Mycorrhizae Resource Allocation in Root Development and Root Morphology

  • Ibrahim OrtaşEmail author
  • Mazhar Rafique
  • Md Toufiq Iqbal


Plant root systems are influenced by genetics and environmental conditions which are leading to varied root system architectures. Different plant species have diverse root system architectures, and mineral nutrient availability is mainly determined by the root system. Also, the availability of mineral nutrient uptake is played by the role of mycorrhizal fungi. In this chapter, the role of plant root development, root architecture, and mycorrhizal inoculation on mineral nutrition was reviewed. The root development, mainly the physiological, morphological, and molecular responses of plant roots to diverse nutrient uptake in assistance to the mycorrhizal fungi, is one of the hot research areas for plant scientists and plant nutritionists. Keeping in mind the importance of this subject, the present chapter is compiled which covers the importance of nutrient uptake in plant growth and development. Moreover, the importance of roots in nutrient uptake and establishing the symbiotic relationship is essential. Underground relations are set up by the plant roots in coordination with different soil microorganisms. Arbuscular mycorrhizal fungi (AMF) as a major soil organism participate in symbiotic relationship and facilitate the plant in growth and root development. Moreover, it shapes the plant roots for the better cooperation with AMF in nutrient and water uptake facilitation. It may change the root morphology, physiology, and molecular behavior which may vary plant to plant.


Nutrient uptake Root systems Root architecture Mycorrhizae Field crops Horticultural crop root systems 


  1. Arines J, Ballester A (1992) Mycorrhization of micropropagated Prunus avium L. plantlets. Micropropagation, root regeneration, and mycorrhizas Joint meeting between COST, Dijon, France, p 45Google Scholar
  2. Atkinson D (1992) Tree root development: the role of models in understanding the consequences of arbuscular endomycorrhizal infection. Agronomie 12:817–820CrossRefGoogle Scholar
  3. Atkinson D, Berta G, Hooker J (1994) Impact of mycorrhizal colonisation on root architecture, root longevity and the formation of growth regulators. In: Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Springer, BerlinGoogle Scholar
  4. Azcón-Aguilar C, Barcelo A, Vidal M, De La Vina G (1992) Further studies on the influence of mycorrhizae on growth and development of micropropagated avocado plants. Agronomie 12:837–840CrossRefGoogle Scholar
  5. Azcon-Aguilar C, Padilla I, Encina C, Azcon R, Barea J (1996) Mycorrhizal inoculation (Glomus deserticola) enhances plant growth and changes root system morphology in micropropagated Annona cherimola Mill. Novel biotechnological approaches to plant production: from sterile root to mycorrhizosphere Joint COST meeting, Pisa, Italy, p 21Google Scholar
  6. Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Berta G, Fusconi A, Trotta A (1993) VA mycorrhizal infection and the morphology and function of root systems. Environ Exp Bot 33:159–173CrossRefGoogle Scholar
  8. Black R, Tinker P (1977) Interaction between effects of vesicular–arbuscular mycorrhiza and fertiliser phosphorus on yields of potatoes in the field. Nature 267:510–511CrossRefGoogle Scholar
  9. Bolan N (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207CrossRefGoogle Scholar
  10. Bouhired L, Gianinazzi S, Gianinazzi-Pearson V (1992) Influence of endomycorrhizal inoculation on the growth of Phoenix dactylifera. Micropropagation, root regeneration and mycorrhizas Joint meeting between Cost, Dijon, France, p 53Google Scholar
  11. Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible W-R, Krajinski F (2010) Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant-Microbe Interact 23:915–926PubMedCrossRefPubMedCentralGoogle Scholar
  12. Branzanti B, Gianinazzi-Pearson V, Gianinazzi S (1992) Influence of phosphate fertilization on the growth and nutrient status of micropropagated apple infected with endomycorrhizal fungi during the weaning stage. Agronomie 12:841–845CrossRefGoogle Scholar
  13. Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bücking H, Kafle A (2015) Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5:587CrossRefGoogle Scholar
  15. Cassells A, Mark G, Periappuram C (1996) Establishment of arbuscular mycorrhizal fungi in autotrophic strawberry cultures in vitro. Comparison with inoculation of microplants in vivo. Agronomie 16:625–632CrossRefGoogle Scholar
  16. Castillo C, Puccio F, Morales D, Borie F, Sieverding E (2012) Early arbuscular mycorrhiza colonization of wheat, barley and oats in Andosols of southern Chile. J Soil Sci Plant Nutr 12:511–524Google Scholar
  17. Cheng L, Bucciarelli B, Liu J, Zinn K, Miller S, Patton-Vogt J, Allan D, Shen J, Vance CP (2011) White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases. Plant Physiol 156:1131–1148PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cruz-Ramirez A, Calderon-Vazquez C, Herrera-Estrella L (2009) Effect of nutrient availability on root system development.
  19. Davies FT, Calderón CM, Huaman Z, Gómez R (2005) Influence of a flavonoid (formononetin) on mycorrhizal activity and potato crop productivity in the highlands of Peru. Sci Hortic 106:318–329CrossRefGoogle Scholar
  20. Declerck S, Risede J-M, Delvaux B (2002) Greenhouse response of micropropagated bananas inoculated with in vitro monoxenically produced arbuscular mycorrhizal fungi. Sci Hortic 93:301–309. CrossRefGoogle Scholar
  21. Desnos T (2008) Root branching responses to phosphate and nitrate. Curr Opin Plant Biol 11:82–87PubMedCrossRefPubMedCentralGoogle Scholar
  22. Dolcet-Sanjuan R, Claveria E, Camprubi A, Estaun V, Calvet C (1996) Micropropagation of walnut trees (Juglans regia L) and response to arbuscular mycorrhizal inoculation. Agronomie 16:639–645CrossRefGoogle Scholar
  23. Douds DD Jr, Nagahashi G, Reider C, Hepperly PR (2007) Inoculation with arbuscular mycorrhizal fungi increases the yield of potatoes in a high P soil. Biol Agric Hortic 25:67–78CrossRefGoogle Scholar
  24. Douds DD, Millner P (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agric Ecosyst Environ 74:77–93. CrossRefGoogle Scholar
  25. Duan X, Neuman DS, Reiber JM, Green CD, Saxton AM, Augé RM (1996) Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 47:1541–1550CrossRefGoogle Scholar
  26. Epstein E (1997) The science of composting. CRC Press LLC, Boca Ratón, FLGoogle Scholar
  27. Estrada-Luna AA, Davies FT (2003) Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J Plant Physiol 160:1073–1083PubMedCrossRefPubMedCentralGoogle Scholar
  28. Fageria NK, Moreira A (2011) The role of mineral nutrition on root growth of crop plants. In: Sparks DL (ed) Advances in agronomy, vol 110. Elsevier Academic, San DiegoGoogle Scholar
  29. Feddermann N, Finlay R, Boller T, Elfstrand M (2010) Functional diversity in arbuscular mycorrhiza–the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecol 3:1–8CrossRefGoogle Scholar
  30. Fester T, Kiess M, Strack D (2002) A mycorrhiza-responsive protein in wheat roots. Mycorrhiza 12:219–222PubMedCrossRefPubMedCentralGoogle Scholar
  31. Fiorilli V, Vallino M, Biselli C, Faccio A, Bagnaresi P, Bonfante P (2015) Host and non-host roots in rice: cellular and molecular approaches reveal differential responses to arbuscular mycorrhizal fungi. Front Plant Sci 6:636PubMedPubMedCentralCrossRefGoogle Scholar
  32. Giri B, Prasad R, Varma A (2018) Root biology. Springer International Publishing (ISBN 978-3-319-75910-4)
  33. Gutjahr C, Casieri L, Paszkowski U (2009) Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytol 182:829–837PubMedCrossRefGoogle Scholar
  34. He Y, Liao H, Yan X (2003) Localized supply of phosphorus induces root morphological and architectural changes of rice in split and stratified soil cultures. Plant Soil 248:247–256CrossRefGoogle Scholar
  35. Hemsley AR, Poole I (2004) The evolution of plant physiology. Elsevier, LondonGoogle Scholar
  36. Hetrick B, Wilson G, Todd T (1996) Mycorrhizal response in wheat cultivars: relationship to phosphorus. Can J Bot 74:19–25CrossRefGoogle Scholar
  37. Hijri M (2016) Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26:209–214PubMedCrossRefGoogle Scholar
  38. Hochholdinger F (2009) The maize root system: morphology, anatomy, and genetics. In: Handbook of maize: its biology. Springer, New YorkGoogle Scholar
  39. Hochholdinger F, Woll K, Sauer M, Dembinsky D (2004) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot 93:359–368PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hoshyar Z, Abedi B, Ganji Moghadam E, Davari Nejad G (2017) Effect of arbuscular mycorrhiza on growth and physiological behavior of PHL-C rootstock. J Plant Physiol Breed 7:53–60Google Scholar
  41. Ilag LL, Rosales A, Elazegui F, Mew T (1987) Changes in the population of infective endomycorrhizal fungi in a rice-based cropping system. Plant Soil 103:67–73CrossRefGoogle Scholar
  42. Jaizme-Vega M, Rodríguez-Romero A, Hermoso CM, Declerck S (2003) Growth of micropropagated bananas colonized by root-organ culture produced arbuscular mycorrhizal fungi entrapped in Ca-alginate beads. Plant Soil 254:329–335CrossRefGoogle Scholar
  43. Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129CrossRefGoogle Scholar
  44. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918PubMedCrossRefPubMedCentralGoogle Scholar
  45. Khan MH, Meghvansi M, Prasad K, Siddiqui S, Varma A (2017) Arbuscular mycorrhizal symbiosis and nutrient resource limitation: predicting the linkages and effectiveness of partnership. In: Mycorrhiza-nutrient uptake, biocontrol, ecorestoration. Springer, ChamGoogle Scholar
  46. Koide RT, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148:511–517. CrossRefGoogle Scholar
  47. Krishna H, Singh S, Minakshi PV, Khawale R, Deshmukh P, Jindal P (2006) Arbuscular-mycorrhizal fungi alleviate transplantation shock in micropropagated grapevine (Vitis vinifera L.). J Hortic Sci Biotechnol 81:259–263CrossRefGoogle Scholar
  48. Kungu JB, Lasco RD, Dela Cruz LU, Dela Cruz RE, Husain T (2008) Effect of vesicular arbuscular mycorrhiza (VAM) fungi inoculation on coppicing ability and drought resistance of senna spectabilis. Pak J Bot 40:2217–2224Google Scholar
  49. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31. CrossRefGoogle Scholar
  52. Li XL, George E, Marschner H (1991) Phosphorus depletion and pH decrease at the root soil and hyphae soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol 119:397–404CrossRefGoogle Scholar
  53. Li XL, George E, Marschner H, Zhang JL (1997) Phosphorus acquisition from compacted soil by hyphae of a mycorrhizal fungus associated with red clover (Trifolium pratense). Can J Bot Revue Canadienne De Botanique 75:723–729Google Scholar
  54. López-Bucio J, Cruz-Ramırez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287PubMedCrossRefPubMedCentralGoogle Scholar
  55. Lumini E, Vallino M, Alguacil MM, Romani M, Bianciotto V (2011) Different farming and water regimes in Italian rice fields affect arbuscular mycorrhizal fungal soil communities. Ecol Appl 21:1696–1707PubMedCrossRefPubMedCentralGoogle Scholar
  56. Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7PubMedPubMedCentralCrossRefGoogle Scholar
  57. Maillet F, Poinsot V, Andre O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58PubMedCrossRefPubMedCentralGoogle Scholar
  58. Manoharan P, Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Sharma MP, Muthuchelian K (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. Grown under different water stress conditions. Eur J Soil Biol 46:151–156CrossRefGoogle Scholar
  59. Marin M, Mari A, Ibarra M, Garcia-Ferriz L (2003) Arbuscular mycorrhizal inoculation of micropropagated persimmon plantlets. J Hortic Sci Biotechnol 78:734–738CrossRefGoogle Scholar
  60. Marschener H (1998) Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crop Res 56:203–207CrossRefGoogle Scholar
  61. Marschner H (1995) Mineral nutrition of high plants. Academic, LondonGoogle Scholar
  62. Marschner H (1996) Mineral nutrient acquisition in nonmycorrhizal and mycorrhizal plants. Phyton Annales Rei Botanicae 36:61–68Google Scholar
  63. Marschner H (2011) Marschner’s mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  64. Marschner P (2012) Marschner’s mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  65. Marschner H, Romheld V, Horst WJ, Martin P (1986) Root-induced changes in the rhizosphere – importance for the mineral-nutrition of plants. Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 149:441–456CrossRefGoogle Scholar
  66. Mohammad MJ, Malkawi HI (2004) Root, shoot and nutrient acquisition responses of mycorrhizal and nonmycorrhizal wheat to phosphorus application to highly calcareous soils. Asian J Plant Sci 3:363–369CrossRefGoogle Scholar
  67. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074PubMedPubMedCentralCrossRefGoogle Scholar
  68. Neumann E, George E (2010) Nutrient uptake: the arbuscular mycorrhiza fungal symbiosis as a plant nutrient acquisition strategy. In: Arbuscular mycorrhizas: physiology and function. Springer, AmsterdamGoogle Scholar
  69. Neumann G, Martinoia E (2002) Cluster roots–an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167PubMedCrossRefPubMedCentralGoogle Scholar
  70. Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382CrossRefGoogle Scholar
  71. Norman J, Atkinson D, Hooker J (1996) Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae. Plant Soil 185:191–198CrossRefGoogle Scholar
  72. Ortas I (1997) Determination of the extent of rhizosphere soil. Commun Soil Sci Plant Anal 28:1767–1776. CrossRefGoogle Scholar
  73. Ortas I (2003) Effect of selected mycorrhizal inoculation on phosphorus sustainability in sterile and non-sterile soils in the Harran Plain in South Anatolia. J Plant Nutr 26:1–17. CrossRefGoogle Scholar
  74. Ortas I (2012) The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions. Field Crop Res 125:35–48. CrossRefGoogle Scholar
  75. Ortas I (2015) Comparative analyses of Turkey agricultural soils: potential communities of indigenous and exotic mycorrhiza species’ effect on maize (Zea mays L.) growth and nutrient uptakes. Eur J Soil Biol 69:79–87. CrossRefGoogle Scholar
  76. Ortas I, Akpinar C (2011) Response of maize genotypes to several mycorrhizal inoculums in terms of plant growth, nutrient uptake and spore production. J Plant Nutr 34:970–987. CrossRefGoogle Scholar
  77. Ortas I, Rafique M, Akpinar C, Aka Kacar Y (2017) Growth media and mycorrhizal species effect on acclimatization and nutrient uptake of banana plantlets. Sci Hortic 217:55–60CrossRefGoogle Scholar
  78. Pearson J, Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol 124:481–488CrossRefGoogle Scholar
  79. Pinior A, Grunewaldt-Stöcker G, von Alten H, Strasser RJ (2005) Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring. Mycorrhiza 15:596PubMedCrossRefGoogle Scholar
  80. Ponton F, Piche Y, Parent S, Caron M (1990) The use of vesicular-arbuscular mycorrhizae in Boston fern production: I. Effects of peat-based mixes. Hortscience 25:183–189CrossRefGoogle Scholar
  81. Prasad R, Bhola D, Akdi K, Cruz C, Sairam K, Tuteja N, Varma A (2017) Introduction to mycorrhiza: historical development. In: Mycorrhiza-function, diversity, state of the art. Springer, ChamGoogle Scholar
  82. Pritchard SG, Rogers HH (2000) Spatial and temporal deployment of crop roots in CO2-enriched environments. New Phytol 147:55–71CrossRefGoogle Scholar
  83. Puthur JT, Prasad K, Sharmila P, Saradhi PP (1998) Vesicular arbuscular mycorrhizal fungi improves establishment of micropropagated Leucaena leucocephala plantlets. Plant Cell Tissue Organ Cult 53:41CrossRefGoogle Scholar
  84. Quatrini P, Gentile M, Carimi F, Pasquale FD, Puglia AM (2003) Effect of native arbuscular mycorrhizal fungi and Glomus mosseae on acclimatization and development of micropropagated Citrus limon (L.) Burm. J Hortic Sci Biotechnol 78:39–45CrossRefGoogle Scholar
  85. Rancillac M, Cadoux F, Leduc D, Kahane R (1996) Improvement of a protocol to establish in vitro arbuscular mycorrhizal strains with vitro bulbs of onion, Allium cepa L. Novel biotechnological approaches to plant production: from sterile root to mycorrhizosphere Joint COST meetingGoogle Scholar
  86. Rapparini F, Baraldi R, Bertazza G (1996) Growth and carbohydrate status of Pyrus communis L plantlets inoculated with Glomus sp. Agronomie 16:653–661CrossRefGoogle Scholar
  87. Rodríguez-Romero AS, Guerra MSP, Jaizme-Vega MDC (2005) Effect of arbuscular mycorrhizal fungi and rhizobacteria on banana growth and nutrition. Agron Sustain Dev 25:395–399CrossRefGoogle Scholar
  88. Rogers HH, Runion GB, Prior A (1999) Response of plants to elevated atmospheric CO2: root growth, mineral. Carbon dioxide and environmental stress, p 215Google Scholar
  89. Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, Pascale SD, Bonini P, Colla G (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic 196:91–108. CrossRefGoogle Scholar
  90. Sbrana C, Vitagliano C, Avio L, Giovanneti M (1992) Influence of vesicular-arbuscular mycorrhizae on transplant stress of micropropagated apple and peach rootstocks. Micropropagation, root regeneration, and mycorrhizas Joint meeting between COSTGoogle Scholar
  91. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453PubMedPubMedCentralCrossRefGoogle Scholar
  92. Schubert A, Bodrino C, Gribaudo I (1992) Vesicular-arbuscular mycorrhizal inoculation of kiwifruit (Actinidia deliciosa) micropropagated plants. Agronomie 12:847–850CrossRefGoogle Scholar
  93. Sharma S, Sharma AK, Prasad R, Varma A (2017) Arbuscular mycorrhiza: a tool for enhancing crop production. In: Mycorrhiza-nutrient uptake, biocontrol, ecorestoration. Springer, New YorkGoogle Scholar
  94. Shrivastava S, Prasad R, Varma A (2014) Anatomy of root from eyes of a microbiologist. In: Root engineering. Springer, BerlinGoogle Scholar
  95. Singh S, Minakshi G, Khawale R, Patel V, Krishna H, Saxena A (2003) Mycorrhization as an aid for biohardening of in vitro raised Grape (Vitis vinifera L.) plantlets. VII International symposium on temperate zone fruits in the tropics and subtropics, p 662Google Scholar
  96. Smith S, De Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philos Trans R Soc B Biol Sci 367(1595):1441–1452CrossRefGoogle Scholar
  97. Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic, San Diego, CAGoogle Scholar
  98. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250PubMedCrossRefPubMedCentralGoogle Scholar
  99. Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20CrossRefGoogle Scholar
  100. Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057PubMedPubMedCentralCrossRefGoogle Scholar
  101. Solaiman M, Hirata H (1998) Glomus-wetland rice mycorrhizas influenced by nursery inoculation techniques under high fertility soil conditions. Biol Fertil Soils 27:92–96CrossRefGoogle Scholar
  102. Taylor J, Harrier LA (2001) A comparison of development and mineral nutrition of micropropagated Fragaria× ananassa cv. Elvira (strawberry) when colonised by nine species of arbuscular mycorrhizal fungi. Appl Soil Ecol 18:205–215CrossRefGoogle Scholar
  103. Teotia P, Kumar M, Prasad R, Kumar V, Tuteja N, Varma A (2017) Mobilization of micronutrients by mycorrhizal fungi. Mycorrhiza-function, diversity, state of the art. Springer, ChamGoogle Scholar
  104. Tingey DT, Phillips DL, Johnson MG (2000) Elevated CO2 and conifer roots: effects on growth, life span and turnover. New Phytol 147:87–103CrossRefGoogle Scholar
  105. Uosukainen M, Vestberg M (1997) Timing of AMF inoculation to microcuttings of crab apple cv. Marjatta. COST Action 821: arbuscular mycorrhizas in sustainable soil-plant systems: report of 1996 activitiesGoogle Scholar
  106. Upadhyaya CP, Gururani MA, Prasad R, Varma A (2013) A cell wall extract from Piriformospora indica promotes tuberization in potato (Solanum tuberosum L.) via enhanced expression of Ca+2 signaling pathway and lipoxygenase gene. Appl Biochem Biotechnol 170(4):743–755PubMedCrossRefPubMedCentralGoogle Scholar
  107. Vallino M, Fiorilli V, Bonfante P (2014) Rice flooding negatively impacts root branching and arbuscular mycorrhizal colonization, but not fungal viability. Plant Cell Environ 37:557–572PubMedCrossRefPubMedCentralGoogle Scholar
  108. Vance CP (2010) Quantitative trait loci, epigenetics, sugars, and microRNAs: quaternaries in phosphate acquisition and use. Plant Physiol 154:582–588PubMedPubMedCentralCrossRefGoogle Scholar
  109. Varma A, Prasad R, Tuteja N (2017) Mycorrhiza: nutrient uptake, biocontrol, ecorestoration. Springer International Publishing (ISBN: 978-3-319-68867-1)
  110. Vidal M, Azcón-Aguilar C, Barea J, Pliego-Alfaro F (1992) Mycorrhizal inoculation enhances growth and development of micropropagated plants of avocado. Hortscience 27:785–787CrossRefGoogle Scholar
  111. Volkmar K (1997) Water stressed nodal roots of wheat: effects on leaf growth. Funct Plant Biol 24:49–56CrossRefGoogle Scholar
  112. Wang B, Tang X, Cheng L, Zhang A, Zhang W, Zhang F, Liu J, Cao Y, Allan D, Vance C (2010) Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol 187:1112–1123PubMedCrossRefPubMedCentralGoogle Scholar
  113. Wirsel SG (2004) Homogenous stands of a wetland grass harbour diverse consortia of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 48:129–138PubMedCrossRefPubMedCentralGoogle Scholar
  114. Wu Q-S, Zou Y-N, He X-H (2010) Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plant 32:297–304CrossRefGoogle Scholar
  115. Wu F, Wang W, Ma Y, Liu Y, Ma X, An L, Feng H (2013) Prospect of beneficial microorganisms applied in potato cultivation for sustainable agriculture. Afr J Microbiol Res 7:2150–2158CrossRefGoogle Scholar
  116. Wu Q-S, Srivastava A, Zou Y-N, Malhotra S (2017a) Mycorrhizas in citrus: beyond soil fertility and plant nutrition. Indian J Agric Sci 87:427–443Google Scholar
  117. Wu QS, Sun P, Srivastava AK (2017b) AMF diversity in citrus rhizosphere. Indian J Agric Sci 87:653–656Google Scholar
  118. Yao M, Tweddell R, Desilets H (2002) Effect of two vesicular-arbuscular mycorrhizal fungi on the growth of micropropagated potato plantlets and on the extent of disease caused by Rhizoctonia solani. Mycorrhiza 12:235–242PubMedCrossRefGoogle Scholar
  119. Zhu X, Song F, Liu S, Liu F (2016) Role of arbuscular mycorrhiza in alleviating salinity stress in wheat (Triticum aestivum L.) grown under ambient and elevated CO2. J Agron Crop Sci 202:486–496CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ibrahim Ortaş
    • 1
    Email author
  • Mazhar Rafique
    • 2
  • Md Toufiq Iqbal
    • 3
  1. 1.Department of Soil Science and Plant NutritionUniversity of CukurovaAdanaTurkey
  2. 2.Department of Plant SciencesQuaid-i-Azam UniversityIslamabadPakistan
  3. 3.Department of Agronomy and Agricultural ExtensionUniversity of RajshahiRajshahiBangladesh

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