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Arbuscular mycorrhizae and silicon alleviate arsenic toxicity by enhancing soil nutrient availability, starch degradation and productivity in Cajanus cajan (L.) Millsp.

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Abstract

Arsenic (As) pollution of soil reduces the growth and reproductive potential of plants. Silicon (Si) and arbuscular mycorrhizal (AM) fungi play significant roles in alleviating adverse effects of As stress. However, studies are scant regarding alleviative effects of Si in pigeonpea (Cajanus cajan L. Millsp.) because legumes are considered low Si-accumulators. We investigated the individual as well as synergistic potential of Si with two AM species (M1-Claroideoglomus etunicatum and M2-Rhizoglomus intraradices) in modulating soil properties, thereby improving growth and productivity of pigeonpea genotype Pusa 2001 grown in AsV and AsIII challenged soils. Both As species hampered the establishment of AM symbiosis, thus, reducing nutrient uptake, growth and yield, with AsIII more toxic than AsV. Exogenously applied Si and AM species enhanced soil glomalin and phosphatases activity, hence decreased metal bioavailability in soil, increased plant nutrient acquisition, biomass and chlorophylls; with maximum benefits provided by M2, closely followed by Si and least by M1. These amendments boosted the activities of starch hydrolytic enzymes (α-, β-amylase, starch phosphorylase) in plants, along with a simultaneous increase in total soluble sugars (TSS). This enhanced sugar accumulation directly led to improved reproductive attributes, more efficiently by M2 and Si than by M1. Moreover, there was a substantial increase in proline biosynthesis due to significantly enhanced activities of its biosynthetic enzymes. Additionally, combined applications of Si and AM, especially +Si+M2, complemented each other where AM enhanced Si uptake, while Si induced mycorrhization, suggesting their mutual and beneficial roles in ameliorating metal(loid) toxicity and achieving sustainability in pigeonpea production under As stress.

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Acknowledgements

The authors gratefully acknowledge the Pulse Research Laboratory and Department of Microbiology of the Indian Agricultural Research Institute (IARI), New Delhi, India and The Energy and Research Institute (TERI), New Delhi, India, for providing the biological research material. We are sincerely thankful to the Sophisticated Analytical Instrumentation Facility (SAIF), Panjab University, Chandigarh, for technical support.

Funding

The authors are thankful to the Council of Scientific and Industrial Research (CSIR), New Delhi, India [09/135(0806)/2018-EMR-I] for providing financial assistance in undertaking the research.

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Authors and Affiliations

  1. Department of Botany, Panjab University, Chandigarh-160014, India

    Shyna Bhalla & Neera Garg

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  1. Shyna Bhalla
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  2. Neera Garg
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The corresponding author (NG) planned and designed the research experiments. The first author (SB) performed the experiments, collected the data, and analyzed it. The corresponding author (NG) monitored the experiments and gave final shape to the manuscript.

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Correspondence to Neera Garg.

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572_2021_1056_MOESM1_ESM.tif

Supplementary file1 ESM Fig. 1 Effect of silicon (Si) and two arbuscular mycorrhizal (AM) species-M1 (Claroideoglomus etunicatum) and M2 (Rhizoglomus intraradices) on a α-amylase in leaves and roots (mg maltose produced min−1 g−1 FW); b β-amylase in leaves and roots (mg maltose produced min−1 g−1 FW) and c starch phosphorylase in leaves and roots (µmol Pi liberated mg−1 protein min−1) of pigeonpea genotype Pusa 2001 under different levels of AsV (AsV20 – 20 mg kg−1 and AsV40 – 40 mg kg−1) and AsIII (AsIII4 – 4 mg kg−1 and AsIII8 – 8 mg kg−1) stress. Values represented are means of six replicates ± standard error (SE). Means followed by same letter do not differ significantly by Tukey’s HSD tests at p ≤ 0.05. Si–AM– = Si and AM absent; Si +  = Si present; M1 +  = M1 present; M2 +  = M2 present; Si + M1 +  = Si and M1 present; Si + M2 +  = Si and M2 present.(TIF 16998 KB)

572_2021_1056_MOESM2_ESM.tif

Supplementary file2 ESM Fig. 2 Effect of silicon (Si) and two arbuscular mycorrhizal (AM) species-M1 (Claroideoglomus etunicatum) and M2 (Rhizoglomus intraradices) on a starch in roots (mg g−1 FW) and b total soluble sugars (mg g−1 FW) in roots of pigeonpea genotype Pusa 2001 under different levels of AsV (AsV20 – 20 mg kg−1 and AsV40 – 40 mg kg−1) and AsIII (AsIII4 – 4 mg kg−1 and AsIII8 – 8 mg kg−1) stress. Values represented are means of six replicates ± standard error (SE). Means followed by same letter do not differ significantly by Tukey’s HSD tests at p ≤ 0.05. Si–AM– = Si and AM absent; Si +  = Si present; M1 +  = M1 present; M2 +  = M2 present; Si + M1 +  = Si and M1 present; Si + M2 +  = Si and M2 present.(TIF 17187 KB)

572_2021_1056_MOESM3_ESM.tif

Supplementary file3 ESM Fig. 3 Effect of silicon (Si) and two arbuscular mycorrhizal (AM) species-M1 (Claroideoglomus etunicatum) and M2 (Rhizoglomus intraradices) on a proline in roots (mg g−1 DW) and b proline dehydrogenase activity (ProDH; nkat mg−1 protein) in roots of pigeonpea genotype Pusa 2001 under different levels of AsV (AsV20 – 20 mg kg−1 and AsV40 – 40 mg kg−1) and AsIII (AsIII4 – 4 mg kg−1 and AsIII8 – 8 mg kg−1) stress. Values represented are means of six replicates ± standard error (SE). Means followed by same letter do not differ significantly by Tukey’s HSD tests at p ≤ 0.05. Si–AM– = Si and AM absent; Si +  = Si present; M1 +  = M1 present; M2 +  = M2 present; Si + M1 +  = Si and M1 present; Si + M2 +  = Si and M2 present.(TIF 14422 KB)

572_2021_1056_MOESM4_ESM.tif

Supplementary file4 ESM Fig. 4 Effect of silicon (Si) and two arbuscular mycorrhizal (AM) species-M1 (Claroideoglomus etunicatum) and M2 (Rhizoglomus intraradices) on a glutamate dehydrogenase activity (GDH; nkat mg−1 protein) in leaves and roots; b pyrroline-5-carboxylase synthetase activity (P5CS; nkat mg−1 protein) in leaves and roots and c ornithine aminotransferase activity (OAT; nkat mg−1 protein) in leaves and roots of pigeonpea genotype Pusa 2001 under different levels of AsV (AsV20 – 20 mg kg−1 and AsV40 – 40 mg kg−1) and AsIII (AsIII4 – 4 mg kg−1 and AsIII8 – 8 mg kg−1) stress. Values represented are means of six replicates ± standard error (SE). Means followed by same letter do not differ significantly by Tukey’s HSD tests at p ≤ 0.05. Si–AM– = Si and AM absent; Si +  = Si present; M1 +  = M1 present; M2 +  = M2 present; Si + M1 +  = Si and M1 present; Si + M2 +  = Si and M2 present.(TIF 16230 KB)

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Bhalla, S., Garg, N. Arbuscular mycorrhizae and silicon alleviate arsenic toxicity by enhancing soil nutrient availability, starch degradation and productivity in Cajanus cajan (L.) Millsp.. Mycorrhiza 31, 735–754 (2021). https://doi.org/10.1007/s00572-021-01056-z

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