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Molecular Genetics and Genomics

, Volume 294, Issue 6, pp 1441–1453 | Cite as

Transcriptome sequencing and functional analysis of Sedum lineare Thunb. upon salt stress

  • Yingjin Song
  • Xiaopei Yang
  • Shaohui Yang
  • Jiehua WangEmail author
Original Article

Abstract

Soil salinization is one major constraint to plant geographical distribution, yield, and quality, and as an ideal plant for the “greening” of flat-roofed buildings, Sedum lineare Thunb. has strong tolerance against a variety of environmental adversities including salinity with the underlying mechanism still remaining unknown. In this study, we performed de novo transcriptome sequencing on leaf and root samples of NaCl-treated S. lineare Thunb. and identified 584 differentially expressed genes (DEGs), which were further annotated by gene function classification and pathway assignments using the public data repositories. In addition to the increased gene expression level verified by qRT-PCR, the elevated activities of the corresponding enzymes were also demonstrated for peroxidase (POD), glutathione peroxidases (GPX), and cysteine synthase (CSase) in the NaCl-treated roots. Furthermore, two highly inducible genes without known functions related to salt tolerance were selected to be overexpressed and tested for their effects on salt tolerance in the model plant, Arabidopsis thaliana. Upon 150 mM NaCl treatment, 35S:SlCXE but not 35S:SlCYP72A transgenic Arabidopsis seedlings exhibited improved salt resistance as shown by the increased seed germination rates and longer primary roots of transgenic seedlings when compared to wild-type plants. Taken together, this work laid a foundation for a better understanding of the salt adaptation mechanism of S. lineare Thunb. and genes identified could serve as useful resources for the development of more salt-tolerant varieties of other species through genetic engineering.

Keywords

Salt stress Sedum lineare Thunb. Transcriptome Enzymatic activities Transgenic Arabidopsis 

Notes

Acknowledgements

There is no financial support for this work.

Author contributions

In this work, all authors conceived and designed the experiments. XY performed the experiments and analyzed the data. JW and XY wrote the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

438_2019_1587_MOESM1_ESM.docx (1.4 mb)
Supplementary material 1 (DOCX 1390 kb)

References

  1. Agra HE, Klein T, Vasl A, Shalom H, Kadas G, Blaustein L (2017) Sedum-dominated green-roofs in a semi-arid region increase CO2 concentrations during the dry season. Sci Total Environ 584–585:1147–1151PubMedGoogle Scholar
  2. Chandran D (2015) Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance. IUBMB Life 67:461–471PubMedGoogle Scholar
  3. Chen LQ (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155PubMedGoogle Scholar
  4. Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281PubMedPubMedCentralGoogle Scholar
  5. Cheng P, Gao J, Feng Y, Zhang Z, Liu Y, Fang W, Chen S, Chen F, Jiang J (2018) The chrysanthemum leaf and root transcript profiling in response to salinity stress. Gene 674:161–169PubMedGoogle Scholar
  6. Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, longdistance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111:6497–6502PubMedGoogle Scholar
  7. Chunthaburee S, Dongsansuk A, Sanitchon J, Pattanagul W, Theerakulpisut P (2016) Physiological and biochemical parameters for evaluation and clustering of rice cultivars differing in salt tolerance at seedling stage. Saudi J Biol Sci 23:467–477PubMedGoogle Scholar
  8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedPubMedCentralGoogle Scholar
  9. Duan L, Sebastian J, Dinneny JR (2015) Salt-stress regulation of root system growth and architecture in Arabidopsis seedlings. Methods Mol Biol 1242:105–122PubMedGoogle Scholar
  10. Flowers TJ, Colmer TD (2010) Salinity tolerance in halophytes. New Phytol 179:945–963Google Scholar
  11. Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, Klessig DF, Tong L (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102(5):1773–1778PubMedGoogle Scholar
  12. Galvan-Ampudia CS, Julkowska MM, Darwish E, Gandullo J, Korver RA, Brunoud G, Haring MA, Munnik T, Vernoux T, Testerink C (2013) Halotropism is a response of plant roots to avoid a saline environment. Curr Biol 23(20):2044–2050PubMedGoogle Scholar
  13. Gershater MC, Sharples K, Edwards R (2006) Carboxylesterase activities toward pesticide esters in crops and weeds. Phytochemistry 67:2561–2567PubMedGoogle Scholar
  14. Gershater MC, Cummins I, Edwards R (2007) Role of a carboxylesterase in herbicide bioactivation in Arabidopsis thaliana. J Biol Chem 282:21460–21466PubMedGoogle Scholar
  15. Ghosh S (2017) Triterpene structural diversification by plant cytochrome P450 enzymes. Front Plant Sci 8:1886PubMedPubMedCentralGoogle Scholar
  16. Hosseinpour B, Sepahvand S, Aliabad KK, Bakhtiarizadeh M, Imani A, Assareh R, Salami SA (2018) Transcriptome profiling of fully open flowers in a frost-tolerant almond genotype in response to freezing stress. Mol Genet Genomics 293:151–163PubMedGoogle Scholar
  17. Julkowska MM, Hoefsloot HCJ, Mol S, Feron R, de Boer GJ, Haring MA, Testerink C (2014) Capturing Arabidopsis root architecture dynamics with ROOT-FIT reveals diversity in responses to salinity. Plant Physiol 166:1387–1402PubMedPubMedCentralGoogle Scholar
  18. Julkowska MM, Koevoets IT, Mol S, Hoefsloot H, Feron R, Tester MA, Keurentjes JJB, Korte A, Haring MA, de Boer GJ, Testerink C (2017) Genetic components of root architecture remodeling in response to salt stress. Plant Cell 29:3198–3213PubMedPubMedCentralGoogle Scholar
  19. Kaleem F, Shabir G, Aslam K, Rasul S, Manzoor H, Shah SM, Khan AR (2018) An overview of the genetics of plant response to salt stress: present status and the way forward. Appl Biochem Biotech 186:1–29Google Scholar
  20. Krishnamurthy P, Mohanty B, Wijaya E, Lee DY, Lim TM, Lin Q, Xu J, Loh CS, Kumar PP (2017) Transcriptomics analysis of salt stress tolerance in the roots of the mangrove Avicennia officinalis. Sci Rep 7:10031PubMedPubMedCentralGoogle Scholar
  21. Le Guan MSH, Nadeem Khan, Maazullah Nasim, Songtao Jiu, Muhammad Fiaz, Xudong Zhu, Kekun Zhang and Jinggui Fang (2018) Transcriptome sequence analysis elaborates a complex defensive mechanism of grapevine (Vitis vinifera L.) in response to salt stress. Int J Mol Sci 19:E4019.  https://doi.org/10.3390/ijms19124019 PubMedCentralGoogle Scholar
  22. Li H, Gao Y, Dai Y, Deng D, Chen J (2013) ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis. Plant Growth Regul 70:207–216Google Scholar
  23. Mansour MMF, Ali EF (2017) Glycinebetaine in saline conditions: an assessment of the current state of knowledge. Acta Physiol Plant 39:56Google Scholar
  24. Munns R (2010) Approaches to identifying genes for salinity tolerance and the importance of timescale. Methods Mol Biol 639:25–38PubMedGoogle Scholar
  25. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681Google Scholar
  26. Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342PubMedGoogle Scholar
  27. Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760PubMedPubMedCentralGoogle Scholar
  28. Ricardo M, Ricardo S (2017) Soil salinity: effect on vegetable crop growth Management practices to prevent and mitigate soil salinization. Horticulturae 13:30Google Scholar
  29. Robbins NE, Trontin C, Duan L, Dinneny JR (2014) Beyond the barrier: communication in the root through the endodermis. Plant Physiol 166:551–559PubMedPubMedCentralGoogle Scholar
  30. Robinson MD, Mccarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140Google Scholar
  31. Shan Q, Liu X, Zhang J, Chen G, Liu S, Zhang P, Ying W (2011) Analysis on the tolerance of four ecotype plants against copper stress in soil. Procedia Environ Sci 10:1802–1810Google Scholar
  32. Shi W, Liu D, Hao L, Wu CA, Guo X, Li H (2014) GhWRKY39, a member of the WRKY transcription factor family in cotton, has a positive role in disease resistance and salt stress tolerance. Plant Cell Tiss Org 118:17–32Google Scholar
  33. Shigeto J, Tsutsumi Y (2016) Diverse functions and reactions of class III peroxidases. New Phytol 209:1395–1402Google Scholar
  34. Storey JD, Tibshirani R (2003) Statistical significance for genome wide studies. Proc Nat Acad Sci USA 100:9440–9445PubMedGoogle Scholar
  35. Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Method Enzymol 428:419–438Google Scholar
  36. Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86PubMedPubMedCentralGoogle Scholar
  37. Vyrides I, Stuckey DC (2017) Compatible solute addition to biological systems treating waste/wastewater to counteract osmotic and other environmental stresses: a review. Crit Rev Biotechnol 37:865–879PubMedGoogle Scholar
  38. Warrilow AGS, Hawkesford MJ (1998) Separation, subcellular location and influence of sulphur nutrition on isoforms of cysteine synthase in spinach. J Exp Bot 49:1625–1636Google Scholar
  39. Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32:667–685PubMedGoogle Scholar
  40. Yang Q, Shohag MJI, Feng Y, He Z, Yang X (2017) Transcriptome comparison reveals the adaptive evolution of two contrasting ecotypes of Zn/Cd hyperaccumulator Sedum alfredii Hance. Front Plant Sci 8:425PubMedPubMedCentralGoogle Scholar
  41. Yao J, Guo H, Chaiprasongsuk M, Zhao N, Chen F, Yang X, Guo H (2015) Substrate-assisted catalysis in the reaction catalyzed by salicylic acid binding protein 2 (SABP2), a potential mechanism of substrate discrimination for some promiscuous enzymes. Biochemistry 54(34):5366–5375PubMedGoogle Scholar
  42. You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Front Plant Sci 6:1092PubMedPubMedCentralGoogle Scholar
  43. Zagorchev L, Seal CE, Kranner I, Odjakova M (2012) Redox state of low-molecular-weight thiols and disulphides during somatic embryogenesis of salt-treated suspension cultures of Dactylis glomerata L. Free Radic Res 46:656–664PubMedGoogle Scholar
  44. Zhai CZ, Zhao L, Yin LJ, Chen M, Wang QY, Li LC, Xu ZS, Ma YZ (2013) Two wheat glutathione peroxidase genes whose products are located in chloroplasts improve salt and H2O2 tolerances in Arabidopsis. PLoS One 8:e73989.  https://doi.org/10.1371/journal.pone.0073989 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Zhang JL, Shi HZ (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115:1–22PubMedGoogle Scholar
  46. Zhao N, Lin H, Lan S, Jia Q, Chen X, Guo H, Chen F (2016) VvMJE1 of the grapevine (Vitis vinifera) VvMES methylesterase family encodes for methyl jasmonate esterase and has a role in stress response. Plant Physiol Biochem 102:125–132PubMedGoogle Scholar
  47. Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273Google Scholar
  48. Zhu JY, Shi X, Lu H, Xia B, Li Y, Li X, Zhang Q, Yang G (2016) RNA-seq transcriptome analysis of extensor digitorum longus and soleus muscles in large white pigs. Mol Genet Genom 291(2):687–701Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yingjin Song
    • 1
  • Xiaopei Yang
    • 1
  • Shaohui Yang
    • 1
  • Jiehua Wang
    • 1
    Email author
  1. 1.School of Environmental Science and EngineeringTianjin UniversityTianjinChina

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