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Morpho-physiological characterization coupled with expressional accord of exclusion mechanism in wild and cultivated lentil under aluminum stress

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Abstract

Aluminum stress deteriorates lentil production under acidic soils. Enhanced insight into Al tolerance traits is needed to improve its productivity. Therefore, Al-resistant (L-4602, PAL-8) and Al-sensitive (BM-4, EC-223229) cultivars along with a resistant wild (ILWL-15) were characterized for morpho-physiological traits viz. seedling root architecture (SRA), Al accumulation, and localization via fluorescent and non-fluorescent staining under control and Al-treated conditions. Also, antioxidant activities and organic acid secretion were quantified, and expressions of 10 associated genes were analyzed. Roots of Al-resistant cultivars and wild genotype showed higher root growth, antioxidant enzyme activities, and organic acid secretion than Al-sensitive ones. Among these traits, higher organic acid secretion was influenced by enhanced expression of genes, especially—aluminum sensitive-3 (ALS 3), aluminum-activated malate transporter (ALMT), multidrug and toxic compound extrusion (MATE), citrate synthase (CS), and phospho enol pyruvate carboxylase (PEPC)—which helped in reducing Al and callose accumulation. These genes were located on lentil chromosomes via sequence alignment with lentil draft genome. A strong link between morpho-physiological variation and organic acid secretion was noted which reinforced the prominence of exclusion mechanism. It was complemented by enhanced antioxidant activities at seedling stage which mitigated Al stress effects on SRA. Wild outperformed over cultivars indicating its impregnable evolution which can be exploited to better understand tolerance mechanisms. Al-resistant cultivars had significantly higher seed yield than Al-sensitive and national checks on Al-toxic fields, confirming—tolerance is sustained till reproductive stage in lentil. This study elucidated role of gene families in eliminating Al toxicity that will assist breeders to formulate strategies for developing Al-resistant cultivars.

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Abbreviations

Al:

Aluminum

PEPC:

Phosphoenolpyruvate carboxylase

CS:

Citrate synthase

ICDH:

Isocitrate dehydrogenase

MDH:

Malate dehydrogenase

MATE-a:

Multidrug and toxic compound extrusion-a

MATE-b:

Multidrug and toxic compound extrusion-b

MATE-c:

Multidrug and toxic compound extrusion-c

ALS3:

Al-sensitive3

ALMT1:

Al-activated malate transporter

VDAC:

Voltage dependent anion channel

SOD:

Superoxide dismutase

APX:

Ascorbate peroxidase

GPX:

Glutathione peroxidase

CAT:

Catalase

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Acknowledgements

Authors thank Director, Joint Director (Research), ICAR-Indian Agricultural Research Institute (IARI), New Delhi; Head, Division of Genetics and Incharge, National Phytotron Facility, IARI, New Delhi, for their support provided to accomplish the research activities.

Funding

This work has been financially supported by grant provided by ICAR-Indian Agricultural Research Institute, New Delhi (Project no- JAN 09 / 16) and DBT (No. BT/PR25565/NER/95/1254/2017) The funding bodies had no role in the design of the study, data analysis interpretation and writing the manuscript.

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Authors and Affiliations

  1. Division of Genetics, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Chandan Kumar Singh, Dharmendra Singh & Shristi Sharma

  2. Amity Institute of Biotechnology, Amity University, Noida, 201313, Uttar Pradesh, India

    Chandan Kumar Singh & Shivani Chandra

  3. Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi, 110012, India

    Jyoti Taunk & Madan Pal

  4. College of Post Graduate Studies in Agricultural Sciences, (Central Agricultural University – Imphal), Umiam, Meghalaya, 793103, India

    Noren Singh Konjengbam

  5. Depatment of Botany, Meerut College, Meerut, Uttar Pradesh, 250001, India

    Deepti Singh

  6. National Phytotron Facility, ICAR- Indian Agricultural Research Institute, New Delhi, 110012, India

    Arun Kumar

  7. INSA Senior Scientist, School of Life Sciences, Jawaharlal Nehru University, New Delhi, 110067, India

    K. C. Upadhyaya

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  1. Chandan Kumar Singh
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Contributions

Conceived and designed the experiments: DS, KCU, MP, and SC. Performed the experiments: CKS, SS and DPS. Analyzed the data: DS and CKS. Contributed reagents/materials/analysis tools: AK and MP. Wrote the paper: DS, CKS, and JT. All authors have read and approved the final manuscript.

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Correspondence to Dharmendra Singh or Madan Pal.

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Singh, C.K., Singh, D., Sharma, S. et al. Morpho-physiological characterization coupled with expressional accord of exclusion mechanism in wild and cultivated lentil under aluminum stress. Protoplasma 258, 1029–1045 (2021). https://doi.org/10.1007/s00709-021-01619-z

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