Influence of Different Encapsulation Types of Arbuscular Mycorrhizal Fungi on Physiological Adaptation and Growth Promotion of Maize (Zea mays L.) Subjected to Water Deficit


  • Suravoot YOOYONGWECH Mahidol University, Kanchanaburi Campus, School of Interdisciplinary Studies, Kanchanaburi 71150 (TH)
  • Suriyan CHA-UM National Science and Technology Development Agency (NSTDA), National Center for Genetic Engineering and Biotechnology (BIOTEC), Pathum Thani 12120 (TH)
  • Rujira TISARUM National Science and Technology Development Agency (NSTDA), National Center for Genetic Engineering and Biotechnology (BIOTEC), Pathum Thani 12120 (TH)
  • Cattarin THERAWITAYA National Science and Technology Development Agency (NSTDA), National Center for Genetic Engineering and Biotechnology (BIOTEC), Pathum Thani 12120 (TH)
  • Thapanee SAMPHUMPHUNG National Science and Technology Development Agency (NSTDA), National Center for Genetic Engineering and Biotechnology (BIOTEC), Pathum Thani 12120 (TH)
  • Supatida AUMTONG Maejo University, Faculty of Agricultural Production, Chiang Mai 50290 (TH)
  • Jeerun KINGKAEW Mahidol University, Kanchanaburi Campus, School of Interdisciplinary Studies, Kanchanaburi 71150 (TH)
  • Muenduen PHISALAPHONG Chulalongkorn University, Faculty of Engineering, Department of Chemical Engineering, Bangkok 10330 (TH)



arbuscular mycorrhiza, encapsulation, maize, organic fertilizer, water deficit


Under drought environment, arbuscular mycorrhizal fungi (AMF) can serve as a long-term biofertilizer to sustain the water and nutrient availability for the host plants. A study was conducted to check the effect of AMF and the encapsulations of the AMF and an organic fertilizer (Fer) with alginate (Al-FA) and agar-agar (Ag-FA) on maize (Zea mays L.) in response to water deficit conditions. The maximum quantum efficiency of PS II (Fv/Fm) of the maize inoculated with Al-FA and Ag-FA under the water deficit was recorded to be 0.70 and 0.50, respectively. Shoot and root water content of the Al-FA plants were found to be maintained under the water deficit and were better than Ag-FA. Besides, phosphorus content in the root tissues of the Al-FA plants grown under the water deficit stress was 1.56-folds greater than in the Ag-FA plants, thereby promoting the photosynthetic abilities and plant height in the former case. The study indicated that the Al-FA type of encapsulation may perform better than the Ag-FA in case of maize plants, leading to its better development under water limited conditions.


Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005). Microbial cooperation in rhizosphere. Journal of Experimental Botany 56:1761-1778.

Bates LS, Waldren RP, Teare ID (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39:205-207.

Borriello R, Lumini E, Girlanda M, Bonfante P, Bianciotto V (2012). Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biology and Fertility Soil 48:911-922.

Brundrett MC, Bougher N, Dell B, Grove T, Malajczuk N (1996). Working with mycorrhizas in forestry and agriculture (ACIAR Monograph 32). Australian Centre for International Agricultural Research, Canberra.

Coleto I, Pineda M, Rodiño AP, De Ron AM, Alamillo JM (2014). Comparison of inhibition of N2 fixation and ureide accumulation under water deficit in four common bean genotypes of contrasting drought tolerance. Annals of Botany 113:1071-1082.

Daryanto S, Wang L, Jacinthe PA (2017). Global synthesis of drought effects on cereal, legume, tuber and root crops production: A review. Agricultural Water Management 179:18-33.

de Jaeger N, de la Providencia IE, Rouhier H, Declerck S (2011). Co-entrapment of Trichoderma harzianum and Glomus sp. within alginate beads: Impact on the arbuscular mycorrhizal fungi life cycle. Journal of Applied Microbiology 111:125-135.

Derelle D, Declerck S, Genet P, Dajoz I, van Aarle IM (2012). Association of highly and weakly mycorrhizal seedlings can promote the extra- and intra-radical development of a common mycorrhizal network. FEMS Microbiology Ecology 79:251-259.

Fan HM, Wang XW, Sun X, Li YY, Sun XZ, Zheng CS (2014). Effects of humic acid derived from sediments on growth, photosynthesis and chloroplast ultrastructure in chrysanthemum. Scientia Horticulturae 177:118-123.

Gauthier PPG, Crous KY, Ayub G, Duan H, Weerashinghe LK, Ellsworth DS, … Atkin OK (2014). Drought increase heat tolerance of leaf respiration in Eucalyptus globulus saplings grown under both ambient and elevated atmospheric [CO2] and temperature. Journal of Experimental Botany 65:6471-6485.

Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012). Role of proline under changing environments. Plant Signaling & Behavior 7:1456-1466.

Herrmann L, Lesueur D (2013). Challenges of formulation and quality of biofertilizers for successful inoculation. Applied Microbiology and Biotechnology 97:8859-8873.

Hodge A, Helgason T, Fitter AH (2010). Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecology 3:267-273.

Jackson ML (1958). Soil Chemical Analysis. Prentice Hall, Englewood Cliffs, New Jersey.

Jinyou D, Xiaoyang C, Wei L, Qiong G (2004). Osmoregulation mechanism of drought stress and genetic engineering strategies for improving drought resistance in plants. Forest Studies in China 6:56-62.

John RP, Tyagi RD, Brar SK, Surampalli RY, Prévost D (2011).Bio-encapsulation of microbial cells for targeted agricultural delivery. Critical Reviews in Biotechnology 31:211-226.

Kreuzwieser J, Gessler A (2010). Global climate change and tree nutrition: Influence of water availability. Tree Physiology 30:1221-1234.

Lanfermeijer FC, Koerselman-Kooij JW, Borstlap AC (1991). Osmosensitivity of sucrose uptake by immature pea cotyledons disappears during development. Plant Physiology 95:832-838.

Liu T, Li Z, Hui C, Tang M, Zhang H (2016). Effect of Rhizophagus irregularis on osmotic adjustment, antioxidation and aquaporin PIP genes expression of Populus × canadensis ‘Neva’ under drought stress. Acta Physiologiae Plantarum 38:191.

Mena-Violante HG, Ocampo-Jiménez O, Dendooven L, Martínez-Soto G, González-Castañeda J, Davies, FT Jr, 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 16:261-267.

Mirshad PP, Puthur JT (2016). Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass (Saccharum arundinaceum Retz.). Environmental Monitoring and Assessment 188:425.

Mo Y, Wang Y, Yang R, Zheng J, Liu C, Li H, Ma J, Zhang Y, Wei C, Zhang X (2016). Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Frontiers in Plant Science 7:644.

Neumann E, Schmid B, Römheld V, George E (2009). Extraradical development and contribution to plant performance of an arbuscular mycorrhizal symbiosis exposed to complete or partial root zone drying. Mycorrhiza 20:13-23.

Park HJ, Floss DS, Levesque-Tremblay V, Bravo A, Harrison MJ (2015). Hyphal branching during arbuscule development requires reduced arbuscular mycorrhiza. Plant Physiology 169:2774-2788.

Plenchette C, Strullu DG (2003). Long-term viability and infectivity of intraradical forms of Glomus intraradices vesicles encapsulated in alginate beads. Mycological Research 107:614-616.

Porcel R, Ruiz-Lozano JM (2004). Arbuscular mycorrhizal in?uence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of Experimental Botany 55:1743-1750.

Rampino P, Pataleo S, Gerardi C, Mita G, Perrotta C (2006). Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant, Cell & Environment 29:2143-2152.

Ren B, Wang M, Chen Y, Sun G, Li Y, Shen Q, Guo S (2015). Water absorption is affected by the nitrogen supply to rice plants. Plant and Soil 396:397-410.

Rentel MC, Knight MR (2004). Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiology 135:1471-1479.

Rigano MM, Arena C, Di Matteo A, Sellitto S, Frusciante L, Barone A (2016). Eco-physiological response to water stress of drought-tolerant and drought-sensitive tomato genotypes. Plant Biosystems 150:682-691.

Rigou L, Mignard E, Plassard C, Arvieu JC, Remy JC (1995). Influence of ectomycorrhizal infection on the rhizosphere pH around roots of maritime pine (Pinus pinaster Soland in Ait.). New Phytologist 130:141-147.

Ruiz-Lozano JM (2003). Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13:309-317.

Sajedi NA, Ardakani MR, Rejali F, Mohabbati F, Miransari M (2010).Yield and yield components of hybrid corn (Zea mays L.) as affected by mycorrhizal symbiosis and zinc sulfate under drought stress. Physiology and Molecular Biology of Plants 16:343-351.

Shabala SN, Shabala SI, Martynenko AI, Babourina O, Newman IA (1998). Salinity effect on bioelectric activity growth, Na+ accumulation and chlorophyll fluorescence of maize leaves: a comparative survey and prospects for screening. Australian Journal of Plant Physiology 25:609-616.

Sharma MP, Reddy UG, Adholeya A (2011). Response of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) grown conventionally and on beds in a sandy loam soil. Indian Journal of Microbiology 51(3):384-389.

Shao HB, Song WY, Chu LY (2008). Advances of calcium signals involved in plant anti-drought. Comptes Rendus Biologies331:587-596.

Smith SE, Read DJ (2008). Mycorrhizal symbiosis (3rd ed). Academic Press, Amsterdam; Boston.

Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014). Abiotic and biotic stress combinations. New Phytologist 203:32-43.

Toljander JF, Santos-González JC, Tehler A, Finlay RD (2008). Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a longterm fertilization trial. FEMS Microbiology Ecology 65:323-338.

Tuteja N, Mahajan S (2007). Calcium signalling network in plants: An overview. Plant Signaling & Behavior 2:79-85.

Vassilev N, Vassileva M, Azcon R, Medina A (2001). Interactions of an arbuscular mycorrhizal fungus with free or co-encapsulated cells of Rhizobium trifoli and Yarowia lipolytica inoculated into a soil-plant system. Biotechnology Letters 23:149-151.

Vassilev N, Vassileva M, Lopez A, Martos V, Reyes A, Maksimovic I, Eichler-Löbermann B, Malusà E (2015). Unexploited potential of some biotechnological techniques for biofertilizer production and formulation. Applied Microbiology and Biotechnology 99:4983-4996.

Vemmer M, Patel AV (2013). Review of encapsulation methods suitable for microbial biological agents. Biological Control 67:380-389.

Wheeler T, von Braun J (2013). Climate change impacts on global food security. Science 341:508-513.

Xu C, Li X, Zhang L (2013). The effect of calcium chloride on growth, photosynthesis, and antioxidant responses of Zoysia japonica under drought conditions. PLoS One 8:e68214.

Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-um S (2016). Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Scientia Horticulturae 198:107-117.

Zou YN, Srivastava AK, Ni QD, Wu QS (2015). Disruption of mycorrhizal extraradical mycelium and changes in leaf water status and soil aggregate stability in root box-grown trifoliate orange. Frontiers in Microbiology 6:203.




How to Cite

YOOYONGWECH, S., CHA-UM, S., TISARUM, R., THERAWITAYA, C., SAMPHUMPHUNG, T., AUMTONG, S., KINGKAEW, J., & PHISALAPHONG, M. (2018). Influence of Different Encapsulation Types of Arbuscular Mycorrhizal Fungi on Physiological Adaptation and Growth Promotion of Maize (Zea mays L.) Subjected to Water Deficit. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 47(1), 213–220.



Research Articles
DOI: 10.15835/nbha47111249

Most read articles by the same author(s)