Skip to main content
SpringerLink
Log in
Book cover

Plant Microbe Interface pp 27–67Cite as

Plant-Mycorrhizal and Plant-Rhizobial Interfaces: Underlying Mechanisms and Their Roles in Sustainable Agroecosystems

  • Chapter
  • First Online:

Abstract

Rhizospheric plant-microbe symbiotic interactions involve numerous microbial populations which have a significant impact on plant growth and productivity. Abiotic stresses are serious threats to agriculture and negatively affect the soil-microbe-plant continuum, which is also responsible for reduced yield. Rhizospheric microbes, especially arbuscular mycorrhizal fungi (AMF) and rhizobia (Rh), are potential economical and eco-friendly resources for counteracting abiotic stresses in plants. These microbial interactions involve the release of signaling molecules, such as Myc factors by AMF and Nod factors by Rh, which initiate communication between these microbes and plants leading to colonization, nodulation, and arbuscule formation. Both these microbes are relatively tolerant to extreme adverse conditions and can improve growth and productivity of stressed plants by improving soil and root system architecture (RSA), nutrient uptake, ion homeostasis, sequestration, and compartmentalization, reducing osmotic and oxidative stress, etc. Moreover, both these symbionts act synergistically and provide various beneficial effects in stressed plants. However, there are a number of gaps in understanding the various steps involved in the establishment of symbioses, the signaling molecules, nutrient exchange through the symbiotic interface and genes involved, as well as the modes of action/mechanism of the AMF and Rh in imparting abiotic stress resistance in plants. This chapter bridges the gap and summarizes the mechanisms adopted by AMF and Rh in imparting stress resistance and enhancing crop productivity for a sustainable agroecosystem.

This is a preview of subscription content, 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   109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   199.99
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

Learn about institutional subscriptions

References

  • Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169:704–709

    Article  CAS  PubMed  Google Scholar 

  • Abd-Alla MH, Issa AA, Ohyama T (2014) Impact of harsh environmental conditions on nodule formation and dinitrogen fixation of legumes. In Adv Biol Ecol of Nitrogen Fixation (InTech) https://doi.org/10.5772/56997

    Google Scholar 

  • Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. Strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Garni SMS (2006) Increasing NaCl-salt tolerance of a halophytic plant Phragmites australis by mycorrhizal symbiosis. Am Eurasian J Agric Environ Sci 1:119–126

    Google Scholar 

  • Alizadeh O (2011) Mycorrhizal symbiosis. Adv Stud Biol 3(6):273–281

    Google Scholar 

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297

    Article  Google Scholar 

  • Amballa H, Bhumi NR (2016) Significance of arbuscular mycorrhizal fungi and rhizosphere microflora in plant growth and nutrition. In: Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 417–452

    Chapter  Google Scholar 

  • Amir H, Jourand P, Cavaloc Y, Ducousso M (2014) Role of mycorrhizal fungi in the alleviation of heavy metal toxicity in plants. In: Solaiman ZM, Abbott LK, Varma A (eds) Mycorrhizal fungi: use in sustainable agriculture and land restoration. Springer, Berlin, pp 241–258

    Chapter  Google Scholar 

  • Ariel F, Romero-Barrios N, Jégu T, Benhamed M, Crespi M (2015) Battles and hijacks: noncoding transcription in plants. Trends Plant Sci 20:362–371

    Article  CAS  PubMed  Google Scholar 

  • Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM (2009) Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and non-stressed mycelium. Mol Plant-Microbe Interact 22:1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Aroca R, Porcel R, Ruiz-Lozano JM (2011) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Ruiz-Lozano JM, Zamarreno AM, Paz JA, Garcia-Mina JM, Pozo MJ, Lopez-Raez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650

    Article  CAS  PubMed  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, Mackill D (2010) Submergence tolerant rice: SUB1’s journey from landrace to modern cultivar. Rice 3:138–147

    Article  Google Scholar 

  • Balestrini R, Gomez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant-Microbe Interact 20:1055–1062

    Article  CAS  PubMed  Google Scholar 

  • Bano SA, Ashfaq D (2013) Role of mycorrhiza to reduce heavy metal stress. Nat Sci 5:16–20

    CAS  Google Scholar 

  • Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45:405–413

    Article  Google Scholar 

  • Barzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, Ruiz-Lonazo JM (2012) Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot 109:1009–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becard G, Doner LW, Rolin DB, Douds DD, Pfeffer PE (1991) Identification and quantification of trehalose in vesicular arbuscular mycorrhizal fungi by in vivo C-13 NMR and HPLC analyses. New Phytol 118:547–552

    Article  CAS  Google Scholar 

  • Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signaling. New Phytol 181:413–423

    Article  CAS  PubMed  Google Scholar 

  • Berruti A, Borriello R, Orgiazzi A, Barbera AC, Lumini E, Bianciotto V (2014) Arbuscular mycorrhizal fungi and their value for ecosystem management. In: Biodiversity-the dynamic balance of the planet. InTech, Rijeka. https://doi.org/10.5772/58231

    Chapter  Google Scholar 

  • Bhandari P, Garg N (2017) Dynamics of arbuscular mycorrhizal symbiosis and its role in nutrient acquisition: an overview. In: Mycorrhiza-nutrient uptake, biocontrol, ecorestoration. Springer, Cham, pp 21–43

    Chapter  Google Scholar 

  • Bharti N, Barnawal D, Awasthi A, Yadav A, Kalra A (2014) Plant growth promoting rhizobacteria alleviate salinity induced negative effects on growth, oil content and physiological status in Mentha arvensis. Acta Physiol Plant 34:45–60

    Article  CAS  Google Scholar 

  • Bonfante P (2003) Plants, mycorrhizal fungi and endobacteria: a dialog among cells and genomes. Biol Bull 204:215–220

    Article  CAS  PubMed  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 1:1–11

    Article  CAS  Google Scholar 

  • Brear EM, Day DA, Smith PMC (2013) Iron: an essential micronutrient for the legume-rhizobium symbiosis. Front Plant Sci 4:1–15

    Article  Google Scholar 

  • Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family prote in AMT2;3. Plant Cell 27:1352–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cailliatte R, Schikora A, Briat JF, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calabrese S, Perez-Tienda J, Ellerbeck M, Arnould C, Chatagnier O, Boller T, Schussler A, Brachmann A, Wipf D, Ferrol N, Courty PE (2016) GintAMT3-a low-affinity ammonium transporter of the arbuscular mycorrhizal Rhizophagus irregularis. Front Plant Sci 7:1–14

    Article  Google Scholar 

  • Casieri L, Gallardo K, Wipf D (2012) Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235:1431–1447

    Article  CAS  PubMed  Google Scholar 

  • Chen YL, Dunbabin VM, Postma JA, Diggle AJ, Palta JA, Lynch JP, Siddique KH, Rengel Z (2011) Phenotypic variability and modelling of root structure of wild Lupinus angustifolius genotypes. Plant Soil 348:345–364

    Article  CAS  Google Scholar 

  • Clarke VC, Loughlin PC, Day DA, Smith P (2014) Transport processes of the legume symbiosome membrane. Front Plant Sci 5:1–9

    Article  Google Scholar 

  • Corticeiro SC, Lima AIG, De EM, Figueira AP (2006) The importance of glutathione in oxidative status of Rhizobium leguminosarum biovar viciae under Cd exposure. Enzym Microb Technol 40:132–137

    Article  CAS  Google Scholar 

  • Courty PE, Smith P, Koegel S, Redecker D, Wipf D (2015) Inorganic nitrogen uptake and transport in beneficial plant root-microbe interactions. Crit Rev Plant Sci 34:4–16

    Article  CAS  Google Scholar 

  • Curie C, Cassin G, Couch D, Divol F, Higuchi K, Jean ML, mission J, Schikora A, Czernic P, Mari S (2008) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103(1):1–11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Damodaran T, Rai RB, Jha SK, Kannan R, Pandey BK, Sah V, Mishra VK, Sharma DK (2014) Rhizosphere and endophytic bacteria for induction of salt tolerance in gladiolus grown in sodic soils. J Plant Interact 9:577–584

    Article  CAS  Google Scholar 

  • Dary M, Chamber-Perez M, Palomares A, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330

    Article  CAS  PubMed  Google Scholar 

  • Datta A, Singh RK, Tabassum S (2015) Isolation, characterization and growth of Rhizobium strains under optimum conditions for effective biofertilizer production. Int J Pharm Sci Rev Res 32:199–208

    CAS  Google Scholar 

  • Delgado MJ, Tresierra-Ayala A, Talbi C, Bedmar EJ (2006) Functional characterization of the Bradyrhizobium japonicum modA and modB genes involved in molybdenum transport. Microbiology 152(1):199–207

    Article  CAS  PubMed  Google Scholar 

  • Diedhiou I, Diouf D (2018) Transcription factors network in root endosymbiosis establishment and development. World J Microbiol Biotechnol 34(3):1–14

    Article  CAS  Google Scholar 

  • Doidy J, van Tuinen D, Lamotte O, Corneillat M, Alcaraz G, Wipf D (2012) The Medicago truncatula sucrose transporter family: characterization and implication of key members in carbon partitioning towards arbuscular mycorrhizal fungi. Mol Plant 5:1346–1358

    Article  CAS  PubMed  Google Scholar 

  • Egamberdieva D, Kucharova Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571

    Article  Google Scholar 

  • Estrada B, Aroca R, Maathuis FJ, Barea JM, Ruiz-Lozano JM (2013) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36:1771–1782

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faber BA, Zasoski RJ, Burau RG, Uriu K (1990) Zinc uptake by corn as affected by vesicular-arbuscular mycorrhizae. Plant Soil 129:121–130

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In: agronomy for sustainable development. Springer, Dordrecht, pp 153–188

    Google Scholar 

  • Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52:61–76

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo MV, Burity HA, Martinez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40(1):182–188

    Article  Google Scholar 

  • Flemetakis E, Dimou M, Cotzur D, Efrose RC, Aivalakis G, Colebatch G, Udvardi MK, Katinakis P (2003) A sucrose transporter, Lj SUT4, is up-regulated during Lotus japonicus nodule development. J Exp Bot 54:1789–1791

    Article  CAS  PubMed  Google Scholar 

  • Fortin MG, Morrison NA, Verma DPS (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15:813–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fusconi A (2013) Regulation of root morphogenesis in arbuscular mycorrhizae: what role do fungal exudates, phosphate, sugars and hormones play in lateral root formation? Ann Bot 113:19–33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallardo K, Courty PE, Le Signor C, Wipf D, Vernoud V (2014) Sulfate transporters in the plant’s response to drought and salinity: regulation and possible functions. Front Plant Sci 5(580):1–15

    Google Scholar 

  • Gao JS, Wu FF, Shen ZL, Meng Y, Cai YP, Lin Y (2016) A putative molybdate transporter LjMOT1 is required for molybdenum transport in Lotus japonicus. Physiol Plant 158:331–340

    Article  CAS  PubMed  Google Scholar 

  • Garg N, Singh S (2018) Mycorrhizal inoculations and silicon fortifications improve rhizobial symbiosis, antioxidant defense, trehalose turnover in pigeon pea genotypes under cadmium and zinc stress. Plant Growth Regul 86(1):105–119

    Article  CAS  Google Scholar 

  • Garcia K, Chasman D, Roy S, Ane JM (2017) Physiological responses and gene co-expression network of mycorrhizal roots under K+ deprivation. Plant Physiol 173:1811–1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garg N, Baher N (2013) Role of arbuscular mycorrhizal symbiosis in proline biosynthesis and metabolism of Cicer arietinum L. (chickpea) genotypes under salt stress. J Plant Growth Regul 32:767–778

    Article  CAS  Google Scholar 

  • Garg N, Bharti A (2018) Salicylic acid improves arbuscular mycorrhizal symbiosis, and chickpea growth and yield by modulating carbohydrate metabolism under salt stress. Mycorrhiza 28(8):727–746. https://doi.org/10.1007/s00572-018-0856-6

    Article  CAS  PubMed  Google Scholar 

  • Garg N, Manchanda G (2007) Symbiotic nitrogen fixation in legume nodules: process and signaling: a review. Agron Sustain Dev 27:59–68

    Article  CAS  Google Scholar 

  • Garg N, Manchanda G (2009) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (Pigeonpea). J Agron Crop Sci 195(2):110–123

    Article  CAS  Google Scholar 

  • Garg N, Singla P, Bhandari P (2015) Metal uptake, oxidative metabolism, and mycorrhization in pigeonpea and pea under arsenic and cadmium stress. Turk J Agric For 39:234–250

    Article  CAS  Google Scholar 

  • Garg N, Bhandari P, Kashyap L, Singh S (2017) Arbuscular mycorrhizal symbiosis: a boon for sustainable legume production under salinity and heavy metal stress. In: Aggarwal A, Yadav K (eds) Mycorrhizal fungi. Astral International, New Delhi, pp 247–273

    Google Scholar 

  • Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20:1407–1420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genre A, Ivanov S, Fendrych M, Faccio A, Zarsky V, Bisseling T, Bonfante P (2012) Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell Physiol 53:244–255

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Tolosano M, Volpe V, Kopriva S, Bonfante P (2014) Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol 204:609–619

    Article  CAS  PubMed  Google Scholar 

  • Gobbato E, Marsh JF, Vernié T, Wang E, Maillet F, Kim J, Ratet P, Mysore KS (2012) A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 22:2236–2241

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Chavez C, D’haen J, Vangronsveld J, Dodd JC (2002) Copper sorption and accumulation by the extraradical mycelium of different Glomus spp. (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240(2):287–297

    Article  CAS  Google Scholar 

  • Gonzalez-Guerrero M, Azcon-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Guerrero M, Escudero V, Saez A, Tejada-Jimenez M (2016) Transition metal transport in plants and associated endosymbionts: arbuscular mycorrhizal fungi and rhizobia. Front Plant Sci 7:1–21

    Article  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  CAS  PubMed  Google Scholar 

  • Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochem Biophys Acta Mol Cell Res 1763:595–608

    Article  CAS  Google Scholar 

  • Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gusmao A, Cacoilo S, Figueira EM (2006) Glutathione-mediated cadmium sequestration in Rhizobium leguminosarum. Enzym Microb Technol 39:763–769

    Article  CAS  Google Scholar 

  • Gutjahr C, Radovanovic D, Geoffroy J, Zhang Q, Siegler H, Chiapello M, Casieri L, Guiderdoni E, Kumar CS (2012) The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant J 69:906–920

    Article  CAS  PubMed  Google Scholar 

  • Hall BP, Guerinot ML (2006) The role of ZIP family members in iron transport. In: Iron nutrition in plants and rhizospheric microorganisms. Springer, Dordrecht, pp 311–326

    Chapter  Google Scholar 

  • Han HS, Lee KD (2005) Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agric Biol Sci 1:210–215

    Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJ (2012) Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15:691–698

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hashem A, Abd-Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D, Wirth S (2016) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23:272–281

    Article  CAS  PubMed  Google Scholar 

  • Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani ABF, Aldehaish HA, Egamberdieva D, Abd-Allah EF (2018) Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J Biol Sci 25:1102–1114. https://doi.org/10.1016/j.sjbs.2018.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    Article  CAS  Google Scholar 

  • Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howitt SM, Udvardi MK, Day DA, Gresshoff PM (1986) Ammonia transport in free-living and symbiotic Rhizobium sp. ANU289. Microbiology 132:257–261

    Article  CAS  Google Scholar 

  • Huang Z, Zhao L, Chen D, Liang M, Liu Z, Shao H, Long X (2013) Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS One 8:e62085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang JH (2013) Soybean nodulin 26: a channel for water and ammonia at the symbiotic interface of legumes and nitrogen-fixing rhizobia bacteria. Doctoral dissertations, University of Tennessee, Knoxville

    Google Scholar 

  • Izmailov SF (2003) Calcium-based interactions of symbiotic partners in legumes: role of peribacteroid membrane. Russ J Plant Physiol 50:553–566

    Article  CAS  Google Scholar 

  • Ivanov S, Fedorova EE, Limpens E, De Mita S, Genre A, Bonfante P, Bisseling T (2012) Rhizobium–legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci U S A 109:8316–8321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jabajihare S, Deschene A, Kendrick B (1984) Lipid-content and composition of vesicles of a vesicular-arbuscular mycorrhizal fungus. Mycologia 76:1024–1030

    Article  CAS  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular arbuscular mycorrhizal fungi associated with Trifolium subterraneum L 2 Hyphal transport of P-32 over defined distances. New Phytol 120:509–516

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, Wang E (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–1175

    Article  CAS  PubMed  Google Scholar 

  • Johansen A, Finlay RD, Olsson PA (1996) Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 133:705–712

    Article  CAS  Google Scholar 

  • Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RA (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci U S A 107:2093–2098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat Rev Microbiol 5(8):619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kader JC, Delseny M (2011) Advances in botanical research, vol 60. Academic, London

    Google Scholar 

  • Kamboj D, Kumar R, Kumari A, Kundu BS, Pathak D, Sharma PK (2008) Rhizobia, nod factors and nodulation–a review. Agric Rev 29:200–206

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kaur H, Garg N (2017) Zinc-arbuscular mycorrhizal interactions: effect on nutrient pool, enzymatic antioxidants, and osmolyte synthesis in pigeonpea nodules subjected to Cd stress. Commun Soil Sci Plant Anal 48:1684–1700

    Article  CAS  Google Scholar 

  • Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the proteobacteria. In: The prokaryotes. Springer, New York

    Google Scholar 

  • Khalvati MA, Hu Y, Mozafar A, Schmidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–712

    Article  CAS  PubMed  Google Scholar 

  • Khan MR, Khan I, Ibrar Z, Leon J, Naz AA (2017) Drought-responsive genes expressed predominantly in root tissues are enriched with homotypic cis-regulatory clusters in promoters of major cereal crops. Crop J 5(3):195–206

    Article  Google Scholar 

  • Koltai H, Kapulnik Y (2009) Effect of arbuscular mycorrhizal symbiosis on enhancement of tolerance to abiotic stresses. In: White JF, Torres MS (eds) Defensive mutualism in microbial symbiosis CRC. Taylor Francis, Boca Raton, FL, pp 217–234

    Google Scholar 

  • Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci U S A 105:9823–9828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272

    Article  PubMed  CAS  Google Scholar 

  • Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344

    Article  CAS  PubMed  Google Scholar 

  • Krusell L, Krause K, Ott T, Desbrosses G, Krämer U, Sato S, Nakamura Y, Tabata S, James EK, Snadal N, Stougaard J, Kawaguchi M, Miyamoto A, Suganuma N, Udvardi MK (2005) The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17:1625–1636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krylova VV, Andreev IM, Zartdinova R, Izmailov SF (2017) Ca2+-ATPase in the symbiosome membrane from broad bean root nodules: further evidence for its functioning as ATP-driven Ca2+/H+ exchanger. Acta Physiol Plant 39(11):1–8

    Article  CAS  Google Scholar 

  • Kryvoruchko IS, Sinharoy S, Torres-Jerez I, Sosso D, Pislariu CI, Guan D, Murray JD, Benedito VA, Frommer WB, Udvardi MK (2016) MtSWEET11, a nodule-specific sucrose transporter of Medicago truncatula root nodules. Plant Physiol 171(1):554–565. https://doi.org/10.1104/pp.15.01910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lace B, Ott T (2018) Commonalities and differences in controlling multipartite intracellular infections of legume roots by symbiotic microbes. Plant Cell Physiol 59:661–672

    Article  PubMed  CAS  Google Scholar 

  • Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207

    Article  CAS  PubMed  Google Scholar 

  • Lelandais-Brière C, Moreau J, Hartmann C, Crespi M (2016) Noncoding RNAs, emerging regulators in root endosymbioses. Mol Plant-Microbe Interact 29:170–180

    Article  PubMed  CAS  Google Scholar 

  • Li J, Shah S, Moffatt BA, Glick BR (2001) Isolation and characterization of an unusual 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase gene from Enterobacter cloacae UW4. Anton Van Leeuw 80:255–261

    Article  CAS  Google Scholar 

  • Li T, Hu YJ, Hao ZP, Li H, Chen BD (2013) Aquaporin genes GintAQPF1 and GintAQPF2 from Glomus intraradices contribute to plant drought tolerance. Plant Signal Behav 8(5):e24030

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Limpens E, Moling S, Hooiveld G, Pereira PA, Bisseling T, Becker JD, Küster H (2013) Cell-and tissue-specific transcriptome analyses of Medicago truncatula root nodules. PLoS One 8(5):1–15

    Article  CAS  Google Scholar 

  • Lindstrom K, Terefework Z, Suominen L, Lortet G (2002) Signalling and development of rhizobium: legume symbioses. Biol Environ Proc R Ir Acad 102:61–64

    Article  Google Scholar 

  • Liu W, Zhang Y, Jiang S, Deng Y, Christie P, Murray PJ, Li X, Zhang J (2016) Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil. Sci Rep 6:24902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Zhang C, Yang J, Yu N, Wang E (2018) Hormone modulation of legume-rhizobial symbiosis. J Integr Plant Biol 60(8):632–648. https://doi.org/10.1111/jipb.12653

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Pedrosa A, Gonzalez-Guerrero M, Valderas A, Azcon-Aguilar C, Ferrol N (2006) GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43:102–110

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Becard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874

    Article  CAS  PubMed  Google Scholar 

  • Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, Oldroyd GE, Eastmond PJ (2017) Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356:1175–1178

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg BJ, Malfanova N, Kamilova F, Berg G (2013) Plant growth promotion by microbes. Mol Microbiol Ecol Rhizosphere 1–2:559–573

    Article  Google Scholar 

  • Ma W, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Anton Van Leeuw 83:285–291

    Article  CAS  Google Scholar 

  • Ma Y, Oliveira RS, Freitas H, Zhang C (2016) Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:1–19. https://doi.org/10.3389/fpls.2016.00918

    Article  PubMed  PubMed Central  Google Scholar 

  • MacLean AM, Bravo A, Harrison MJ (2017) Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. Plant Cell 29(10):2319–2335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:1–12

    Article  CAS  Google Scholar 

  • Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63

    Article  CAS  PubMed  Google Scholar 

  • Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant-Microbe Interact 14:1140–1148

    Article  CAS  PubMed  Google Scholar 

  • Malekzadeh E, Alikhani HA, Savaghebi-Firoozabadi GR, Zarei M (2011) Influence of arbuscular mycorrhizal fungi and an improving growth bacterium on Cd uptake and maize growth in Cd-polluted soils. Span J Agric Res 9:1213–1223

    Article  Google Scholar 

  • Manck-Gotzenberger J, Requena N (2016) Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Front Plant Sci 7:487

    Article  PubMed  PubMed Central  Google Scholar 

  • Mary P, Ochin D, Tailliez R (1986) Growth status of rhizobia in relation to their tolerance to low water activities and desiccation stress. Soil Biol Biochem 18:179–184

    Article  CAS  Google Scholar 

  • Masalkar P, Wallace IS, Hwang JH, Roberts DM (2010) Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J Biol Chem 285:23880–23888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masson-Boivin C, Sachs JL (2018) Symbiotic nitrogen fixation by rhizobia—the roots of a success story. Curr Opin Plant Biol 44:7–15

    Article  CAS  PubMed  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530

    Article  CAS  Google Scholar 

  • McAdam EL, Reid JB, Foo E (2018) Gibberellins promote nodule organogenesis but inhibit the infection stages of nodulation. J Exp Bot 69:2117–2130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina MJH, Gagnon H, Piche Y, Ocampo JA, Garrido JMG, Vierheilig H (2003) Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci 164:993–998

    Article  CAS  Google Scholar 

  • Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:1–25

    Article  Google Scholar 

  • Menendez E, Martínez-Hidalgo P, Silva LR, Velazquez E, Mateos PF, Peix A (2017) Recent advances in the active biomolecules involved in rhizobia-legume symbiosis. In: Microbes for legume improvement. Springer, Cham, pp 45–74

    Chapter  Google Scholar 

  • Meng L, Zhang A, Wang F, Han X, Wang D, Li S (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci 6:1–10

    Google Scholar 

  • Michiels J, Verreth C, Vanderleyden J (1994) Effects of temperature stress on bean-nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mohanty SK, Arthikala MK, Nanjareddy K, Lara M (2018) Plant-symbiont interactions: the functional role of expansins. Symbiosis 74:1–10

    Article  CAS  Google Scholar 

  • Moreau S, Day DA, Puppo A (1998) Ferrous iron is transported across the peribacteroid membrane of soybean nodules. Planta 207:83–87

    Article  CAS  Google Scholar 

  • Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem 277:4738–4746

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Murset V, Hennecke H, Gabriella P (2012) Disparate role of rhizobial ACC deaminase in root-nodule symbioses. Symbiosis 57:43–50

    Article  CAS  Google Scholar 

  • Nanjareddy K, Arthikala MK, Gómez BM, Blanco L, Lara M (2017) Differentially expressed genes in mycorrhized and nodulated roots of common bean are associated with defense, cell wall architecture, N metabolism, and P metabolism. PLoS One 12(8):e0182328

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nasim G (2013) Host allelopathy and arbuscular mycorrhizal fungi. In: Cheema ZA, Farooq M, Wahid A (eds) Allelopathy. Springer, Berlin, pp 429–450

    Chapter  Google Scholar 

  • Naveed M, Mehboob I, Hussain MB, Zahir ZA (2015) Perspectives of rhizobial inoculation for sustainable crop production. In: Arora NK (ed) Plant microbes symbiosis: applied facets. Springer, New Delhi, pp 209–239

    Google Scholar 

  • Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta, Mol Cell Res 1763:609–620

    Article  CAS  PubMed  Google Scholar 

  • Nukui N, Minamisawa K, Ayabe SI, Aoki T (2006) Expression of the 1-aminocyclopropane-1-carboxylic acid deaminase gene requires symbiotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti MAFF303099. Appl Environ Microbiol 72:4964–4969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ocon A, Hampp R, Requena N (2007) Trehalose turnover during abiotic stress in arbuscular mycorrhizal fungi. New Phytol 174:879–891

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE, Engstrom EM, Long SR (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13:1835–1849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  PubMed  Google Scholar 

  • Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649

    Article  CAS  PubMed  Google Scholar 

  • Pajuelo E, Rodriguez-Llorente ID, Lafuente A, Caviedes MA (2011) Legume–rhizobium symbioses as a tool for bioremediation of heavy metal polluted soils. In: Biomanagement of metal-contaminated soils. Springer, Dordrecht, pp 95–123

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses 2006. New Phytol 172:35–46

    Article  CAS  PubMed  Google Scholar 

  • Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441

    Article  CAS  PubMed  Google Scholar 

  • Pelissier HC, Frerich A, Desimone M, Schumacher K, Tegeder M (2004) PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiol 134:664–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira SIA, Lima AIG, Figueirs EMAP (2008) Rhizobium leguminosarum isolated from agricultural ecosystems subjected to different climatic influences: the relation between genetic diversity, salt tolerance and nodulation efficiency. In: Liu T-X (ed) Soil ecology research developments. Nova Science, New York, pp 247–263

    Google Scholar 

  • Perez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcon Aguilar C, Ferrol N (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48:1044–1055

    Article  CAS  PubMed  Google Scholar 

  • Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can J Bot 82:1074–1088

    Article  Google Scholar 

  • Pfau T (2013) Modelling metabolic interactions in the legume-rhizobia symbiosis. Doctoral dissertation, University of Aberdeen, Aberdeen, United Kingdom

    Google Scholar 

  • Pfeffer PE, Douds DD, Bécard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120:587–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips DA, Joseph CM, Maxwell CA (1992) Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol 99:1526–1531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pierre O, Engler G, Hopkins J, Brau F, Boncompagni E, Herouart D (2013) Peribacteroid space acidification: a marker of mature bacteroid functioning in Medicago truncatula nodules. Plant Cell Environ 36:2059–2070

    CAS  PubMed  Google Scholar 

  • Pilon M (2011) Moving copper in plants. New Phytol 192(2):305–307

    Article  CAS  PubMed  Google Scholar 

  • Plett JM, Martin F (2015) Reconsidering mutualistic plant–fungal interactions through the lens of effector biology. Curr Opin Plant Biol 26:45–50

    Article  PubMed  Google Scholar 

  • Poole P, Ramachandran V, Terpolilli J (2018) Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol 16(5):291–303

    Article  CAS  PubMed  Google Scholar 

  • Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750

    Article  CAS  PubMed  Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200

    Article  CAS  Google Scholar 

  • Prasad R, Bhola D, Akdi K, Cruz C, Sairam KVSS, Tuteja N, Varma A (2017) Introduction to mycorrhiza: historical development. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza. Springer International Publishing AG, Cham, pp 1–7

    Google Scholar 

  • Pumplin N, Harrison MJ (2009) Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 15:809–819

    Article  CAS  Google Scholar 

  • Rajtor M, Piotrowska-Seget Z (2016) Prospects for arbuscular mycorrhizal fungi (AMF) to assist in phytoremediation of soil hydrocarbon contaminants. Chemosphere 162:105–116

    Article  CAS  PubMed  Google Scholar 

  • Ramos AC, Martins MA, Okorokova-Facanha AL, Olivares FL, Okorokov LA, Sepulveda N, Feijo JA, Facanha AR (2009) Arbuscular mycorrhizal fungi induce differential activation of the plasma membrane and vacuolar H+ pumps in maize roots. Mycorrhiza 19:69–80

    Article  CAS  PubMed  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466

    Article  CAS  PubMed  Google Scholar 

  • Reichman SM (2007) The potential use of legume-rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593

    Article  CAS  Google Scholar 

  • Ren G (2018) The evolution of determinate and indeterminate nodules within the Papilionoideae subfamily. Doctoral dissertation, Wageningen University

    Google Scholar 

  • Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388

    Article  CAS  PubMed  Google Scholar 

  • Rinaudo M (2004) Role of substituents on the properties of some polysaccharides. Biomacromolecules 5:1155–1165

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Haas B, Finney L, Vogt S, Gonzalez-Melendi P, Imperial J, González-Guerrero M (2013) Iron distribution through the developmental stages of Medicago truncatula nodules. Metallomics 5:1247–1253

    Article  CAS  PubMed  Google Scholar 

  • Rook MB, Bisseling T, Emons AMC (1998) Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13:341–350

    Article  Google Scholar 

  • Roth R, Paszkowski U (2017) Plant carbon nourishment of arbuscular mycorrhizal fungi. Curr Opin Plant Biol 39:50–56

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcon R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Azcon C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Aroca R, Zamarreno AM, Molina S, Andreo-Jimenez B, Porcel R, Garcia-Mina JM, Ruyter-Spira C, Lopez-Raez JA (2016) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39:441–452

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Sanchez M, Aroca R, Munoz Y, Polon R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869

    Article  CAS  PubMed  Google Scholar 

  • Ruth B, Khalvati M, Schmidhalter U (2011) Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 342:459–468

    Article  CAS  Google Scholar 

  • Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saxena M, Saxena J, Nema R, Singh D, Gupta A (2013) Phytochemistry of medicinal plants. J Pharmacogn Phytochem 1(6):168–182

    Google Scholar 

  • Schaarschmidt S, Gonzalez MC, Roitsch T, Strack D, Sonnewald U, Hause B (2007) Regulation of arbuscular mycorrhization by carbon: the symbiotic interaction cannot be improved by increased carbon availability accomplished by root specifically enhanced invertase activity. Plant Physiol 143:1827–1840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert M, Koteyeva NK, Wabnitz PW, Santos P, Büttner M, Sauer N, Demchenko K, Pawlowski K (2011) Plasmodesmata distribution and sugar partitioning in nitrogen-fixing root nodules of Datisca glomerata. Planta 233:139–152

    Article  CAS  PubMed  Google Scholar 

  • Schussler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936

    Article  PubMed  CAS  Google Scholar 

  • Senovilla M, Castro-Rodríguez R, Abreu I, Escudero V, Kryvoruchko I, Udvardi MK, Imperial J, González-Guerrero M (2018) Medicago truncatula copper transporter 1 (MtCOPT1) delivers copper for symbiotic nitrogen fixation. New Phytol 218:696–709

    Article  CAS  PubMed  Google Scholar 

  • Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett Appl Microbiol 42:155–159

    Article  CAS  PubMed  Google Scholar 

  • Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430

    Article  PubMed  Google Scholar 

  • Sidahmed NEM (2016) The effect of compost, rhizobium inoculation and urea on peanut plant growth. Doctoral dissertation, Sudan University of Science and Technology

    Google Scholar 

  • Sieberer B, Emons AMC (2000) Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma 214:118–127

    Article  Google Scholar 

  • Sieberer BJ, Chabaud M, Fournier J, Timmers AC, Barker DG (2012) A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J 69:822–830

    Article  CAS  PubMed  Google Scholar 

  • Silver S, Phung LT (2005) A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotechnol 32:587–605

    Article  CAS  PubMed  Google Scholar 

  • Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York, p 800

    Google Scholar 

  • Soka G, Ritchie M (2014) Arbuscular mycorrhizal symbiosis and ecosystem processes: prospects for future research in tropical soils. Open J Ecol 4:11–22

    Article  Google Scholar 

  • Song YY, Ye M, Li CY, Wang RL, Wei XC, Luo SM, Zeng RS (2013) Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol 39:1036–1044

    Article  PubMed  CAS  Google Scholar 

  • Staudinger C, Mehmeti-Tershani V, Gil-Quintana E, Gonzalez EM, Hofhansl F, Bachmann G, Wienkoop S (2016) Evidence for a rhizobia-induced drought stress response strategy in Medicago truncatula. J Proteome 136:202–213

    Article  CAS  Google Scholar 

  • Suarez R, Wong A, Ramirez M, Barraza A, Orozco MDC, Cevallos MA, Lara M, Hernandez G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe Interact 21:958–966

    Article  CAS  PubMed  Google Scholar 

  • Tamayo E, Gomez-Gallego T, Azcon-Aguilar C, Ferrol N (2014) Genome-wide analysis of copper, iron and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 5:1–13

    Article  Google Scholar 

  • Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53

    Article  PubMed  Google Scholar 

  • Tejada-Jimenez M, Gil-Diez P, Leon-Mediavilla J, Wen J, Mysore K, Imperial J, Gonzalez-Guerrero M (2017) Medicago truncatula MOT1. 3 is a plasma membrane molybdenum transporter required for nitrogenase activity in root nodules. BioRxiv. https://doi.org/10.1101/102517

  • Terpolilli JJ, Masakapalli SK, Karunakaran R, Webb I, Green R, Watmough NJ, Kruger NJ, Ratcliffe RG, Poole PS (2016) Lipogenesis and redox balance in nitrogen-fixing pea bacteroids. J Bacteriol 198:2864–2875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trotta A, Falaschi P, Cornara L, Minganti V, Fusconi A, Drava G, Berta G (2006) Arbuscular mycorrhizae increase the arsenic translocation factor in the As hyperaccumulating fern Pteris vittata L. Chemosphere 65:74–81

    Article  CAS  PubMed  Google Scholar 

  • Tsyganova AV, Kitaeva AB, Tsyganov VE (2018) Cell differentiation in nitrogen-fixing nodules hosting symbiosomes. Funct Plant Biol 45(2):47–57

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  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 

  • Udvardi MK, Price GD, Gresshoff PM, Day DA (1988) A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett 231:36–40

    Article  CAS  Google Scholar 

  • Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Biol 42:373–390

    Article  CAS  Google Scholar 

  • Varma A, Prasad R, Tuteja N (2017a) Mycorrhiza: eco-physiology, secondary metabolites, nanomaterials. Springer International Publishing, Cham. http://www.springer.com/us/book/9783319578484. ISBN: 978-3-319-57849-1

    Book  Google Scholar 

  • Varma A, Prasad R, Tuteja N (2017b) Mycorrhiza: function, diversity and state-of-art. Springer International Publishing, Berlin. http://www.springer.com/us/book/9783319530635. ISBN: 978-3-319-53064-2

    Book  Google Scholar 

  • Varma A, Prasad R, Tuteja N (2017c) Mycorrhiza: nutrient uptake, biocontrol, ecorestoration. Springer International Publishing, Cham. http://www.springer.com/us/book/9783319688664. ISBN: 978-3-319-68867-1

    Book  Google Scholar 

  • Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21(3):187–198

    Article  CAS  PubMed  Google Scholar 

  • Vriezen Jan AC, Bruijn FJDB, Nusslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl Environ Microbiol 73(11):3451–3459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wais RJ, Keating DH, Long SR (2002) Structure-function analysis of nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis. Plant Physiol 129:211–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692

    Article  CAS  PubMed  Google Scholar 

  • Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultz M, Kamoun S, Oldroyd GE (2012) A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 22:2242–2246

    Article  CAS  PubMed  Google Scholar 

  • Wang E, Yu N, Bano SA, Liu C, Miller AJ, Cousins D, Zhang X, Ratet P, Tadege M, Mysore KS, Downie JA (2014) A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell 26:1818–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Wang L, Zhou Y, Duanmu D (2017a) Use of CRISPR/Cas9 for symbiotic nitrogen fixation research in legumes. In: Progress in molecular biology and translational science, vol 149. Academic, San Diego, pp 187–213

    Google Scholar 

  • Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E (2017b) Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol Plant 10(9):1147–1158. https://doi.org/10.1016/j.molp.2017.07.012

    Article  CAS  PubMed  Google Scholar 

  • Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322

    Article  CAS  PubMed  Google Scholar 

  • Webb BA, Karl Compton K, Castañeda Saldaña R, Arapov TD, Keith Ray W, Helm RF, Scharf BE (2017) Sinorhizobium meliloti chemotaxis to quaternary ammonium compounds is mediated by the chemoreceptor McpX. Mol Microbiol 103(2):333–346

    Article  CAS  PubMed  Google Scholar 

  • Weaver CD, Crombie B, Stacey G, Roberts DM (1991) Calcium-dependent phosphorylation of symbiosome membrane proteins from nitrogen-fixing soybean nodules: evidence for phosphorylation of nodulin-26. Plant Physiol 95:222–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu QS, Levy Y, Zou YN (2009) Arbuscular mycorrhizae and water relations in citrus. In: Tennant P, Benkeblia N (eds) Tree and forestry and science biotechnology, vol 3, pp 105–112

    Google Scholar 

  • Wu QS, He XH, Zou YN, He KP, Sun YH, Cao MQ (2012) Spatial distribution of glomalin-related soil protein and its relationships with root mycorrhization, soil aggregates, carbohydrates, activity of protease and β-glucosidase in the rhizosphere of Citrus unshiu. Soil Biol Biochem 45:181–183

    Article  CAS  Google Scholar 

  • Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87

    Article  CAS  Google Scholar 

  • Xie X, Lin H, Peng X, Xu C, Sun Z, Jiang K, Huang A, Wu X, Tang N, Salvioli A, Bonfante P (2016) Arbuscular mycorrhizal symbiosis requires a phosphate transceptor in the Gigaspora margarita fungal symbiont. Mol Plant 9:1583–1608

    Article  CAS  PubMed  Google Scholar 

  • Xiong H, Kobayashi T, Kakei Y, Senoura T, Nakazono M, Takahashi H, Nakanishi H, Shen H, Duan P, Nishizawa NK, Zuo Y (2012) AhNRAMP1 iron transporter is involved in iron acquisition in peanut. J Exp Bot 63:4437–4446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaya-Ito H, Shimoda Y, Hakoyama T, Sato S, Kaneko T, Hossain MS, Shibata S, Kawaguchi M, Hayashi M, Kouchi H, Umehara Y (2018) Loss-of-function of ASPARTIC PEPTIDASE NODULE-INDUCED 1 (APN1) in Lotus japonicus restricts efficient nitrogen-fixing symbiosis with specific Mesorhizobium loti strains. Plant J 93:5–16

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki A, Hayashi M (2015) Building the interaction interfaces: host responses upon infection with microorganisms. Curr Opin Plant Biol 23:132–139

    Article  PubMed  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  CAS  PubMed  Google Scholar 

  • Yang SY, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S (2012) Non-redundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 24:4236–4251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, He C, Huang L, Ban Y, Tang M (2017) The effects of arbuscular mycorrhizal fungi on glomalin-related soil protein distribution, aggregate stability and their relationships with soil properties at different soil depths in lead-zinc contaminated area. PLoS One 12(8):1–19

    Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zandalinas SI, Mittler R, Balfagon D, Arbona V, Gomez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12

    Article  CAS  PubMed  Google Scholar 

  • Zheng L, Yamaji N, Yokosho K, Ma JF (2012) YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. Plant Cell 24:3767–3782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zipfel C, Oldroyd GE (2017) Plant signalling in symbiosis and immunity. Nature 543(7645):328

    Article  CAS  PubMed  Google Scholar 

  • Zsogon A, Lambais MR, Benedito VA, Figueira AVDO, Peres LEP (2008) Reduced arbuscular mycorrhizal colonization in tomato ethylene mutants. Sci Agric 65:259–267

    Article  CAS  Google Scholar 

Download references

Acknowledgment

The authors acknowledge the financial support from Department of Biotechnology (DBT), Ministry of Science and Technology, and University Grants Commission (UGC), Government of India, for carrying out related research.

Conflict of Interest

There is no conflict of interest between the authors.

Author information

Authors and Affiliations

  1. Department of Botany, Panjab University, Chandigarh, India

    Neera Garg, Amrit Bharti, Amrita Sharma & Shyna Bhalla

Authors
  1. Neera Garg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amrit Bharti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amrita Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shyna Bhalla
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

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

    Ajit Varma

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

    Swati Tripathi

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

    Ram Prasad

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Garg, N., Bharti, A., Sharma, A., Bhalla, S. (2019). Plant-Mycorrhizal and Plant-Rhizobial Interfaces: Underlying Mechanisms and Their Roles in Sustainable Agroecosystems. In: Varma, A., Tripathi, S., Prasad, R. (eds) Plant Microbe Interface. Springer, Cham. https://doi.org/10.1007/978-3-030-19831-2_2

Download citation

Publish with us

Policies and ethics

Search

Navigation