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Transcriptome skimming of lentil (Lens culinaris Medikus) cultivars with contrast reaction to salt stress

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Abstract

Extensive transcriptomic skimming was conducted to decipher molecular, morphological, physiological, and biochemical responses in salt-tolerant (PDL-1) and salt-sensitive (L-4076) cultivars under control (0 mM NaCl) and salinity stress (120 mM NaCl) conditions at seedling stage. Morphological, physiological, and biochemical studies revealed that PDL-1 exhibited no salt injury and had higher K+/Na+ ratio, relative water content (RWC), chlorophyll, glycine betaine, and soluble sugars in leaves while lower H2O2 induced fluorescence signals in roots as compared to L-4076. Transcriptomic profile revealed a total of 17,433 significant differentially expressed genes (DEGs) under different treatments and cultivar combinations that include 2557 upregulated and 1533 downregulated transcripts between contrasting cultivars under salt stress. Accuracy of transcriptomic analysis was validated through quantification of 10 DEGs via quantitative real-time polymerase chain reaction (qRT-PCR). DEGs were functionally characterized by Gene Ontology (GO) analysis and assigned to various metabolic pathways using MapMan. DEGs were found to be significantly associated with phytohormone-mediated signal transduction, cellular redox homoeostasis, secondary metabolism, nitrogen metabolism, and cellular stress signaling. The present study revealed putative molecular mechanism of salinity tolerance in lentil together with identification of 5643 simple sequence repeats (SSRs) and 176,433 single nucleotide polymorphisms (SNPs) which can be utilized to enhance linkage maps density along with detection of quantitative trait loci (QTLs) associated with traits of interests. Stress-related pathways identified in this study divulged plant functioning that can be targeted to improve salinity stress tolerance in crop species.

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Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files. Sequences were deposited in Sequence Read Archive (SRA) (BioProject Accession: PRJNA423135).

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Acknowledgments

The 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. Authors also thank Ashwani Kumar Mishra, DNA Xperts Pvt Ltd, Delhi for support in Bioinformatics data analysis.

Funding

This work has been financially supported by Department of Biotechnology, Ministry of Science and Technology (Grant No. BT/PR31301/AGIII/103/1115/2019) and ICAR-Indian Agricultural Research Institute (IARI), New Delhi (Project No. JAN 09 / 16).

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Authors and Affiliations

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

    Dharmendra Singh, Chandan Kumar Singh, Jyoti Taunk & Shristi Sharma

  2. ICAR-National Institute of Plant Biotechnology, Pusa Campus, New Delhi, 110012, India

    Kishor Gaikwad

  3. Division of Crop Improvement, Central Soil Salinity Research Institute, Karnal, 132001, India

    Vijayata Singh, Satish Kumar Sanwal & PC Sharma

  4. Depatment of Botany, Meerut College, Meerut, 250002, India

    Deepti Singh

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

    Madan Pal

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  1. Dharmendra Singh
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Contributions

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

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Correspondence to Dharmendra Singh or Madan Pal.

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Supplementary information

Supp. Fig 1

. Salinity score denoting the effect of salinity stress on tolerant and sensitive cultivars for 5, 7 and 10 d of time interval. Mean values amid same small letters (a, b, c, d) on the bar are non-significantly different by Tukey test at P ≤ 0.05 (JPG 47 kb)

Supp. Fig 2

. Morphological responses of seedling are visualized under (a) control and (b) salt stress condition. (JPG 104 kb)

Supp. Fig 3

. Bar graph representing (a) total chlorophyll content, (b) proline content, (c) soluble sugars, (d) glycine betaine, (e) relative water content, (f) membrane stability index of two cultivars, PDL-1 (tolerant) and L-4076 (sensitive) under salinity stress. Mean values amid same small letters (a, b, c, d) on the bar are non-significantly different by Tukey test at P ≤ 0.05 (JPG 76 kb)

Supp. Fig 4

. Flow chart representing work flow used for generation as well as annotation of contigs from different samples. (JPG 74 kb)

Supp. Fig 5

. De-novo assembly and annotations representing (a) total number of contigs (bp)(b) mapped reads (c) overall read mapping rates for different samples. Biological replicates are named as SL_Treated_1, SL_Treated_1_1, SL_Treated_1_2 for tolerant treated; SL_Treated_2, SL_Treated_2_1, SL_Treated_2_2 for sensitive treated; SL_control_1, SL_Control_1_1, SL_Control_1_2 for tolerant control, SL_control_1, SL_Control_2_1, SL_Control_2_2 for Sensitive control. (JPG 132 kb)

Supp. Fig 6

. Wego plot for showing percentage of genes for different GO terms for tolerant and sensitive cultivar under salt stress condition. (JPG 159 kb)

Supp. Fig 7

. Venn diagram representing total number as well as common DEGs in tolerant (1T) and sensitive (2T) cultivars under salt stress. (JPG 37 kb)

Supp. Fig 8

. Total number of SNPs and SSRs detected for different samples. Biological replicates are named as SL_Treated_1, SL_Treated_1_1, SL_Treated_1_2 for tolerant treated; SL_Treated_2, SL_Treated_2_1, SL_Treated_2_2 for sensitive treated; SL_control_1, SL_Control_1_1, SL_Control_1_2 for tolerant control, SL_control_1, SL_Control_2_1, SL_Control_2_2 for Sensitive control. (JPG 129 kb)

Supp. Table 1

Top 20 up regulated DEGs for combination: tolerant treated (T1) and sensitive treated (T2) using EdgeR. (DOCX 17 kb)

Supp. Table 2

. Top 20 down regulated DEGs for combination: tolerant treated (T1) and sensitive treated (T2) using EdgeR. (XLSX 1711 kb)

Supp. Table 3

. Heat map showing differentially expressed genes (DEGs) related to (a) Basic Leucine Zipper Domain (bZIP), Zinc finger motif, WRKY, MYB, basic helix-loop-helix (bHLH, ) transcription factors, phyto-hormones, cell wall modulators, epigenetic modulators andprotein kinases (XLSX 16 kb)

Supp. Table 4

. List of Primers used for validation of NGS data through RT-PCR. (DOCX 14 kb)

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Singh, D., Singh, C.K., Taunk, J. et al. Transcriptome skimming of lentil (Lens culinaris Medikus) cultivars with contrast reaction to salt stress. Funct Integr Genomics 21, 139–156 (2021). https://doi.org/10.1007/s10142-020-00766-5

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