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Agriculture  2013 

Enhanced Accumulation of Vitamins, Nutraceuticals and Minerals in Lettuces Associated with Arbuscular Mycorrhizal Fungi (AMF): A Question of Interest for Both Vegetables and Humans

DOI: 10.3390/agriculture3010188

Keywords: arbuscular mycorrhizal fungi, ascorbate, carbon dioxide, carotenoids, drought, Lactuca sativa, minerals, phenolics, seasonality, tocopherol

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Lettuce ( Lactuca sativa L.) is extensively grown and is the most widely used food crop for the called “Fourth Range” of vegetables. Lettuce exhibits healthy properties mainly due to the presence of antioxidant compounds (vitamins C and E, carotenoids, polyphenols) alongside significant fibre content and useful amounts of certain minerals. Lettuce can establish a mutualistic association with arbuscular mycorrhizal fungi (AMF). The establishment of the symbiosis involves a continuous cellular and molecular dialogue between both symbionts, which includes the activation of antioxidant, phenylpropanoid or carotenoid metabolic pathways. The presence of AMF colonizing roots of greenhouse-grown lettuces can induce an accumulation of secondary metabolites, vitamins and minerals in leaves that overcome the dilution effect due to the increased size of mycorrhizal plants. Therefore, AMF would allow the intake of minerals and compounds with antioxidant properties to be enhanced without increasing the consumption of lettuce in the diet. In addition, increased quantities of secondary metabolites may help lettuce plants to withstand biotic and abiotic stresses. Our review discusses the influence exerted by several environmental factors and agronomic practices on the ability of AMF for enhancing the levels of vitamins, nutraceuticals and minerals in leaves of green and red-leaf types of lettuces.


[1]  Edreva, A.; Velikova, V.; Tsonev, T.; Dagnon, S.; Gürel, A.; Akta?, L.; Gesheva, E. Stress-protective role of secondary metabolites: Diversity of functions and mechanisms. Gen. Appl. Plant Physiol. 2008, 34, 67–78.
[2]  Bennett, R.N.; Wallsgrove, R.M. Secondary metabolites in plant defence mechanisms. New Phytol. 1994, 127, 617–633, doi:10.1111/j.1469-8137.1994.tb02968.x.
[3]  Simopoulos, A.P. Redefining dietary recommendations and food safety. World Rev. Nutr. Diet. 1998, 83, 219–222, doi:10.1159/000059666.
[4]  Calvo, M.M. Lutein: A valuable ingredient of fruit and vegetables. Crit. Rev. Food Sci. 2005, 45, 671–696, doi:10.1080/10408690590957034.
[5]  Rao, A.V.; Rao, L.G. Carotenoids and human health. Pharmacol. Res. 2007, 55, 207–216, doi:10.1016/j.phrs.2007.01.012.
[6]  You, Q.; Wang, B.; Chen, F.; Huang, Z.; Wang, X.; Luo, P.G. Comparison of anthocyanins and phenolics in organically and conventionally grown blueberries in selected cultivars. Food Chem. 2011, 125, 201–208, doi:10.1016/j.foodchem.2010.08.063.
[7]  Serafini, M.; Bugianesi, R.; Salucci, M.; Azzini, E.; Raguzzini, A.; Maiani, G. Effect of acute ingestion of fresh and stored lettuce (Lactuca sativa) on plasma total antioxidant capacity and antioxidant levels in human subjects. Br. J. Nutr. 2002, 88, 615–623, doi:10.1079/BJN2002722.
[8]  Llorach, R.; Martínez-Sánchez, A.; Tomás-Barberán, F.A.; Gil, M.I.; Ferreres, F. Characterisation of polyphenols and antioxidant properties of five lettuce varieties and escarole. Food Chem. 2008, 108, 1028–1038, doi:10.1016/j.foodchem.2007.11.032.
[9]  Nicolle, C.; Cardinault, N.; Gueux, E.; Jaffrelo, L.; Rock, E. Health effect of vegetable-based diet: Lettuce consumption improves cholesterol metabolism and antioxidant status in the rat. Clin. Nutr. 2004, 23, 605–614, doi:10.1016/j.clnu.2003.10.009.
[10]  Borghi, S. Special: IV range (vegetables). Colt. Protette 2003, 32, 21–43.
[11]  Mou, B. Nutrient content of lettuce and its improvement. Curr. Nutr. Food Sci. 2009, 5, 242–248, doi:10.2174/157340109790218030.
[12]  Kader, A.A. Fresh-Cut Produce: Tracks and Trends. In Fresh-Cut Fruits and Vegetables: Science, Technology, and Market; Lamikanra, O., Ed.; CRC Press: Boca Raton, FL, USA, 2002; pp. 21–30.
[13]  Jain, A.K.; Nessler, C.L. Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol. Breed. 2000, 6, 73–78, doi:10.1023/A:1009680818138.
[14]  Yabuta, Y.; Tanaka, H.; Yoshimura, S.; Suzuki, A.; Tamoi, M.; Maruta, T.; Shigeoka, S. Improvement of vitamin E quality and quantity in tobacco and lettuce by chloroplast genetic engineering. Transgenic Res. 2012, doi:10.1007/s11248-012-9656-5.
[15]  Goto, F.; Yoshihara, T.; Saiki, H. Iron accumulation and enhanced growth in transgenic lettuce plants expressing the iron-binding protein ferritin. Theor. Appl. Genet. 2000, 100, 658–664, doi:10.1007/s001220051336.
[16]  Smith, F.A.; Smith, S.E. What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants? Plant Soil 2011, 348, 63–79, doi:10.1007/s11104-011-0865-0.
[17]  Gianinazzi, S.; Gollote, A.; Binet, M.-N.; van Tuinen, D.; Redecker, D.; Wipf, D. Agroecology: The key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 2010, 20, 519–530, doi:10.1007/s00572-010-0333-3.
[18]  Hause, B.; Mrosk, C.; Isayenkov, S.; Strack, D. Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 2007, 68, 101–110.
[19]  Walter, M.H.; Floss, D.S.; Strack, D. Apocarotenoids: Hormones, mycorrhizal metabolites and aroma volatiles. Planta 2010, 232, 1–17, doi:10.1007/s00425-010-1156-3.
[20]  Aroca, R.; Ruiz-Lozano, J.M.; Zamarre?o, A.M.; Paz, J.A.; García-Mina, J.M.; Pozo, M.J.; López-Ráez, J.A. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 2013, 170, 47–55, doi:10.1016/j.jplph.2012.08.020.
[21]  Garmendia, I.; Goicoechea, N.; Aguirreolea, J. Antioxidant metabolism in asymptomatic leaves of Verticillium-infected pepper associated with an arbuscular mycorrhizal fungus. J. Phytopathol. 2004, 152, 593–599, doi:10.1111/j.1439-0434.2004.00901.x.
[22]  Vosátka, M.; Látr, A.; Gianinazzi, S.; Albrechtová, J. Development of arbuscular mycorrhizal biotechnology and industry: Current achievements and bottlenecks. Symbiosis 2013, doi:10.1007/s13199-012-0208-9.
[23]  Fitter, A.H.; Helgason, T.; Hodge, A. Nutritional exchanges in the arbuscular mycorrhizal symbiosis: Implications for sustainable agriculture. Fungal Biol. Rev. 2011, 25, 68–72, doi:10.1016/j.fbr.2011.01.002.
[24]  Mulabagal, V.; Ngouajio, M.; Nair, A.; Zhang, Y.; Gottumukkala, A.L.; Nair, M.G. In vitro evaluation of red and green lettuce (Lactuca sativa) for functional food properties. Food Chem. 2010, 118, 300–306, doi:10.1016/j.foodchem.2009.04.119.
[25]  Afek, U.; Rinaldelli, E.; Menge, J.A.; Johnson, E.L.V.; Pond, E. Mycorrhizal species, root age, and position of mycorrhizal inoculum influence colonization of cotton, onion, and pepper Seedlings. J. Am. Soc. Hort. Sci. 1990, 115, 938–942.
[26]  Borkowska, B. Growth and photosynthetic activity of micropropagated strawberry plants inoculated with endomycorrhizal fungi (AMF) and growing under drought stress. Acta. Physiol. Plant 2002, 24, 365–370, doi:10.1007/s11738-002-0031-7.
[27]  Bolandnazar, S.A.; Neyshabouri, M.R.; Aliasgharzad, N.; Chaparzadeh, N. Effects of mycorrhizal colonization on growth parameters of onion under different irrigation and soil conditions. Pak. J. Biol. Sci. 2007, 10, 1491–1495, doi:10.3923/pjbs.2007.1491.1495.
[28]  Sohrabia, Y.; Heidaria, G.; Weisanya, W.; Ghasemi-Golezanib, K.; Mohammadic, K. Some physiological responses of chickpea cultivars to arbuscular mycorrhiza under drought stress. Russ. J. Plant Physl. 2012, 59, 708–716, doi:10.1134/S1021443712060143.
[29]  Wu, Q.S.; Zou, Y.N. Evaluating effectiveness of four inoculation methods with arbuscular mycorrhizal fungi on trifoliate orange seedlings. Int. J. Agric. Biol. 2012, 14, 266–270.
[30]  Selvaraj, T.; Nisha, M.C.; Rajeshkumar, S. Effect of indigenous arbuscular mycorrhizal fungi on some growth parameters and phytochemical constituents of Pogostemon patchouli Pellet. Maejo. Int. J. Sci. Technol. 2009, 3, 222–234.
[31]  Baslam, M.; Garmendia, I.; Goicoechea, N. Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse grown lettuce. J. Agric. Food Chem. 2011, 59, 5504–5515.
[32]  Baslam, M.; Esteban, R.; García-Plazaola, J.I.; Goicoechea, N. Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces. Appl. Microbiol. Biotechnol. 2012, doi:10.1007/s00253-012-4526-x.
[33]  Baslam, M.; Pascual, I.; Sánchez-Díaz, M.; Erro, J.; García-Mina, J.M.; Goicoechea, N. Improvement of nutritional quality of greenhouse-grown lettuce by arbuscular mycorrhizal fungi is conditioned by the source of phosphorus nutrition. J. Agric. Food Chem. 2011, 59, 11129–11140.
[34]  Baslam, M.; Goicoechea, N. Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiza 2012, 22, 347–359, doi:10.1007/s00572-011-0408-9.
[35]  Demming-Adams, B.; Adams, W.W., III. Chlorophyll and carotenoid composition in leaves of Euonymus kiautschovicus acclimated to different degrees of light stress in the field. Aust. J. Plant Physiol. 1996, 23, 649–659, doi:10.1071/PP9960649.
[36]  Cazzonelli, D.I. Carotenoids in nature: Insights from plants and beyond. Funct. Plant Biol. 2011, 38, 833–847, doi:10.1071/FP11192.
[37]  Cazzonelli, C.I.; Pogson, B.J. Source to sink: Regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 2010, 15, 266–274, doi:10.1016/j.tplants.2010.02.003.
[38]  Sommer, A.; Davidson, F.R. Assessment and control of vitamin A deficiency: The Annecy Accords. J. Nutr. 2002, 132, 2845S–2850S.
[39]  Tapiero, H.; Townsend, D.M.; Tew, K.D. The role of carotenoids in the prevention of human pathologies. Biomed. Pharmacother. 2004, 58, 100–110, doi:10.1016/j.biopha.2003.12.006.
[40]  Voutilainen, S.; Nurmi, T.; Mursu, J.; Rissanen, T. Carotenoids and cardiovascular health. Am. J. Clin. Nutr. 2006, 83, 1265–1271.
[41]  Paiva, S.A.R.; Russell, R.M. β-Carotene and other carotenoids as antioxidants. J. Am. Coll. Nutr. 1999, 18, 426–433.
[42]  Strack, D.; Fester, T. Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol. 2006, 172, 22–34, doi:10.1111/j.1469-8137.2006.01837.x.
[43]  Walter, M.H.; Floss, D.S.; Hans, J.; Fester, T.; Strack, D. Apocarotenoid biosynthesis in arbuscular mycorrhizal roots: Contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation. Phytochemistry 2007, 68, 130–138.
[44]  Ulrichs, C.; Fischer, G.; Büttner, C.; Mewis, I. Comparison of lycopene, β-carotene and phenolic contents of tomato using conventional and ecological horticultural practices, and arbuscular mycorrhizal fungi (AMF). Agron. Colomb. 2008, 26, 40–46.
[45]  Mena-Violante, H.G.; Ocampo-Jiménez, O.; Dendooven, L.; Martínez-Soto, G.; González-Casta?eda, J.; Davies, F.T., Jr.; Olalde-Portugal, V. Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 2006, 16, 261–267, doi:10.1007/s00572-006-0043-z.
[46]  Giovannetti, M.; Avio, L.; Barale, R.; Ceccarelli, N.; Cristofani, R.; Lezzi, A.; Mignolli, F.; Picciarelli, P.; Pinto, B.; Reali, D.; et al. Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. Brit. J. Nutr. 2012, 107, 242–251, doi:10.1017/S000711451100290X.
[47]  Kainulainen, P.; Utriainen, J.; Holopainen, J.K.; Oksanen, J.; Holopainen, T. Influence of elevated ozone and limited nitrogen availability on conifer seedlings in an open-air fumigation system: Effects on growth, nutrient content, mycorrhiza, needle ultrastructure, starch and secondary compouds. Glob. Change Biol. 2000, 6, 335–344, doi:10.1046/j.1365-2486.2000.00313.x.
[48]  Valladares, F.; García Plazaola, J.I.; Morales, F.; Niinemets, U. Photosynthetic Responses to Radiation. In Terrestrial Photosynthesis in a Changing Environment. A Molecular, Physiological, and Ecological Approach; Flexas, J., Loreto, F., Medrano, H., Eds.; Cambridge University Press: Cambridge, UK, 2012; pp. 239–256.
[49]  Ma, L.; Lin, X.M. Effects of lutein and zeaxanthin on aspects of eye health. J. Sci. Food Agric. 2010, 90, 2–12, doi:10.1002/jsfa.3785.
[50]  Caldwell, C.R.; Britz, S.J. Effect of supplemental ultraviolet radiation on the carotenoid and chlorophyll composition of green house-grown leaf lettuce (Lactuca sativa L.) cultivars. J. Food Compos. Anal. 2006, 19, 637–644, doi:10.1016/j.jfca.2005.12.016.
[51]  Baslam, M.; Garmendia, I.; Goicoechea, N. Elevated CO2 may impair the beneficial effect of arbuscular mycorrhizal fungi (AMF) on the mineral and phytochemical quality of lettuce. Ann. Appl. Biol. 2012, 161, 180–191, doi:10.1111/j.1744-7348.2012.00563.x.
[52]  Bravo, L. Polyphenols: Chemistry, dietary sources, metabolism, and nutritional significance. Nutr. Rev. 1998, 11, 317–333.
[53]  Lattanzio, V.; Lattanzio, V.M.T.; Cardinali, A. Role of Phenolics in the Resistance Mechanisms of Plants against Fungal Pathogens and Insects. In Phytochemistry: Advances in Research; Imperato, F., Ed.; Research Signpost: Kerala, India, 2006; pp. 23–67.
[54]  Cai, Y.; Luo, Q.; Sun, M.; Corke, H. Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci. 2004, 74, 2157–2184, doi:10.1016/j.lfs.2003.09.047.
[55]  Fu, L.; Xu, B.T.; Xu, X.R.; Gan, R.Y.; Zhang, Y.; Xia, E.Q.; Li, H.B. Antioxidant capacities and total phenolic contents of 62 fruits. Food Chem. 2011, 129, 345–350, doi:10.1016/j.foodchem.2011.04.079.
[56]  Francisco, A.; Tomás-Barberán, F.A.; Juan, C.E. Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. J. Sci. Food Agric. 2001, 81, 853–876, doi:10.1002/jsfa.885.
[57]  Ganz, T.R.; Kailis, S.G.; Abbott, L.K. Mycorrhizal colonization and its effect on growth phosphorus uptake and tissue phenolic content in the European olive (Olea europaea L.). Adv. Hortic. Sci. 2002, 16, 109–116.
[58]  Toussaint, J.P.; Smith, F.A.; Smith, S.E. Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 2007, 17, 291–297, doi:10.1007/s00572-006-0104-3.
[59]  Lee, J.M.; Scagel, C.F. Chicoric acid found in basil (Ocimum basilicum L.) leaves. Food Chem. 2009, 115, 650–656, doi:10.1016/j.foodchem.2008.12.075.
[60]  Castellanos-Morales, V.; Villegas, J.; Wendelin, S.; Vierheilig, H.; Eder, R.; Cárdenas-Navarro, R. Root colonisation by the arbuscular mycorrhizal fungus Glomus intraradices alters the quality of strawberry fruits (Fragaria ananassa Duch.) at different nitrogen levels. J. Sci. Food Agric. 2010, 90, 1774–1782.
[61]  Cavagnaro, T.R.; Gleadow, R.M.; Miller, R.E. Plant nutrient acquisition and utilization in a high carbon dioxide world. Funct. Plant Biol. 2011, 38, 87–96, doi:10.1071/FP10124.
[62]  Mandal, S.M.; Chakraborty, D.; Dey, S. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal. Behav. 2010, 5, 359–368, doi:10.4161/psb.5.4.10871.
[63]  Janagath, I.B.; Crozier, A. Dietary Flavonoids and Phenolic Compounds. In Plant Phenolics and Human Health. Biochemistry, Nutrition, and Pharmacology; Fraga, C.G., Ed.; Wiley & Sons, Inc.: Hoboken, NJ, USA, 2010; pp. 1–50.
[64]  Chalker-Scott, L. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 1999, 70, 1–9, doi:10.1111/j.1751-1097.1999.tb01944.x.
[65]  Stintzing, F.C.; Carle, R. Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends Food Sci. Technol. 2004, 15, 19–38, doi:10.1016/j.tifs.2003.07.004.
[66]  Ross, J.A.; Kasum, C.M. Dietary flavonoids: Bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 2002, 22, 19–34, doi:10.1146/annurev.nutr.22.111401.144957.
[67]  Poulton, J.L.; Koide, R.T.; Stephenson, A.G. Effects of mycorrhizal infection and soil phosphorus availability on in vitro and in vivo pollen performance in Lycopersicon esculentum (Solanaceae). Am. J. Bot. 2001, 88, 1786–1793, doi:10.2307/3558354.
[68]  Smirnoff, N.; Wheeler, G.L. Ascorbic acid in plants: Biosynthesis and function. CRC Crit. Rev. Biochem. Mol. Biol. 2000, 35, 291–314, doi:10.1080/10409230008984166.
[69]  Arrigoni, O.; de Tullio, M.C. The role of ascorbic acid in cell metabolism: Between gene-directed functions and unpredictable chemical reactions. J. Plant Physiol. 2000, 157, 481–488, doi:10.1016/S0176-1617(00)80102-9.
[70]  Smirnoff, N. Ascorbate biosynthesis and function in photoprotection. Philos. Trans. R. Soc. Lond. BBiol. Sci. 2000, 355, 1455–1464, doi:10.1098/rstb.2000.0706.
[71]  Davey, M.W.; van Montagu, M.; Inzé, D.; Sanmartin, M.; Kanellis, A.; Smirnoff, N.; Benzie, I.J.J.; Strain, J.J.; Favell, D.; Fletcher, J. Plant l-ascorbic acid: Chemistry, function, metabolism, bioavailability and effects of processing. J. Sci. Food Agric. 2000, 80, 825–860, doi:10.1002/(SICI)1097-0010(20000515)80:7<825::AID-JSFA598>3.0.CO;2-6.
[72]  Lee, S.K.; Kader, A.A. Preharvest and postharvest factors influencing vitamin C content of horticultural crops. Postharvest Biol. Technol. 2000, 20, 207–220, doi:10.1016/S0925-5214(00)00133-2.
[73]  Marshall, J.R. Prevention of colorectal cancer: Diet, chemoprevention and lifestyle. Gastroenterol. Clin. N 2008, 37, 73–82, doi:10.1016/j.gtc.2007.12.008.
[74]  Davidson, P.G.; Touger-Decker, R. Chemopreventive role of fruits and vegetables in oropharyngeal cancer. Nutr. Clin. Pract. 2009, 24, 250–260, doi:10.1177/0884533609332088.
[75]  Qiang-Sheng, W.; Ren-Xue, X.; Ying-Ning, Z. Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J. Plant Physiol. 2006, 163, 1101–1110, doi:10.1016/j.jplph.2005.09.001.
[76]  Oh, M.-M.; Trick, H.N.; Rajashekar, C.B. Secondary metabolism and antioxidants are involved in environmental adaptation and stress tolerance in lettuce. J. Plant Physiol. 2009, 166, 180–191, doi:10.1016/j.jplph.2008.04.015.
[77]  Potters, G.; Horemans, N.; Jansen, M.A.K. The cellular redox state in plant stress biology—A charging concept. Plant Physiol. Bioch. 2010, 48, 292–300, doi:10.1016/j.plaphy.2009.12.007.
[78]  Kohler, J.; Hernández, J.A.; Caravaca, F.; Roldán, A. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 2009, 65, 245–252, doi:10.1016/j.envexpbot.2008.09.008.
[79]  Falk, J.; Munné-Bosch, S. Tocochromanol functions in plants: Antioxidation and beyond. J. Exp. Bot. 2010, 61, 1549–1566, doi:10.1093/jxb/erq030.
[80]  Bramley, P.M.; Elmadfa, I.; Kafatos, A.; Kelly, F.J.; Manios, Y.; Roxborough, H.E.; Schuch, W.; Sheehy, P.J.A.; Wagner, K.H. Review: Vitamin E. J. Sci. Food Agric. 2000, 80, 913–938, doi:10.1002/(SICI)1097-0010(20000515)80:7<913::AID-JSFA600>3.0.CO;2-3.
[81]  Clarke, M.W.; Burnett, J.R.; Croft, K.D. Vitamin E in human health and disease. Crit. Rev. Clin. Lab. Sci. 2008, 45, 417–450, doi:10.1080/10408360802118625.
[82]  Lira, F.S.; Rosa, J.C.; Cunha, C.A.; Ribeiro, E.B.; Oller do Nascimento, C.; Oyama, L.M.; Mota, J.F. Supplementing alpha-tocopherol (vitamin E) and vitamin D3 in high fat diet decrease IL-6 production in murine epididymal adipose tissue and 3T3-L1 adipocytes following LPS stimulation. Lipids Health Dis. 2011, 10, 37, doi:10.1186/1476-511X-10-37.
[83]  Lizarazo, K.; Fernández-Marín, B.; Becerril, J.M.; García-Plazaola, J.I. Ageing and irradiance enhance vitamin E content in green edible tissues from crop plants. J. Sci. Food Agric. 2010, 90, 1994–1999.
[84]  Garmendia, I.; Goicoechea, N.; Aguirreolea, J. Effectiveness of three Glomus species in protecting pepper (Capsicum annuum L.) against verticillium wilt. Biol. Control 2004, 31, 296–305, doi:10.1016/j.biocontrol.2004.04.015.
[85]  Martínez-Ballesta, M.C.; Dominguez-Perles, R.; Moreno, D.A.; Muries, B.; Alcaraz-López, C.; Bastías, E.; García-Viguera, C.; Carvajal, M. Minerals in plant food: Effect of agricultural practices and role in human health. Agron. Sustain. Dev. 2010, 30, 295–309, doi:10.1051/agro/2009022.
[86]  Welch, R.M.; Graham, R.D. Breeding for micronutrients in staple food crops from a human nutrition perspective. J. Exp. Bot. 2004, 55, 353–364, doi:10.1093/jxb/erh064.
[87]  Graham, R.D.; Welch, R.M.; Bouis, H.E. Addressing micronutrient malnutrition through enhancing the nutritional quality of staple foods: Principles, perspectives and knowledge gaps. Adv. Agronom. 2001, 70, 77–142, doi:10.1016/S0065-2113(01)70004-1.
[88]  ACC/SCN (Administrative Committee on Coordination, Subcommitee on Nutrition); International Food Policy Research Institute. Fourth Report on the World Nutrition Situation: United Nations, 2000.
[89]  Brown, K.H.; Wuehler, S.E. Zinc and Human Health: The Results of Recent Trials and Implications for Programmed Interventions and Research; The Micronutrient Initiative/International Development Research Centre: Ottawa, Canada, 2000.
[90]  Copper Development Association. Copper in Human Health. Available online: http://www.copperinfo.co.uk/health/ (accessed on 5 November 2012).
[91]  Clark, R.B.; Zeto, S.K. Mineral acquisition by arbuscular mycorrhizal plants. J. Plant Nutr. 2000, 23, 867–902, doi:10.1080/01904160009382068.
[92]  Kothari, S.K.; Marschner, H.; R?mheld, V. Contribution of VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant Soil 1991, 131, 177–185, doi:10.1007/BF00009447.
[93]  Li, X.L.; Marschner, H.; George, E. Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant Soil 1991, 136, 49–57, doi:10.1007/BF02465219.
[94]  Azcón, R.; Ambrosano, E.; Charest, C. Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci. 2003, 165, 1137–1145, doi:10.1016/S0168-9452(03)00322-4.
[95]  Goicoechea, N.; Antolín, M.C.; Sánchez-Díaz, M. Influence of arbuscular mycorrhizae and Rhizobium on nutrient content and water relations in drought stressed alfalfa. Plant Soil 1997, 192, 261–268, doi:10.1023/A:1004216225159.
[96]  Augé, R.M. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 2001, 11, 3–42, doi:10.1007/s005720100097.
[97]  Zuccarini, P. Mycorrhizal infection ameliorates chlorophyll content and nutrient uptake of lettuce exposed to saline irrigation. Plant Soil Environ. 2007, 53, 283–289.
[98]  Loladze, I. Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends Ecol. Evol. 2002, 17, 457–461, doi:10.1016/S0169-5347(02)02587-9.
[99]  Jifon, J.L.; Graham, J.H.; Drouillard, D.L.; Syvertsen, J.P. Growth depression of mycorrhizal Citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2. New Phytol. 2002, 153, 133–142, doi:10.1046/j.0028-646X.2001.00294.x.
[100]  Treseder, K.K.; Allen, M.F. Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol. 2000, 147, 189–200, doi:10.1046/j.1469-8137.2000.00690.x.


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