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Influence of Tomato Plant Mycorrhization on Nitrogen Metabolism, Growth and Fructification on P-Limited Soil

  • Catello Di MartinoEmail author
  • Antonietta Fioretto
  • Davide Palmieri
  • Valentina Torino
  • Giuseppe Palumbo
Article
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Abstract

The application of mycorrhizal fungi in agricultural soils as bio-fertilizers is going to be established as an agronomic practice for enhancing crop nutrients acquisition and production. In this work, the effects of tomato root colonization by arbuscular mycorrhizal fungus Glomus mosseae, on nitrogen metabolism, fructification and environmental sustainability without P soil fertilization have been studied. At the harvesting fruit stage, the mycorrhizal (M) plants present a significantly higher concentration of mineral nutrients and organic nitrogen compounds. In particular, GLU, GLN, ASP and ASN have risen about 35% more than non-mycorrhizal (NM) plants. Tomato root mycorrhization improved nitrogen metabolism in plants, too by increasing the nitrate reductase and the glutamine synthetase enzymatic activity. Moreover, mycorrhization affects many aspects of vegetative and reproductive growth. In particular, the fruit production turns from inoculated (M) plants into non-inoculated (NM) plants, rising up to 50%.

Keywords

Nitrogen-metabolism Mycorrhizal plant Tomato P-limited soil 
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Notes

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest and there has been no significant financial support for this work that could have influenced its outcome.

References

  1. Aissa E, Mougou A, Kouki Khalfallah K (2016) Influence of mycorrhizal inoculation and source of phosphorus on growth and nutrient uptake of pepper (Capsicum annuum L.) in calcareous soil. J New Sci Agric Biotechnol 28:1589–1595Google Scholar
  2. Aldesuquy HS, Ibrahim HA (2000) The role of shikimic acid in regulation of growth, transpiration, pigmentation, photosynthetic activity and productivity of Vigna sinensis plants. Phyton 40:277–292Google Scholar
  3. Al-Karaki G (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hortic 109:1–7CrossRefGoogle Scholar
  4. Ardakani MR, Mazaheri D, Mafakheri S, Moghaddam A (2011) Absorption efficiency of N, P, K through triple inoculation of wheat (Triticum aestivum L.) by Azospirillum brasilense, Streptomyces sp., Glomus intraradices and manure application. Physiol Mol Biol Plants 17:181–192CrossRefGoogle Scholar
  5. Arnebrantand K, Soderstrom B (1992) Effect of different fertilizer treatments on ectomycorrhizal colonization potential in two scots pine forests in Sweden. For Ecol Manage 53:77–89CrossRefGoogle Scholar
  6. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  7. Azcón R, Tobar MR (1998) Activity of nitrate reductase and glutamine synthetase in shoot and root of mycorrhizal Allium cepa: effect of drought stress. Plant Sci 133:1–8CrossRefGoogle Scholar
  8. Azcòn R, Gòmez M, Tobar MR (1992) Effects of nitrogen source on growth, nutrition, photosynthetic rate and nitrogen matabolism of mycorrhizal and phosphorus-fertilized plants of Lactuca sativa L. New Phytol 121:227–234CrossRefGoogle Scholar
  9. Balzergue C, Chabaud M, Barker DG, Bécard G, Rochange SF (2013) High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Front Plant Sci Plant Nutr.  https://doi.org/10.3389/fpls.2013.00426 Google Scholar
  10. Balzerque C, Puech-Pages V, Becard G, Rochange SF (2011) The regulation of arbuscular mycorrhizal simbiosis by phosphate in pea involves early and systemic signalling events. J Exp Bot 625:1049–1060CrossRefGoogle Scholar
  11. Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15:620–627CrossRefGoogle Scholar
  12. Berruti A, Lumini E, Balestrini R, Bianciotto V (2015) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559Google Scholar
  13. Botton B, Chalot M (1999) Nitrogen assimilation: enzymology in ectomycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology, 2nd edn. Springer, Berlin, pp 333–372CrossRefGoogle Scholar
  14. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64(6):1002–1017CrossRefGoogle Scholar
  15. Breuninger M, Trujillo CG, Serrano E, Fhisher R, Requena N (2004) Different nitrogen source modulate activity but not expression of glutamine synthetase in arbuscolar fungi. Fungal Genet Biol 41:542–552CrossRefGoogle Scholar
  16. Bryla D, Koide R (1998) Mycorrhizal response of two tomato genotypes relates to their ability to acquire and utilize phosphorus. Ann Bot 82:849–857CrossRefGoogle Scholar
  17. Bücking H, Kafle A (2015) Review: role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5:587–612CrossRefGoogle Scholar
  18. Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes, Cph 4. In: Vasanthaiah H (ed) Plants and environment.  https://doi.org/10.5772/5257
  19. Calabrese S, Pérez-Tienda J, Ellerbeck M, Arnould C, Chatagnier O, Boller T, Schüßler A, Brachmann A, Wipf D, Nuria Ferrol N, Courty P (2016) GintAMT3—a low-affinity ammonium transporter of the arbuscular mycorrhizal Rhizophagus irregularis. Front Plant Sci 7:679CrossRefGoogle Scholar
  20. Carillo P, Mastronardo G, Nacca F, Fuggi A (2005) Nitrate reductase in durum wheat seedlings as affected by nitrate nutrition and salinity. Funct Plant Biol 32:209–219CrossRefGoogle Scholar
  21. Carter MR, Gregorich EG (2008) Soil sampling and methods of analysis (Second Edition). Edited by M. R. Carter and E. G. Gregorich. Boca Raton, Fl, USA: CRC Press (2004). Exp Agric 44(3):437.  https://doi.org/10.1017/S0014479708006546 Google Scholar
  22. Cavagnaro TR, Smith FA, Smith SE, Jakobsen I (2005) Functional diversity in arbuscular mycorrhizas, exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant Cell Environ 28:642–650CrossRefGoogle Scholar
  23. Chen S, Zhao H, Zou C, Li Y, Chen Y, Wang Z, Jiang Y, Liu A, Zhao P, Wang M, Ahammed GJ (2017) Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front Microbiol 8:2516.  https://doi.org/10.3389/fmicb.2017.02516 CrossRefGoogle Scholar
  24. Copetta A, Bardi L, Bertolone E, Berta G (2011) Fruit production and quality of tomato plants (Solanum lycopersicum L.) are affected by green compost and arbuscular mycorrhizal fungi. Plant Biosyst 145:106–115CrossRefGoogle Scholar
  25. Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loucao MA, Jakobsen I (2007) Enzymatic evidence for the key role of argininein nitrogen translocation by arbuscolar mycorrhizal fungi. Plant Physiol 144:782–792CrossRefGoogle Scholar
  26. Di Martino C, Rigano V, Vona V, Esposito S, Di Martino C, Rigano C (1991) Carbon skeleton sources for ammonium assimilation in N-sufficient and N-limited cells of Cyanidium caldarium (Rhodophyta). J Phycol 27:220–223CrossRefGoogle Scholar
  27. Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455–463CrossRefGoogle Scholar
  28. Di Martino C, Pizzuto R, Pallotta ML, De Santis A, Passarella S (2006) Mitochondrial transport in proline catabolism in plants: the existence of two separate translocators in mitochondria isolated from durum wheat seedlings. Planta 223:1123–1133CrossRefGoogle Scholar
  29. Di Martino C, Palumbo G, Vitullo D, Di Santo P, Fuggi A (2018) Regulation of mycorrhiza development in durum wheat by P fertilization: effect on plant nitrogen metabolism. J Plant Nutr Soil Sci.  https://doi.org/10.1002/jpln.201700110 Google Scholar
  30. Ericsson T (1995) Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil 169:205–214CrossRefGoogle Scholar
  31. Fan X, Gordon-Weeks R, Shen Q, Miller AJ (2006) Glutamine transport and feedback regulation of nitrate reductase activity in barley roots leads to changes in cytosolic nitrate pools. J Exp Bot 57:1333–1340CrossRefGoogle Scholar
  32. Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2012a) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 109:2666–2671CrossRefGoogle Scholar
  33. Fellbaum CR, Mensah JA, Philip E, Pfeffer PE, Kiers ET, Bücking H (2012b) The role of carbon in fungal nutrient uptake and transport Implications for resource exchange in the arbuscular mycorrhizal symbiosis. Plant Signal Behav 7:1509–1512CrossRefGoogle Scholar
  34. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Höhne M, Hendriks JH, Palacios N, Cross J, Selbig J, Stitt M (2004) A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell.  https://doi.org/10.1105/tpc.104.025973 Google Scholar
  35. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  36. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular-mycorrhizal symbiosis. Nature 435:819–823CrossRefGoogle Scholar
  37. Grant C, Bittman S, Montreal M, Plenchette C, Morel C (2005) Soil and fertilizer phosphorus: effects on plant P supply and mycorrhizal development. Can J Plant Sci 85:15–21CrossRefGoogle Scholar
  38. Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signalling in Solanum lycopersicum. Physiol Plant 138:226–237CrossRefGoogle Scholar
  39. Guru V, Tholkappian P, Viswanathan K (2011) Influence of arbuscular mycorrhizal fungi and Azospirillum co-inoculation on the growth characteristics, nutritional content, and yield of tomato crops grown in south India. Indian J Fundam Appl Life Sci 1:84–92Google Scholar
  40. Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. Tansley review. New Phytol 164:243–266CrossRefGoogle Scholar
  41. Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429CrossRefGoogle Scholar
  42. 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(10):3812–3823.  https://doi.org/10.1105/tpc.111.089813 CrossRefGoogle Scholar
  43. Hildebrandt U, Katharina J, Bothe H (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microbiol 68:1919–1924CrossRefGoogle Scholar
  44. Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57:401–411CrossRefGoogle Scholar
  45. Hussain S, Sharif M, Ahmad W, Khan F, Hina Nihar H (2018) Soil and plants nutrient status and wheat growth after mycorrhiza inoculation with and without vermicompost. J Plant Nutr 41:1534–1546CrossRefGoogle Scholar
  46. Jansa J, Finlay R, Wallander H, Smith FA, Smith SE (2011) Role of mycorrhizal symbioses in phosphorus cycling. phosphorus in action biological processes in soil phosphorus cycling. Soil Biol 26:137–168.  https://doi.org/10.1007/978-3-642-15271-9_6 CrossRefGoogle Scholar
  47. Javot H, PeControletsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. PNAS 104:1720–1725CrossRefGoogle Scholar
  48. Jiang Z, Xu C, Huang B (2011) Enzymatic metabolism of nitrogen in leaves and roots of creeping bentgrass under nitrogen deficiency conditions. J Am Soc Hortic Sci 136:320–328Google Scholar
  49. Jin H, Pfeffer PE, Douds DD, Piotrowski E, Lammers PJ, Shachar-Hill Y (2005) The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168:687–669CrossRefGoogle Scholar
  50. 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
  51. Kaldorf M, Zimmer W, Bothe H (1994) Genetic evidence for the occurrence of assimilatory nitrate reductase in arbuscular-mycorrhizal and other fungi. Mycorrhiza 5:23–28CrossRefGoogle Scholar
  52. Kaldorf M, Schmelzer E, Bothe H (1998) Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. Mol Plant Microbe Interact 11:439–448CrossRefGoogle Scholar
  53. Kato K, Okamura Y, Kanahama K, Kanayama Y (2003) Nitrate-independent expression of plant nitrate reductase in Lotus japonicus root nodules. J Exp Bot 54:1685–1690.  https://doi.org/10.1093/jxb/erg189 CrossRefGoogle Scholar
  54. Koide RT, Suomi L, Stevens CM, Mc Cormik L (1998) Interactions between needles of pinus resinosa and ectomycorrhizal fungi. New Phytol 140:539–547CrossRefGoogle Scholar
  55. Lam HM, Peng SSY, Coruzzi GM (1994) Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol 106:1347–1357CrossRefGoogle Scholar
  56. Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and Chlorophyll a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–603CrossRefGoogle Scholar
  57. Liu W, Zhang Y, Jiang S, Deng Y, Christie P, Murray P, 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.  https://doi.org/10.1038/srep24902 Google Scholar
  58. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the arabidopsis root system. Plant Physiol 129:244–256CrossRefGoogle Scholar
  59. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275Google Scholar
  60. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102CrossRefGoogle Scholar
  61. Merlo L, Ferretti M, Passera C, Ghisi R (1995) Light-modulation of nitrate reductase activity in leaves and roots of maize. Physiol Plant 24:305–311CrossRefGoogle Scholar
  62. Navarro RA, Roias P (1984) Determination of ammoniacal and total nitrogen in fertilizers by ammonia-selective electrode. J Assoc Off Anal Chem 67:890–892Google Scholar
  63. Noctor G, Foyer CH (1999) Homeostasis of adenylate status during photosynthesis in a fluctuating environment. J Exp Bot 51:347–356CrossRefGoogle Scholar
  64. Nouri E, Breuillin-Sessoms F, Feller U, Reinhardt D (2014) Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS ONE 9(3):e90841CrossRefGoogle Scholar
  65. Pfautsch S, Bell TL, Gessler (2015) Uptatake, transport and redistribution of amino nitrogen in woody plants, Chap 18. In: D’Mello JPF (ed) Amino acids in higher plant. CABI, Boston, pp 315–339:  https://doi.org/10.1079/9781780642635.0315 Google Scholar
  66. Pintea A, Bele C, Andrei S, Socaciu C (2003) HPLC analysis of carotenoids in four varieties of Calendula officinalis L. flowers. Acta Biol Szegediensis 47:37–40Google Scholar
  67. Polacco JC, Todd CD (2011) Ecological aspects of nitrogen metabolism in plants. Wiley, ChichesterCrossRefGoogle Scholar
  68. Postma JA, Dathe A, Lynch JP (2014) The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiol 166:590–602CrossRefGoogle Scholar
  69. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego, p 605Google Scholar
  70. 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 62:227–250CrossRefGoogle Scholar
  71. 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 156:1050–1057CrossRefGoogle Scholar
  72. Stout MJ, Brovont RA, Duffey SS (1998) Effect of nitrogen availability on expression of constitutive and induciuble chemical defenses in tomato, Lycopersicon esculentum. J Chem Ecol 24:945–963CrossRefGoogle Scholar
  73. Sun T, Yuan H, Cao H, Yazdani M, Tadmor Y, Li L (2018) Carotenoid metabolism in plants: the role of plastids. Mol Plant Rev 11:58–74CrossRefGoogle Scholar
  74. Sundaresan P, Ubalthoose-Raja N, Gunasekaran P, Lakshaman M (1988) Studies on nitrate reduction by VAMfungal spores. Curr Sci 57:84–85Google Scholar
  75. Teste FP, Veneklaas EJ, Dixon KW, Lambers H (2014) Complementary plant nutrient-acquisition strategies promote growth of neighbour species. Funct Ecol 28:819–828CrossRefGoogle Scholar
  76. Tian C, Kasiborski B, Koul R, Lammers PJ, Bücking H, Shachar-Hill Y (2010) Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen Flux1[W][OA].. Plant Physiol 153:1175–1187CrossRefGoogle Scholar
  77. Tobin AK, Yamaya T (2001) Cellular compartmentation of ammonium assimilation in rice and barley. J Exp Bot 52:591–604CrossRefGoogle Scholar
  78. Treseder KK (2004) A meta-analysis of Mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355CrossRefGoogle Scholar
  79. Treseder KK, Allen MF (2002) Direct nitrogen and phosphorous, and atmospheric CO2 in fiel studies. New Phytol 164:347–355CrossRefGoogle Scholar
  80. Utkhede R (2006) Increased growth and yield of hydroponically grown greenhouse tomato plants inoculated with arbuscular mycorrhizal fungi Fusarium oxysporum f. sp. Radices-lycopersici. BioControl 51:393–400CrossRefGoogle Scholar
  81. Van Miegroet H (1995) Inorganic nitrogen determined by laboratory and field extractions of two forest soils. Soil Sci Soc Am J.  https://doi.org/10.2136/sssaj1995.03615995005900020040x Google Scholar
  82. Van Hees PAW, Jones DL, Jentschke G, Godbold DL (2004) Mobilization of aluminum, iron and silicon by Picea abies and ectomycorrhizas in a forest soil. Eur J Soil Sci 55:101–111CrossRefGoogle Scholar
  83. Van Scholl L, Smits MM, Hoffland E (2006) Ectomycorrhizal weathering of the soil minerals muscovite and hornblende. New Phytol 171:805–814CrossRefGoogle Scholar
  84. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefGoogle Scholar
  85. Wardlaw IF (1990) Tansley review no. 27. The control of carbon partitioning in plants. New Phytol.  https://doi.org/10.1111/j.1469-8137.1990.tb00524 Google Scholar
  86. Zhang L, Tan Q, Lee R, Trethewy A, Lee YH, Tegeder M (2010) Altered xylem–phloem transfer of amino acids affects metabolism and leads to increased seed yield and oil content in Arabidopsis. Plant Cell 22:3603–3620CrossRefGoogle Scholar
  87. Zubek S, Turnau K, Błaszkowski J (2008) Arbuscular mycorrhiza of endemic and endangered plants from the Tatra Mts. Acta Soc Bot Pol 77(2):149–156CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Catello Di Martino
    • 1
    Email author
  • Antonietta Fioretto
    • 2
  • Davide Palmieri
    • 1
  • Valentina Torino
    • 1
  • Giuseppe Palumbo
    • 1
  1. 1.Department of Agriculture, Environmental and FoodUniversity of MoliseCampobassoItaly
  2. 2.Department of Environmental, Biological and Pharmaceutical Science and TechnologiesUniversity of Campania “Luigi Vanvitelli”CasertaItaly

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