Elsevier

Rhizosphere

Volume 18, June 2021, 100345
Rhizosphere

Inoculation with Arbuscular mycorrhizae, Penicillium funiculosum and Fusarium oxysporum enhanced wheat growth and nutrient uptake in the saline soil

https://doi.org/10.1016/j.rhisph.2021.100345Get rights and content

Abstract

Soil salinity limits wheat growth, but several fungal species can promote the productivity under saline conditions. This study investigated how Arbuscular mycorrhizal fungi (AMF), and Penicillium funiculosum and Fusarium oxysporum (PFFO) affected wheat growth under saline conditions.

Wheat, inoculated with AMF, or PFFO, or with AMF and PFFO, was stressed with 75, or 150 mM NaCl in the soil. AMF colonization, grain yield, shoot and root dry weights, nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), sodium (Na), and chloride (Cl), relative permeability, chlorophyll and proline contents and root malondialdehyde (MDA) were determined.

Salinity limited the grain yield, and reduced N, P and K uptake and chlorophyll content. As soil salinity increased, shoot Na and Cl contents, relative permeability and proline content, and MDA increased. PFFO enhanced root colonization with AMF, N and P uptake and AMF significantly increased N, P and K uptake and chlorophyll content and decreased proline, Na, Cl and MDA contents. Compared to AMF, or PFFO, dual inoculation with AMF and PFFO decreased shoot Na and Cl uptake, increased chlorophyll, shoot N and P contents and K/Na ratio and resulted in approximately 25, 35 and 43% higher grain yield at 0, 75 and 150 mM NaCl, respectively.

Data showed that Penicillium funiculosum and Fusarium oxysporum promoted AMF symbiotic effects and alleviated the deleterious effects of NaCl salts on wheat growth.

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.

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