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Harnessing the role of arbuscular mycorrhizae in arresting nodular senescence by modulating osmolyte synthesis and ascorbate-glutathione pool in cadmium stressed pigeon pea

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Abstract

Contamination of soil with cadmium (Cd) is a severe environmental problem, worldwide. Different arbuscular mycorrhizal fungal (AMF) species with suitable host plant combinations plays a crucial role in alleviating the impact of metal toxicity. The present study investigated the relative effects of AMF species: Claroideoglomus claroideum (M1), Claroideoglomus etunicatum (M2), Funneliformis mosseae (M3), Rhizoglomus intraradices (M4), in imparting tolerance to Cajanus cajan (L.) Millsp. - (Pigeon pea) under Cd (0, 25, 50 mg/kg) stress. The Cd had a negative impact on plant growth, nitrogen fixing efficacy, trehalose metabolism and nutrient acquisition in the nodules. The AMF supplementations improved the functional efficiency of nodules by enhancing nutrient uptake and reducing Cd absorption in plants. The mycorrhizations accelerated the synthesis of osmolytes such as trehalose (Tre), total protein (TP), total soluble sugars (TSS), total free amino acids (TFAA) and proline, responsible for maintaining the osmotic balance, otherwise disturbed in Cd-stressed pigeon pea. Furthermore, mycorrhizal inoculations upregulated the activity of enzymes involved in the ascorbate and glutathione cycle impending redox homeostasis by enhancing the ratios of ascorbate/dehydroascorbate and reduced glutathione/oxidised glutathione [ASA/DHA and GSH/GSSG]. However, among the four AMF species, M4 was the most beneficial in improving the nodulation potential and nutrient acquisition, followed by M3 and M2 (almost equally competent), with the least positive impact of M1. The differential abilities of four AMF species could be associated with their differential responsiveness to improve root biomass responsible for establishing an effective microbial symbiosis (mycorrhizal and rhizobial) and restricting metal uptake. Overall, the study suggested selecting the most efficient AMF species that provide functional complementarity to symbiosomes for inducing Cd tolerance in pigeon pea plants.

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Data Availability

The data used or analyzed during the present study are available from the corresponding author on request.

Abbreviations

AMF:

Arbuscular mycorrhizal fungi

APOX:

Ascorbate peroxidase

ARA:

Acetylene reduction assay

ASA:

Ascorbate

Cd:

Cadmium

DHA:

Dehydroascorbate

DHAR:

Dehydroascorbate reductase

GDH:

Glutamate dehydrogenase

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

HM:

Heavy metal

H2O2 :

Hydrogen peroxide

LHb:

Leghemoglobin

M1:

Claroideoglomus claroideum

M2:

Claroideoglomus etunicatum

M3:

Funneliformis mosseae

M4:

Rhizoglomus intraradices

MDHAR:

Monodehydroascorbate reductase

NaHCO3 :

Sodium bicarbonate

NN:

Nodule number

NDW:

Nodule dry weight

O2 ·- :

Superoxide anion radical

OAT:

Ornithine- δ aminotransferase

P5CS:

Δ1-pyrroline-5-carboxylate synthase

PDH:

Proline dehydrogenase

RC:

Root colonization

ROS:

Reactive oxygen species

Tre:

Trehalose

TP:

Total protein

TSS:

Total soluble sugars

TFAA:

Total free amino acids

T6PS:

Trehalose-6-phosphate synthetase

T6PP:

Trehalose-6-phosphate phosphatase

WD-XRF:

Wavelength Dispersive X-Ray Fluorescence

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Acknowledgements

We gratefully acknowledge Pulse Laboratory and TERI, New Delhi, India for providing biological material for research and SAIF (Sophisticated Analytical Instrumentation Facility), Panjab University, Chandigarh for WD-XRF study.

Funding

We are thankful to the Council of Scientific & Industrial Research (CSIR), New Delhi, India [09/135(0819)/2018-EMR-I] and the Department of Biotechnology, Government of India [BT/PR13409/BPA/118/122/2015] for providing financial support in undertaking the present research work.

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

    Aditi Bisht & Neera Garg

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  1. Aditi Bisht
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The corresponding author (NG) designed and monitored the research experiments. The first author (AB) performed the experiments under the direct supervision and involvement of the corresponding author (NG). Both authors have contributed equally to the preparation of the manuscript.

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Correspondence to Neera Garg.

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Bisht, A., Garg, N. Harnessing the role of arbuscular mycorrhizae in arresting nodular senescence by modulating osmolyte synthesis and ascorbate-glutathione pool in cadmium stressed pigeon pea. Plant Growth Regul 102, 409–427 (2024). https://doi.org/10.1007/s10725-023-01069-y

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