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Influence of indigenous arbuscular mycorrhizal fungus and bacterial bioinoculants on growth and yield of Capsicum chinense cultivated in non-sterilized soil

Published online by Cambridge University Press:  10 April 2019

K. Surendirakumar
Affiliation:
Department of Life Sciences, Manipur University, Canchipur, Imphal-795 003, Manipur, India
R. R. Pandey*
Affiliation:
Department of Life Sciences, Manipur University, Canchipur, Imphal-795 003, Manipur, India
T. Muthukumar
Affiliation:
Department of Botany, Root and Soil Biology Laboratory, Bharathiar University, Coimbatore-641 046, Tamilnadu, India
*
Author for correspondence: R. R. Pandey, E-mail: [email protected]

Abstract

Despite the global importance of Capsicum species, there is limited information on the indigenous endomycorrhizal fungal association in this crop. Therefore, the diversity and colonization patterns of arbuscular mycorrhizal fungi (AMF) in roots of Naga King chilli (Capsicum chinense) were assessed during pre-flowering, flowering and fruit ripening growth stages under a sub-tropical shifting cultivation system of North Eastern India. All the roots examined had AMF colonization and the presence of Paris-type arbuscular mycorrhizal morphology is reported for the first time in C. chinense. A total of 11 AMF spore morphotypes were isolated from both field and trap culture soils. Maximum AMF spore density and root colonization were recorded during the pre-flowering and flowering stages, respectively. The influence of Funneliformis geosporum, individually or in combination with Pseudomonas fluorescens and Azotobacter chroococcum, on growth and yield of C. chinense, was evaluated in a pot experiment using sterilized and non-sterilized soils. The application of AMF and P. fluorescens to sterilized soil significantly increased the growth, flower and fruit production, and nutrient content of C. chinense. The highest growth rates and yields of C. chinense in non-sterilized soils were achieved when AMF was combined with both P. fluorescens and A. chroococcum. The results of the current study indicate the value of applying microorganisms to improve plant growth and performance in chillies. One of the mechanisms for this could be the facilitated assimilation of nutrients promoted by AMF and bacterial bioinoculants.

Type
Crops and Soils Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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References

Aguilar-Fernández, M, Jaramillo, VJ, Varela-Fregoso, L and Gavito, ME (2009) Short-term consequences of slash-and-burn practices on the arbuscular mycorrhizal fungi of a tropical dry forest. Mycorrhiza 19, 179186.Google Scholar
Allen, SE, Grimshaw, HM, Parkinson, JA and Quarmby, C (1974) Chemical Analysis of Ecological Materials. Oxford, UK: Blackwell Scientific Publications.Google Scholar
Alori, ET, Glick, BR and Babalola, OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Frontiers in Microbiology 8, Article no. 971. 1–8. https://doi.org/10.3389/fmicb.2017.00971Google Scholar
Antoun, H (2012) Beneficial microorganisms for the sustainable use of phosphates in agriculture. Procedia Engineering 46, 6267.Google Scholar
Bagyaraj, DJ (1992) Vesicular-arbuscular mycorrhiza: application in agriculture. In Norris, JR, Read, DJ and Verma, AK (eds), Methods in Microbiology vol. 24: Techniques for the Study of Mycorrhiza. London, UK: Academic Press, pp. 359373.Google Scholar
Barea, JM and Jeffries, P (1995) Arbuscular mycorrhizas in sustainable soil plant systems. In Hock, B and Varma, A (eds), Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology. Heidelberg, Germany: Springer, pp. 521559.Google Scholar
Baum, C, El-Tohamy, W and Gruda, N (2015) Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Scientia Horticulturae 187, 131141.Google Scholar
Bhagowati, RR and Changkija, S (2009) Genetic variability and traditional practices in naga king chili landraces of Nagaland. Asian Agri-History 13, 171180.Google Scholar
Bhattarai, ID and Mishra, RR (1984) Study on the vesicular-arbuscular mycorrhiza of three cultivars of potato (Solanum tuberosum L.). Plant and Soil 79, 299303.Google Scholar
Boonlue, S, Surapat, W, Pukahuta, C, Suwanarit, P, Suwanarit, A and Morinaga, T (2012) Diversity and efficiency of arbuscular mycorrhizal fungi in soils from organic chili (Capsicum frutescens) farms. Mycoscience 53, 1016.Google Scholar
Brundrett, MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320, 3777.Google Scholar
Carballar-Hernández, S, Hernández-Cuevas, LV, Montaño, NM, Larsen, J, Ferrera-Cerrato, R, Taboada-Gaytán, OR, Montiel-González, AM and Alarcón, A (2017) Native communities of arbuscular mycorrhizal fungi associated with Capsicum annuum L. respond to soil properties and agronomic management under field conditions. Agriculture, Ecosystems and Environment 245, 4351.Google Scholar
Castillo, CF, Morales, AJ, Rubio, RI, Barea, JM and Borie, F (2013) Interactions between native arbuscular mycorrhizal fungi and phosphate solubilizing fungi and their effect to improve plant development and fruit production by Capsicum annuum L. African Journal of Microbiology Research 7, 33313340.Google Scholar
Chen, K, Liu, W, Guo, SS, Liu, R and M, L (2012) Diversity of arbuscular mycorrhizal fungi in continuous cropping soils used for pepper production. African Journal of Microbiology Research 6, 24692474.Google Scholar
Constantino, M, Gómez-Álvarez, R, Álvarez-Solís, JD, Geissen, V, Huerta, E and Barba, E (2008) Effect of inoculation with rhizobacteria and arbuscular mycorrhizal fungi on growth and yield of Capsicum chinense Jacquin. Journal of Agriculture and Rural Development in the Tropics and Subtropics 109, 169180.Google Scholar
Dai, O, Singh, RK and Nimasow, G (2011) Effect of arbuscular mycorrhizal (AM) inoculation on growth of chili plant in organic manure amended soil. African Journal of Microbiology Research 5, 50045012.Google Scholar
Daniell, TJ, Husband, R, Fitter, AH and Young, JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiology Ecology 36, 203209.Google Scholar
David, BV, Chandrasehar, G and Selvam, PN (2018) Pseudomonas fluorescens: a plant-growth-promoting rhizobacterium (PGPR) with potential role in biocontrol of pests of crops. In Prasad, R, Gill, SS and Tuteja, N (eds), Crop Improvement Through Microbial Biotechnology: New and Future Developments in Microbial Biotechnology and Bioengineering. Dordrecht, the Netherlands: Elsevier, pp. 221243.Google Scholar
Davies, FT Jr., Olalde-Portugal, V, Aguilera-Gómez, L, Alvarado, MJ, Ferrera-Cerrato, RC and Boutton, TW (2002) Alleviation of drought stress of chile ancho pepper (Capsicum annuum L. cv San Luis) with arbuscular mycorrhiza indigenous to Mexico. Scientia Horticulturae 92, 347359.Google Scholar
Davis, DJ (1962) Emission and absorption spectrochemical methods. In Peach, K and Tracey, MV (eds), Modern Methods of Plant Analysis. Heidelberg, Germany: Springer, pp. 125.Google Scholar
Dey, R, Sarkar, K, Dutta, S, Murmu, S and Mandal, N (2017) Role of Azotobacter sp. isolates as a plant growth promoting agent and their antagonistic potentiality against soil borne pathogen (Rhizoctonia solani) under in vitro condition. International Journal of Current Microbiology and Applied Sciences 6, 28302836.Google Scholar
Dickson, S (2004) The Arum-Paris continuum of mycorrhizal symbioses. New Phytologist 163, 187200.Google Scholar
Dickson, S, Smith, FA and Smith, SE (2007) Structural differences in arbuscular mycorrhizal symbioses: more than 100 years after Gallaud, where next? Mycorrhiza 17, 375393.Google Scholar
Elahi, FE, Mridha, MAU and Aminuzzaman, FM (2012) Role of AMF on plant growth, nutrient uptake, arsenic toxicity and chlorophyll content of chili grown in arsenic amended soil. Bangladesh Journal of Agricultural Research 37, 635644.Google Scholar
FAO (2010) Greening Agriculture in India: An Overview of Opportunities and Constraints. Rome, Italy: FAO. Available online from: http://www.fao.org/docrep/article/agrippa/658_en00.htm#TopOfPage (Accessed 14 February 2019).Google Scholar
Gamalero, E, Trotta, A, Massa, N, Copetta, A, Martinotti, MG and Berta, G (2004) Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and P acquisition. Mycorrhiza 14, 185192.Google Scholar
Gerdemann, JW and Nicolson, TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Transaction of the British Mycological Society 46, 235244.Google Scholar
Gosling, P, Hodge, A, Goodlass, G and Bending, GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agriculture, Ecosystems and Environment 113, 1735.Google Scholar
Hazarika, R and Neog, B (2014) Investigation of intraspecific diversity in Capsicum chinense using morphological and molecular markers. Indian Journal of Genetics and Plant Breeding 74, 392395.Google Scholar
Jackson, ML (1971) Soil Chemical Analysis. New Delhi, India: Prentice Hall.Google Scholar
Johansson, JF, Paul, LR and Finlay, RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiology Ecology 48, 113.Google Scholar
Koske, RE and Gemma, JN (1989) A modified procedure for staining roots to detect VA-mycorrhizas. Mycological Research 92, 486488.Google Scholar
Krishna, KR, Shetty, KG, Dart, PJ and Andrews, DJ (1985) Genotype dependent variation in mycorrhizal colonization and response to inoculation of pearl millet. Plant and Soil 86, 113125.Google Scholar
Li, LF, Zhang, Y and Zhao, ZW (2007) Arbuscular mycorrhizal colonization and spore density across different land-use types in a hot and arid ecosystem, Southwest China. Journal of Plant Nutrition and Soil Science 170, 419425.Google Scholar
Mathur, R, Dangi, RS, Dass, SC and Malhotra, RC (2000) The hottest chilli variety in India. Current Science 79, 287288.Google Scholar
McGonigle, TP, Miller, MH, Evans, DG, Fairchild, GL and Swan, JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115, 495501.Google Scholar
Meghvansi, MK, Siddiqui, S, Khan, MH, Gupta, VK, Vairale, MG, Gogoi, HK and Singh, L (2010) Naga chilli: a potential source of capsaicinoids with broad spectrum ethnopharmacological applications. Journal of Ethnopharmacology 132, 114.Google Scholar
Menge, JA and Timmer, LW (1982) Procedure for inoculation of plants vesicular-arbuscular mycorrhizal in laboratory, green house and field. In Schenck, NC (ed), Methods and Principles of Mycorrhizal Research. St. Paul, Minnesota, USA: American Phytopathological Society, pp. 5968.Google Scholar
Muthukumar, T and Tamilselvi, V (2010) Occurrence and morphology of endorrhizal fungi in crop species. Tropical and Sub-tropical Agroecosystems 12, 593604.Google Scholar
Muthukumar, T and Udaiyan, K (2002) Seasonality of vesicular-arbuscular mycorrhizae in sedges in a semi-arid tropical grassland. Acta Oecologica 23, 337347.Google Scholar
Newman, EI (1966) A method of estimating the total root length in a sample. Journal of Applied Ecology 3, 139145.Google Scholar
Oehl, F, Laczko, E, Bogenrieder, A, Stahr, K, Bösch, R, van der Heijden, M and Sieverding, E (2010) Soil type or land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biology and Biochemistry 42, 724738.Google Scholar
Okon, IE (2014) Growth response of okra [Abelmoschus esculentus (L.) Moench] to arbuscular mycorrhizal fungus inoculation in sterile and non-sterile soil. International Journal of Research in Humanities, Arts and Literature 2, 3138.Google Scholar
Öpik, M, Moora, M, Liira, J and Zobel, M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. Journal of Ecology 94, 778790.Google Scholar
Ortas, I (2003) Effect of selected mycorrhizal inoculation on phosphorus sustainability in sterile and non-sterile soils in the Harran Plain in South Anatolia. Journal of Plant Nutrition 26, 117.Google Scholar
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. European Journal of Soil Biology 69, 7987.Google Scholar
Pandey, RR, Chongtham, I and Muthukumar, T (2016) Influence of season and edaphic factors on endomycorrhizal fungal associations in sub-tropical plantation forest trees of north-eastern India. Flora: Morphology, Distribution, Functional Ecology of Plants 222, 112.Google Scholar
Pereira, JAP, Vieira, IJC, Freitas, MSM, Prins, CL, Martins, MA and Rodrigues, R (2016) Effects of arbuscular mycorrhizal fungi on Capsicum spp. Journal of Agricultural Science, Cambridge 154, 828849.Google Scholar
Pérez-de-Luque, A, Tille, S, Johnson, I, Pascual-Pardo, D, Ton, J and Cameron, DD (2017) The interactive effects of arbuscular mycorrhiza and plant growth-promoting rhizobacteria synergistically enhance host plant defences against pathogens. Scientific Reports 7, Article no. 16409, 1–10. doi: 10.1038/s41598-017-16697-4.Google Scholar
Porter, WM (1979) The most probable number method for enumerating infective propagules of vesicular–arbuscular mycorrhizal fungi in soil. Australian Journal of Soil Research 17, 515519.Google Scholar
Priyadharsini, P, Pandey, RR and Muthukumar, T (2012) Arbuscular mycorrhizal and dark septate fungal associations in shallot (Allium cepa L. var. aggregatum) under conventional agriculture. Acta Botanica Croatica 71, 159175.Google Scholar
Rajeshkumar, PP, Hosagoudar, VB and Gopakumar, B (2013) Mycorrhizal association of Ochlandra travancorica in Kerala, India. Journal of Threatened Taxa 5, 36733677.Google Scholar
Rouphael, Y, Franken, P, Schneider, C, Schwarz, D, Giovannetti, M, Agnolucci, M, De Pascale, S, Bonini, P and Colla, G (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Scientia Horticulturae 196, 91108.Google Scholar
Sabannavar, SJ and Lakshman, HC (2008) Interactions between Azotobacter, Pseudomonas and arbuscular mycorrhizal fungi on two varieties of Sesamum indicum L. Journal of Agronomy and Crop Science 194, 470478.Google Scholar
Sabannavar, SJ and Lakshman, HC (2011) Synergistic interactions among Azotobacter, Pseudomonas, and arbuscular mycorrhizal fungi on two varieties of Sesamum indicum L. Communications in Soil Science and Plant Analysis 42, 21222133.Google Scholar
SBI – Spices Board of India (2017) Major Itemwise Export 2016–2017. Kerala, India: Spices Board of India. Available from: http://www.indianspices.com/export/major-itemwise-export (Accessed 14 February 2019).Google Scholar
Schenck, NC and Perez, Y (1990) Manual for Identification of Vesicular Arbuscular Mycorrhizal Fungi. Gainesville, Fla, USA: University of Florida, INVAM.Google Scholar
Sehgal, JL, Sen, TK, Chamuah, GS, Singh, RS, Nayak, DC, Saxena, RK, Baruah, U and Maji, UK (1993) Soils of Manipur for Land Use Planning. Nagpur, India: National Bureau of Soil Survey and Land Use Planning.Google Scholar
Singh, SS, Tiwari, SC and Dkhar, MS (2003) Species diversity of vesicular–arbuscular mycorrhizal (VAM) fungi in jhum fallow and natural forest soils of Arunachal Pradesh, North eastern India. Tropical Ecology 44, 207215.Google Scholar
Soil Survey Staff (1999) Soil Taxonomy: A Basic System of Soil Classification for Making and Interpreting Soil Surveys, 2nd Edn. U.S. Department of Agriculture Handbook 436. Washington, D.C., USA: Natural Resources Conservation Service.Google Scholar
Smith, SE and Read, DJ (2008) Mycorrhizal Symbiosis. London, UK: Academic Press.Google Scholar
Smith, SE and Smith, FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104, 113.Google Scholar
Soleimanzadeh, H and Ghooshchi, F (2013) Response of growth and yield of maize to biofertilizers in organic and conventional cropping systems. International Journal of Agriculture and Crop Sciences 5, 797801.Google Scholar
Srivastava, P, Singh, R, Tripathi, S and Raghubanshi, AS (2016) An urgent need for sustainable thinking in agriculture – an Indian scenario. Ecological Indicators 67, 611622.Google Scholar
Tanwar, A and Aggarwal, A (2014) Multifaceted potential of bioinoculants on red bell pepper (F1 hybrid, Indam Mamatha) production. Journal of Plant Interactions 9, 8291.Google Scholar
Tanwar, A, Aggarwal, A, Kadian, N and Gupta, A (2013) Arbuscular mycorrhizal inoculation and super phosphate application influence plant growth and yield of Capsicum annuum. Journal of Soil Science and Plant Nutrition 13, 5566.Google Scholar
Thilagar, G and Bagyaraj, DJ (2015) Influence of different arbuscular mycorrhizal fungi on growth and yield of chilly. Proceedings of the National Academy of Sciences, India, Section B: Biological Sciences 85, 7175.Google Scholar
Verbruggen, E, van der Hijden, MGA, Weedon, JT, Kowalchuk, GA and Röling, WFM (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Molecular Ecology 21, 23412353.Google Scholar
Vo, AT, Magurno, F and Posta, K (2015) Evaluation of different Vietnamese soils as potential source of arbuscular mycorrhizal fungal inoculum in Capsicum frutescens. Columella: Journal of Agricultural and Environmental Sciences 2, 4958.Google Scholar
Vyas, M and Vyas, A (2012) Diversity of arbuscular mycorrhizal fungi associated with rhizosphere of Capsicum annuum in Western Rajasthan. International Journal of Plant, Animal and Environmental Sciences 2, 256262.Google Scholar
Walkley, A and Black, IA (1934) An examination of the Det Jareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 2938.Google Scholar
Wang, P, Shu, B, Wang, Y, Zhang, DJ, Liu, JF and Xia, RX (2013) Diversity of arbuscular mycorrhizal fungi in red tangerine (Citrus reticulata Blanco) root stock rhizospheric soils from hillside citrus orchards. Pedobiologia 56, 161167.Google Scholar
Wubs, AM, Ma, Y, Hemerik, L and Heuvelink, E (2009) Fruit set and yield patterns in six Capsicum cultivars. HortScience 44, 12961301.Google Scholar
Yamato, M and Iwasaki, M (2002) Morphological types of arbuscular mycorrhizal fungi in roots of understory plants in Japanese deciduous broadleaved forests. Mycorrhiza 12, 291296.Google Scholar
Zhao, D and Zhao, Z (2007) Biodiversity of arbuscular mycorrhizal fungi in the hot dry valley of the Jinsha River, southwest China. Applied Soil Ecology 37, 118128.Google Scholar