fusarium might be responsible for mango malformation. Plant Physiol Biochem 69:34–38

    Article  CAS  PubMed  Google Scholar 

  • Ansari MW, Gill SS, Tuteja N (2014) Piriformospora indica a powerful tool for crop improvement. Proc Indian Natl Sci Acad 80:317–324

    Article  Google Scholar 

  • Archetti M, Scheuring I, Hoffman M, Frederickson ME, Pierce NE, Yu DW (2011) Economic game theory for mutualism and cooperation. Ecol Lett 14:1300–1312

    Article  PubMed  Google Scholar 

  • Arnebrant K, Hans EK, Finlay RD, Söderström B (1993) Nitrogen translocation between Alnus glutinosa (L.) Gaertn. seedlings inoculated with Frankia sp. and Pinus contorta Doug, ex Loud seedlings connected by a common ectomycorrhizal mycelium. New Phytol 124(2):231–242

    Article  PubMed  Google Scholar 

  • Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24

    Article  PubMed  Google Scholar 

  • Badenoch-Jones J, Summons RE, Rolfe BG, Letham DS (1984) Phytohormones, Rhizobium mutants, and nodulation in legumes IV Auxin metabolites in pea root nodules. J Plant Growth Regul 3:23–39

    Article  CAS  Google Scholar 

  • Bago B, Cano C (2005) Breaking myths on arbuscular mycorrhizas in vitro biology. In: Declerck S, Strullu DG, Fortin A (eds) Soil biology, vol 4. Springer, Berlin, pp 111–138

    Google Scholar 

  • Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nutr 12:547–562

    Article  Google Scholar 

  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510

    Article  CAS  PubMed  Google Scholar 

  • Bandou E, Lebailly F, Muller F, Dulormne M, Toribio A, Chabrol J, Courtecuisse R, Plenchette C, Prin Y, Duponnois R, Thiao M, Sylla S, Dreyfus B, Bâ AM (2006) The ectomycorrhizal fungus Scleroderma bermudense alleviates salt stress in seagrape (Coccoloba uvifera L.) seedlings. Mycorrhiza 16(8):559–565

    Article  CAS  PubMed  Google Scholar 

  • Banfalvi Z, Sakanyan V, Koncz C, Kiss A, Dusha I, Kondorosi A (1981) Location of nodulation and nitrogen fixation genes on a high molecular weight plasmid of R. meliloti. Mol Gen Genet 184:318–325

    CAS  PubMed  Google Scholar 

  • Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT (2005) Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146:234–243

    Article  PubMed  Google Scholar 

  • Barea JM, Azcón-Aguilar C (2012) Evolution, biology and ecological effects of arbuscular mycorrhizas. In: Camisao AF, Pedroso CC (eds) Symbiosis: evolution, biology and ecological effects. Nova, Hauppauge, pp 1–34

    Google Scholar 

  • Becker M, Ladha JK, Ottow JCG (1988) Stem nodulating legumes as green manure for lowland rice. Philipp J Crop Sci 13:121–127

    Google Scholar 

  • Beniwal RS, Langenfield-Heyser R, Polle A (2010) Ectomycorrhiza and hydrogel protect hybrid poplar from water deficit and unravel plastic responses of xylem anatomy. Environ Exp Bot 69:189–197

    Article  Google Scholar 

  • Bergersen FJ (1974) Formation and function of bacteroids. In: Quispel A (ed) The biology of nitrogen fixation. North-Holland, Amsterdam, pp 473–498

    Google Scholar 

  • Bergersen FJ, Turner GL (1988) Glutamate as a carbon source for N2-fixing bacteroids prepared from soybean nodules. J Gen Microbiol 134:2441–2448

    CAS  Google Scholar 

  • Besserer A, Puech-Pages V, Kiefer P, Gomez-Rolden V, Jauneau A, Roy S, Porttais J-C, Roux C, Becard G, Sejalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226. https://doi.org/10.1372/jpournal.pbio.0040226

    Article  PubMed  PubMed Central  Google Scholar 

  • Blasius D, Feil W, Kottke I, Oberwinkler F (1986) Hartig net structure and formation in fully ensheathed ectomycorrhizas. Nord J Bot 6:837–842

    Article  Google Scholar 

  • Błaszkowski J (2012) Glomeromycota. W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków, p 303

    Google Scholar 

  • Błaszkowski J, Chwat G, Goralska A, Ryska P, Kovacs GM (2015) Two new genera: Dominikia and Kamienska and D. disticha sp nov in Glomeromycota. Nova Hedwigia 100:225–238

    Article  Google Scholar 

  • Bohlool BB, Schmidt EL (1974) Lectins: a possible basis for specificity in the Rhizobium–legume symbiosis. Science 185:269–271

    Article  CAS  PubMed  Google Scholar 

  • Bojarczuk K, Karliński L, Hazubska-Przybył T, Kieliszewska-Rokicka B (2015) Influence of mycorrhizal inoculation on growth of micropropagated Populus × canescens lines in metal-contaminated soils. New For 46(2):195–215

    Article  Google Scholar 

  • Bolan NS (1991) A critical review of the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207

    Article  CAS  Google Scholar 

  • Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13:492–498

    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  CAS  Google Scholar 

  • Bonfante-Fasolo P, Grippiolo R (1982) Ultrastructural and cytochemical changes in the wall of a vesicular-arbuscular mycorrhizal fungus during symbiosis. Can J Bot 60:2303–2312

    Article  Google Scholar 

  • Boroujeni DS, Hemmatinezhad B (2015) Review of application and importance of ectomycorrhiza fungi and their role in the stability of ecosystems. Biosci Biotechnol Res Asia 12(1):153–158

    Article  Google Scholar 

  • Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant–pathogen relations? Ecology 82:3057–3068

    Google Scholar 

  • Brelles-Marino GQ, Ane JM (2008) Nod factors and the molecular dialogue in the rhizobia–legume interaction. In: Couto GN (ed) Nitrogen fixation research progress. Nova Science, New York, pp 173–227

    Google Scholar 

  • Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

    Article  CAS  Google Scholar 

  • Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. In: Dhal NK, Sahu SC (eds) Plant science. Intech, Rijeka. ISBN: 978-953-51-0905-1

    Google Scholar 

  • Callaham DA, Torrey JG (1981) The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can J Bot 59(9):1647–1664

    Article  Google Scholar 

  • Cárdenas L, Vidali L, Dominguez J, Perez H, Sánchez F, Hepler PK, Quinto C (1998) Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 116:871–877

    Article  PubMed Central  Google Scholar 

  • Cárdenas L, Feijo JA, Kunkel JG, Sánchez F, Holdaway-Clarke T, Hepler PK, Quinto C (1999) Rhizobium nod factors induce increases in intracllular free calcium and extracellular calcium influxes in bean root hairs. Plant J 19:347–352

    Article  PubMed  Google Scholar 

  • Carlson RS, Kalembasa S, Tunoroski D, Packori P, Noel KD (1987) Characterization of the lipopolysaccharide from a Rhizobium phaseoli mutant that is defective in infection thread development. J Bacteriol 169:4923–4928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Richardson AE, Rolfe BG (1993) Studies on the physiological and genetic basis of acid tolerance in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 59:1798–1804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WX, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen nov. Int J Syst Bacteriol 38(4):392–397

    Article  Google Scholar 

  • Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487–512

    Article  PubMed  Google Scholar 

  • Coninx L, Martinova V, Rineau F (2017) Mycorrhiza-assisted phytoremediation. In: Cuypers A, Vangronsveld J (eds) Phytoremediation, vol 83. Elsevier, Amsterdam, pp 127–188

    Chapter  Google Scholar 

  • Dangar TK, Basu PS (1987) Studies on plant growth substances, IAA metabolism and nitrogenase activity in root nodules of Phaseolus aureus Roxb.var. mungo. Biol Plant 29:350–354

    Article  CAS  Google Scholar 

  • Das A, Kamal S, Shakil Najam A, Sherameti I, Oelmuller R, Dua M, Tuteja N, Johri AK, Varma A (2012) The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Signal Behav 7:1–10

    Article  CAS  Google Scholar 

  • Dazzo FB, Truchet GL, Sherwood JE, Hrabak EM, Abe M, Pankratz SH (1984) Specific phases of root hair attachment in the Rhizobium trifolii–clover symbiosis. Appl Environ Microbiol 48:1140–1150

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Mita (2007) Investigation of the demographic and selective forces shaping the nucleotide diversity of genes involved in nod factor signaling in Medicago truncatula. Genetics 177:2123–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M (1998) Allorhizobium undicola gen nov, sp nov, nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48:1277–1290

    Article  PubMed  Google Scholar 

  • Debelle F, Rosenberg C, Vasse J, Maillet F, Martinez E, Dénarie J, Truchet G (1986) Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti. J Bacteriol 168:1075–1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denarie J, Debelle F, Prome JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535

    Article  CAS  PubMed  Google Scholar 

  • Deshmukh SD, Kogel KH (2007) Piriformospora indica protects barley from root rot caused by Fusarium graminearum. J Plant Dis Protect 114:263–268

    Article  Google Scholar 

  • Diaz CL, Van Spronsen PC, Bakhuizen R, Logman GJJ, Lugtenberg EJJ, Kijne JW (1986) Correlation between infection by Rhizobium leguminosarum and lectin on the surface of Pisum sativum roots. Planta 168:350–359

    Article  CAS  PubMed  Google Scholar 

  • Diaz CL, Melchers LS, Hooykaas PJJ, Lugtenberg BJJ, Kijne JW (1989) Root lectin as a determinant of host-plant specificity in Rhizobium-legume symbiosis. Nature 338:579–581

    Article  CAS  Google Scholar 

  • Dighton J (2009) Mycorrhizae. In: Encyclopedia of microbiology, 3rd edn. Elsevier, SanDiego

    Chapter  Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitogen fixation. Nat Rev Microbiol 2:621–631

    Article  CAS  PubMed  Google Scholar 

  • Dobert RC, Breil BT, Triplett EW (1994) DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationships to those of other nodulating bacteria. Mol Plant-Microbe Interact 7:564–572

    Article  CAS  PubMed  Google Scholar 

  • Dolatabadi HK, Goltapeh EM, Jaimand K, Rohani N, Varma A (2011) Effects of Piriformospora indica and Sebacina vermifera on growth and yield of essential oil in fennel (Foeniculum vulgare) under greenhouse conditions. J Basic Microbiol 51:33–39

    Article  CAS  PubMed  Google Scholar 

  • Downie JA (2014) Legume nodulation. Curr Biol 24:184–190

    Article  CAS  Google Scholar 

  • Downie JA, Oldroyd GE (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576

    Article  PubMed  CAS  Google Scholar 

  • Downie JA, Rossen L, Knight CD, Robertson JG, Wells B, Johnston AW (1985) Rhizobium leguminosarum genes involved in early stages of nodulation. J Cell Sci Suppl 2:347–354

    Article  CAS  PubMed  Google Scholar 

  • Dreyfus BL, Dommergues YR (1981) Nitrogen-fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata. FEMS Microbiol Lett 10:313–317

    Article  CAS  Google Scholar 

  • Dreyfus BL, Garcia J, Gillis M (1988) Characterization of Azorhizobium caulinodans gen nov sp nov, a stemnodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int J Syst Bacteriol 38:89–98

    Article  CAS  Google Scholar 

  • Dudley ME, Jacobs TW, Long SR (1987) Microscopic studies of cell divisions induced in alfalfa roots by Rhizobium meliloti. Planta 171:289–301

    Article  CAS  PubMed  Google Scholar 

  • Durand TC, Baillif P, Albe’Ric P, Carpin S, Label P, Hausman JF, Morabito D (2011) Cadmium and zinc are differentially distributed in Populus tremula × P. alba exposed to metal excess. Plant Biosyst 145:397–405

    Article  Google Scholar 

  • Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681

    Article  CAS  PubMed  Google Scholar 

  • Eshel A, Beeckman T (2013) Plant roots: the hidden half, 4th edn. CRC Press, Boca Raton

    Google Scholar 

  • Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Büttner C, Grosch R, Schwarz D, Franken P (2009) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191–200

    Article  PubMed  Google Scholar 

  • Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Buttner C, Grosch R, Schwarz D, Franken P (2010) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191–200

    Article  PubMed  Google Scholar 

  • Faucher C, Gamut S, Dénarie J, Truchet G (1989) The nodH and nodQ host range genes of Rhizobium meliloti behave as avirulence genes in R. leguminosarum bv viciae and determine changes in the production of plant-specific extracellular signals. Mol Plant Microbe Interact 2:291–300

    Article  Google Scholar 

  • Felle HH, Kondorosi E, Kondorosi A, Schultze M (1996) Rapid alkalization of root hairs in response to rhizobial lipochitooligosaccharide signals. Plant J 10:295–301

    Article  CAS  Google Scholar 

  • Felten J, Martin F, Legué V (2012) Signalling in ectomycorrhizal symbiosis. In: Perotto S, Baluška F (eds) Signaling and communication in plant symbiosis. Springer, Berlin, pp 123–142

    Chapter  Google Scholar 

  • Ferguson BJ (2013) Rhizobia and legume nodulation genes. In: Maloy S, Hughes K (eds) Brenner’s encyclopedia of genetics. Academic, New York, pp 236–239

    Chapter  Google Scholar 

  • Fisher RF, Egelhoff TT, Mulligan JT, Long SR (1988) Specific binding of protein from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev 2:282–293

    Article  CAS  PubMed  Google Scholar 

  • France RC, Reid CPP (1984) Pure culture growth of ectomycorrhizal fungi on inorganic nitrogen sources. Microb Ecol 10:187–195

    Article  CAS  PubMed  Google Scholar 

  • Francisco PB, Akao S (1993) Autoregulation and nitrate inhibition of nodule formation in soybean cv Enrei and its nodulation mutants. J Exp Bot 44:547–553

    Article  CAS  Google Scholar 

  • Frank AB (1885) U ¨ ber die auf Würzelsymbiose beruhende Ehrna ¨hrung gewisser Ba ¨um durch unterirdische Pilze. Ber Deut Bot Ges (in German) 3:128–145

    Google Scholar 

  • Gagnon H, Ibrahim RK (1998) Aldonic acids: a novel family of nod gene inducers of Mesorhizobium loti, Rhizobium lupini and Sinorhizobium meliloti. Mol Plant-Microbe Interact 11:988–998

    Article  CAS  Google Scholar 

  • Gamas P, Niebel FDC, Lescure N, Cullimore JV (1996) Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol Plant Microbe Interact 9:233–242

    Article  CAS  PubMed  Google Scholar 

  • Garg R, Jain M (2013) Transcriptome analyses in legumes: a resource for functional genomics. Plant Genome 6. https://doi.org/10.3835/plantgenome2013.04.0011

  • Garg N, Geetanjali, Kaur A (2006) Arbuscular mycorrhiza: nutritional aspects. Arch Agron Soil Sci 52:593606

    Article  CAS  Google Scholar 

  • Gerdeman JW (1968) Vesicular- arbuscular mycorrhiza and plant growth. Annu Rev Phytopathol 6:297–418

    Article  Google Scholar 

  • Gerdemann JW, Trappe JM (1974) The Endogonaceae in the Pacific northwest. Mycol Mem 5:1–76

    Google Scholar 

  • Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106−114

    Article  Google Scholar 

  • Gianinazzi S, Trouvelot A, Lovato P, Van Tuinen D, Franken P, Gianinazzi-Pearson V (1995) Arbuscular mycorrhizal fungi in plant production of temperate agroecosystems. Crit Rev Biotechnol 15:305–311

    Article  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet M-N, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils. Soil Biol Biochem 30(10-11):1389–1414

    Article  CAS  Google Scholar 

  • Goormachtig S, Alves-Ferreira M, Van Montagu M, Engler G, Holsters M (1997) Expression of cell cycle genes during Sesbania rostrata stem nodule development. Mol Plant Microbe Interact 10:316–325

    Article  CAS  PubMed  Google Scholar 

  • Gordon AJ, Minchin FR, James CL, Komina O (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol 120:867–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goto BT, Silva GA, Assis DMA, Silva DKA, Souza RG, Ferreira ACA, Jobim K, Mello CMA, Vieira HEE, Maia LC, Oehl F (2012) Intraornatosporaceae (Gigasporales), a new family with two new genera and two new species. Mycotaxon 119:117–132

    Article  Google Scholar 

  • Granqvist E, Sun J, Op den Camp R, Pujic P, Hill L, Normand P, Oldroyd GED (2015) Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and non-legumes. New Phytol 207(3):551–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN (2011) Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe Interact 24:1276–1288

    Article  CAS  PubMed  Google Scholar 

  • Hameed A, Egamberdieva D, Abd Allah EF, Hashem A, Kumar A, Ahmad P (2014) Salinity stress and arbuscular mycorrhizal symbiosis in plants. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses, vol 1. Springer Science, New York, pp 139–159

    Chapter  Google Scholar 

  • Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Fujita M, Islam MN, Ahamed KU, Nahar K (2009) Performance of four irrigated rice varieties under different levels of salinity stress. Int J Integr Biol 6:85–90

    Google Scholar 

  • Hasanuzzaman M, Gill SS, Fujita M (2013) Physiological role of nitric oxide in plants grown under adverse environmental conditions. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer Science, New York, pp 269–322

    Chapter  Google Scholar 

  • Hastwell AH, Gresshoff PM, Ferguson BJ (2015) The structure and activity of nodulation-suppressing CLE peptide hormones of legumes. Funct Plant Biol 42:229–238

    CAS  PubMed  Google Scholar 

  • He X, Bledsoe CS, Zasoski RJ, Southworth D (2006) Rapid nitrogen transfer from ectomycorrhizal pines to adjacent ectomycorrhizal and arbuscular mycorrhizal plants in a California oak woodland. New Phytol 170(1):143–115

    Article  CAS  PubMed  Google Scholar 

  • He JL, Li H, Luo J, Ma CF, Li SJ, Qu L, Gai Y, Jiang XN, Janz D, Polle A, Tyree M, Luo ZB (2013) A transcriptomic network underlies microstructural and physiological responses to cadmium in Populus x canescens. Plant Physiol 162:424–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heath KD, Tiffin P (2009) Stabilizing mechanisms in a legume-Rhizobium mutualism. Evolution 63:652–662

    Article  PubMed  Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    Article  CAS  PubMed  Google Scholar 

  • Hirsch AM, McKhann HI, Reddy A, Liao JY, Fang YW, Marshall CR (1995) Assessing horizontal transfer of Nifhdk genes in eubacteria – nucleotide sequence of Nifk from Frankia strain Hfpcci3. Mol Biol Evol 12:16–27

    Article  CAS  PubMed  Google Scholar 

  • Husaini AM, Abdin MZ, Khan S, Xu YW, Aquil S, Anis M (2012) Modifying strawberry for better adaptability to adverse impact of climate change. Curr Sci 102:1660–1673

    CAS  Google Scholar 

  • Jacobs PF, Peterson RL, Massicotte HB (1989) Altered fungal morphogenesis during early stages of ectomycorrhiza formation in Eucalyptus pilularis. Scanning Microsc 3:249–255

    Google Scholar 

  • Jarvis BDW, Van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-marel JC, Gillis M (1997) Transfer of Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tiashanense to Mesorhizobium gen. Nov. Int J Syst Bacteriol 47(3):895–898

    Article  Google Scholar 

  • Jeffries P, Barea JM (2012) Arbuscular mycorrhiza – a key component of sustainable plant-soil ecosystems. In: Hock B (ed) Fungal associations, The Mycota, vol IX, 2nd edn. Springer, Berlin, pp 51–75

    Chapter  Google Scholar 

  • Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Trop Agric 52(2):103–122

    Google Scholar 

  • Jordan DC (1982) Transfer of Rhizobium japonicum to Bradyrhizobium gen nov, a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32(1):136–139

    Article  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    Article  CAS  PubMed  Google Scholar 

  • Kabata-Pendias A, Mukherjee AB (2007) Trace element from soil to huma. Springer, Heidelberg, 550 p

    Book  Google Scholar 

  • Kamalvanshi M, Kumar A, Jha A, Dhyani SK (2012) Occurrence of arbuscular mycorrhizal fungi in rhizosphere of Jatropha curcas L. in arid and semi arid regions of India. Indian J Microbiol 52(3):492–494

    Article  PubMed  Google Scholar 

  • Kapoor R, Evelin H, Giri B (2013) Arbuscular mycorrhiza approaches for abiotic stress tolerance in crop plants for sustainable agriculture. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, New York, pp 359–401

    Chapter  Google Scholar 

  • Karimi A, Khodaverdilo H, Sepiheri M, Sadaghiani MR (2011) Arbuscular mycorrhizal fungi and heavy metal contaminated soil. Afr J Microbiol Res 5(13):1571–1576

    CAS  Google Scholar 

  • Kaschuk G, Leffelaar PA, Giller KE, Alberton O, Hungria M, Kuyper TW (2010) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biol Biochem 42:125–127

    Article  CAS  Google Scholar 

  • Kaur R, Singh A, Kang JS (2014) Influence of different types mycorrhizal fungi on crop productivity. Curr Agric Res 2(1):51–54

    Article  Google Scholar 

  • Keller C, McGrath SP, Dunham SJ (2002) Trace metal leaching through a soil–grassland system after sewage sludge application. J Environ Qual 31:1550–1560

    Article  CAS  PubMed  Google Scholar 

  • Khodaverdiloo H, Samadi A (2011) Batch equilibrium study on sorption, desorption, and immobilization of cadmium in some semiarid-zone soils as affected by soil properties. Soil Res 49(5):444–454

    Article  CAS  Google Scholar 

  • Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobium mutualism. Nature 425:78–81

    Article  CAS  PubMed  Google Scholar 

  • Kijne JW, Pluvque K (1979) Ultrastructural study of the endomembrane system in infected cells of pea and soybean root nodules. Physiol Plant Pathol 14:339–345

    Article  Google Scholar 

  • Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518

    Article  CAS  PubMed  Google Scholar 

  • Kondorosi E, Banfalvi Z, Kondorosi A (1984) Physical and genetic analysis of a symbiotic region of Rhizobium meliloti: identification of nodulation genes. Mol Gen Genet 193:445–452

    Article  CAS  Google Scholar 

  • Kosslak RM, Bookland R, Barkei J, Paaren HE, Appelbaum ER (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci 84:7428–7432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ladha JK, Pareek RP, Becker M (1992) Stem-nodulating legume-Rhizobium symbiosis and its agronomic use in lowland rice. Adv Soil Sci 20:147–192

    Article  Google Scholar 

  • Laloum T, Baudin M, Frances L, Lepage A, Billault-Penneteau B, Cerri MR (2014) Two CCAAT box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis. Plant J 79:757–768

    Article  CAS  PubMed  Google Scholar 

  • Lang C, Seven J, Polle A (2011) Host preferences and differential contributions of deciduous tree species shape mycorrhizal species richness in mixed Central European forest. Mycorrhiza 21:297–308

    Article  PubMed  Google Scholar 

  • Le Strange KK, Bender GL, Djordjevic MA, Rolfe BG, Redmond JW (1990) The Rhizobium strain NGR234 nodD1 gene product responds to activation by simple phenolic compounds vanillin and isovanillin present in wheat seedling extracts. Mol Plant Microbe Interact 3:214–220

    Article  Google Scholar 

  • Lee BR, Muneer S, Avice JC, Jin Jung W, Kim TH (2012) Mycorrhizal colonisation and P-supplement effects on N uptake and N assimilation in perennial ryegrass under well-watered and drought-stressed conditions. Mycorrhiza 22:525–534

    Article  CAS  PubMed  Google Scholar 

  • Legocki RP, Verma DP (1980) Identification of “nodule-specific” host proteins (nodulins) involved in the development of Rhizobium-legume symbiosis. Cell 20(1):153–163

    Article  CAS  PubMed  Google Scholar 

  • Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784

    Article  CAS  PubMed  Google Scholar 

  • Libbenga KR, Harkes PAA (1973) Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta 114:17–28

    Article  CAS  PubMed  Google Scholar 

  • Lipsanen P, Lindström K (1988) Infection and root nodule structure in the Rhizobium galegae sp nov-Galega sp symbiosis. Symbiosis 6:81–96

    Google Scholar 

  • Lum MR, Hirsch AM (2003) Roots and their symbiotic microbes: strategies to obtain nitrogen and phosphorus in a nutrientlimiting environment. J Plant Growth Regul 21:368–382

    Article  CAS  Google Scholar 

  • Luo ZB, Janz D, Jiang X, Göbel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: Insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151(4):1902–1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo ZB, Wu C, Zhang C, Li H, Lipka U, Polle A (2014) The role of ectomycorrhizas in heavy metal stress tolerance of host plants. Environ Exp Bot 108:47–62

    Article  CAS  Google Scholar 

  • Mabood F, Souleimanov A, Khan W, Smith DL (2006) Jasmonates induce Nod factor production by Bradyrhizobium japonicum. Plant Physiol Biochem 44:759–765

    Article  CAS  PubMed  Google Scholar 

  • Manchanda G, Garg N (2007) Endomycorrhizal and rhizobial symbiosis: how much do they share? J Plant Interact 2(2):7988

    Article  CAS  Google Scholar 

  • Manoharachary C, Laxami AN, Kunwar AK (2000) Microbial ecology of polluted soil: some aspects. In: Mukerji KG, Chamola BP, Sharma AK (eds) Glimpses in botany. APH, New Delhi, pp 314–325

    Google Scholar 

  • Manoharachary C, Kunwar IK, Mukerji KG (2002) Some aspects of monotropoid mycorrhizas. In: Mukerji KG et al (eds) Techniques in mycorrhizal studies. Kluwer Academic, Drodrecht, pp 435–441

    Chapter  Google Scholar 

  • Marinho F, Silva GA, Ferreira ACA, Veras JSN, Sousa NMF, Goto BT, Maia LC, Oehl F (2014) Bulbospora minima, new genus and new species in the Glomeromycetes from semi-arid Northeast Brazil. Sydowia 66:313–323

    Google Scholar 

  • Martin KJ (2007) Introduction to molecular analysis of ectomycorrhizal communities. Soil Sci Soc Am J 71:601–610

    Article  CAS  Google Scholar 

  • Martinez E, Puopot R, Prome JC, Pardo MA, Segovia L, Truchet G, Denarie J (1993) Chemical signaling of Rhizobium nodulating bean. In: Palacios R, Mora J, Newton WE (eds) New horizons in nitrogen fixation. Kluwer Academic, Dordrecht, pp 171–176

    Chapter  Google Scholar 

  • Marvel DJ, Torrey JG, Ausubel FM (1987) Rhizobium symbiotic genes required for nodulation of legume and nonlegume hosts. Proc Natl Acad Sci 84(5):1319–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marx J (2004) The roots of plant-microbe collaborations. Science 304:234–236

    Article  PubMed  Google Scholar 

  • Massicotte HB, Ackerley CA, Peterson RL (1987) The root-fungus interface as a indicator of symbiont interaction in ectomycorrhizae. Can J Forest Res 17:846–854

    Article  Google Scholar 

  • Mathur N, Singh J, Bohra S, Vyas A (2007) Arbuscular mycorrhizal status of medicinal halophytes in saline areas of Indian Thar Desert. Int J Soil Sci 2:119–127

    Article  Google Scholar 

  • Medina J, Cornejo P, Borie F, Meyer S, Palenzuela J, Vieira HEE, Ferreira ACA, Silva GA, Sánchez-Castro I, Oehl F (2014) Corymbiglomus pacificum, a new glomeromycete from a saline lakeshore in Chile. Mycotaxon 127:173–183

    Article  Google Scholar 

  • Miyasaka SC, Habte M, Friday JB, Johnson EV (2003) Manual on arbuscular mycorrhizal fungus production and inoculation techniques. Soil Crop Manage 5:4

    Google Scholar 

  • Molina R, Trappe JM (1982) Lack of mycorrhizal specificity by the ericaceous hosts Arbutus menziesii and Arctostaphylos uva-ursi. New Phytol 90:495–509

    Article  Google Scholar 

  • Monika A, Gorzelak AKA, Pickles BJ, Suzanne WS (2015) Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 2:7

    Google Scholar 

  • Moore D, Robson GD, Anthony TAPJ (2011) 21st Century guidebook to fungi. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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 37:471–491

    Google Scholar 

  • Morton JB, Redecker D (2001) Two new families of Glomales, Archaeosporaceae and Paraglomaceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93:181–195

    Article  Google Scholar 

  • Newcomb W (1979) Control of morphogenesis and differentiation of pea root nodules. In: Newton WE, Orme-Johnson WH (eds) Nitrogen fixation symbiotic associations and cyanobacteria, vol 2. University Park Press, Baltimore, pp 87–102

    Google Scholar 

  • Noe R, Hammerstein P (1994) Biological markets–supply-and-demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol 35:1–11

    Article  Google Scholar 

  • Noel KD, Vanden Bosch KA, Kulpaca B (1986) Mutations in Rhizobium phaseoli that lead to arrested development of infection threads. J Bacteriol 168:1392–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuti MP, Lepidi AA, Prakash RK, Schilperoort RA, Cannon FC (1979) Evidence for nitrogen fixation (nif) genes on indigenous Rhizobium plasmids. Nature 282:533–535

    Article  CAS  Google Scholar 

  • Oehl F, Souza F, Sieverding E (2008) Revision of Scutellospora and description of five new genera and three new families in the arbuscular mycorrhiza forming Glomeromycetes. Mycotaxon 106:311–360

    Google Scholar 

  • Oehl F, Silva GA, Goto BT, Maia LC, Sieverding E (2011a) Glomeromycota: two new classes and a new order. Mycotaxon 116:365–379

    Article  Google Scholar 

  • Oehl F, Sieverding E, Palenzuela J, Ineichen K, Alves da Silva G (2011b) Advances in Glomeromycota taxonomy and classification. IMA Fungus 2(2):191–199

    Article  PubMed  PubMed Central  Google Scholar 

  • Oehl F, Sánchez-Castro I, Palenzuela J, Silva GA (2015) Palaeospora spainii, a new arbuscular mycorrhizal fungus from Swiss agricultural soils. Nova Hedwigia 101:89–102

    Article  Google Scholar 

  • Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17

    Article  CAS  Google Scholar 

  • Oke V, Long SR (1999) Bacteroid formation in the Rhizobium-legume-symbiosis. Curr Opin Microbiol 2:641–646

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546

    Article  CAS  PubMed  Google Scholar 

  • Ott T, van Dongen JT, Günther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531–535

    Article  CAS  PubMed  Google Scholar 

  • Pagano MC, Oehl F, Silva, GA, Maia LC, Silva DK, Cabello MN (2016) Advances in arbuscular mycorrhizal taxonomy. In: Pagano M (ed) Recent advances on mycorrhizal fungi. Fungal biology. Springer, Cham

    Chapter  Google Scholar 

  • Palenzuela J, Ferrol N, Boller T, Azcón-Aguilar C, Oehl F (2008) Otospora bareai, a new fungal species in the Glomeromycetes from a dolomitic shrub-land in the National Park of Sierra de Baza (Granada, Spain). Mycologia 100:282–291

    Article  Google Scholar 

  • Pandolfini T, Gremigni P, Gabbrielli R (1997) Biomonitoring of soil health by plants. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CAB International, New York, pp 325–347

    Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  CAS  PubMed  Google Scholar 

  • Peng G, Yuan Q, Li H, Zhang W, Tan Z (2008) Rhizobium oryzae sp nov, isolated from the wild rice Oryza alta. Int J Syst Evol Microbiol 58:2158–2163

    Article  CAS  PubMed  Google Scholar 

  • Peskan-Berghofer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelmuller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant–microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plant 122:465–477

    Article  CAS  Google Scholar 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980

    Article  CAS  PubMed  Google Scholar 

  • Pham GH, Kumari R, Singh A, Sachdev M, Prasad R, Kaldorf M, Buscot F, Oelmüller R, Tatjana P, Weiss M, Hampp R, Varma A (2004) Axenic cultures of Piriformospora indica. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Heidelberg, pp 593–616

    Google Scholar 

  • Phillips DA (1971) Abscisic acid inhibition of root nodule initiation in Pisum sativum. Planta 100:181–190

    Article  CAS  PubMed  Google Scholar 

  • Phillips DA, Torrey JG (1970) Cytokinin production by Rhizobium japonicum. Physiol Plant 23:1057–1063

    Article  CAS  Google Scholar 

  • Pontes JS, Sánchez-Castro I, Palenzuela J, Maia LC, Silva GA, Oehl F (2013) Scutellospora alterata, a new gigasporalean species from the semi-arid Caatinga biome in Northeastern Brazil. Mycotaxon 125:169–181

    Article  Google Scholar 

  • Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315

    Article  CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  • Prakash RK, Schilperoort RA, Nuti MP (1981) Large plasmids of fast-growing rhizobia: homology studies and location of structural nitrogen fixation (nif) genes. J Bacteriol 145:1129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R (2013) Hydrogen peroxide and nitric oxide: key regulators of the legume Rhizobium and mycorrhizal symbioses. Antioxid Redox Signal 18:2202–2219

    Article  CAS  PubMed  Google Scholar 

  • Qiang X, Weiss M, Kogel KH, Schäfer P (2011) Piriformospora indica – a mutualistic basidiomycete with an exceptionally large plant host range. Mol Plant Pathol 13:508–518

    Article  PubMed  PubMed Central  Google Scholar 

  • Rae AL, Bonfante-Fasolo P, Brewin NJ (1992) Structure and growth of infection threads in the legume symbiosis with Rhizobium leguminosarum. Plant J 2:385–395

    Article  Google Scholar 

  • Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128

    Article  PubMed  Google Scholar 

  • Ray JG, Valsalakumar N (2010) Arbuscular mycorrhizal fungi and Piriformospora indica individually and in combination with Rhizobium on green gram. J Plant Nutr 33:285–298

    Article  CAS  Google Scholar 

  • Raziuddin F, Hassan G, Akmal M, Shah SS, Mohammad F, Shafi M, Bakht J, Zhou W (2011) Effects of cadmium and salinity on growth and photosynthesis parameters of Brassica species. Pak J Bot 43(1):333–340

    CAS  Google Scholar 

  • Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374

    Article  CAS  Google Scholar 

  • Read DJ, Duckett JG, Francis R, Ligrone R, Russel A (2000a) Symbiotic fungal associations in “lower” land plants. Philos Trans R Soc Biol Sci 355:815–831

    Article  CAS  Google Scholar 

  • Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000b) Symbiotic fungal associations in ‘lower’ land plants. Philos Trans R Soc Lond B Biol Sci 355:815–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redecker D, Schüßler A (2014) Glomeromycota. In: Mclaughlin DJ, Spatafora JW (eds) The Mycota: a comprehensive treatise on fungi as experimental systems for basic and applied research, systematics and evolution Part A. Springer, New York

    Google Scholar 

  • Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature 323:632–635

    Article  CAS  Google Scholar 

  • Reid DE, Ferguson BJ, Hayashi S, Lin YH, Gresshoff PM (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108:789–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhijn V, Vanderleyden J (1995) The Rhizobium-plant symbiosis. Microbiol Rev 59:124–142

    PubMed  PubMed Central  Google Scholar 

  • Rhijn V, Feys PJS, Verreth BC, Vanderleyden J (1993) Multiple copies of nodD in Rhizobium tropici CIAT899 and BR816. J Bacteriol 175:438–447

    Article  PubMed  PubMed Central  Google Scholar 

  • Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45

    Google Scholar 

  • Rosas JC, Castro JA, Robleto EA, Handelsman J (1998) A method for screening Phaseolus vulgaris L germplasm for preferential nodulation with a selected Rhizobium etli strain. Plant Soil 203:71–78

    Article  CAS  Google Scholar 

  • Rosenberg C, Boistard P, Denarie J, Casse-Delbart F (1981) Genes controlling early and late functions in symbiosis are located on a megaplasmid in Rhizobium meliloti. Mol Gen Genet 184:326–333

    CAS  PubMed  Google Scholar 

  • Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178:253–266

    Article  PubMed  Google Scholar 

  • Rossen L, Shearman CA, Johnston AWB, Downie JA (1985) The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant exudate induces the nodA,B,C genes. EMBO J 4:3369–3373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rostas K, Kondorosi E, Horvath B, Simoncsits A, Kondorosi A (1986) Conservation of extended promoter regions of nodulation genes in Rhizobium. Proc Natl Acad Sci 83:1757–1761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roth LE, Stacey G (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49(1):13–23

    CAS  PubMed  Google Scholar 

  • Roth LE, Jeon K, Stacey G (1988) Homology in endosymbiotic systems. In: Palcios R, Verma DPS, St Paul MN (eds) The term “symbiosome”. Molecular genetics of plant microbe interactions. ADS Press, St Paul, pp 220–225

    Google Scholar 

  • Rozahon M, Ismayil N, Hamood B, Erkin R, Abdurahman M, Mamtimin H, Abdukerim M, La R, Rahman E (2014) Rhizobiun populi sp. nov., an endophytic bacterium isolated from Populus euphratica. Int J Syst Evol Microbiol 64:3215–3221

    Article  CAS  PubMed  Google Scholar 

  • Salminen SO, Streeter JG (1992) Labeling of carbon pools in Bradyrhizobium japonicum and Rhizobium leguminosarum bv viciae bacteroids following incubation of intact nodules with 14CO2. Plant Physiol 100:597–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandeep C, Mohanb V, Viswanatha S (2015) Significance of ectomycorrhizae in forest ecosystems of India. Int J Plant Anim Environ Sci 5:23–31

    Google Scholar 

  • Sanders IR, Croll D (2010) Arbuscular mycorrhiza: a challenge to understand the genetics of the fungal partner. Ann Rev Genet 44:271–292

    Article  CAS  PubMed  Google Scholar 

  • Schouteden N, De Waele D, 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. Published in libraries at The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University

    Google Scholar 

  • Schüßler 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 163–185

    Chapter  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schüßler A, Krüger M, Walker C (2009) Phylogeny, evolution and origin of the ‘plant-symbiotic’ phylum Glomeromycota. In: Wöstemeyer J, Martin W (eds) The Mycota XIV – evolution of fungi and fungal-like organisms. Springer, Berlin

    Google Scholar 

  • Selosse MA, Setaro S, Glatard F, Richard F, Urecelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878

    Article  CAS  PubMed  Google Scholar 

  • Sethi IK, Walia SK (2018) Text book of Fungi and their allies, 2nd edn. Scientific International, New Delhi

    Google Scholar 

  • Sharifi E (1983) Parasitic origins of nitrogen-fixing Rhizobium-legume symbioses: a review of the evidence. Biosystems 16:269–289

    Article  PubMed  Google Scholar 

  • Sherameti I, Tripathi S, Varma A, Oelmuller R (2008) The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant Microbe Interact 21:799–807

    Article  CAS  PubMed  Google Scholar 

  • Sieberer BJ, Timmers AC, Emons AM (2005) Nod factors alter the microtubule cytoskeleton in Medicago truncatula root hairs to allow root hair reorientation. Mol Plant Microbe Interact 18:1195–1204

    Article  CAS  PubMed  Google Scholar 

  • Sieverding E, Silva GA, Berndt R, Oehl F (2014) Rhizoglomus, a new genus in the Glomeraceae. Mycotaxon 129:373–386

    Article  Google Scholar 

  • Silva GA, Maia LC, Oehl F (2012) Phylogenetic systematics of the Gigasporales. Mycotaxon 122:207–222

    Article  Google Scholar 

  • Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69

    Article  Google Scholar 

  • Singh A, Varma A (2000) Orchidaceous mycorrhizal fungi. In: Mukerji KG (ed) Mycorrhizal biology. Kluwer Academic/Plenum, New York, pp 265–288

    Chapter  Google Scholar 

  • Singh A, Sharma J, Rexer KH, Varma A (2000) Plant productivity determinants beyond minerals, water and light. Piriformospora indica: a revolutionary plant growth promoting fungus. Curr Sci 79:101–106

    Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, San Diego

    Google Scholar 

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

    Google Scholar 

  • Smith SE, Smith AF, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spain JL, Sieverding E, Oehl F (2006) Appendicispora, a new genus in the arbuscular mycorrhizal-forming Glomeromycetes, with a discussion of the genus Archaeospora. Mycotaxon 97:163–182

    Google Scholar 

  • Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ (1987) Promoters in nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1Jl. Plant Mol Biol 9:29–37

    Article  Google Scholar 

  • Sprent (1980) Root nodule anatomy, type of export product and evolutionary origin of some Leguminosae. Plant Cell Environ 3:35–43

    CAS  Google Scholar 

  • Srivastava D, Kapoor R, Srivastava SK, Mukerji KG (1996) Vesicular arbuscular mycorrhiza-an overview. In: Mukerji KG (ed) Concepts in mycorrhizal research, vol 813. Kluwer Academic, Dordrecht, pp 1–39

    Google Scholar 

  • Sudha KH, Narula A, Kumar S, Srivastava PS, Varma A (1999) Mycorrhiza aided biological hardening of in vitro raised plantlets. In: Tewari JP, Lakhanpal TN, Singh J, Gupta R, Chamola BP (eds) Advances in microbial biotechnology. APH, Delhi, pp 469–485

    Google Scholar 

  • Sun CA, Johnson J, Cai DG, Sherameti I, Oelmuller R, Lou BG (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017

    Article  CAS  PubMed  Google Scholar 

  • Szuba A, Karliński L, Krzesłowska M, Hazubska-Przybył T (2017) Inoculation with a Pb-tolerant strain of Paxillus involutus improves growth and Pb tolerance of Populus × canescens under in vitro conditions. Plant Soil 412(1–2):253–266

    Article  CAS  Google Scholar 

  • Tedersoo L, Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytol 185:351–354

    Article  PubMed  Google Scholar 

  • Thamer S, Schädler M, Bonte D, Ballhorn DJ (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant Soil 34:1209–1219

    Google Scholar 

  • Tillard P, Drevon JJ (1988) Nodulation and nitrogenase activity of chickpea cultivar INRA199 inoculated with different strains of Rhizobium ciceri. Agronomie 8:387–392

    Article  Google Scholar 

  • Torok I, Kondorosi E, Stepkowski T, Pósfai J, Kondorosi A (1984) Nucleotide sequence of Rhizobium meliloti nodulation genes. Nucleic Acids Res 12(24):9509–9524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 U S A 112(25):7785–7790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trinchant JC, Rigaud J (1989) Alternative energy-yielding substrates for bacteroids isolated from stem and root nodules of Sesbania rostrata submitted to O2 restricted conditions. Plant Sci 59:141–149

    Article  CAS  Google Scholar 

  • Trinick MJ (1979) Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii Planch. Can J Microbiol 25:565–578

    Article  CAS  PubMed  Google Scholar 

  • Truchet G, Roche P, Lerouge P, Vasse J, Camut S, de Billy F, Promé JC, Dénarié J (1991) Sulphated lipooligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfafa. Nature 351:670–673

    Article  CAS  Google Scholar 

  • Tu JC (1977) Structural organization of the rhizobial root nodule of alfalfa. Can J Bot 55:35–43

    Article  Google Scholar 

  • Turk MA, Asaf TA, Hameed KM, Al-Tawaha AM (2006) Significance of mycorrhizae. World J Agric Sci 2(1):16–20

    Google Scholar 

  • Udvardi MK, Day DA (1990) Ammonia (’4C-methylamine) transport across the bacteroid and peribacteroid membranes of soybean root nodules. Plant Physiol 94:71–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Physiol Plant Mol Biol 48:493–523

    Article  CAS  PubMed  Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805

    Article  CAS  PubMed  Google Scholar 

  • Unnikumar KR, Sowjanya SK, Varma A (2013) Piriformospora indica: a versatile root endophytic symbiont. Symbiosis 60:107–113

    Article  Google Scholar 

  • Van Brussel AAN, Bakhulzen R, Van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJJ, Keijne JW (1992) Induction of pre-infection thread structures in the host plant by lipo-oligosaccharides of Rhizobium. Science 257:70–72

    Article  PubMed  Google Scholar 

  • 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 11:296–310

    Article  PubMed  Google Scholar 

  • Vandenbosch KA, Noel KD, Kaneko Y, Newcomb EH (1985) Nodule initiation elicited by noninfective mutants of Rhizobium phaseoli. J Bacteriol 162(3):950–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Varma A, Verma S, Sudha SN, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65(6):2741–2744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Varma A, Singh A, Sudha M, Sahay NS, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K, Hurek T, Blechert O, Rexer KH, Kost G, Hahn A, Maier W, Walter M, Strack D, Kranner I (2001) Piriformospora indica: a cultivable mycorrhiza-like endosymbiotic fungus. In: Hock B (ed) The Mycota IX. Springer, Berlin, pp 125–150

    Google Scholar 

  • Varma A, Bakshi M, Lou B, Hartmann B, Oelmueller R (2012) Piriformospora indica: a novel plant growth-promoting mycorrhizal fungus. Agric Res 1:117. https://doi.org/10.1007/s40003-012-0019-5

    Article  Google Scholar 

  • Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–216

    Article  PubMed  Google Scholar 

  • Verma S, Varma A, Rexer K-H, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:898–905

    Article  Google Scholar 

  • Vierheilig H, Lerat S, Piché Y (2003) Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170

    Article  CAS  PubMed  Google Scholar 

  • Vierheilig H, Schweigerb P, Brundrettc M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiol Plant 125:393–404

    CAS  Google Scholar 

  • Voegelin A, Barmettler K, Kretzschmar R (2003) Heavy metal release from contaminated soils: comparison of column leaching and batch extraction results. J Environ Qual 32:865–875

    Article  CAS  PubMed  Google Scholar 

  • Walker C (1992) Systematics and taxonomy of the arbuscular endomycorrhizal fungi (Glomales)-a possible way forward. Agronomie 12:887–897

    Article  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Qui YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299–363

    Article  CAS  PubMed  Google Scholar 

  • Weiβ M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1002–1010

    Google Scholar 

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227

    Article  Google Scholar 

  • Williams PM, Mallorca MS (1982) Abscisic acid and gibberellin-like substances in roots and root nodules of Glycine max. Plant Soil 65:19–26

    Article  CAS  Google Scholar 

  • Wilson GWT, Hartnett DC, Rice WC (2006) Mycorrhizal-mediated phosphorus transfer between tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana. Funct Ecol 20:427–435

    Article  Google Scholar 

  • Wu QS, Xia RX (2003) Research and application on vesicular-arbuscular mycorrhiza of fruit trees. Plant Physiol Commun 39:536–540

    Google Scholar 

  • Wu QS, Xia SR (2004) The relation between vesicular -arbuscular mycorrhizae and water metabolism in plants. Chin Agric Sci Bull 1:188–192

    Google Scholar 

  • Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaat SAJ, Wijffelman CA, Spaink HP, van Brussel AAN, Okker RJH, Lugtenberg BJJ (1987) Induction of the nodA promoter of Rhizobium leguminosarum sym plasmid pRL1JI by plant flavanones and flavones. J Bacteriol 169:198–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zahran HH (1999) Rhizobium-Legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 3(4):968–989

    Google Scholar 

  • Zarea MJ, Hajinia S, Karimi N, Goltapeh EM, Rejali F, Varma A (2012) Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol Biochem 45:139–146

    Article  CAS  Google Scholar 

  • Zhang XX, Sun L, Ma XT, Sui XH, Jiang RB (2011) Rhizobium pseudoryzae sp. nov., isolated from the rhizosphere of rice. Int J Syst Evol Microbiol 61:2425–2429

    Article  CAS  PubMed  Google Scholar 

  • Zhang YJ, Zheng WT, Everall I, Young JP, Zhang XX (2015) Rhizobium anhuiense sp. nov., isolated from effective nodules of Vicia faba and Pisum sativum. Int J Syst Evol Microbiol 65:2960–2967

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, SGTB Khalsa College, University of Delhi, Delhi, India

    Surinder Kaur & Gurpreet Kaur

Authors
  1. Surinder Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gurpreet Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Botany, Swami Shraddhanand College, University of Delhi, Delhi, India

    Bhoopander Giri

  2. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ram Prasad

  3. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ajit Varma

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kaur, S., Kaur, G. (2018). Morphological and Physiological Aspects of Symbiotic Plant–Microbe Interactions and Their Significance. In: Giri, B., Prasad, R., Varma, A. (eds) Root Biology. Soil Biology, vol 52. Springer, Cham. https://doi.org/10.1007/978-3-319-75910-4_15

Download citation

Publish with us

Policies and ethics

Search

Navigation