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Salicylic acid improves arbuscular mycorrhizal symbiosis, and chickpea growth and yield by modulating carbohydrate metabolism under salt stress

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Abstract

Salt stress is a major abiotic stress restricting plant growth and reproductive yield. Salicylic acid (SA) and arbuscular mycorrhizal (AM) symbioses play key roles in eliminating adverse effects of salt stress by modulating ion homeostasis and carbohydrate metabolism in crop plants. Sugars synthesized via carbohydrate metabolism act as osmotic adjustors and signaling molecules in activation of various defense responses against salt stress. The present study investigated the role of SA (0.5 mM) seed priming in establishment of AM symbiosis with Rhizoglomus intraradices and the impact on growth, ion-homeostasis, nutrient uptake, and sugar metabolism in Cicer arietinum L. (chickpea) genotypes under salt stress. Salinity had a negative correlation with plant growth and AM symbiosis in both genotypes with more negative effects in relatively salt-sensitive genotype than tolerant. SA enhanced the percent root colonization by significantly increasing the number of arbuscules and vesicles under salt stress. AM symbiosis was more effective in improving root biomass, root to shoot ratio, and nutrient acquisition than SA, while SA was more effective in maintaining ion equilibrium and modulating carbohydrate metabolism and reproductive yield when compared with AM inoculation. SA priming directed the utilization of total soluble sugars (TSS) towards reproductive attributes more efficiently than did AM inoculation by activating TSS metabolic consumption. In AM plants, TSS concentrations were more directed towards sink demand by the fungus itself rather than developing reproductive structures. SA priming further increased sugar export to roots of AM plants, thus favored AM symbiosis. Hence, SA seed priming-induced improvement in AM symbiosis can be a promising strategy in achieving sustainable production of chickpea genotypes under salt stress.

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Acknowledgements

We gratefully acknowledge the Pulses Section, Department of Plant Breeding and Genetics, Punjab Agricultural University (PAU), Ludhiana, Punjab; Pulse laboratory, Department of Microbiology, (Indian Agricultural Institute (IARI), New Delhi; and The Energy and Resource Institute (TERI), New Delhi, for providing the biological research material.

Funding

We are thankful to the University Grants Commission and Department of Biotechnology, Government of India, for providing financial support in undertaking this research work.

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Authors and Affiliations

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

    Neera Garg & Amrit Bharti

Authors
  1. Neera Garg
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  2. Amrit Bharti
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Correspondence to Neera Garg.

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Electronic supplementary material

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Effect of salicylic acid (SA) and/or arbuscular mycorrhizal (AM) inoculation on A magnesium concentrations (mg g-1FW) in leaves, B magnesium concentrations (mg g-1FW) in roots and C phosphorous concentrations (mg g-1FW) in roots of Cicer arietinum L. genotypes (salt tolerant–PBG 5 and salt sensitive–BG 256) under different concentrations of salinity at 90 DAS. Values are means of 6 replicates±standard error (SE). Points topped by the same letter do not differ significantly at p ≤ 0.05 as assessed by Duncan’s multiple range test (DMRT). –SA–AM: SA unprimed non AM plants, +SA–AM: SA primed non AM plants, –SA+AM: SA unprimed AM plants, +SA+AM: SA primed AM plants (PNG 1855 kb)

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Effect of salicylic acid (SA) and/or arbuscular mycorrhizal (AM) fungi on A anthocyanin concentrations (mg g-1FW) and B phenylalanine ammonia lyase enzyme activity in (μg min-1 mg-1 protein) roots of Cicer arietinum L. genotypes (salt tolerant–PBG 5 and salt sensitive–BG 256) under different concentrations of salinity at 90 DAS. Values are means of 6 replicates±standard error (SE). Points topped by the same letter do not differ significantly at p ≤ 0.05 as assessed by Duncan’s multiple range test (DMRT). –SA–AM: SA unprimed non AM plants, +SA–AM: SA primed non AM plants, –SA+AM: SA unprimed AM plants, +SA+AM: SA primed AM plants (PNG 1508 kb)

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Effect of salicylic acid (SA) and/or arbuscular mycorrhizal (AM) fungi on A relative membrane permeability (%) B sodium ion concentrations (mg g-1DW) C K+/Na+ ratio and D Ca2+/Na+ in roots of Cicer arietinum L. genotypes (salt tolerant–PBG 5 and salt sensitive–BG 256) under different concentrations of salinity at 90 DAS. Values are means of 6 replicates±standard error (SE). Points topped by the same letter do not differ significantly at p ≤ 0.05 as assessed by Duncan’s multiple range test (DMRT). –SA–AM: SA unprimed non AM plants, +SA–AM: SA primed non AM plants, –SA+AM: SA unprimed AM plants, +SA+AM: SA primed AM plants (PNG 2560 kb)

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Effect of salicylic acid (SA) and/or arbuscular mycorrhizal (AM) fungi on A TSS concentrations (mg g-1FW) B Glucose concentrations (mg g-1FW) C Sucrose concentrations (mg g-1FW) and D Starch concentrations (mg g-1FW) in roots of Cicer arietinum L. genotypes (salt tolerant–PBG 5 and salt sensitive–BG 256) under different concentrations of salinity at 90 DAS. Values are means of 6 replicates±standard error (SE). Points topped by the same letter do not differ significantly at p ≤ 0.05 as assessed by Duncan’s multiple range test (DMRT). –SA–AM: SA unprimed non AM plants, +SA–AM: SA primed non AM plants, –SA+AM: SA unprimed AM plants, +SA+AM: SA primed AM plants (PNG 2467 kb)

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Effect of salicylic acid (SA) and/or arbuscular mycorrhizal (AM) fungi on A sucrose phosphate synthase (SPS) activity (μg sucrose produced min-1 mg-1protein) B sucrose synthase (SS) activity (μg UDPG produced min-1 mg-1protein) and C acid invertase (AI) activity (mg sucrose produced min-1 g-1FW) in roots of Cicer arietinum L. genotypes (salt tolerant–PBG 5 and salt sensitive–BG 256) under different concentrations of salinity at 90 DAS. Values are means of 6 replicates±standard error (SE). Points topped by the same letter do not differ significantly at p ≤ 0.05 as assessed by Duncan’s multiple range test (DMRT). –SA–AM: SA unprimed non AM plants, +SA–AM: SA primed non AM plants, –SA+AM: SA unprimed AM plants, +SA+AM: SA primed AM plants (PNG 1924 kb)

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Effect of salicylic acid (SA and/or arbuscular mycorrhizal (AM) fungi on A α-amylase activity (mg maltose produced min-1 g-1FW) and B β-amylase activity (mg maltose produced min-1 g-1FW) in roots of Cicer arietinum L. genotypes (salt tolerant–PBG 5 and salt sensitive–BG 256) under different concentrations of salinity at 90 DAS. Values are means of 6 replicates±standard error (SE). Points topped by the same letter do not differ significantly at p ≤ 0.05 as assessed by Duncan’s multiple range test (DMRT). –SA–AM: SA unprimed non AM plants, +SA–AM: SA primed non AM plants, –SA+AM: SA unprimed AM plants, +SA+AM: SA primed AM plants (PNG 1440 kb)

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Garg, N., Bharti, A. Salicylic acid improves arbuscular mycorrhizal symbiosis, and chickpea growth and yield by modulating carbohydrate metabolism under salt stress. Mycorrhiza 28, 727–746 (2018). https://doi.org/10.1007/s00572-018-0856-6

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