Plant and Soil

, Volume 372, Issue 1–2, pp 361–374 | Cite as

Effects of single and mixed inoculation with two arbuscular mycorrhizal fungi in two different levels of phosphorus supply on β-carotene concentrations in sweet potato (Ipomoea batatas L.) tubers

  • Yu TongEmail author
  • Elke Gabriel-Neumann
  • Benard Ngwene
  • Angelika Krumbein
  • Susanne Baldermann
  • Monika Schreiner
  • Eckhard George
Regular Article



This study aimed to determine the effect of arbuscular mycorrhizal (AM) fungi and phosphorus (P) supply levels on β-carotene concentrations in sweet potato (Ipomoea batatas L.) tubers.


Two commercial AM fungal isolates of Glomus intraradices (IFP Glintra) and Glomus mosseae (IFP Glm) which differ in their life cycles were used. Sweet potato plants were grown in a horizontal split-root system that consisted of two root compartments. A root-free fungal compartment that allowed the quantification of mycelial development was inserted into each root compartment. The two root compartments were inoculated either with the same or with different AM isolates, or remained free of mycorrhizal propagules. Each fungal treatment was carried out in two P supply levels.


In the low P supply level, mycorrhizal colonization significantly increased β-carotene concentrations in sweet potato tubers compared with the non-mycorrhizal plants. Glomus intraradices appeared to be more efficient in increasing β-carotene concentrations than G. mosseae. Dual inoculation of the root system with the two mycorrhizal fungi did not result in a higher increase in tuber β-carotene concentrations than inoculation with the single isolates. Improved P nutrition led to higher plant tuber biomass but was not associated with increased β-carotene concentrations.


The results indicate a remarkable potential of mycorrhizal fungi to improve β-carotene concentrations in sweet potato tubers in low P fertilized soils. These results also suggest that β-carotene metabolism in sweet potato tubers might be specifically activated by root mycorrhizal colonization.


β-carotene Glomus intraradices Glomus mosseae Phosphorus Sweet potato 



This work was supported by China Scholarship Council. We appreciate technical assistance in laboratory work by Andrea Jankowsky, Susanne Jeserigk and Kerstin Bieler. We thank Dr. Michael H. Walter (Leibniz-Institute of Plant Biochemistry, Halle) for the helpful discussion.


  1. Akiyama K (2007) Chemical identification and functional analysis of apocarotenoids involved in the development of arbuscular mycorrhizal symbiosis. Biosci Biotechnol Biochem 71:1405–1414PubMedCrossRefGoogle Scholar
  2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  3. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351PubMedCrossRefGoogle Scholar
  4. Alkan N, Gadkar V, Yarden O, Kapulnik Y (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Appl Environ Microbiol 72:4192–4199PubMedCrossRefGoogle Scholar
  5. Azcón R, Ambrosano E, Charest C (2003) Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci 165:1137–1145CrossRefGoogle Scholar
  6. Baslam M, Pascual I, Sánchez-Díaz M, Erro J, García-Mina JM, Goicoechea N (2011) Improvement of nutritional quality of greenhouse-grown lettuce by arbuscular mycorrhizal fungi is conditioned by the source of phosphorus nutrition. J Agric Food Chem 59:11129–11140PubMedCrossRefGoogle Scholar
  7. Bååth E, Söderström BE (1980) Degradation of macromolecules by microfungi isolated from different podzolic soil horizons. Can J Bot 58:422–425Google Scholar
  8. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J (2008) Maternal and child under nutrition: Global and regional exposures and health consequences. Lancet 371:243–260PubMedCrossRefGoogle Scholar
  9. 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
  10. Edathil TT, Manian S, Udaiyan K (1996) Interaction of multiple VAM fungal species on root colonization, plant growth and nutrient status of tomato seedlings (Lycopersicon esculentum Mill.). Agric Ecosyst Environ 59:63–68CrossRefGoogle Scholar
  11. Fernández MC, Boem FHG, Rubio G (2011) Effect of indigenous mycorrhizal colonization on phosphorus acquisition efficiency in soybean and sunflower. J Plant Nutr Soil Sci 174:673–677CrossRefGoogle Scholar
  12. Floss DS, Hause B, Lange PR, Küster H, Strack D, Walter MH (2008) Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J 56:86–100PubMedCrossRefGoogle Scholar
  13. Gericke S, Kurmies B (1952) Die colorimetrische Phosphorsäurebestimmung mit Ammonium-Vanadat-Molybdat und ihre Anwendung in der Pflanzenanalyse. J Plant Nutr Soil Sci 159:11–21Google Scholar
  14. Graham JH, Duncan LW, Eissenstat DM (1997) Carbohydrate allocation patterns in citrus genotypes as affected by phosphorus nutrition, mycorrhizal colonisation and mycorrhizal dependency. New Phytol 135:335–343CrossRefGoogle Scholar
  15. Gustafson DJ, Casper BB (2006) Differential host plant performance as a function of soil arbuscular mycorrhizal fungal communities: Experimentally manipulating co-occurring Glomus species. Plant Ecol 183:257–263CrossRefGoogle Scholar
  16. Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agron Sustain Dev 23:481–488Google Scholar
  17. Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789PubMedCrossRefGoogle Scholar
  18. Jedrszczyk E (2010) Effect of potassium foliar nutrition on changes in the content of carotenoid pigments and on some parameters of the nutritional value of tomato fruit. Veg Crops Res Bull 72:105–114Google Scholar
  19. Kapinga R, Namanda S, Stathers T (2005) Sweetpotato in Sub-Saharan Africa. In: Stathers T, Namanda S, Mwanga ROM, Khisa G, Kapinga R (eds) Manual for sweetpotato integrated production and pest management farmer field schools in sub-Saharan Africa. International Potato Center, Kampala, Uganda, pp 13–16. ISBN 9970-895-01-XGoogle Scholar
  20. Kopsell DA, Kopsell DE (2006) Assessing bioavailability of carotenoids in vegetable crops. Trends Plant Sci 11:499–507PubMedCrossRefGoogle Scholar
  21. Kopsell DA, Kopsell DE, Curran-Celentano J (2007) Carotenoid pigments in kale are influenced by nitrogen concentration and form. J Sci Food Agric 87:900–907CrossRefGoogle Scholar
  22. Kormanik P, McGraw AC (1982) Quantification of vesicular-arbuscular mycorrhizae in plant roots. In: Methods and principals of mycorrhizal research, Amer Phytopathological Society, USA, pp 37–45Google Scholar
  23. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505CrossRefGoogle Scholar
  24. Krishna H, Singh SK, Sharma RR, Khawale RN, Grover M, Patel VB (2005) Biochemical changes in micropropagated grape (Vitis vinifera L.) plantlets due to arbuscular mycorrhizal fungi (AMF) inoculation during ex vitro acclimatization. Sci Hortic 106:554–567CrossRefGoogle Scholar
  25. Krumbein A, Schonhof I, Schreiner M (2005) Composition and contents of phytochemicals (glucosinolates, carotenoids and chlorophylls) and ascorbic acid in selected Brassica species (B. juncea, B. rapa subsp. nipposinica var. chinoleifera, B. rapa subsp. chinensis and B. rapa subsp. rapa). J Appl Bot Food Qual 79:168–174Google Scholar
  26. Li HY, Zhu YG, Marschner P, Smith FA, Smith SE (2005) Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant Soil 277:221–232CrossRefGoogle Scholar
  27. Long LK, Yao Q, Huang YH, Yang RH, Guo J, Zhu HH (2010) Effects of arbuscular mycorrhizal fungi on zinnia and the different colonization between Gigaspora and Glomus. World J Microbiol Biotechnol 26:1527–1531CrossRefGoogle Scholar
  28. Low JW, Arimond M, Osman N, Cunguara B, Zano F, Tschirley D (2007) A food-based approach introducing orange-fleshed sweet potatoes increased vitamin A intake and serum retinol concentrations in young children in rural Mozambique. J Nutr 137:1320–1327PubMedGoogle Scholar
  29. López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, Vos RD, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874PubMedCrossRefGoogle Scholar
  30. Mena-Violante HG, Ocampo-Jiménez O, Dendooven L, Martínez-Soto G, González-Castañeda J, Davies FT, Olalde-Portugal V (2006) Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 16:261–267PubMedCrossRefGoogle Scholar
  31. Miranda JCC, Harris PJ (1994) Effects of soil phosphorus on spore germination and hyphal growth of arbuscular mycorrhizal fungi. New Phytol 128:103–108CrossRefGoogle Scholar
  32. Neumann E (2007) The influence of the soil phosphorus fertilization level and the light supply to the host plant on interactions between the two arbuscular mycorrhizal fungi Glomus intraradices and Glomus mosseae colonizing the same plant root system. In: Mycorrhiza technology for sustainable agriculture: Results and ideas, Dissertation, University of Hohenheim, Germany pp 181–216Google Scholar
  33. Neumann E, George E (2005) Extraction of extraradical arbuscular mycorrhizal mycelium from compartments filled with soil and glass beads. Mycorrhiza 15:533–537PubMedCrossRefGoogle Scholar
  34. Neumann E, George E (2010) Nutrient uptake: The arbuscular mycorrhiza fungal symbiosis as a plant nutrient acquisition strategy. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: Physiology and function, 2nd edn. Springer, London, New York, pp 137–167CrossRefGoogle Scholar
  35. Neumann E, Schmid B, Romheld V, George E (2009) Extraradical development and contribution to plant performance of an arbuscular mycorrhizal symbiosis exposed to complete or partial rootzone drying. Mycorrhiza 20:13–23PubMedCrossRefGoogle Scholar
  36. Ngwene B (2011) Compatible host/fungus combination: Contribution of life cycle synchronisation to the success of the AM symbiosis. In: Management of the mycorrhizosphere: Innovative symbiosis technology for sustainable vegetable production, Dissertation, Humboldt University of Berlin, Germany pp 80–95Google Scholar
  37. Olaofe O, Sanni CO (1988) Mineral contents of agricultural products. Food Chem 30:73–77CrossRefGoogle Scholar
  38. Olsson PA, van Aarle IM, Allaway WG, Ashford AE, Rouhier H (2002) Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiol 130:1162–1171PubMedCrossRefGoogle Scholar
  39. Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790CrossRefGoogle Scholar
  40. O’Sullivan JN, Asher CJ, Blarney FPC (1997) Nutrient disorders of sweet potato. ACIAR Monograph. Canberra, Australia. ISBN 1 863202102Google Scholar
  41. Rochange (2010) Striogolactones and their role in arbuscular mycorrhizal symbiosis. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: Physiology and function, 2nd edn. Springer, London, New York, pp 73–90CrossRefGoogle Scholar
  42. Schüller H (1969) Die CAL-Methode, eine neue Methode zur Bestimmung des pflanzenverfügbaren Phosphates im Boden. Ztg Pflanzenernähr Bodenkunde 123:48–63CrossRefGoogle Scholar
  43. Sedghi M, Pirzad A, Amanpour-Balaneji B (2011) Light absorption and carotenoid synthesis of pot marigold (Calendula officinalis L.) in response to phosphorous and potassium varying levels. Not Sci Biol 3:46–50Google Scholar
  44. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, LondonGoogle Scholar
  45. Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: The contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524CrossRefGoogle Scholar
  46. Tanaka T, Shnimizu M, Moriwaki H (2012) Cancer chemoprevention by carotenoids. Molecules 17:3202–3242PubMedCrossRefGoogle Scholar
  47. Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001CrossRefGoogle Scholar
  48. Thonar C, Schnepf A, Frossard E, Roose T, Jansa J (2011) Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339:231–245CrossRefGoogle Scholar
  49. Walter MH, Floss DS, Hans J, Fester T, Strack D (2007) Apocarotenoid biosynthesis in arbuscular mycorrhizal roots: Contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation. Phytochem 68:130–138CrossRefGoogle Scholar
  50. Walter MH, Floss DS, Strack D (2010) Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232:1–17PubMedCrossRefGoogle Scholar
  51. Yang C, Hamel C, Schellenberg MP, Perez JC, Berbara RL (2010) Diversity and functionality of arbuscular mycorrhizal fungi in three plant communities in semiarid Grasslands National Park, Canada. Microb Ecol 59:724–733PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Yu Tong
    • 1
    • 2
    Email author
  • Elke Gabriel-Neumann
    • 1
    • 3
  • Benard Ngwene
    • 1
  • Angelika Krumbein
    • 1
  • Susanne Baldermann
    • 1
  • Monika Schreiner
    • 1
  • Eckhard George
    • 1
    • 2
  1. 1.Leibniz-Institute of Vegetable and Ornamental Crops Grossbeeren and Erfurt e.V.GrossbeerenGermany
  2. 2.Department of Crop SciencesHumboldt UniversityBerlinGermany
  3. 3.Department of Aridland Agriculture, Faculty of Food and AgricultureUAE UniversityAl AinUnited Arab Emirates

Personalised recommendations