Advertisement

Exploring the Role of Plant-Microbe Interactions in Improving Soil Structure and Function Through Root Exudation: A Key to Sustainable Agriculture

  • Kanchan Vishwakarma
  • Mitali Mishra
  • Shruti Jain
  • Jaspreet Singh
  • Neha Upadhyay
  • Rishi Kumar Verma
  • Pankaj Verma
  • Durgesh Kumar Tripathi
  • Vivek Kumar
  • Rohit Mishra
  • Shivesh SharmaEmail author
Chapter

Abstract

The most astonishing feature of plant roots is their capability of secreting a broad variety of compounds ranging from low molecular to high molecular weights into the rhizosphere. These compounds act as signals for establishing and regulating the interactions among plant roots and microorganisms present in rhizosphere through different mechanisms. The mechanism of establishment of these relationships includes complex signaling cascades and involves different transporter proteins. Exudation is an important process that influences the microbial diversity and relevant biological activities. In addition, these secretions mediate the phenomena of mineral uptake in soil with low nutrient content either through chelation directly or by affecting biological activity of microbes. Further, microbes associated with plants have the potential to upgrade phytoremediation efficiency by facilitating phytoextraction and phytostabilization and through increase in biomass production by plants. Overall these exudation-mediated plant-microbe interactions influence the soil structurally and functionally via orchestrating microbial richness, nutrient acquisition, and phytoremediation. Hence, in light of this, the chapter is intended to provide the perceptivity to comprehend the impact of root exudation-mediated plant-microbe interactions in enriching the structural and functional characteristics of soil.

Keywords

Root exudates Microbial diversity Soil Phytoremediation Rhizobacteria 

Notes

Acknowledgment

The authors are thankful to Director MNNIT Allahabad and Design and Innovation Centre (DIC) MNNIT Allahabad for providing necessary facilities to carry out the research work.

References

  1. Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Azaizeh HA, Marschner H, Romheld V, Wittenmayer L (1995) Effects of a vesicular-arbuscular mycorrhizal fungus and other soil microorganisms on growth, mineral nutrient acquisition and root exudation of soil-grown maize plants. Mycorrhiza 5:321–327CrossRefGoogle Scholar
  3. Azcon-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens—an overview of the mechanisms involved. Mycorrhiza 6:457–464CrossRefGoogle Scholar
  4. Babu AG, Reddy S (2011) Dual inoculation of arbuscular mycorrhizal and phosphate solubilizing fungi contributes in sustainable maintenance of plant health in fly ash ponds. Water Air Soil Pollut 219:3–10CrossRefGoogle Scholar
  5. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  6. Badri DV, Loyola-Vargas VM, Broeckling CD (2008) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 146:762–771PubMedPubMedCentralCrossRefGoogle Scholar
  7. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013a) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512PubMedPubMedCentralCrossRefGoogle Scholar
  8. Badri DV, Zolla G, Bakker MG, Manter DK, Vivanco JM (2013b) Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol 198:264–273PubMedCrossRefGoogle Scholar
  9. Bais HP, Park S-W, Stermitz FR, Halligan KM, Vivanco JM (2002a) Exudation of fluorescent -carbolines from Oxalis tuberosa L. roots. Phytochemistry 61:539–543PubMedCrossRefGoogle Scholar
  10. Bais HP, Walker TS, Schweizer HP, Vivanco JM (2002b) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of sweet basil (Ocimum basilicum L.) Plant Physiol Biochem 40:983–995CrossRefGoogle Scholar
  11. Bais HP, Walker TS, Stermitz FR, Hufbauer RA, Vivanco JM (2002c) Enantiomeric dependent phytotoxic and antimicrobial activity of (±)-catechin; a rhizosecreted racemic mixture from Centaurea maculosa (spotted knapweed). Plant Physiol 128:1173–1179PubMedCrossRefGoogle Scholar
  12. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trend Plant Sci 9:26–32CrossRefGoogle Scholar
  13. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266PubMedCrossRefGoogle Scholar
  14. Bais HP, Broeckling CD, Vivanco JM (2008) Root exudates modulate plant–microbe interactions in the rhizosphere in secondary metabolites in soil ecology. Soil Biol 14(241):252Google Scholar
  15. Bar-Yosef B (1991) Root excretions and their environmental effects: influence on availability of phosphorus. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 529–557Google Scholar
  16. Becard G, Douds DD, Pfeffer PE (1992) Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in presence of CO2 and flavonols. Appl Environ Microbiol 58:821–825PubMedPubMedCentralGoogle Scholar
  17. Becard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW (1995) Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbiosis. Mol Plant-Microbe Interact 8:252–258CrossRefGoogle Scholar
  18. Bennett AE, Alers-Garcia J, Bever JD (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. Am Nat 167:141–152PubMedGoogle Scholar
  19. Benoit LF, Berry AM (1997) Flavonoid-like compounds from seeds of red alder (Alnus rubra) influence host nodulation by Frankia (Actinomycetales). Plant Physiol 99:588–593CrossRefGoogle Scholar
  20. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83CrossRefGoogle Scholar
  21. Besserer A, Puech-Page ‘s V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Be Card G, Sejalon Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoSBiol 4:e226CrossRefGoogle Scholar
  22. Bowen GD (1979) Integrated and experimental approaches to study the growth of organisms around root and seeds. In: Schippers B, Gams W (eds) Soil-borne pathogens. Academic, London, pp 209–227Google Scholar
  23. Bowen GD, Rovira AD (1991) The rhizosphere: the hidden half of the hidden half. In: Waisel Y, Eshel A, Kalkafi U (eds) Plant Roots: The Hidden Half. Marcel Dekker, New York, pp 641–669Google Scholar
  24. Brigham LA, Michaels PJ, Flores HE (1999) Cell-specific production and antimicrobial activity of naphthoquinones in roots of Lithospermum erythrorhizon. Plant Physiol 119:417–428PubMedPubMedCentralCrossRefGoogle Scholar
  25. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744PubMedCrossRefGoogle Scholar
  26. Buee M, Rossigno M, Jauneaul A, Ranjeva R, Becard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Am Phyto-Pathol Soc, MPMI 13(6):693–698Google Scholar
  27. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 90:521–523CrossRefGoogle Scholar
  28. Cameron DD, Neal AL, Van Wees SCM, Ton J (2013) Mycorrhiza induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chabot S, Bel-Rhlid R, Chênevert R, Piché Y (1992) Hyphal growth promotion in vitro of the VA mycorrhizal fungus, Gigaspora margarita Becker & Hall, by the activity of structurally specific flavonoids compounds under CO2-enriched conditions. New Phytol 122:461–467CrossRefGoogle Scholar
  30. Chandler D, Davidson G, Grant WP, Greaves J, Tatchell GM (2008) Microbial biopesticides for integrated crop management: an assessment of environmental and regulatory sustainability. Trends Food Sci Tech 19:275–283CrossRefGoogle Scholar
  31. Chaparro JM, SheflinAM MDK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499CrossRefGoogle Scholar
  32. Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS One 8:e5573CrossRefGoogle Scholar
  33. Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365PubMedCrossRefGoogle Scholar
  34. Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249PubMedCrossRefGoogle Scholar
  35. Czarnota MA, Rimando AM, Weston LA (2003) Evaluation of root exudates of seven sorghum accessions. J Chem Ecol 29:2073–2083PubMedCrossRefGoogle Scholar
  36. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47CrossRefGoogle Scholar
  37. de Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by pseudomonas fluorescens. Mol Plant-Microbe Interact 15:1173–1180PubMedCrossRefGoogle Scholar
  38. Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci U S A 101:15249–15254PubMedPubMedCentralCrossRefGoogle Scholar
  39. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium tolerance and mineral nutrition. FEBS Lett 581:2255–2262PubMedCrossRefGoogle Scholar
  40. Derrien D, Marol C, Balesdent J (2004) The dynamics of neutral sugars in the rhizosphere of wheat. An approach by 13C pulse-labelling and GC/C/IRMS. Plant Soil 267:243–253CrossRefGoogle Scholar
  41. Diener AC, Gaxiola RA, Fink GR (2001) Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell 13:1625–1637PubMedPubMedCentralCrossRefGoogle Scholar
  42. Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7PubMedCentralCrossRefGoogle Scholar
  43. Flores HE, Pickard JJ, Hoy MW (1988) Production of polyacetylenes and thiophenes in heterotrophic and photosynthetic root cultures of Asteraceae. Biol Mol 7:233–254Google Scholar
  44. Flores HE, Vivanco JM, Loyola-Vargas VM (1999) “Radicle” biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226PubMedCrossRefGoogle Scholar
  45. Fray RG (2002) Altering plant-microbe interaction through artificially manipulating bacterial quorum sensing. Ann Bot 89:245–253PubMedPubMedCentralCrossRefGoogle Scholar
  46. Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091PubMedCrossRefGoogle Scholar
  47. Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279PubMedCrossRefGoogle Scholar
  48. Geibel M (1994) Sensitivity of the fungus Cytospora persoonii to the flavonoids of Prunus cerasus. Phytochemistry 38:599–601CrossRefGoogle Scholar
  49. Giovannetti M, Sbrana C, Citernesi AS, Avio L (1996) Analysis of factors involved in fungal recognition responses to host-derived signals by arbuscular mycorrhizal fungi. New Phytol 133:65–71CrossRefGoogle Scholar
  50. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374PubMedCrossRefGoogle Scholar
  51. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Hindawi Publishing Corporation, ScientificaGoogle Scholar
  52. Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242CrossRefGoogle Scholar
  53. Goodman CD, Casati P, Walbot V (2004) A multidrug resistance associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hammad Y, Nalin R, Marechal K, Fiasson K, Pepin R, Berry AM, Normand P, Domenach AM (2003) A possible role for phenylacetic acid (PAA) in Alnus glutinosa nodulation by Frankia. Plant Soil 254:193–205CrossRefGoogle Scholar
  55. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedCrossRefGoogle Scholar
  56. Hertenberger G, Zampach P, Bachmann G (2002) Plant species affect the concentration of free sugars and free amino acids in different types of soil. J Plant Nutr Soil Sci 165:557–565CrossRefGoogle Scholar
  57. Hirsch AM (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84:858–868CrossRefGoogle Scholar
  58. Hirsch AM, Lum MR, Downie JA (2001) What makes rhizobia-legume symbiosis so special? Plant Physiol 127:1484–1492PubMedPubMedCentralCrossRefGoogle Scholar
  59. Horiuchi J, Prithiviraj B, Bais HP, Kimball BA, Vivanco JM (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222:848–857PubMedCrossRefGoogle Scholar
  60. Hutchison WD, Campbell CD (1994) Economic impact of sugarbeet root aphid (Homoptera: Aphididae) on sugarbeet yield and quality in Southern Minnesota restricted access. J Eco Entmo 28:465–475CrossRefGoogle Scholar
  61. Hutsch BW, Augustin J, Merbach W (2000) Plant rhizodeposition an important source for carbon turnover in soils. J Plant Nut Soil Sci 165:397–407CrossRefGoogle Scholar
  62. Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier MH (2003) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. European J Biochem 270:799–813CrossRefGoogle Scholar
  63. Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286:24649–24655PubMedPubMedCentralCrossRefGoogle Scholar
  64. Jain V, Nainawatee HS (2002) Plant flavonoids: signals to legume nodulation and soil microorganisms. J Plant Biochem Biotechnol 11:1–10CrossRefGoogle Scholar
  65. Jasinski M, Stukkens Y, Degand H, Purnell B (2002) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13:1095–1107CrossRefGoogle Scholar
  66. Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44CrossRefGoogle Scholar
  67. Jones DL, Darrah PR (1994a) Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant Soil 163:1–12CrossRefGoogle Scholar
  68. Jones DL, Darrah PR (1994b) Role of root derived organic acids in the mobilization of nutrients in the rhizosphere. Plant Soil 166:247–257CrossRefGoogle Scholar
  69. Kamilova F (2006) Organic acids, sugars, and L-tryptophan in exudates of vegetables growing on stone wool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe 19:250–256CrossRefGoogle Scholar
  70. Kang BG, Kim WT, Yun HS, Chang SC (2010) Use of plant growth-promoting rhizobacteria to control stress responses of plant roots. Plant Biotechnol Rep 4:179–183CrossRefGoogle Scholar
  71. Keyes WJ, O’Malley RC, Kim D, Lynn DG (2000) Signaling organogenesis in parasitic angiosperms: xenognosin generation, perception, and response. J Plant Growth Regul 19:217–231PubMedGoogle Scholar
  72. Khan MS, Zaidi A, Musarrat J (eds) (2009a) Microbes in sustainable agriculture, Nova science Publisher. USA, New YorkGoogle Scholar
  73. Khan MS, Zaidi A, Wani PA, Oves M (2009b) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19CrossRefGoogle Scholar
  74. Kidd P, Barcelo J, Bernal MP, Navari-Izzo F, Poschenrieder C, Shilev S et al (2009) Trace element behaviour at the root–soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259CrossRefGoogle Scholar
  75. Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581:2273–2280PubMedCrossRefGoogle Scholar
  76. Kim HB, Oh CJ, Lee H, Sun An C (2003) A type-i chalcone isomerase mRNA is highly expressed in the root nodules of Elaeagnus umbellata. J Plant Biol 46:263–270CrossRefGoogle Scholar
  77. Kim D-Y, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50(207):218Google Scholar
  78. Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097PubMedCrossRefGoogle Scholar
  79. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, vanVeen JA (2002) Effects of above-ground species composition and diversity on the diversity of soil borne microorganisms. Antonie Van Leeuwenhoek 81:509–520PubMedCrossRefGoogle Scholar
  80. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) Putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363PubMedCrossRefGoogle Scholar
  81. Kuang Y, Wen D, Zhong C, Zhou G (2002) Root exudates and their roles in phytoremediation. Acta Phyto Ecol Sinica 27(5):709–717Google Scholar
  82. Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M et al (2010) Culturable bacteria from Zn- and cd accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108(4):1471–1484PubMedCrossRefGoogle Scholar
  83. Larson RA, Marley KA, Tuveson RW, Berenbaum MR (1988) Carboline alkaloids: mechanisms of phototoxicity to bacteria and insects. Photochem Photobiol 48:665–674PubMedCrossRefGoogle Scholar
  84. Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522PubMedCrossRefGoogle Scholar
  85. Li L, He Z, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterisation of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277:5360–5368PubMedCrossRefGoogle Scholar
  86. Ling N, Raza W, Ma JH, Huang QW, Shen QR (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Eur J Soil Biol 47:374–379CrossRefGoogle Scholar
  87. Liu JP, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminium tolerance. Plant J 57:389–399PubMedCrossRefGoogle Scholar
  88. Luo SL, Chen L, Chen JI, Xiao X, Xu TY, Wan Y et al (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd hyperaccumulator Solanum nigrum L and their potential use for phytoremediation. Chemosphere 85:1130–1138PubMedCrossRefGoogle Scholar
  89. Luo S, Xu T, Chen L, Chen J, Rao C, Xiao X et al (2012) Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Appl Microbiol Biotechnol 93:1745–1753PubMedCrossRefGoogle Scholar
  90. Lupwayi NZ, Rice WA, Clayton GW (1998) Soil microbial diversity and community structure under wheat as influenced by tillage and crop rotation. Soil Biol Biochem 30:1733–1741CrossRefGoogle Scholar
  91. Lynch JM, Whipps JM (1990) Substrate flows in the rhizosphere. Plant Soil 129:1–10CrossRefGoogle Scholar
  92. Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278PubMedCrossRefGoogle Scholar
  93. Ma Y, Rajkumar M, Luo Y, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants – effects on plant growth and Ni uptake. J Hazard Mater 196:230–237CrossRefGoogle Scholar
  94. Magalhaes JV (2010) How a microbial drug transporter became essential for crop cultivation on acid soils: aluminium tolerance conferred by the multidrug and toxic compound extrusion (MATE) family. Ann Bot 106:199–203PubMedPubMedCentralCrossRefGoogle Scholar
  95. Magalhaes JV, Liu J, Guimaraes CT (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161PubMedCrossRefGoogle Scholar
  96. Marschner H, Romheld V, Kissel M (1987) Localization of phytosiderophore release and of iron uptake along intact barley roots. Plant Physiol 71:157–162CrossRefGoogle Scholar
  97. Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu U, Muller-Rober B, Schulz B (2002) Multifunctionality of plant ABC transporters: more than just detoxifiers. Planta 214:345–355PubMedCrossRefGoogle Scholar
  98. McDougali BM, Rovira AD (1970) Sites of exudation of 14C-labelled compounds from wheat roots. New Phytol 69:999–1003CrossRefGoogle Scholar
  99. Micallef SA, Shiaris MP, Colon-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742PubMedPubMedCentralCrossRefGoogle Scholar
  100. Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. BiotechnolAdv 29:645–653Google Scholar
  101. Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interaction, and their potential role in biology control. Plant Soil 185:241–251CrossRefGoogle Scholar
  102. Munees A, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ-Sci 26(1):1–20Google Scholar
  103. Nagahashi G (2000) In vitro and in situ techniques to examination the role of roots and root exudates during AM fungus-host interactions. In: Kapulink Y, DoudsJr D (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Netherlands, pp 278–300Google Scholar
  104. Nagahashi G, Jr-Douds DD (2003) Action spectrum for the induction of hyphal branches of an arbuscular mycorrhizal fungus: exposure sites versus branching sites. Mycol Res 107:1075–1082PubMedCrossRefGoogle Scholar
  105. Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R, Parvoli G (2000) Soil organic matter mobilization by root exudates. Chemosphere 5:653–658CrossRefGoogle Scholar
  106. Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract pseudomonas putida to the rhizosphere. PLoS One 7:e35498PubMedPubMedCentralCrossRefGoogle Scholar
  107. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396CrossRefGoogle Scholar
  108. Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454PubMedPubMedCentralCrossRefGoogle Scholar
  109. Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454PubMedCrossRefGoogle Scholar
  110. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610PubMedCrossRefGoogle Scholar
  111. Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188:5417–5427PubMedPubMedCentralCrossRefGoogle Scholar
  112. Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980PubMedCrossRefGoogle Scholar
  113. Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619PubMedPubMedCentralCrossRefGoogle Scholar
  114. Popovici J, Comte G, Bagnarol E, Alloisio N, Fournier P, Bellvert F, Bertrand C, Fernandez MP (2010) Differential effects of rare specific flavonoids on compatible and incompatible strains in the Myrica gale-Frankia actinorhizal symbiosis. Appl Environ Microbiol 76:2451–2460PubMedPubMedCentralCrossRefGoogle Scholar
  115. Poulin MJ, Bel-Rhlid R, Piché Y, Chênevert R (1993) Flavonoids released by carrot (Daucus carota) seedlings stimulate hyphal development of vesicular-arbuscular mycorrhizal fungi in the presence of optimal CO2 enrichment. J Chem Ecol 19:2317–2327PubMedCrossRefGoogle Scholar
  116. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398PubMedCrossRefGoogle Scholar
  117. Prin Y, Rougier M (1987) Preinfection events in the establishment of Alnus-Frankia symbiosis: study of the root haïrs deformation step. Plant Physiol 6:99–106Google Scholar
  118. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149PubMedCrossRefGoogle Scholar
  119. Rajkumar M, Sandhya S, Prasad MN, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30(6):1562–1574PubMedCrossRefGoogle Scholar
  120. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906Google Scholar
  121. Rougier M (1981) Secretory activity at the root cap. In: Tanner W, Loews FA (eds) Encyclopedia of Plant Physiology, New Series. Springer Verlag, Berlin. 13B, Plant Carbohydrates 2:542–574Google Scholar
  122. Rovira AD (1973) Zones of exudation along plant roots and spatial distribution of micro-organisms in the rhizosphere. Science 4:361–366Google Scholar
  123. Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556PubMedPubMedCentralCrossRefGoogle Scholar
  124. Ryan PR, Tyerman SD, Sasaki T, Yamamoto Y, Zhang WH, Delhaize E (2011) Identification of aluminium-resistance genes in plants provides an opportunity for enhancing the acid-soil tolerance of crop species. J Exp Bot 62:9–20PubMedCrossRefGoogle Scholar
  125. Scervino JM, PonceMA E-BR, Vierheilig H, Ocampo JA, Godeas A (2005) Flavonoids exclusively present in mycorrhizal roots of white clover exhibit different effects on arbuscular mycorrhizal fungi than flavonoids exclusively present in non-mycorrhizal roots of white clover. J Plant Interact 15:22–30Google Scholar
  126. Shaw LJ, Morris P, Hooker JE (2006) Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ Microbiol 8:1867–1880PubMedCrossRefGoogle Scholar
  127. Shukla KP, Singh NK, Sharma S (2010) Bioremediation: developments, current practices and perspectives. Gen Eng Biotechnol J 3:1–20Google Scholar
  128. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser Set al. (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751PubMedPubMedCentralCrossRefGoogle Scholar
  129. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, LondonGoogle Scholar
  130. Sood SG (2003) Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiol Ecol 45:219–227CrossRefGoogle Scholar
  131. Stein M, Dittgen J, Sanchez-Rodrıguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Shauna Somervillea S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to non-host resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746PubMedPubMedCentralCrossRefGoogle Scholar
  132. Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12 oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci 97:10625–10630PubMedPubMedCentralCrossRefGoogle Scholar
  133. Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell OT (2000) Induced plant defense responses against chewing insects, ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamond back moth. Plant Physiol 124:1007–1018PubMedPubMedCentralCrossRefGoogle Scholar
  134. Sugiyama A, Shitan N, Yazaki K (2007) Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume–rhizobium symbiosis. Plant Physiol 144:2000–2008PubMedPubMedCentralCrossRefGoogle Scholar
  135. Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant-Microbe Interact 13:637–648PubMedCrossRefGoogle Scholar
  136. Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–378PubMedCrossRefGoogle Scholar
  137. Van der Heijden MGA, Sanders IR (eds) (2002) Mycorrhizal ecology. Springer-Verlag, BerlinGoogle Scholar
  138. Van Ghelue M, Lovaas E, Ringo E, Solheim B (1997) Early interactions between Alnus glutinosa and Frankia strain ArI3. Production and specificity of root hair deformation factor(s). Plant Physiol 99:579–587CrossRefGoogle Scholar
  139. Vierheilig H, Bago B (2005) Host and non-host impact on the physiology of the AM symbiosis. In: Declerck S, Strullu DG, Fortin JA (eds) In vitro culture of mycorrhizas. Springer, Heidelberg, pp 139–158CrossRefGoogle Scholar
  140. Vishwakarma K, Sharma S, Kumar N, Upadhyay N, Devi S, Tiwari A (2016) Contribution of microbial inoculants to soil carbon sequestration and sustainable agriculture. In: Microbial inoculants in sustainable agricultural productivity. Springer, New Delhi, pp 101–113CrossRefGoogle Scholar
  141. Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161PubMedPubMedCentralCrossRefGoogle Scholar
  142. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedPubMedCentralCrossRefGoogle Scholar
  143. Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182PubMedGoogle Scholar
  144. Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GE (2012) A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 22:2242–2246PubMedCrossRefGoogle Scholar
  145. Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479PubMedCrossRefGoogle Scholar
  146. Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408CrossRefGoogle Scholar
  147. White PJ (2003) Ion transport. In: Thomas B, Murphy DJ, Murray DJ (eds) Encyclopedia of applied plant sciences. Academic, London, pp 625–634CrossRefGoogle Scholar
  148. Wu T, Wittkamper J, Flores HE (1999) Root herbivory In vitro: interactions between roots and aphids grown in aseptic coculture. In vitro. Cell Dev Biol-Plant 35:259–264CrossRefGoogle Scholar
  149. Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135PubMedCrossRefGoogle Scholar
  150. Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 66:345–351PubMedPubMedCentralCrossRefGoogle Scholar
  151. Yoder JI (2001) Host-plant recognition by parasitic Scrophulariaceae. Curr Opin Plant Bio l4:359–365CrossRefGoogle Scholar
  152. Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Kanchan Vishwakarma
    • 1
  • Mitali Mishra
    • 2
  • Shruti Jain
    • 2
  • Jaspreet Singh
    • 1
  • Neha Upadhyay
    • 1
  • Rishi Kumar Verma
    • 1
  • Pankaj Verma
    • 1
  • Durgesh Kumar Tripathi
    • 2
  • Vivek Kumar
    • 3
  • Rohit Mishra
    • 2
  • Shivesh Sharma
    • 1
    • 2
    Email author
  1. 1.Department of BiotechnologyMotilal Nehru National Institute of Technology (MNNIT) AllahabadAllahabadIndia
  2. 2.Centre for Medical Diagnostic and Research (CMDR)MNNIT AllahabadAllahabadIndia
  3. 3.Amity Institute of Microbial TechnologyAMITY UniversityNoidaIndia

Personalised recommendations