Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T08:40:22.006Z Has data issue: false hasContentIssue false
  • English
  • Français

Transcriptome analysis of a Triticum aestivum landrace (Roshan) in response to salt stress conditions

Published online by Cambridge University Press:  26 May 2021

Jamshid Azimian ,
Eslam Majidi Hervan ,
Amin Azadi Open the ORCID record for Amin Azadi [Opens in a new window] ,
Mohammad Reza Bakhtiarizadeh  and
Reza Azizinezhad
Jamshid Azimian
Affiliation:
Department of Plant Breeding and Biotechnology, Science and Research Branch, Islamic Azad University, Tehran, Iran
Eslam Majidi Hervan
Affiliation:
Department of Plant Breeding and Biotechnology, Science and Research Branch, Islamic Azad University, Tehran, Iran
Amin Azadi*
Affiliation:
Department of Plant Breeding, Yadegar-e-Imam Khomeini (RAH) Shahre Rey Branch, Islamic Azad University, Tehran, Iran
Mohammad Reza Bakhtiarizadeh
Affiliation:
Department of Animal and Poultry Science, College of Aburaihan, University of Tehran, Tehran, Iran
Reza Azizinezhad
Affiliation:
Department of Plant Breeding and Biotechnology, Science and Research Branch, Islamic Azad University, Tehran, Iran
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In order to better understand the molecular mechanisms associated with salinity tolerance, transcriptome analysis of a local salt-tolerant wheat landrace (i.e. Roshan) was performed under salt stress. Transcriptome sequencing yielded 137,508,542 clean reads using the Illumina HiSeq 2000 platform. The results of two alignment programs, i.e. STAR and HISAT2, were used separately to perform the analysis of differentially expressed genes (DEGs) using DESeq2. Finally, a total of 17,897 DEGs were identified by DESeq2. Moreover, gene ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses identified 108 GO terms and 62 significant KEGG pathways, of which ‘metabolic process’ and ‘metabolic pathways’ were the most abundant enriched term and pathway, respectively. Additionally, key salinity-tolerant genes, including asparagine synthetase, were also identified in the present study. Out of 87 identified families of transcription factors, GAI‐RGA ‐ and ‐SCR (GRAS) was one of the most important, which participates in signal transduction, and meristem maintenance and development. Eventually, to validate the gene expression levels, six DEGs were selected for a quantitative real-time polymerase chain reaction, and the results were in line with those of RNA-Seq. The findings of the current study can guide future genetic and molecular studies and allow a better understanding and improvement of salt tolerance in wheat.

Keywords

Illumina HiSeq 2000NGS (next-generation sequencing)RNA-Seqsalinity stresstranscriptome
Type
Research Article
Information
Plant Genetic Resources , Volume 19 , Issue 3 , June 2021 , pp. 261 - 274
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of NIAB

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Afzal, Z, Howton, T, Sun, Y and Mukhtar, MS (2016) The roles of aquaporins in plant stress responses. Journal of Developmental Biology 4: 9.CrossRefGoogle ScholarPubMed
Al-Whaibi M, H (2011) Plant heat-shock proteins: a mini-review. Journal of King Saud University - Science 23: 139–150.CrossRefGoogle Scholar
Amirbakhtiar, N, Ismaili, A, Ghaffari, MR, Nazarian Firouzabadi, F and Shobbar, ZS (2019) Transcriptome response of roots to salt stress in a salinity-tolerant bread wheat cultivar. PLoS ONE 14: e0213305.CrossRefGoogle Scholar
Anders, S, Pyl, PT and Huber, W (2015) HTSeq – a Python framework to work with high-throughput sequencing data. Bioinformatics (Oxford, England) 31: 166–169.CrossRefGoogle ScholarPubMed
Andrews, S (2017) FastQC: A quality control tool for high throughput sequence data. http://www.Bioinformatics.Babraham.Ac.Uk/Projects/Fastqc 1.Google Scholar
Ashraf, M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora - Morphology, Distribution, Functional Ecology of Plants 199: 361–376.CrossRefGoogle Scholar
Aung, K, Hu, J (2012) Differential roles of Arabidopsis Dynamin-Related Proteins DRP3A, DRP3B, and DRP5B in Organelle Division. Journal of Integrative Plant Biology 54: 921–931. doi:10.1111/j.1744-7909.2012.01174.xGoogle ScholarPubMed
Bahieldin, A, Atef, A, Sabir, JSM, Gadalla, NO, Edris, S, Alzohairy, AM, Radhwan, NA, Baeshen, MN, Ramadan, AM, Eissa, HF, Hassan, SM, Baeshen, NA, Abuzinadah, O, Al-Kordy, MA, El-Domyati, FM and Jansen, RK (2015) RNA-Seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress. Comptes Rendus Biologies 338: 285–297.CrossRefGoogle ScholarPubMed
Bailey, PC, Martin, C, Toledo-Ortiz, G, Quail, PH, Huq, E, Heim, MA, Jakoby, M, Werber, M and Weisshaar, B (2003) Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell 15: 2497–2502.CrossRefGoogle ScholarPubMed
Belda-Palazón, B, Adamo, M, Valerio, C, Ferreira, LJ, Confraria, A, Reis-Barata, D, Rodrigues, A, Meyer, C, Rodriguez, PL and Baena-González, E (2020) A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nature Plants 6: 1345–1353. https://doi.org/10.1038/s41477-020-00778-w.CrossRefGoogle ScholarPubMed
Bi, H, Li, F, Wang, H and Ai, X (2018) Overexpression of transketolase gene promotes chilling tolerance by increasing the activities of photosynthetic enzymes, alleviating oxidative damage and stabilizing cell structure in Cucumis sativus L. Physiologia Plantarum 167: 502–515. doi: 10.1111/ppl.12903.CrossRefGoogle Scholar
Bolger, AM, Lohse, M and Usadel, B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England) 30: 2114–2120.CrossRefGoogle ScholarPubMed
Bolle, C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218: 683–692.CrossRefGoogle ScholarPubMed
Büyük, İ, İlhan, E, Şener, D, Özsoy, AU and Aras, S (2019) Genome-wide identification of CAMTA gene family members in Phaseolus vulgaris L. and their expression profiling during salt stress. Molecular Biology Reports 46: 2721–2732. https://doi.org/10.1007/s11033-019-04716-8.CrossRefGoogle ScholarPubMed
Çelik, Ö, Meriç, S, Ayan, A and Atak, Ç (2019) Epigenetic analysis of WRKY transcription factor genes in salt stressed rice (Oryza sativa L.) plants. Environmental and Experimental Botany 159: 121–131.CrossRefGoogle Scholar
Chaichi, M, Sanjarian, F, Razavi, K and Gonzalez-Hernandez, JL (2019) Analysis of transcriptional responses in root tissue of bread wheat landrace (Triticum aestivum L.) reveals drought avoidance mechanisms under water scarcity. PLoS ONE 14: 0212671.CrossRefGoogle ScholarPubMed
Chakradhar, T, Reddy, RA and Chandrasekhar, T (2019) Protein kinases and phosphatases in stress transduction: role in crop improvement. In: Khan, MIR, Reddy, PS, Ferrante, A and Khan, NA (eds.) Plant Signaling Molecules: Chapter 34. Sawston, Cambridge, UK: Woodhead Publishing, pp. 533–547.CrossRefGoogle Scholar
Chen, L, Song, Y, Li, S, Zhang, L, Zou, C and Yu, D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1819: 120–128.CrossRefGoogle ScholarPubMed
Chen, Y, Zhu, P, Wu, S, Lu, Y, Sun, J, Cao, Q, Li, Z and Xu, T (2019) Identification and expression analysis of GRAS transcription factors in the wild relative of sweet potato Ipomoea trifida. BMC Genomics 20: 911.CrossRefGoogle ScholarPubMed
Cho, S, Garvin, DF and Muehlbauer, GJ (2006) Transcriptome analysis and physical mapping of barley genes in wheat–barley chromosome addition lines. Genetics 172: 1277–1285.CrossRefGoogle ScholarPubMed
Chono, M, Matsunaka, H, Seki, M, Fujita, M, Kiribuchi-Otobe, C, Oda, S, Kojima, H and Nakamura, S (2015) Molecular and genealogical analysis of grain dormancy in Japanese wheat varieties, with specific focus on Mother of FT and TFL1 on chromosome 3A. Breeding Science 65: 103–109.CrossRefGoogle ScholarPubMed
Christensen, H (1964) Free Amino Acids and Peptides in Tissues. https://doi.org/10.1016/B978-1-4832-3209-6.50011-6CrossRefGoogle Scholar
Crepin, N and Rolland, F (2019) SnRK1 activation, signaling, and networking for energy homeostasis. Current Opinion in Plant Biology 51: 29–36.CrossRefGoogle ScholarPubMed
Cui, LL, Ys, L, Li, Y, Yang, C and Peng, XX (2016) Overexpression of glycolate oxidase confers improved photosynthesis under high light and high temperature in rice. Frontiers in Plant Science 7: 1165.CrossRefGoogle ScholarPubMed
Da Fonseca, RR, Albrechtsen, A, Themudo, GE, Ramos-Madrigal, J, Sibbesen, JA, Maretty, L, Zepeda-Mendoza, ML, Campos, PF, Heller, R and Pereira, RJ (2016) Next-generation biology: sequencing and data analysis approaches for non-model organisms. Marine Genomics 30: 3–13.CrossRefGoogle ScholarPubMed
Dehdari, A, Rezai, A and Maibody, SAM (2005) Salt tolerance of seedling and adult bread wheat plants based on ion contents and agronomic traits. Communications in Soil Science and Plant Analysis 36: 2239–2253.CrossRefGoogle Scholar
Dinh, TT, Girke, T, Liu, X, Yant, L, Schmid, M and Chen, X (2012) The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development (Cambridge, England) 139: 1978–1986.CrossRefGoogle ScholarPubMed
Dobin, A, Davis, CA, Schlesinger, F, Drenkow, J, Zaleski, C, Jha, S, Batut, P, Chaisson, M and Gingeras, TR (2012) STAR: ultrafast universal RNA-seq aligner. Bioinformatics (Oxford, England) 29: 15–21.CrossRefGoogle ScholarPubMed
Du, J, Yap, K, Chan, LY, Rehm, FBH, Looi, FY, Poth, AG, Gilding, EK, Kaas, Q, Durek, T and Craik, DJ (2020) A bifunctional asparaginyl endopeptidase efficiently catalyzes both cleavage and cyclization of cyclic trypsin inhibitors. Nature Communications 11: 1575.CrossRefGoogle ScholarPubMed
Dubos, C, Stracke, R, Grotewold, E, Weisshaar, B, Martin, C and Lepiniec, L (2010) MYB transcription factors in Arabidopsis. Trends in Plant Science 15: 573–581.CrossRefGoogle ScholarPubMed
EL Mahi, H, Hormaeche, JP, Luca, AD, Villalta, I, Espartero, J, Arjona, FG, Fernandez, JL, Bundo, M, Mendoza, I, Mieulet, D, Lalanne, E, Lee, SY, Yun, DJ, Guiderdoni, E, Aguilar, M, Leidi, E, Pardo, JM and Quintero, FJ (2019) A critical role of sodium flux via the plasma membrane Na + /H + 7 exchanger SOS1 in the salt tolerance of rice. Plant Physiology 180: 1046–1065. DOI: https://doi.org/10.1104/pp.19.00324CrossRefGoogle Scholar
FAO (2019) Salt-affected soils. http://www.fao.org/3/ca7123en/CA7123EN.pdfGoogle Scholar
Feng, CZ, Chen, Y, Wang, C, Kong, YH, Wu, WH and Chen, YF (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. The Plant Journal 80: 654–668.CrossRefGoogle ScholarPubMed
Finkler, A, Ashery-Padan, R and Fromm, H (2007) CAMTAs: calmodulin-binding transcription activators from plants to human. FEBS Letters 581: 3893–3898.CrossRefGoogle ScholarPubMed
Ge, Y, Li, Y, Zhu, YM, Bai, X, Lv, DK, Guo, D, Ji, W and Cai, H (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biology 10: 153.CrossRefGoogle ScholarPubMed
Goldfarb, M (2020) Identification and characterization of three putative beta-alanine aminotransferases in Arabidopsis thaliana. Honors Theses 253. https://digital.kenyon.edu/honorstheses/253.Google Scholar
Goyal, E, Amit, SK, Singh, RS, Mahato, AK, Chand, S and Kanika, K (2016) Transcriptome profiling of the salt stress response in Triticum aestivum cv. Kharchia Local. Scientific Reports 6: 27752. https://doi.org/10.1038/srep27752CrossRefGoogle ScholarPubMed
Grattan, S (2002) Irrigation Water Salinity and Crop Production. Oakland, CA: UCANR Publications.CrossRefGoogle Scholar
Guimarães, PM, Brasileiro, ACM, Morgante, CV, Martins, ACQ, Pappas, G, Silva, OB Jr, Togawa, R, Leal-Bertioli, SCM, Araujo, ACG, Moretzsohn, MC and Bertioli, DJ (2012) Global transcriptome analysis of two wild relatives of peanut under drought and fungi infection. BMC Genomics 13: 387.CrossRefGoogle ScholarPubMed
Guo, Y, Zhao, S, Sheng, Q, Guo, M, Lehmann, B, Pietenpol, J, Samuels, DC and Shyr, Y (2015) RNASeq by total RNA library identifies additional RNAs compared to poly(A) RNA library. BioMed Research International 2015: 862130, 9 pages. https://doi.org/10.1155/2015/862130CrossRefGoogle ScholarPubMed
Han, H, Wang, Q, Wei, L, Liang, Y, Dai, J, Xia, G and Liu, S (2018) Small RNA and degradome sequencing used to elucidate the basis of tolerance to salinity and alkalinity in wheat. BMC Plant Biology 18: 195.CrossRefGoogle ScholarPubMed
Hirsch, S and Oldroyd, GED (2009) GRAS-domain transcription factors that regulate plant development. Plant Signaling & Behavior 4: 698–700.CrossRefGoogle ScholarPubMed
Hogland, D and Arnon, D (1950) The water- culture method for growing plants without soil. Circular. California Agricultural Experiment Station 1950 Vol.347 No.2nd edit pp.32 pp.Google Scholar
Hu, CW, Chang, YL, Chen, SJ, Kuo-Huang, LL, Liao, JC, Huang, HC and Juan, HF (2011) Revealing the functions of the transketolase enzyme isoforms in Rhodopseudomonas palustris using a systems biology approach. PLoS ONE 6: e28329.CrossRefGoogle ScholarPubMed
Inada, N (2017) Plant actin depolymerizing factor: actin microfilament disassembly and more. Journal of Plant Research 130: 227–238.CrossRefGoogle ScholarPubMed
Jackson, MA, Gilding, EK, Shafee, T, Harris, KS, Kaas, Q, Poon, S, Yap, K, Jia, H, Guarino, R, Chan, LY, Durek, T, Anderson, MA and Craik, DJ (2018) Molecular basis for the production of cyclic peptides by plant asparaginyl endopeptidases. Nature Communications 9: 2411.CrossRefGoogle ScholarPubMed
Jin, J, Tian, F, Yang, DC, Meng, YQ, Kong, L, Luo, J and Gao, G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Research 45: D1040–D1045.CrossRefGoogle Scholar
Kanehisa, M and Goto, S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28: 27–30.CrossRefGoogle ScholarPubMed
Kato, Y and Sakamoto, W (2018) FtsH protease in the thylakoid membrane: physiological functions and the regulation of protease activity. Frontiers in Plant Science 9: 855.CrossRefGoogle ScholarPubMed
Kaya, C, Tuna, AL and Yokaş, I (2009) The Role of Plant Hormones in Plants Under Salinity Stress. In: Ashraf, M, Ozturk, M and Athar, H (eds.) Salinity and Water Stress. Tasks for Vegetation Sciences, vol 44. Dordrecht: Springer, pp. 45–50.Google Scholar
Kim, J and Kim, HY (2006) Functional analysis of a calcium-binding transcription factor involved in plant salt stress signaling. FEBS Letters 580: 5251–5256.CrossRefGoogle ScholarPubMed
Kim, D, Langmead, B and Salzberg, SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12: 357–360.CrossRefGoogle ScholarPubMed
Krasnoperova, OE, Buy, DD, Goriunova, II, Isayenkov, SV, Karpov, PA, Blume, YB and Yemets, AI (2019) The potential role of SnRK1 protein kinases in the regulation of cell division in Arabidopsis thaliana. Cytology and Genetics 53: 185–191.CrossRefGoogle Scholar
Lee, JW, Lee, SH, Han, JW and Kim, GH (2020) Early light-inducible protein (ELIP) can enhance resistance to cold-induced photooxidative stress in Chlamydomonas reinhardtii. Frontiers in Physiology 11: 1083. doi: 10.3389/fphys.2020.01083CrossRefGoogle ScholarPubMed
Li, H, Li, D, Chen, A, Tang, H, Li, J and Huang, S (2016) RNA-seq for comparative transcript profiling of Kenaf under salinity stress. Journal of Plant Research 130: 365–372.CrossRefGoogle ScholarPubMed
Li, C, Dong, S, Liu, X, Bo, K, Miao, H, Beckles, DM, Zhang, S and Gu, X (2020) Genome-Wide characterization of cucumber (Cucumis sativus L.) GRAS genes and their response to various abiotic stresses. Horticulturae 6: 110.CrossRefGoogle Scholar
Lindemose, S, O'Shea, C, Jensen, MK and Skriver, K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. International Journal of Molecular Sciences 14: 5842–5878.CrossRefGoogle ScholarPubMed
Liu, H, Xing, M, Yang, W, Mu, X, Wang, X, Lu, F, Wang, Y and Zhang, L (2019) Genome-wide identification of and functional insights into the late embryogenesis abundant (LEA) gene family in bread wheat (Triticum aestivum). Scientific Reports 9: 13375. https://doi.org/10.1038/s41598-019-49759-wCrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods (San Diego, Calif.) 25: 402–408. PMID:11846609CrossRefGoogle Scholar
Lomelino, CL, Andring, JT, McKenna, R and Kilberg, MS (2017) Asparagine synthetase: Function, structure, and role in disease. Journal of Biological Chemistry 292: 19952–19958. https://doi.org/10.1074/jbc.R117.819060CrossRefGoogle Scholar
Love, MI, Huber, W and Anders, S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 550.CrossRefGoogle ScholarPubMed
Luo, Q, Teng, W, Fang, S, Li, H, Li, B, Chu, J, Li, Z and Zheng, Q (2019) Transcriptome analysis of salt-stress response in three seedling tissues of common wheat. The Crop Journal 7: 378–392. doi:10.1016/j.cj.2018.11.009.CrossRefGoogle Scholar
Ma, X, Gu, P, Liang, W, Zhang, Y, Jin, X, Wang, S, Shen, Y and Huang, Z (2016) Analysis on the transcriptome information of two different wheat mutants and identification of salt-induced differential genes. Biochemical and Biophysical Research Communications 473: 1197–1204.CrossRefGoogle ScholarPubMed
Mansouri, M, Naghavi, MR, Alizadeh, H, Mohammadi-Nejad, G, Mousavi, SA, Hosseini Salekdeh, G and Tada, Y (2018) Transcriptomic analysis of Aegilops tauschii during long-term salinity stress. Functional & Integrative Genomics 19: 13–28. doi:10.1007/s10142-018-0623-y.CrossRefGoogle ScholarPubMed
Mizoi, J, Shinozaki, K and Yamaguchi-Shinozaki, K (2012) AP2/ERF Family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms 1819: 86–96.CrossRefGoogle ScholarPubMed
Moazzzam Jazi, M, Seyedi, SM, Ebrahimie, E, Ebrahimi, M, De Moro, G and Botanga, C (2017) A genome-wide transcriptome map of pistachio (Pistacia vera L.) provides novel insights into salinity-related genes and marker discovery. BMC Genomics 18: 627.CrossRefGoogle ScholarPubMed
Mohannath, G, Jackel, JN, Lee, YH, Buchmann, RC, Wang, H, Patil, V, Adams, AK and Bisaro, DM (2014) A Complex containing SNF1-related kinase (SnRK1) and adenosine kinase in Arabidopsis. PLoS ONE 9: e87592.CrossRefGoogle ScholarPubMed
Munns, R and Tester, M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651–681.CrossRefGoogle ScholarPubMed
Nakamura, S, Makiko, C, Stehno, Z, Holubec, V, Morishige, H, Pourkheirandish, M, Kanamori, H, Wu, J, Matsumoto, T and Komatsuda, T (2015) Diversification of the promoter sequences of wheat Mother of FT and TFL1 on chromosome 3A. Molecular Breeding 35: 164. https://doi.org/10.1007/s11032-015-0358-6CrossRefGoogle Scholar
Ning, P, Liu, C, Kang, J and Lv, J (2017) Genome-wide analysis of WRKY transcription factors in wheat (Triticum aestivum L.) and differential expression under water deficit condition. PeerJ 5: e3232.CrossRefGoogle ScholarPubMed
Nuruzzaman, M, Sharoni, AM and Kikuchi, S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Frontiers in Microbiology 4: 248. doi: 10.3389/fmicb.2013.00248CrossRefGoogle ScholarPubMed
O'Brien, M, Chantha, SC, Rahier, A and Matton, DP (2005) Lipid signaling in plants. Cloning and expression analysis of the obtusifoliol 14 -demethylase from Solanum chacoense bitt., a pollination- and fertilization-induced gene with both obtusifoliol and lanosterol demethylase activity. Plant Physiology 139: 734–749.CrossRefGoogle ScholarPubMed
O'Neill, KC and Lee, YJ (2020) Visualizing genotypic and developmental differences of free amino acids in maize roots with mass spectrometry imaging. Frontiers in Plant Science 11: 639.CrossRefGoogle ScholarPubMed
Oyiga, BC, Sharma, RC, Baum, M, Ogbonnaya, FC, Léon, J and Ballvora, A (2018) Allelic variations and differential expressions detected at quantitative trait loci for salt stress tolerance in wheat. Plant, Cell and Environment 41: 919–935.CrossRefGoogle ScholarPubMed
Poustini, K and Siosemardeh, A (2004) Ion distribution in wheat cultivars in response to salinity stress. Field Crops Research 85: 125–133.CrossRefGoogle Scholar
Qadir, M, Quillérou, E, Nangia, V, Murtaza, G, Singh, M, Thomas, RJ, Drechsel, P and Noble, AD (2014) Economics of salt-induced land degradation and restoration. Natural Resources Forum 38: 282–295.CrossRefGoogle Scholar
Qadir, M, Qureshi, AS and Cheraghi, SAM (2008) Extent and characterisation of salt-affected soils in Iran and strategies for their amelioration and management. Land Degradation & Development 19: 214–227.CrossRefGoogle Scholar
Qin, D, Wu, H, Peng, H, Yao, Y, Ni, Z, Li, Z, Zhou, C and Sun, Q (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using wheat genome array. BMC Genomics 9: 432.CrossRefGoogle ScholarPubMed
Rao, AQ, Din, S, Akhtar, S, Sarwar, MB, Ahmed, M, Rashid, B, Azmat Ullah Khan, M, Qaisar, U, Shahid, AA, Ahmad Nasir, I and Husnain, T (2016) Genomics of salinity tolerance in plants. In: Abdurakhmonov, IY (ed.) Plant Genomics, Chapter 11. London, UK: IntechOpen, pp. 273–299.Google Scholar
Ravikumar, R, Steiner, A and Assaad, FF (2017) Multisubunit tethering complexes in higher plants. Current Opinion in Plant 40: 97–105.CrossRefGoogle ScholarPubMed
Roberts, TH and Hejgaard, J (2008) Serpins in plants and green algae. Functional & Integrative Genomics 8: 1–27.CrossRefGoogle ScholarPubMed
Sairam, R and Tyagi, A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Current Science 3: 407–421. Retrieved May 9, 2021, from http://www.jstor.org/stable/24108735.Google Scholar
Sakuma, Y, Maruyama, K, Osakabe, Y, Qin, F, Seki, M, Shinozaki, K and Shinozaki, KY (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. The Plant Cell Online 18: 1292–1309.CrossRefGoogle ScholarPubMed
Shao, Q, Liu, X, Su, T, Ma, C and Wang, P (2019) New insights into the role of seed Oil body proteins in metabolism and plant development. Frontiers in Plant Science 10: 1568.CrossRefGoogle ScholarPubMed
Shavrukov, Y, Suchecki, R, Eliby, S, Abugalieva, A, Kenebayev, S and Langridge, P (2014) Application of next-generation sequencing technology to study genetic diversity and identify unique SNP markers in bread wheat from Kazakhstan. BMC Plant Biology 14: 258.CrossRefGoogle ScholarPubMed
Sun, X, Jones, WT and Rikkerink, EHA (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. Biochemical Journal 442: 1–12.CrossRefGoogle ScholarPubMed
Takahashi, F, Tilbrook, J, Trittermann, C, Berger, B, Roy, SJ, Seki, M, Shinozaki, K and Tester, M (2015) Comparison of leaf sheath transcriptome profiles with physiological traits of bread wheat cultivars under salinity stress. PLoS ONE 10: e0133322.CrossRefGoogle ScholarPubMed
Thimm, O, Blasing, O, Gibon, Y, Nagel, A, Meyer, S, Kruger, P, Selbig, J, Muller, LA, Rhee, SY and Stitt, M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37: 914–939.CrossRefGoogle ScholarPubMed
Timerbaev, V and Dolgov, S (2019) Functional characterization of a strong promoter of the early light-inducible protein gene from tomato. Planta 250: 1307–1323. doi: 10.1007/s00425-019-03227-x.CrossRefGoogle Scholar
Untergasser, A, Nijveen, H, Rao, X, Bisseling, T, Geurts, R and Leunissen, JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research 35: W71–W74.CrossRefGoogle ScholarPubMed
Verhertbruggen, Y, Yin, L, Oikawa, A and Scheller, HV (2011) Mannan synthase activity in the CSLD family. Plant Signaling & Behavior 6: 1620–1623.CrossRefGoogle ScholarPubMed
Wang, W, Vinocur, B, Shoseyov, O and Altman, A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9: 244–252.CrossRefGoogle ScholarPubMed
Wang, Y, Mortimer, JC, Davis, J, Dupree, P and Keegstra, K (2012) Identification of an additional protein involved in mannan biosynthesis. The Plant Journal 73: 105–117.CrossRefGoogle ScholarPubMed
Wang, Q, Geng, T, Zhu, S, Li, R, Tong, Y, Wang, S, Chen, F, Tang, L and He, Y (2017) Analysis of miRNA-seq combined with gene expression profile reveals the complexity of salinity stress response in Oryza sativa. Acta Physiologiae Plantarum 39: 272. https://doi.org/10.1007/s11738-017-2570-yCrossRefGoogle Scholar
Wang, K, Ding, Y, Cai, C, Chen, Z and Zhu, C (2018a) The role of C2H2 zinc finger proteins in plant responses to abiotic stresses. Physiologia Plantarum, 165: 690–700. doi: 10.1111/ppl.12728.CrossRefGoogle Scholar
Wang, YX, Liu, ZW, Wu, ZJ, Li, H, Wang, WL, Cui, X and Zhuang, J (2018b) Genome-wide identification and expression analysis of GRAS family transcription factors in tea plant (Camellia sinensis). Scientific Reports 8: 3949. https://doi.org/10.1038/s41598-018-22275-z.CrossRefGoogle Scholar
Wang, P, Wang, L, Liu, Z, Zhang, T, Wang, Y, Li, Y and Gao, C (2019) Molecular characterization and expression profiles of GRAS genes in response to abiotic stress and hormone treatment in Tamarix hispida. Trees 33: 213–225.CrossRefGoogle Scholar
Wani, SH, Tripathi, P, Zaid, A, Challa, GS, Kumar, A, Kumar, V, Upadhyay, J, Joshi, R and Bhatt, M (2018) Transcriptional regulation of osmotic stress tolerance in wheat (Triticum aestivum L.). Plant Molecular Biology 97: 469–487. doi: 10.1007/s11103-018-0761-6.CrossRefGoogle Scholar
Welner, DH, Deeba, F, Leggio, LL and Skriver, K (2016) NAC transcription factors: from structure to function in stress-associated networks. In: Gonzalez, DH (ed.) Plant Transcription Factors: Chapter 13. London, UK: Academic Press, pp. 199–212.CrossRefGoogle Scholar
Winfield, MO, Lu, C, Wilson, LD, Coghill, JA and Edwards, KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnology Journal 8: 749–771.CrossRefGoogle ScholarPubMed
Woo, HR, Kim, JH, Kim, J, Kim, J, Lee, U, Song, IJ, Kim, JH, Lee, HY, Nam, HG and Lim, PO (2010) The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis. Journal of Experimental Botany 61: 3947–3957.CrossRefGoogle ScholarPubMed
Wu, B, Hu, Y, Huo, P, Zhang, Q, Chen, X and Zhang, Z (2017) Transcriptome analysis of hexaploid hulless oat in response to salinity stress. PLoS ONE 12: e0171451.CrossRefGoogle ScholarPubMed
Wu, J, Zhao, Q, Wu, G, Yuan, H, Ma, Y, Lin, H, Pan, L, Li, S and Sun, D (2019) Comprehensive analysis of differentially expressed unigenes under NaCl stress in flax (Linum usitatissimum L.) using RNA-Seq. International Journal of Molecular Sciences 20: 369.CrossRefGoogle ScholarPubMed
Xi, W and Yu, H (2010) Mother of FT and TFL1regulates seed germination and fertility relevant to the brassinosteroid signaling pathway. Plant Signaling & Behavior 5: 1315–1317.CrossRefGoogle ScholarPubMed
Xiong, H, Guo, H, Xie, Y, Zhao, L, Gu, J, Zhao, S, Li, J and Liu, L (2017) RNAseq analysis reveals pathways and candidate genes associated with salinity tolerance in a spaceflight-induced wheat mutant. Scientific Reports 7: 2731.CrossRefGoogle Scholar
Xiong, L, Schumaker, KS, Zhu, JK (2002) Cell Signaling during Cold, Drought, and Salt Stress. The Plant Cell, 14(suppl 1): S165–S183. doi:10.1105/tpc.000596CrossRefGoogle Scholar
Yadav, SP, Bharadwaj, R, Nayak, H, Mahto, R, Singh, RK and Prasad, SK (2019) Impact of salt stress on growth, productivity and physicochemical properties of plants: a review. International Journal of Chemical Studies 7: 1793–1798.Google Scholar
Yang, X, Li, H, Yang, Y, Wang, Y, Mo, Y, Zhang, R, Zhang, Y, Ma, J, Wei, C and Zhang, X (2018) Identification and expression analyses of WRKY genes reveal their involvement in growth and abiotic stress response in watermelon (Citrullus lanatus). PLoS ONE 13: e0191308.CrossRefGoogle Scholar
Yong, HY, Zou, Z, Kok, EP, Kwan, BH, Chow, K, Nasu, S, Nanzyo, M, Kitashiba, H, Nishio, T (2014) Comparative transcriptome analysis of leaves and roots in response to sudden increase in salinity in Brassica napus by RNA-seq. BioMed Research International, 467395, 19 pages. http://dx.doi.org/10.1155/2014/467395CrossRefGoogle ScholarPubMed
Young, MD, Wakefield, MJ, Smyth, GK and Oshlack, A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology 11: R14.CrossRefGoogle ScholarPubMed
Zhang, X, Liao, M, Chang, D and Zhang, F (2014) Comparative transcriptome analysis of the Asteraceae halophyte Karelinia caspica under salt stress. BMC Research Notes. 7: 927 Page 2 of 9. http://www.biomedcentral.com/1756-0500/7/927CrossRefGoogle ScholarPubMed
Zhang, J, Liu, W, Han, H, Song, L, Bai, L, Gao, Z, Zhang, Y, Yang, X, Li, X, Gao, A and Li, L (2015) De novo transcriptome sequencing of Agropyron cristatum to identify available gene resources for the enhancement of wheat. Genomics 106: 129–136.CrossRefGoogle ScholarPubMed
Zhang, N, Wang, S, Zhang, X, Dong, Z, Chen, F and Cui, D (2016) Transcriptome analysis of the Chinese bread wheat cultivar Yunong 201 and its ethyl methanesulfonate mutant line. Gene 575: 285–293.CrossRefGoogle ScholarPubMed
Zhao, Y, Li, X, Wang, F, Zhao, X, Gao, Y, Zhao, C, He, L, Li, Z and Xu, J (2018) Glycerol-3-phosphate dehydrogenase (GPDH) gene family in Zea mays L.: identification, subcellular localization, and transcriptional responses to abiotic stresses. PLOS ONE 13: e0200357.CrossRefGoogle ScholarPubMed
Zhou, Y, Yang, P, Cui, F, Zhang, F, Luo, X and Xie, J (2016) Transcriptome analysis of salt stress responsiveness in the seedlings of Dongxiang wild rice (Oryza rufipogon Griff.). PLOS ONE 11: e0146242.CrossRefGoogle Scholar
Zhu, M, Meng, X, Cai, J, Li, G, Dong, T and Li, Z (2018) Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biology 18: 83. https://doi.org/10.1186/s12870-018-1299-0CrossRefGoogle ScholarPubMed
Supplementary material: File

Azimian et al. supplementary material

Azimian et al. supplementary material

Download Azimian et al. supplementary material(File)
File 3.2 MB