Inoculation with Arbuscular mycorrhizae, Penicillium funiculosum and Fusarium oxysporum enhanced wheat growth and nutrient uptake in the saline soil
Introduction
Soil salinity limits growth and productivity of most crops including wheat due to reduced water potential and excess uptake and accumulation of Na+ and Cl− in plant cells (Munns, 2002; Elgharably, 2011). Increased uptake of salts affects the physiological and biochemical functions in the plant cells by reducing turgor, limiting photosynthesis and increasing deficiency of essential ions (Grattan and Grieve, 1999). The chemical amelioration of saline soils has been tried widely to limit the negative effects of soil salinity on plant growth. However, the biological approach can offer economic and simple means to enhance plant salt tolerance.
Plant growth-promoting bacteria and fungi have beneficial effects on plant growth under saline conditions with their antagonistic relationship with phytopathogenic microorganisms and by providing growth regulators such as auxin and gibberellins (Mokrani et al., 2020).
Arbuscular mycorrhizal fungi (AMF) have regulatory and stimulatory influences on certain solutes (e.g. sucrose, glucose, proline and glycine-betaine) that thus can play a role in osmotic adjustment (Evelin et al., 2019). AMF can also improve plant salt tolerance by enhancing uptake of nutrients, particularly of N and P (Elgharably and Nafady, 2013; Becerra et al., 2014; Nafady and Elgharably, 2018). Fileccia et al. (2017) and Pal and Pandey (2017) showed that inoculation with certain AMF species, particularly Glomus intraradices had positive effects on wheat growth under saline conditions.
Mycorrhizal-colonized plants can interact with soil microorganisms to increase the plant salt tolerance (Nanjundappa et al., 2019). Joint inoculation of AMF (Glomus intraradices or Glomus mosseae) with Pseudomonas mendocina enhanced the salt tolerance of lettuce (Kohler et al., 2009), with rhizobia (Sinorhizobium terangae) resulted in a positive osmotic adjustment of acacia saligna (Soliman et al., 2012), with Methylobacterium oryzae alleviated the salt stress on maize plants (Lee et al., 2015) and with Dietzia natronolimnaea positively influenced the growth of Ocimum basilicum plants under saline conditions (Bharti et al., 2016).
The plant growth-promoting fungi (PGPF) including Aspergillus, Fusarium, Trichoderma, Penicillium, Piriformospora, Phoma and Rhizoctonia, have the natural ability to stimulate growth-related traits of plants (Hossain et al., 2014).
Fusarium oxysporum is a soilborne fungal pathogen, but non-pathogenic isolates of Fusarium oxysporum have been reported as effective biocontrol agents, providing significant reductions in disease incidence (Larkin and Fravel, 1998). Fusarium equiseti contributed to the growth enhancement of wheat roots (Bouzouina et al., 2021) and Fusarium oxysporum increased the root length and shoot fresh and dry biomass of spinach (Islam et al., 2014) under saline conditions. They were also found secreting the plant hormones, indole-3-acetic acid (IAA) and GA, and involved in phosphate solubilization in soil and uptake by plants (Hassan, 2002; Khan et al., 2011). Under non saline conditions, Penicillium bilaii has been found to enhance P availability to wheat plants (Sánchez-Esteva et al., 2016). Several Penicillium species had significant roles with halophyte roots (You et al., 2012) and others such as Penicillium funiculosum, produced gibberellins and enhanced plant tolerance against salinity and drought stresses (Khan et al., 2011). Radhakrishnan et al. (2014) reported that Penicillium funiculosum increased the amounts of chlorophylls, proteins and amino acids in the salt-stressed sesame plants.
Despite the known benefits of the different fungi, studies examining the interactions of AMF with Fusarium oxysporum and Penicillium funiculosum under saline conditions are limited. This knowledge is important for our understanding of their combined effects on the growth of wheat and other crops for the development of economically viable management practices under saline conditions.
Wheat (Triticum aestivum L.) is the most important food plant worldwide, but its production is limited under saline conditions. In this study, we hypothesize that wheat growth is mediated by the synergistic interaction between AMF and Fusarium oxysporum and Penicillium funiculosum by (i) enhancing mycorrhizal colonization in the roots, (ii) controlling Na, Cl and nutrient acquisition and (iii) regulating proline production.
Section snippets
Soil
Sub-samples (0–30 cm depth), collected from a sandy soil near the city of Assiut, Egypt (latitude 27°11′S, longitude 31°45′E), were bulked to give a composite sample. The soil was air-dried and sieved to ~2 mm. Following standard analytical methods (Moodie et al., 1959), the textural class of soil was sandy (88% sand, 8% clay and 4% silt) with pH 7.3, ECe 3.54 dS m−1, organic matter (%) 0.7, calcium carbonate (%) 3.1, total N (%) 0.9, total P (P2O5%) 0.6, total K (K2O %) 1.1, 0.6 and available
AMF colonization
The percent root colonization was significantly (P ≤ 0.05) affected by NaCl level, AMF inoculation, the interaction between PFFO and AM and the interaction between NaCl, PFFO and AM (Table 1). AMF successfully colonized the plant roots at all levels of salinity. AM fungal colonization was not observed in plant roots that were not inoculated. Mycorrhizal colonization declined gradually with increasing NaCl concentration in the soil. Compared to AMF inoculation alone, dual inoculation with AMF
Discussion
Plant roots are generally colonized by soilborne bacteria and fungi that may induce plant adaptation to abiotic stresses. In this study, soil salinity increased shoot content of Na and Cl and reduced the grain yield and shoot biomass of wheat. It also resulted in decreases in the shoot content of N, P and K and shoot chlorophyll. The results of this study showed that the interaction of Arbuscular mycorrhizal fungi (AMF) with Penicillium funiculosum and Fusarium oxysporum (PFFO) have the
Conclusion
The results of this study confirm that NaCl stress disrupts relative leave permeability and ion balance in leaves, resulting in reduced plant growth and biomass. However, plant tolerance to salt stress is improved by Arbuscular mycorrhizae colonization of the plant roots. Our observations in this study indicate that Penicillium funiculosum and Fusarium oxysporum are involved in the plant's adaptation to stress tolerance by enhancing AMF colonization to plant roots and N and P uptake.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Science and Technology Development Fund (STDF), Cairo, Egypt, sponsored the study through the project STDF 4375 - Rehabilitation of salt affected soils in Assiut, Egypt.
References (43)
- et al.
Co-inoculation of Dietzia natronolimnaea and Glomus intraradices with vermicompost positively influences Ocimum basilicum growth and resident microbial community structure in salt affected low fertility soils
Appl. Soil Ecol.
(2016) - et al.
Growth, ion content and proline accumulation in NaCl-selected and non-selected cell lines of Lucerne cultured on sodium and potassium salts
Plant Sci.
(1997) - et al.
Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L
Plant Physiol. Biochem.
(2011) - et al.
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) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes
Metheds Enzymol
(1987)- et al.
Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity
Plant Sci.
(2001) - et al.
Simmons M, Yang XH. Contrasting responses of salinity-stressed salt-tolerant and intolerant winter wheat (Triticum aestivum L.) cultivars to ozone pollution
Plant Physiol. Biochem.
(2012) - et al.
Rapid determination of free proline for water-stress studies
Plant Soil
(1973) - et al.
Arbuscular mycorrhizal fungi in saline soils: vertical distribution at different soil depth
Braz. J. Microbiol.
(2014) - et al.
Fungal endophytes alleviate salt stress in wheat in terms of growth, ion homeostasis and osmoregulation
J. Appl. Microbiol.
(2021)
Comparing the calcium requirements of wheat and canola
J. Plant Nutr.
Effect of salt stress on antioxidant enzymes and lipid peroxidation in leaves in two contrasting corn, 'Lluteno' and 'Jubilee
Chil. J. Agric. Res.
Wheat response to combined application of nitrogen and phosphorus in a saline sandy loam soil
Soil Sci. Plant Nutr.
Effect of arbuscular mycorrhiza on growth and metal uptake of basil and mint plants in wastewater irrigated soil
Egy. J. Soil Sci.
Mitigation of salinity stress in plants by Arbuscular mycorrhizal symbiosis: current understanding and new challenges
Front. Plant Sci.
Arbuscular mycorrhizal symbiosis mitigates the negative effects of salinity on durum wheat
PloS One
Role of Arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeonpea)
J. Agron. Crop Sci.
Salinity-mineral nutrient relations in horticultural crops
Sci. Hortic. (Amst.)
Enhancing NO3- supply confers NaCl tolerance by adjusting Cl- uptake and transport in G. max & G. soja
J. Soil Sci. Plant Nutr.
Elemental composition of Arbuscular mycorrhizal fungi at high salinity
Myco
The plant growth promoting fungi Penicillium spp. GP15-1 enhances growth and confers protection against damping-off and anthracnose in the cucumber
J. Oleo Sci.
Cited by (22)
Microbial consortia of biological products: Do they have a future?
2024, Biological ControlSustainable agricultural management of saline soils in arid and semi-arid Mediterranean regions through halophytes, microbial and soil-based technologies
2023, Environmental and Experimental BotanyArbuscular mycorrhizal fungus regulates cadmium accumulation, migration, transport, and tolerance in Medicago sativa
2022, Journal of Hazardous MaterialsCitation Excerpt :Second, AMF has been reported to regulate Cd migration and chemical state change in plants by regulating the expression of divalent metal transport channels, the secretion of small molecule complexes, and metal ion antagonism (Dobrikova et al., 2021). The process involves the transcription of multiple transporters (such as ZIP (Watts-Williams and Cavagnaro, 2018), calcium channel (Kaiyuan et al., 2017), potassium channel (Elgharably and Nafady, 2021)and etc.) and secretion of organic matter (Liu et al., 2020), as well as the regulation by AMF of the migration and distribution of Cd in the tissues and cells of plants, and the expression of genes that could respond to Cd stress. A less focus on how AMF regulate Cd migration and chemical state change in plants (Liu and Tian, 2015).