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Interaction Between Arbuscular Mycorrhizal Fungi and Bacillus Spp Nanjundappa et al. Fungal Biol Biotechnol (2019) 6:23 https://doi.org/10.1186/s40694-019-0086-5 Fungal Biology and Biotechnology REVIEW Open Access Interaction between arbuscular mycorrhizal fungi and Bacillus spp. in soil enhancing growth of crop plants Anuroopa Nanjundappa1,3, Davis Joseph Bagyaraj1* , Anil Kumar Saxena2, Murugan Kumar2 and Hillol Chakdar2 Abstract Soil microorganisms play an important role in enhancing soil fertility and plant health. Arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria form a key component of the soil microbial population. Arbuscular mycor- rhizal fungi form symbiotic association with most of the cultivated crop plants and they help plants in phosphorus nutrition and protecting them against biotic and abiotic stresses. Many species of Bacillus occurring in soil are also known to promote plant growth through phosphate solubilization, phytohormone production and protection against biotic and abiotic stresses. Synergistic interaction between AMF and Bacillus spp. in promoting plant growth compared to single inoculation with either of them has been reported. This is because of enhanced nutrient uptake, protection against plant pathogens and alleviation of abiotic stresses (water, salinity and heavy metal) through dual inoculation compared to inoculation with either AMF or Bacillus alone. Keywords: AMF, Bacillus, Interaction, Plant nutrition Introduction composition of microorganisms in the rhizosphere. A Te soil is a life supporting system rich in microorgan- recent study brought out that the plant growth strongly isms with many kinds of interactions that determines infuences the fungal alpha diversity in the rhizosphere the growth and activities of plants. Microorganisms in than bulk soil [70]. Interactions between microorganisms soil providing nutrients to plants, protecting them from in the rhizosphere infuence plant health directly by pro- biotic and abiotic stresses, and boosting their growth and viding nutrition and/or indirectly by protecting against yield is well documented [12, 25]. Rhizosphere is the nar- biotic and abiotic stresses. However, most of the studies row zone of soil around plant roots very rich in microbial on rhizosphere microorganisms focused on bacteria than activity due to the presence of root exudates with nutri- fungi [49]. Of the diferent microorganisms colonizing ents, sloughed of root cells and mucilage released by the rhizosphere arbuscular mycorrhizal fungi (AMF) are the plant root. Rhizosphere harbours 10–50 times more unique because they are partly inside the root and partly bacteria and 5–10 times more fungi compared to soil outside the root, thus infuencing other microorganisms away from the roots [60]. Interaction between microor- in the soil and also plant growth. AMF are known for ganisms in the rhizosphere has profound efects on the their evolutionary history. Plant and AMF association growth, nutrition and health of plants in agro-ecosystems has evolved over at least 500 million years which has led and in natural ecosystems [57]. Numerous studies have many to suggest that AMF could have played a major role shown specifc efects of plants on the abundance and in the colonization of land by plants [59]. Tis associa- tion is one of the most ancient symbiotic relationship in the biological world. Tis hypothesis is also supported by *Correspondence: [email protected] 1 Centre for Natural Biological Resources and Community Development, recent molecular studies done on liverworts which are 41 RBI Colony, Anand Nagar, Bangalore 560024, India the most ancient plants [61]. Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Nanjundappa et al. Fungal Biol Biotechnol (2019) 6:23 Page 2 of 10 AMF forming symbiotic association with higher plants saving 50% P fertilizer application with no adverse efect facilitate uptake of difusion-limited plant nutrients such on growth and yield of crops [40, 65]. Tese fungi also as phosphorus, zinc, copper, etc. [13]. Phosphorus which protect the plants against biotic and abiotic stresses [47, is essential for plant growth has a defned role in plant 53]. Tese fungi although not host specifc exhibit host metabolism such as cell division, development, photo- preference, thereby an efcient fungus for inoculating a synthesis, breakdown of sugar, nutrient transport within particular host can be screened and selected [9, 13]. AMF the plant, transfer of genetic characteristics from one are widely used in organic agriculture and plant nurseries generation to another and regulation of metabolic path- to improve the growth of economically important spe- ways [13]. Enhanced phosphorus uptake by mycorrhizal cies [17]. By mediating the nutritional fux between the plants is well documented. Various mechanisms have plant and many microbes in the soil, AM symbiosis con- been suggested for increased phosphorus uptake by myc- stitutes the backbone of the plant holobiont. Even though orrhizal plants like external hyphae exploring greater vol- the importance of the AM symbiosis has been well rec- ume of soil for phosphorus away from the root, efective ognized its circadian chronobiology remains almost com- phosphorus acquisition by external hyphae by produc- pletely unknown [42]. tion of phosphatases and smaller radii of absorptive sys- AMF interact with wide range of microorganisms in tem [13, 45]. Inoculation with efcient AMF enhancing the root and in the rhizosphere. AMF specifcally har- nutrition, growth and yield of crop plants is well docu- bor gene sets and metabolic machineries responsible for mented [23]. Several studies carried out under phospho- successful colonization in plant roots. Till date 321 spe- rus defcient soils have brought out that AMF help in cies of AMF belonging to 36 genera have been described the phosphorus nutrition of crop plants to the extent of (http://www.amf-phylo geny.com). Tese unique species Fig. 1 Internal Transcribed spacer (ITS) based phylogenetic analyses showing the relationship between selected free living fungi and AMF. The values at the nodes indicate bootstrap values. For phylogenetic analyses, ITS sequences were downloaded from NCBI, aligned using CLUSTAL-W option in MEGA 7 and phylogenetic tree was generated using Neighbour Joining method Nanjundappa et al. Fungal Biol Biotechnol (2019) 6:23 Page 3 of 10 are phylogenetically quite diverse and have evolved dif- spp. assist plants in its defense against pathogen attack ferently from the free living fungi. Figure 1 shows a lim- and also enhance stress tolerance by inducing the expres- ited phylogenetic analysis of selected free living fungi and sion of stress-response genes, phytohormones and stress- AMF, indicating their phylogenetic relationship. Tese related metabolites [33]. Te interactive efect of AMF fungi enhancing the number and activity of benefcial with Bacillus spp. in soil and their potential to improve soil microorganisms with consequential benefcial efect plant growth is discussed in this review. on plant growth has been reported by earlier workers [2, 32]. In recent years there has been considerable interest Synergistic interaction of AMF with Bacillus species on plant growth promoting rhizobacteria (PGPR), which in enhancing plant growth improve plant growth by providing growth promot- Most of the Bacillus species directly stimulate plant ing substances and suppressing root pathogens [29, 55]. growth either through enhancement in acquisition of Synergistic interaction between AMF and PGPR beneft- nutrients or through stimulation of host plant’s defense ting the growth of plants compared to single inoculation mechanisms prior to infection or can associate with AMF with either of them has been reported by earlier workers and enhance plant growth [3]. Co-inoculation of AMF [19, 24]. AMF and PGPR in soil and plant tissues mutu- and PGPR has been proposed as an efcient method to ally cooperate with each other in beneftting plant growth increase plant growth by many workers. Several research- through increased nutrition, hyphal permeability in plant ers have investigated the potential of AMF + Bacillus spp. roots, bacterial survival and protection against biotic association in enhancing the growth of plants (Table 1). and abiotic stresses. Impressive molecular works have Medina et al. [48] studied the efects of two Bacillus revealed a number of basic principles underlying plant– strains (Bacillus pumilus and B. licheniformis) on Med- microbe interactions like (i) signals from microbes that icago sativa plants with single or dual inoculation with are perceived by cognate plant immune receptors to ini- three AMF and compared it with P-fertilization. Te tiate defense or symbiotic responses [39], (ii) microbial efectiveness of AMF species was determined by the DNA and/or protein secretion systems that transport bacterial strain associated for most of the plant param- molecules into the host plant cell to modulate
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