Advertisement

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

  • Neera Garg
  • Amrit Bharti
  • Amrita Sharma
  • Shyna Bhalla
Chapter

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.

Keywords

Arbuscular mycorrhizal fungi Rhizobia Rhizospheric interactions Mechanisms Abiotic stresses 

Notes

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.

References

  1. 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 169:704–709PubMedCrossRefPubMedCentralGoogle Scholar
  2. 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
  3. 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 66:3393–3398PubMedPubMedCentralCrossRefGoogle Scholar
  4. Al-Garni SMS (2006) Increasing NaCl-salt tolerance of a halophytic plant Phragmites australis by mycorrhizal symbiosis. Am Eurasian J Agric Environ Sci 1:119–126Google Scholar
  5. Alizadeh O (2011) Mycorrhizal symbiosis. Adv Stud Biol 3(6):273–281Google Scholar
  6. Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297CrossRefGoogle Scholar
  7. 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 417–452CrossRefGoogle Scholar
  8. 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 241–258CrossRefGoogle Scholar
  9. Ariel F, Romero-Barrios N, Jégu T, Benhamed M, Crespi M (2015) Battles and hijacks: noncoding transcription in plants. Trends Plant Sci 20:362–371PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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 22:1169–1178PubMedCrossRefPubMedCentralGoogle Scholar
  11. Aroca R, Porcel R, Ruiz-Lozano JM (2011) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57PubMedCrossRefPubMedCentralGoogle Scholar
  12. 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 170:47–55PubMedCrossRefPubMedCentralGoogle Scholar
  13. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957PubMedPubMedCentralCrossRefGoogle Scholar
  15. 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 3:138–147CrossRefGoogle Scholar
  16. 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 20:1055–1062PubMedCrossRefPubMedCentralGoogle Scholar
  17. Bano SA, Ashfaq D (2013) Role of mycorrhiza to reduce heavy metal stress. Nat Sci 5:16–20Google Scholar
  18. Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45:405–413CrossRefGoogle Scholar
  19. 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 109:1009–1017PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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 118:547–552CrossRefGoogle Scholar
  21. 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 181:413–423PubMedCrossRefPubMedCentralGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 21–43CrossRefGoogle Scholar
  24. 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 34:45–60CrossRefGoogle Scholar
  25. Bonfante P (2003) Plants, mycorrhizal fungi and endobacteria: a dialog among cells and genomes. Biol Bull 204:215–220PubMedCrossRefPubMedCentralGoogle Scholar
  26. Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13:492–498PubMedCrossRefPubMedCentralGoogle Scholar
  27. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:1–11CrossRefGoogle Scholar
  28. Brear EM, Day DA, Smith PMC (2013) Iron: an essential micronutrient for the legume-rhizobium symbiosis. Front Plant Sci 4:1–15CrossRefGoogle Scholar
  29. 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 27:1352–1366PubMedPubMedCentralCrossRefGoogle Scholar
  30. 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 22:904–917PubMedPubMedCentralCrossRefGoogle Scholar
  31. 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 7:1–14CrossRefGoogle Scholar
  32. Casieri L, Gallardo K, Wipf D (2012) Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235:1431–1447PubMedCrossRefPubMedCentralGoogle Scholar
  33. 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 348:345–364CrossRefGoogle Scholar
  34. Clarke VC, Loughlin PC, Day DA, Smith P (2014) Transport processes of the legume symbiosome membrane. Front Plant Sci 5:1–9CrossRefGoogle Scholar
  35. 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 40:132–137CrossRefGoogle Scholar
  36. 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 34:4–16CrossRefGoogle Scholar
  37. 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):1–11PubMedPubMedCentralCrossRefGoogle Scholar
  38. 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 9:577–584CrossRefGoogle Scholar
  39. 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 177:323–330PubMedPubMedCentralCrossRefGoogle Scholar
  40. 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 32:199–208Google Scholar
  41. 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):199–207PubMedCrossRefPubMedCentralGoogle Scholar
  42. Diedhiou I, Diouf D (2018) Transcription factors network in root endosymbiosis establishment and development. World J Microbiol Biotechnol 34(3):1–14CrossRefGoogle Scholar
  43. 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 5:1346–1358PubMedCrossRefPubMedCentralGoogle Scholar
  44. Egamberdieva D, Kucharova Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571CrossRefGoogle Scholar
  45. 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 36:1771–1782PubMedCrossRefPubMedCentralGoogle Scholar
  46. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280PubMedPubMedCentralCrossRefGoogle Scholar
  47. Faber BA, Zasoski RJ, Burau RG, Uriu K (1990) Zinc uptake by corn as affected by vesicular-arbuscular mycorrhizae. Plant Soil 129:121–130CrossRefGoogle Scholar
  48. 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 153–188Google Scholar
  49. 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 52:61–76PubMedCrossRefPubMedCentralGoogle Scholar
  50. 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):182–188CrossRefGoogle Scholar
  51. 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 54:1789–1791PubMedCrossRefPubMedCentralGoogle Scholar
  52. 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 15:813–824PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 113:19–33PubMedPubMedCentralCrossRefGoogle Scholar
  54. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300PubMedPubMedCentralCrossRefGoogle Scholar
  55. 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):1–15Google Scholar
  56. 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 158:331–340PubMedCrossRefPubMedCentralGoogle Scholar
  57. 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):105–119CrossRefGoogle Scholar
  58. Garcia K, Chasman D, Roy S, Ane JM (2017) Physiological responses and gene co-expression network of mycorrhizal roots under K+ deprivation. Plant Physiol 173:1811–1823PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 32:767–778CrossRefGoogle Scholar
  60. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Garg N, Manchanda G (2007) Symbiotic nitrogen fixation in legume nodules: process and signaling: a review. Agron Sustain Dev 27:59–68CrossRefGoogle Scholar
  62. 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):110–123CrossRefGoogle Scholar
  63. 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 39:234–250CrossRefGoogle Scholar
  64. 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 247–273Google Scholar
  65. 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 17:3489–3499PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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 20:1407–1420PubMedPubMedCentralCrossRefGoogle Scholar
  67. 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 53:244–255PubMedCrossRefPubMedCentralGoogle Scholar
  68. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefPubMedCentralGoogle Scholar
  69. Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60PubMedCrossRefPubMedCentralGoogle Scholar
  70. 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 204:609–619PubMedCrossRefPubMedCentralGoogle Scholar
  71. 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 22:2236–2241PubMedCrossRefPubMedCentralGoogle Scholar
  72. 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):287–297CrossRefGoogle Scholar
  73. 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 42:130–140PubMedCrossRefPubMedCentralGoogle Scholar
  74. 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 7:1–21CrossRefGoogle Scholar
  75. 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 435:819–823PubMedCrossRefPubMedCentralGoogle Scholar
  76. Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochem Biophys Acta Mol Cell Res 1763:595–608CrossRefGoogle Scholar
  77. 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 150:73–83PubMedPubMedCentralCrossRefGoogle Scholar
  78. Gusmao A, Cacoilo S, Figueira EM (2006) Glutathione-mediated cadmium sequestration in Rhizobium leguminosarum. Enzym Microb Technol 39:763–769CrossRefGoogle Scholar
  79. 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 69:906–920PubMedCrossRefPubMedCentralGoogle Scholar
  80. 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 311–326CrossRefGoogle Scholar
  81. 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 1:210–215Google Scholar
  82. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedCrossRefPubMedCentralGoogle Scholar
  83. Harrison MJ (2012) Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15:691–698PubMedCrossRefPubMedCentralGoogle Scholar
  84. Harrison MJ, Vanbuuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629PubMedCrossRefPubMedCentralGoogle Scholar
  85. 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 23:272–281PubMedCrossRefPubMedCentralGoogle Scholar
  86. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285CrossRefGoogle Scholar
  88. 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 23:3812–3823PubMedPubMedCentralCrossRefGoogle Scholar
  89. Howitt SM, Udvardi MK, Day DA, Gresshoff PM (1986) Ammonia transport in free-living and symbiotic Rhizobium sp. ANU289. Microbiology 132:257–261CrossRefGoogle Scholar
  90. 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:e62085PubMedPubMedCentralCrossRefGoogle Scholar
  91. 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, KnoxvilleGoogle Scholar
  92. Izmailov SF (2003) Calcium-based interactions of symbiotic partners in legumes: role of peribacteroid membrane. Russ J Plant Physiol 50:553–566CrossRefGoogle Scholar
  93. 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 109:8316–8321PubMedPubMedCentralCrossRefGoogle Scholar
  94. Jabajihare S, Deschene A, Kendrick B (1984) Lipid-content and composition of vesicles of a vesicular-arbuscular mycorrhizal fungus. Mycologia 76:1024–1030CrossRefGoogle Scholar
  95. 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 120:509–516CrossRefGoogle Scholar
  96. 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 104:1720–1725PubMedPubMedCentralCrossRefGoogle Scholar
  97. 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 356:1172–1175PubMedCrossRefPubMedCentralGoogle Scholar
  98. Johansen A, Finlay RD, Olsson PA (1996) Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 133:705–712CrossRefGoogle Scholar
  99. 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 107:2093–2098PubMedPubMedCentralCrossRefGoogle Scholar
  100. 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):619PubMedPubMedCentralCrossRefGoogle Scholar
  101. Kader JC, Delseny M (2011) Advances in botanical research, vol 60. Academic, LondonGoogle Scholar
  102. Kamboj D, Kumar R, Kumari A, Kundu BS, Pathak D, Sharma PK (2008) Rhizobia, nod factors and nodulation–a review. Agric Rev 29:200–206Google Scholar
  103. Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas trends. Plant Sci 10:22–29CrossRefGoogle Scholar
  104. 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 48:1684–1700CrossRefGoogle Scholar
  105. Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the proteobacteria. In: The prokaryotes. Springer, New YorkGoogle Scholar
  106. 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 7:706–712PubMedCrossRefPubMedCentralGoogle Scholar
  107. 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):195–206CrossRefGoogle Scholar
  108. 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 217–234Google Scholar
  109. 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 105:9823–9828PubMedPubMedCentralCrossRefGoogle Scholar
  110. Kramer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272PubMedCrossRefPubMedCentralGoogle Scholar
  111. 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 483:341–344PubMedCrossRefPubMedCentralGoogle Scholar
  112. 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 17:1625–1636PubMedPubMedCentralCrossRefGoogle Scholar
  113. 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):1–8CrossRefGoogle Scholar
  114. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  115. Lace B, Ott T (2018) Commonalities and differences in controlling multipartite intracellular infections of legume roots by symbiotic microbes. Plant Cell Physiol 59:661–672PubMedCrossRefPubMedCentralGoogle Scholar
  116. 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 181:199–207PubMedCrossRefPubMedCentralGoogle Scholar
  117. Lelandais-Brière C, Moreau J, Hartmann C, Crespi M (2016) Noncoding RNAs, emerging regulators in root endosymbioses. Mol Plant-Microbe Interact 29:170–180PubMedCrossRefPubMedCentralGoogle Scholar
  118. 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 80:255–261CrossRefGoogle Scholar
  119. 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):e24030PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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):1–15CrossRefGoogle Scholar
  121. Lindstrom K, Terefework Z, Suominen L, Lortet G (2002) Signalling and development of rhizobium: legume symbioses. Biol Environ Proc R Ir Acad 102:61–64CrossRefGoogle Scholar
  122. 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 6:24902PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  124. 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 43:102–110PubMedCrossRefPubMedCentralGoogle Scholar
  125. 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 178:863–874PubMedCrossRefPubMedCentralGoogle Scholar
  126. 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 356:1175–1178PubMedCrossRefPubMedCentralGoogle Scholar
  127. Lugtenberg BJ, Malfanova N, Kamilova F, Berg G (2013) Plant growth promotion by microbes. Mol Microbiol Ecol Rhizosphere 1–2:559–573CrossRefGoogle Scholar
  128. 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 83:285–291CrossRefGoogle Scholar
  129. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  130. MacLean AM, Bravo A, Harrison MJ (2017) Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. Plant Cell 29(10):2319–2335PubMedPubMedCentralCrossRefGoogle Scholar
  131. 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 1:1–12PubMedCentralCrossRefGoogle Scholar
  132. 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 469:58–63PubMedCrossRefPubMedCentralGoogle Scholar
  133. 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 14:1140–1148PubMedCrossRefPubMedCentralGoogle Scholar
  134. 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 9:1213–1223CrossRefGoogle Scholar
  135. Manck-Gotzenberger J, Requena N (2016) Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Front Plant Sci 7:487PubMedPubMedCentralCrossRefGoogle Scholar
  136. 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 18:179–184CrossRefGoogle Scholar
  137. 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 285:23880–23888PubMedPubMedCentralCrossRefGoogle Scholar
  138. Masson-Boivin C, Sachs JL (2018) Symbiotic nitrogen fixation by rhizobia—the roots of a success story. Curr Opin Plant Biol 44:7–15PubMedCrossRefPubMedCentralGoogle Scholar
  139. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530CrossRefGoogle Scholar
  140. McAdam EL, Reid JB, Foo E (2018) Gibberellins promote nodule organogenesis but inhibit the infection stages of nodulation. J Exp Bot 69:2117–2130PubMedPubMedCentralCrossRefGoogle Scholar
  141. 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 164:993–998CrossRefGoogle Scholar
  142. 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 8:1–25CrossRefGoogle Scholar
  143. 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 45–74CrossRefGoogle Scholar
  144. 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 6:1–10Google Scholar
  145. Michiels J, Verreth C, Vanderleyden J (1994) Effects of temperature stress on bean-nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212PubMedPubMedCentralGoogle Scholar
  146. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467PubMedPubMedCentralCrossRefGoogle Scholar
  147. Mohanty SK, Arthikala MK, Nanjareddy K, Lara M (2018) Plant-symbiont interactions: the functional role of expansins. Symbiosis 74:1–10CrossRefGoogle Scholar
  148. Moreau S, Day DA, Puppo A (1998) Ferrous iron is transported across the peribacteroid membrane of soybean nodules. Planta 207:83–87CrossRefGoogle Scholar
  149. 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 277:4738–4746PubMedCrossRefPubMedCentralGoogle Scholar
  150. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefPubMedCentralGoogle Scholar
  151. Murset V, Hennecke H, Gabriella P (2012) Disparate role of rhizobial ACC deaminase in root-nodule symbioses. Symbiosis 57:43–50CrossRefGoogle Scholar
  152. 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):e0182328PubMedPubMedCentralCrossRefGoogle Scholar
  153. Nasim G (2013) Host allelopathy and arbuscular mycorrhizal fungi. In: Cheema ZA, Farooq M, Wahid A (eds) Allelopathy. Springer, Berlin, pp 429–450CrossRefGoogle Scholar
  154. 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 209–239Google Scholar
  155. Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta, Mol Cell Res 1763:609–620PubMedCrossRefPubMedCentralGoogle Scholar
  156. 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 72:4964–4969PubMedPubMedCentralCrossRefGoogle Scholar
  157. Ocon A, Hampp R, Requena N (2007) Trehalose turnover during abiotic stress in arbuscular mycorrhizal fungi. New Phytol 174:879–891PubMedCrossRefPubMedCentralGoogle Scholar
  158. Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263PubMedCrossRefPubMedCentralGoogle Scholar
  159. Oldroyd GE, Engstrom EM, Long SR (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13:1835–1849PubMedPubMedCentralCrossRefGoogle Scholar
  160. Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144PubMedCrossRefPubMedCentralGoogle Scholar
  161. 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 162:634–649PubMedCrossRefPubMedCentralGoogle Scholar
  162. 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 95–123CrossRefGoogle Scholar
  163. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat Rev Microbiol 6:763–775PubMedCrossRefPubMedCentralGoogle Scholar
  164. Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses 2006. New Phytol 172:35–46PubMedCrossRefPubMedCentralGoogle Scholar
  165. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441PubMedCrossRefPubMedCentralGoogle Scholar
  166. Pelissier HC, Frerich A, Desimone M, Schumacher K, Tegeder M (2004) PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiol 134:664–675PubMedPubMedCentralCrossRefGoogle Scholar
  167. 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 247–263Google Scholar
  168. 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 48:1044–1055PubMedCrossRefGoogle Scholar
  169. Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can J Bot 82:1074–1088CrossRefGoogle Scholar
  170. Pfau T (2013) Modelling metabolic interactions in the legume-rhizobia symbiosis. Doctoral dissertation, University of Aberdeen, Aberdeen, United KingdomGoogle Scholar
  171. 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 120:587–598PubMedPubMedCentralCrossRefGoogle Scholar
  172. Phillips DA, Joseph CM, Maxwell CA (1992) Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol 99:1526–1531PubMedPubMedCentralCrossRefGoogle Scholar
  173. 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 36:2059–2070PubMedPubMedCentralGoogle Scholar
  174. Pilon M (2011) Moving copper in plants. New Phytol 192(2):305–307PubMedCrossRefPubMedCentralGoogle Scholar
  175. Plett JM, Martin F (2015) Reconsidering mutualistic plant–fungal interactions through the lens of effector biology. Curr Opin Plant Biol 26:45–50PubMedCrossRefPubMedCentralGoogle Scholar
  176. Poole P, Ramachandran V, Terpolilli J (2018) Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol 16(5):291–303PubMedCrossRefPubMedCentralGoogle Scholar
  177. 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 55:1743–1750PubMedCrossRefPubMedCentralGoogle Scholar
  178. Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200CrossRefGoogle Scholar
  179. 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 1–7Google Scholar
  180. 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 15:809–819CrossRefGoogle Scholar
  181. Rajtor M, Piotrowska-Seget Z (2016) Prospects for arbuscular mycorrhizal fungi (AMF) to assist in phytoremediation of soil hydrocarbon contaminants. Chemosphere 162:105–116PubMedCrossRefPubMedCentralGoogle Scholar
  182. 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 19:69–80PubMedCrossRefPubMedCentralGoogle Scholar
  183. 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 414:462–466PubMedCrossRefPubMedCentralGoogle Scholar
  184. Reichman SM (2007) The potential use of legume-rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593CrossRefGoogle Scholar
  185. Ren G (2018) The evolution of determinate and indeterminate nodules within the Papilionoideae subfamily. Doctoral dissertation, Wageningen UniversityGoogle Scholar
  186. 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 205:1385–1388PubMedCrossRefPubMedCentralGoogle Scholar
  187. Rinaudo M (2004) Role of substituents on the properties of some polysaccharides. Biomacromolecules 5:1155–1165PubMedCrossRefPubMedCentralGoogle Scholar
  188. 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 5:1247–1253PubMedCrossRefPubMedCentralGoogle Scholar
  189. 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 13:341–350CrossRefGoogle Scholar
  190. Roth R, Paszkowski U (2017) Plant carbon nourishment of arbuscular mycorrhizal fungi. Curr Opin Plant Biol 39:50–56PubMedCrossRefPubMedCentralGoogle Scholar
  191. Ruiz-Lozano JM, Collados C, Barea JM, Azcon R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502CrossRefGoogle Scholar
  192. 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 63:4033–4044PubMedCrossRefPubMedCentralGoogle Scholar
  193. 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 39:441–452PubMedCrossRefPubMedCentralGoogle Scholar
  194. 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 167:862–869PubMedCrossRefPubMedCentralGoogle Scholar
  195. Ruth B, Khalvati M, Schmidhalter U (2011) Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 342:459–468CrossRefGoogle Scholar
  196. Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767PubMedPubMedCentralCrossRefGoogle Scholar
  197. Saxena M, Saxena J, Nema R, Singh D, Gupta A (2013) Phytochemistry of medicinal plants. J Pharmacogn Phytochem 1(6):168–182Google Scholar
  198. 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 143:1827–1840PubMedPubMedCentralCrossRefGoogle Scholar
  199. 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 233:139–152PubMedCrossRefPubMedCentralGoogle Scholar
  200. Schussler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936PubMedCrossRefPubMedCentralGoogle Scholar
  201. 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 218:696–709PubMedCrossRefPubMedCentralGoogle Scholar
  202. 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 42:155–159PubMedCrossRefPubMedCentralGoogle Scholar
  203. Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430PubMedCrossRefPubMedCentralGoogle Scholar
  204. Sidahmed NEM (2016) The effect of compost, rhizobium inoculation and urea on peanut plant growth. Doctoral dissertation, Sudan University of Science and TechnologyGoogle Scholar
  205. 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 214:118–127CrossRefGoogle Scholar
  206. 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 69:822–830PubMedCrossRefPubMedCentralGoogle Scholar
  207. Silver S, Phung LT (2005) A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotechnol 32:587–605PubMedCrossRefPubMedCentralGoogle Scholar
  208. Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60CrossRefGoogle Scholar
  209. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York, p 800Google Scholar
  210. Soka G, Ritchie M (2014) Arbuscular mycorrhizal symbiosis and ecosystem processes: prospects for future research in tropical soils. Open J Ecol 4:11–22CrossRefGoogle Scholar
  211. 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 39:1036–1044PubMedCrossRefPubMedCentralGoogle Scholar
  212. 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 136:202–213CrossRefGoogle Scholar
  213. 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 21:958–966PubMedCrossRefPubMedCentralGoogle Scholar
  214. 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 5:1–13CrossRefGoogle Scholar
  215. Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53PubMedCrossRefPubMedCentralGoogle Scholar
  216. 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
  217. 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 198:2864–2875PubMedPubMedCentralCrossRefGoogle Scholar
  218. 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 65:74–81PubMedCrossRefPubMedCentralGoogle Scholar
  219. Tsyganova AV, Kitaeva AB, Tsyganov VE (2018) Cell differentiation in nitrogen-fixing nodules hosting symbiosomes. Funct Plant Biol 45(2):47–57CrossRefGoogle Scholar
  220. Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Biol 48:493–523CrossRefGoogle Scholar
  221. Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805PubMedCrossRefPubMedCentralGoogle Scholar
  222. Udvardi MK, Price GD, Gresshoff PM, Day DA (1988) A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett 231:36–40CrossRefGoogle Scholar
  223. Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Biol 42:373–390CrossRefGoogle Scholar
  224. 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: 978-3-319-57849-1CrossRefGoogle Scholar
  225. 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: 978-3-319-53064-2CrossRefGoogle Scholar
  226. Varma A, Prasad R, Tuteja N (2017c) Mycorrhiza: nutrient uptake, biocontrol, ecorestoration. Springer International Publishing, Cham. http://www.springer.com/us/book/9783319688664. ISBN: 978-3-319-68867-1CrossRefGoogle Scholar
  227. Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21(3):187–198PubMedPubMedCentralCrossRefGoogle Scholar
  228. 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):3451–3459PubMedPubMedCentralCrossRefGoogle Scholar
  229. Wais RJ, Keating DH, Long SR (2002) Structure-function analysis of nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis. Plant Physiol 129:211–224PubMedPubMedCentralCrossRefGoogle Scholar
  230. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692PubMedCrossRefPubMedCentralGoogle Scholar
  231. 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 22:2242–2246PubMedCrossRefPubMedCentralGoogle Scholar
  232. 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 26:1818–1830PubMedPubMedCentralCrossRefGoogle Scholar
  233. 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 187–213Google Scholar
  234. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  235. Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322PubMedCrossRefPubMedCentralGoogle Scholar
  236. 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):333–346PubMedCrossRefPubMedCentralGoogle Scholar
  237. 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 95:222–227PubMedPubMedCentralCrossRefGoogle Scholar
  238. 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 105–112Google Scholar
  239. 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 45:181–183CrossRefGoogle Scholar
  240. Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87CrossRefGoogle Scholar
  241. 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 9:1583–1608PubMedCrossRefPubMedCentralGoogle Scholar
  242. 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 63:4437–4446PubMedPubMedCentralCrossRefGoogle Scholar
  243. 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 93:5–16PubMedCrossRefPubMedCentralGoogle Scholar
  244. Yamazaki A, Hayashi M (2015) Building the interaction interfaces: host responses upon infection with microorganisms. Curr Opin Plant Biol 23:132–139PubMedCrossRefPubMedCentralGoogle Scholar
  245. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4PubMedCrossRefPubMedCentralGoogle Scholar
  246. 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 24:4236–4251PubMedPubMedCentralCrossRefGoogle Scholar
  247. 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):1–19Google Scholar
  248. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedPubMedCentralGoogle Scholar
  249. Zandalinas SI, Mittler R, Balfagon D, Arbona V, Gomez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12PubMedCrossRefPubMedCentralGoogle Scholar
  250. 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 24:3767–3782PubMedPubMedCentralCrossRefGoogle Scholar
  251. Zipfel C, Oldroyd GE (2017) Plant signalling in symbiosis and immunity. Nature 543(7645):328PubMedCrossRefPubMedCentralGoogle Scholar
  252. Zsogon A, Lambais MR, Benedito VA, Figueira AVDO, Peres LEP (2008) Reduced arbuscular mycorrhizal colonization in tomato ethylene mutants. Sci Agric 65:259–267CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Neera Garg
    • 1
  • Amrit Bharti
    • 1
  • Amrita Sharma
    • 1
  • Shyna Bhalla
    • 1
  1. 1.Department of BotanyPanjab UniversityChandigarhIndia

Personalised recommendations