Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Shedding light on response of Triticum aestivum cv. Kharchia Local roots to long-term salinity stress through transcriptome profiling

  • 68 Accesses

Abstract

Among the various abiotic stresses, salinity is one of the major limitations for production and productivity of wheat. Kharchia Local is the most salt-tolerant wheat cultivar developed from farmers’ selection on salt affected areas of India. Here, to investigate the molecular response of Kharchia Local under salinity stress, transcriptome sequencing of root tissue samples at the anthesis stage was performed. Illumina sequencing generated a total of 82.84 million clean reads and were assembled into 1,18,200 unigenes. A set of 10,805 unigenes were differentially expressed in response to salinity stress. Around 8232 unigene-derived SSRs were mined from these DEGs that can be used as functional molecular markers. Expression pattern of salinity stress-responsive unigenes was validated using real time PCR and results were found to be consistent with that of transcriptome profiling. Functional annotation of DEGs against GO, KEGG, COG and BLASTX using nr protein database was performed. This revealed the upregulation of genes involved in various biological processes including ROS homeostasis, ion transport, signal transduction, ABA biosynthesis and osmoregulation. Genes encoding expansin, xyloglucan endotransglucosylase/hydrolase, dehydrins and peroxidases that take part in enhancement of root growth were found to be upregulated under salinity. This could be the reason for better root growth of Kharchia Local under long-term salinity stress as compared to its susceptible counterpart. The present investigation provides primary information on transcriptome profiling of Kharchia Local roots under long-term salinity stress at the anthesis stage. In conclusion, the data generated in this study provide useful insights in understanding the molecular mechanism of salinity stress tolerance and will also serve as a valuable genomic reservoir for functional characterization of salinity responsive genes to develop tolerant genotypes.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Almeida DM, Oliveira MM, Saibo NJ (2017) Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genet Mol Biol 40:326–345

  2. Altunoglu YC, Baloglu P, Yer EN, Pekol S, Baloglu MC (2016) Identification and expression analysis of LEA gene family members in cucumber genome. Plant Growth Regul 80:225–241

  3. Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Plants 19:307–321

  4. Banerjee A, Roychoudhury A (2016) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17

  5. Bernstein N, Eshel A, Beeckman T (2013) Effects of salinity on root growth. In: Eshel A, Beeckman T (eds) Plant roots: the hidden half. CRC Press, Boca Raton, pp 36.1–36.18

  6. Chen Y, Ren Y, Zhang G, An J, Yang J, Wang Y, Wang W (2018) Overexpression of the wheat expansin gene TaEXPA2 improves oxidative stress tolerance in transgenic Arabidopsis plants. Plant Physiol Biochem 124:190–198

  7. Chen Y, Li C, Zhang B, Yi J, Yang Y, Kong C et al (2019) The role of the late embryogenesis-abundant (LEA) protein family in development and the abiotic stress response: a comprehensive expression analysis of potato (Solanum Tuberosum). Genes. https://doi.org/10.3390/genes10020148

  8. Das P, Majumder AL (2019) Transcriptome analysis of grapevine under salinity and identification of key genes responsible for salt tolerance. Funct Integr Genom 19:61–73

  9. Deng X, Yuan S, Cao H, Lam SM, Shui G, Hong Y, Wang X (2019) Phosphatidylinositol-hydrolyzing phospholipase C4 modulates rice response to salt and drought. Plant Cell Environ 42:536–548

  10. Ding J, Zhao L, Chang Y, Zhao W, Du Z, Hao Z (2015) Transcriptome sequencing and characterization of Japanese scallop Patinopecten yessoensis from different shell color lines. PLoS ONE 10(2):e0116406

  11. Dong W, Liu X, Li D, Gao T, Song Y (2018) Transcriptional profiling reveals that a MYB transcription factor MsMYB4 contributes to the salinity stress response of alfalfa. PLoS ONE 13(9):e0204033

  12. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:64–70

  13. Du X, Wang G, Ji J, Shi L, Guan C, Jin C (2017) Comparative transcriptome analysis of transcription factors in different maize varieties under salt stress conditions. Plant Growth Regul 81:183–195

  14. Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Hassan S, Shan D, Khan F, Ullah N, Faiq M (2015) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75:391–404

  15. Formentin E, Sudiro C, Ronci MB, Locato V, Barizza E, Stevanato P, Ijaz B, Zottini M, Gara LD, Schiavo FL (2018) H2O2 signature and innate antioxidative profile make the difference between sensitivity and tolerance to salt in rice cells. Front plant sci. https://doi.org/10.3389/fpls.2018.01549

  16. Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21

  17. Garg V, Khan AW, Kudapa H, Kale SM, Chitikineni A, Qiwei S, Sharma M, Li C, Zhang B, Xin L, Kishor PK, Varshney RK (2019) Integrated transcriptome, small RNA and degradome sequencing approaches provide insights into Ascochyta blight resistance in chickpea. Plant Biotechnol J. https://doi.org/10.1111/pbi.13026

  18. Goyal E, Singh AK, Singh RS, Mahato AK, Chand S, Kumar K (2016) Transcriptome profiling of the salt-stress response in Triticum aestivum cv. Kharchia Local. Sci Rep 6:27752

  19. Grabherr MG, Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Ido A, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma Fd, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 15:644–652

  20. Guan C, Huang YH, Cui X, Liu SJ, Zhou YZ, Zhang YW (2018) Overexpression of gene encoding the key enzyme involved in proline-biosynthesis (PuP5CS) to improve salt tolerance in switchgrass (Panicum virgatum L.). Plant Cell Rep 37:1187–1199

  21. Guo C, Yao L, You C, Wang S, Cui J, Ge X, Ma H (2016) MID1 plays an important role in response to drought stress during reproductive development. The Plant J 88:280–293

  22. He X, Zeng J, Cao F, Ahmed IM, Zhang G, Vincze E, Wu F (2015) HvEXPB7, a novel β-expansin gene revealed by the root hair transcriptome of Tibetan wild barley, improves root hair growth under drought stress. J Exp Bot 66:7405–7419

  23. He R, Zhuang Y, Cai Y, Agüero CB, Liu S, Wu J et al (2018) Overexpression of 9-cis-epoxycarotenoid dioxygenase cisgene in grapevine increases drought tolerance and results in pleiotropic effects. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00970

  24. Hoang XLT, Nhi DNH, Thu NBA, Thao NP, Tran LP (2017) Transcription factors and their roles in signal transduction in plants under abiotic stresses. Curr Genom 18:483–497

  25. Hong Y, Zhao J, Guo L, Kim SC, Deng X, Wang G, Zhang G, Li M, Wang X (2016) Plant phospholipases D and C and their diverse functions in stress responses. Prog Lipid Res 62:55–74

  26. Hu W, Yan Y, Hou X, He Y, Wei Y, Yang G, He G, Peng M (2015) TaPP2C1, a group F2 protein phosphatase 2C gene, confers resistance to salt stress in transgenic tobacco. PLoS ONE 10(6):e0129589

  27. Huang Q, Wang Y, Li B, Chang J, Chen M, Li K et al (2015) TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biol. https://doi.org/10.1186/s12870-015-0644-9

  28. Isayenkov SV (2019) Genetic sources for the development of salt tolerance in crops. Plant Growth Regul. https://doi.org/10.1007/s10725-019-00519-w

  29. Ji T, Li S, Huang M, Di Q, Wang X, Wei M, Shi Q, Li Y, Gong B, Yang F (2017) Overexpression of cucumber phospholipase D alpha gene (CsPLDα) in tobacco enhanced salinity stress tolerance by regulating Na+-K+ balance and lipid peroxidation. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00499

  30. Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105

  31. Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59:609–619

  32. Kiranmai K, Lokanadha Rao G, Pandurangaiah M, Nareshkumar A, Amaranatha Reddy V, Lokesh U, Venkatesh B, Anthony Johnson AM, Sudhakar C (2018) A novel WRKY transcription factor, MuWRKY3 (Macrotyloma uniflorum lam. Verdc.) enhances drought stress tolerance in transgenic groundnut (Arachis hypogaea L.) plants. Front Plant Sci 9:346. https://doi.org/10.3389/fpls.2018.00346

  33. Kuhl JC, Cheung F, Yuan Q, Martin W, Zewdie Y, McCallum J, Catanach A, Rutherford P, Sink KC, Jenderek M, Prince JP, Town CD, Havey MJ (2004) A unique set of 11,008 onion expressed sequence tags reveals expressed sequence and genomic differences between the monocot orders asparagales and poales. Plant Cell 16:114–125

  34. Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00751

  35. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. https://doi.org/10.1186/gb-2009-10-3-r25

  36. Leng N, Dawson JA, Thomson JA, Ruotti V, Rissman AI, Smits BM, Haag JD, Gould MN, Stewart RM, Kendziorski C (2013) EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics 29:1035–1043

  37. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. https://doi.org/10.1186/1471-2105-12-323

  38. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 1:1658–1659

  39. Li H, Gao Y, Xu H, Dai Y, Deng D, Chen J (2013) ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis. Plant Growth Regul 70:207–216

  40. Li J, Jiang MM, Ren L, Liu Y, Chen HY (2016) Identification and characterization of CBL and CIPK gene families in eggplant (Solanum melongena L.). Mol Genet Genom 291:1769–1781

  41. Li L, Wang F, Yan P, Jing W, Zhang C, Kudla J, Zhang W (2017) A phosphoinositide-specific phospholipase C pathway elicits stress-induced Ca2+ signals and confers salt tolerance to rice. New Phytol 214:1172–1187

  42. Li J, Phan TT, Li YR, Xing YX, Yang LT (2018a) Isolation, transformation and overexpression of sugarcane SoP5CS gene for drought tolerance improvement. Sugar Tech 20:464–473

  43. Li L, Li M, Qi X, Tang X, Zhou Y (2018b) De novo transcriptome sequencing and analysis of genes related to salt stress response in Glehnia littoralis. PeerJ 6:e5681

  44. Long W, Zou X, Zhang X (2015) Transcriptome analysis of canola (Brassica napus) under salt stress at the germination stage. PLoS ONE 10:e0116217

  45. Luo D, Zhou Q, Wu Y, Chai X, Liu W, Wang Y et al (2019) Full-length transcript sequencing and comparative transcriptomic analysis to evaluate the contribution of osmotic and ionic stress components towards salinity tolerance in the roots of cultivated alfalfa (Medicago sativa L). BMC Plant Biol. https://doi.org/10.1186/s12870-019-1630-4

  46. Mahajan MM, Goyal E, Singh AK, Gaikwad K, Kanika K (2017) Transcriptome dynamics provide insights into long-term salinity stress tolerance in Triticum aestivum cv. Kharchia Local. Plant Physiol Biochem 121:128–139

  47. Mansouri M, Naghavi MR, Alizadeh H, Mohammadi-Nejad G, Mousavi SA, Salekdeh GH, Tada Y (2019) Transcriptomic analysis of Aegilops tauschii during long-term salinity stress. Funct Integr Genom 19:13–28

  48. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:182–185

  49. Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218

  50. Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

  51. Nagaraju M, Kumar SA, Reddy PS, Kumar A, Rao DM, Kishor PK (2019) Genome-scale identification, classification, and tissue specific expression analysis of late embryogenesis abundant (LEA) genes under abiotic stress conditions in Sorghum bicolor L. PLoS ONE. https://doi.org/10.1371/journal.pone.0209980

  52. Patel RK, Jain M (2012) NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE. https://doi.org/10.1371/journal.pone.0030619

  53. Qadir M, Quillerou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Resour Forum. https://doi.org/10.1111/1477-8947.12054

  54. Raggi S, Ferrarini A, Delledonne M, Dunand C, Ranocha P, De Lorenzo G, Cervone F, Ferrari S (2015) The Arabidopsis class III peroxidase AtPRX71 negatively regulates growth under physiological conditions and in response to cell wall damage. Plant Physiol 169:2513–2525

  55. Rahman H, Ramanathan V, Nallathambi J, Duraialagaraja S, Muthurajan R (2016) Over-expression of a NAC67 transcription factor from finger millet (Eleusine coracana L.) confers tolerance against salinity and drought stress in rice. BMC Biotechnol. https://doi.org/10.1186/s12896-016-0261-1

  56. Razzaque S, Elias SM, Haque T, Biswas S, Jewel GN, Rahman S, Weng X, Ismail AM, Walia H, Juenger TE, Seraj ZI (2019) Gene expression analysis associated with salt stress in a reciprocally crossed rice population. Sci Rep 9(1):8249

  57. Sadak MS (2019) Physiological role of trehalose on enhancing salinity tolerance of wheat plant. Bull Nat Res Centre 43(1):53

  58. Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00571

  59. Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1046

  60. Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J 28:679–688

  61. Shinde H, Tanaka K, Dudhate A, Tsugama D, Mine Y, Kamiya T, Gupta SK, Liu S, Takano T (2018) Comparative de novo transcriptomic profiling of the salinity stress responsiveness in contrasting pearl millet lines. Environ Exp Bot 155:619–627

  62. Szepesi A, Szollosi R (2018) Plant metabolites and regulation under environmental stress. Academic Press, London

  63. Tatusov RL, Natalie DF, John DJ, Aviva RJ, Boris K, Eugene VK, Dmitri MK et al (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform. https://doi.org/10.1186/1471-2105-4-41

  64. Tuteja N (2007) Mechanism of high salinity tolerance in plants. Method Enzymol 428:419–438

  65. Wang J, Ding B, Guo Y, Li M, Chen S, Huang G, Xie X (2014) Overexpression of a wheat phospholipase D gene, TaPLDα, enhances tolerance to drought and osmotic stress in Arabidopsis thaliana. Planta 240:103–115

  66. Wang J, Li B, Meng Y, Ma X, Lai Y, Si E, Yang K, Ren P, Shang X, Wang H (2015) Transcriptomic profiling of the salt-stress response in the halophyte Halogeton glomeratus. BMC Genom. https://doi.org/10.1186/s12864-015-1373-z

  67. Wang M, Xu Z, Ding A, Kong Y (2018a) Genome-wide identification and expression profiling analysis of the xyloglucan endotransglucosylase/hydrolase gene family in tobacco (Nicotiana tabacum L.). Genes. https://doi.org/10.3390/genes9060273

  68. Wang Z, Yang Q, Shao Y, Zhang B, Feng A, Meng F, Li W (2018b) GmLEA2-1, a late embryogenesis abundant protein gene isolated from soybean (Glycine max (L.) Merr.), confers tolerance to abiotic stress. Acta Biol Hung 69:270–282

  69. Xiao JP, Zhang LL, Zhang HQ, Miao LX (2017) Identification of genes involved in the responses of Tangor (C reticulata × C sinensis) to drought stress. Biomed Res Int. https://doi.org/10.1155/2017/8068725

  70. Xie R, Pan X, Zhang J, Ma Y, He S, Zheng Y, Ma Y (2018) Effect of salt-stress on gene expression in citrus roots revealed by RNA-seq. Funct Integr Genom 18:155–173

  71. Xu P, Cai XT, Wang Y, Xing L, Chen Q, Xiang CB (2014) HDG11 upregulates cell-wall-loosening protein genes to promote root elongation in Arabidopsis. J Exp Bot 65(15):4285–4295

  72. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. https://doi.org/10.1093/nar/gkl031

  73. You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01092

  74. Yuenyong W, Chinpongpanich A, Comai L, Chadchawan S, Buaboocha T (2018) Downstream components of the calmodulin signaling pathway in the rice salt stress response revealed by transcriptome profiling and target identification. BMC Plant Biol. https://doi.org/10.1186/s12870-018-1538-4

  75. Zhang Z, Wang Y, Chang L, Zhang T, An J, Liu Y, Cao Y, Zhao X, Sha X, Hu T, Yang P (2016) MsZEP, a novel zeaxanthin epoxidase gene from alfalfa (Medicago sativa), confers drought and salt tolerance in transgenic tobacco. Plant Cell Rep 35:439–453

  76. Zhao M, Li Q, Chen Z, Lv Q, Bao F, Wang X, He Y (2018) Regulatory mechanism of ABA and ABI3 on vegetative development in the moss Physcomitrella patens. Int J Mol Sci. https://doi.org/10.3390/ijms19092728

  77. Zhu D, Hou L, Xiao P, Guo Y, Deyholos MK, Liu X (2019) VvWRKY30, a grape WRKY transcription factor, plays a positive regulatory role under salinity stress. Plant Sci 280:132–142

Download references

Acknowledgements

This work was financially supported by ICAR-National Institute for Plant Biotechnology, New Delhi, India.

Author information

MMM, KK, and KG, conceived, designed and coordinated the experiment. MMM and EG were associated with wet lab work and carried out experiment. MMM, EG and AKS involved in in silico data analysis. MMM, EG, AKS, KG and KK were involved in result interpretation and integration besides associated with finalising the manuscript. All authors have read and approved the final manuscript.

Correspondence to Kumar Kanika.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Electronic supplementary material 1—Figure S1: Enrichment of GO terms under molecular function category (JPEG 121 kb)

Electronic supplementary material 2—Figure S2: Enrichment of GO terms under biological processes category (JPEG 790 kb)

Electronic supplementary material 3—Figure S3: Enrichment of GO terms under cellular component category (JPEG 394 kb)

Electronic supplementary material 4—Figure S4: Classification of unigenes according to COG database. The most abundantclasses were R- general function prediction only followed by P- inorganic ion transport &metabolism and E- amino acid transport & metabolism (JPG 115 kb)

Electronic supplementary material 5—Figure S5: Distribution of unigenes into TF families. Out of 47 transcription factor families C2H2, WD40-like, AP2-EREBP, CCHC(Zn) and MYB-HB-like were found to be most abundant (JPG 63 kb)

Electronic supplementary material 6 (DOCX 13 kb)

Electronic supplementary material 7 (XLSX 92 kb)

Electronic supplementary material 8 (XLSX 22 kb)

Electronic supplementary material 9 (XLSX 11 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mahajan, M.M., Goyal, E., Singh, A.K. et al. Shedding light on response of Triticum aestivum cv. Kharchia Local roots to long-term salinity stress through transcriptome profiling. Plant Growth Regul 90, 369–381 (2020). https://doi.org/10.1007/s10725-019-00565-4

Download citation

Keywords

  • Kharchia local
  • Salinity
  • Transcriptome profiling
  • Wheat