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Transcriptomic analysis of Aegilops tauschii during long-term salinity stress

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Abstract

Aegilops tauschii is the diploid progenitor of the bread wheat D-genome. It originated from Iran and is a source of abiotic stress tolerance genes. However, little is known about the molecular events of salinity tolerance in Ae. tauschii. This study investigates the leaf transcriptional changes associated with long-term salt stress. Total RNA extracted from leaf tissues of control and salt-treated samples was sequenced using the Illumina technology, and more than 98 million high-quality reads were assembled into 255,446 unigenes with an average length of 1398 bp and an N50 of 2269 bp. Functional annotation of the unigenes showed that 93,742 (36.69%) had at least a significant BLAST hit in the SwissProt database, while 174,079 (68.14%) showed significant similarity to proteins in the NCBI nr database. Differential expression analysis identified 4506 salt stress-responsive unigenes. Bioinformatic analysis of the differentially expressed unigenes (DEUs) revealed a number of biological processes and pathways involved in the establishment of ion homeostasis, signaling processes, carbohydrate metabolism, and post-translational modifications. Fine regulation of starch and sucrose content may be important features involved in salt tolerance in Ae. tauschii. Moreover, 82% of DEUs mapped to the D-subgenome, including known QTL for salt tolerance, and these DEUs showed similar salt stress responses in other accessions of Ae. tauschii. These results could provide fundamental insight into the regulatory process underlying salt tolerance in Ae. tauschii and wheat and facilitate identification of genes involved in their salt tolerance mechanisms.

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Abbreviations

DEUs:

Differentially expressed unigenes

Na:

Sodium

Cl:

Chlorine

K:

Potassium

BLAST:

Basic local alignment search tool

nr :

Non-redundant

qRT-PCR:

Quantitative real-time PCR

References

  • Alptekin B, Budak H (2017) Wheat miRNA ancestors: evident by transcriptome analysis of A, B, and D genome donors. Funct Integr Genomics 17:171–187

    Article  CAS  Google Scholar 

  • Ashraf M, Öztürk MA, Athar H (2008) Salinity and water stress: improving crop efficiency vol 44. Springer Science & Business Media,

  • Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942

    Article  Google Scholar 

  • Balibrea ME, Dell'Amico J, Bolarín MC, Pérez-Alfocea F (2000) Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiol Plant 110:503–511

    Article  CAS  Google Scholar 

  • Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta (BBA)-Biomembr 1465:140–151

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics:btu170

  • Boudsocq M, Sheen J (2013) CDPKs in immune and stress signaling. Trends Plant Sci 18:30–40

    Article  CAS  Google Scholar 

  • Brummell DA, Chen RKY, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ (2011) Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot 62:3519–3534. https://doi.org/10.1093/jxb/err043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capitão C, Paiva JA, Santos DM, Fevereiro P (2011) In Medicago truncatula, water deficit modulates the transcript accumulation of components of small RNA pathways. BMC Plant Biol 11(1)

  • Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43:273–283

    Article  CAS  Google Scholar 

  • Cheng D, Wu G, Zheng Y (2015) Positive correlation between potassium uptake and salt tolerance in wheat. Photosynthetica 53:447–454

    Article  CAS  Google Scholar 

  • Colmer T, Munns R, Flowers T (2005) Improving salt tolerance of wheat and barley: future prospects. Anim Prod Sci 45:1425–1443

    Article  CAS  Google Scholar 

  • Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. J Exp Bot 57:1059–1078

    Article  CAS  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  Google Scholar 

  • Cui MH et al (2013) An Arabidopsis R2R3-MYB transcription factor, AtMYB20, negatively regulates type 2C serine/threonine protein phosphatases to enhance salt tolerance. FEBS Lett 587:1773–1778

    Article  CAS  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community Nucleic acids research:gkq310

  • Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H (2008) Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett 582:943–948

    Article  CAS  Google Scholar 

  • Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought-and salt-tolerant plants result from overexpression of the AVP1 H+−pump. Proc Natl Acad Sci 98:11444–11449

  • Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci 98:6522–6527

    Article  CAS  Google Scholar 

  • Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391

    Article  CAS  Google Scholar 

  • Gorham J, Hardy C, Jones RW, Joppa L, Law C (1987) Chromosomal location of a K/Na discrimination character in the D genome of wheat. Theor Appl Genet 74:584–588

    Article  CAS  Google Scholar 

  • Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • Guo A-Y et al (2008) PlantTFDB: a comprehensive plant transcription factor database. Nucleic Acids Res 36:D966–D969

    Article  CAS  Google Scholar 

  • Gupta B, Huang B (2014, 2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics

  • Halfter U, Ishitani M, Zhu J-K (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci 97:3735–3740

    Article  CAS  Google Scholar 

  • Harmon AC, Gribskov M, Harper JF (2000) CDPKs—a kinase for every Ca 2+ signal? Trends Plant Sci 5:154–159

    Article  CAS  Google Scholar 

  • Horie T et al (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938

    Article  Google Scholar 

  • Horie T et al (2011) Rice sodium-insensitive potassium transporter, OsHAK5, confers increased salt tolerance in tobacco BY2 cells. J Biosci Bioeng 111:346–356

    Article  CAS  Google Scholar 

  • Hussain B, Lucas SJ, Ozturk L, Budak H (2017) Mapping QTLs conferring salt tolerance and micronutrient concentrations at seedling stage in wheat. Sci Rep 7:15662

    Article  Google Scholar 

  • Ishitani M, Liu J, Halfter U, Kim C-S, Shi W, Zhu J-K (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1677

    Article  CAS  Google Scholar 

  • James RA, Blake C, Byrt CS, Munns R (2011) Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1; 4 and HKT1; 5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. J Exp Bot 62:2939–2947

    Article  CAS  Google Scholar 

  • Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413

    Article  CAS  Google Scholar 

  • Jia J et al (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jiang Y, Yang B, Deyholos MK (2009) Functional characterization of the Arabidopsis bHLH92 transcription factor in abiotic stress. Mol Gen Genomics 282:503–516

    Article  CAS  Google Scholar 

  • Jiang Z, Zhu S, Ye R, Xue Y, Chen A, An L, Pei Z-M (2013) Relationship between NaCl-and H 2 O 2-induced cytosolic Ca 2+ increases in response to stress in Arabidopsis. PLoS One 8

  • Kao W-Y, Tsai T-T, Tsai H-C, Shih C-N (2006) Response of three Glycine species to salt stress. Environ Exp Bot 56:120–125

    Article  CAS  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  CAS  Google Scholar 

  • Kawaura K, Mochida K, Ogihara Y (2008) Genome-wide analysis for identification of salt-responsive genes in common wheat. Functional & integrative genomics 8:277–286

    Article  CAS  Google Scholar 

  • Krapp A, Stitt M (1995) An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 195:313–323

    Article  CAS  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  Google Scholar 

  • Liu P, Yang G-D, Li H, Zheng C-C, Wu C-A (2010) Overexpression of NHX1s in transgenic Arabidopsis enhances photoprotection capacity in high salinity and drought conditions. Acta Physiol Plant 32:81–90

    Article  CAS  Google Scholar 

  • Liu J et al (2015a) Down-regulation of a wheat alkaline/neutral invertase correlates with reduced host susceptibility to wheat stripe rust caused by Puccinia striiformis. J Exp Bot 66:7325–7338

    Article  CAS  Google Scholar 

  • Liu Y et al (2015b) Genome-wide association study of 29 morphological traits in Aegilops tauschii. Sci Rep 5:15562

    Article  CAS  Google Scholar 

  • Lohse M et al (2014) Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ 37:1250–1258

    Article  CAS  Google Scholar 

  • Long X-Y et al (2010) Genome-wide identification and evaluation of novel internal control genes for Q-PCR based transcript normalization in wheat. Plant Mol Biol 74:307–311

    Article  CAS  Google Scholar 

  • Luo M-C et al (2017) Genome sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature 551

  • Ma S, Niu H, Liu C, Zhang J, Hou C, Wang D (2013) Expression stabilities of candidate reference genes for RT-qPCR under different stress conditions in soybean. PLoS One 8:e75271

    Article  CAS  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

    Article  CAS  Google Scholar 

  • Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci 174:420–431

    Article  CAS  Google Scholar 

  • Mi S et al (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, CIFTCI-YILMAZ S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ 33:453–467

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185

    Article  Google Scholar 

  • Munnik T, Meijer HJ (2001) Osmotic stress activates distinct lipid and MAPK signalling pathways in plants. FEBS Lett 498:172–178

    Article  CAS  Google Scholar 

  • Munns R (2013) Hoagland’s nutrient solution. csiro

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

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Naghavi MR, Mardi M (2010) Characterization of genetic variation among accessions of Aegilops tauschii. AsPac J Mol Biol Biotechno 18:93–96

    Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta (BBA)-Gene Regul Mech 1819:97–103

    Article  CAS  Google Scholar 

  • Nevo E (2005) Genomic diversity in nature and domestication. In: Henry R (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CABI publishing CAB International, Wallingford, U.K, pp 287–316

  • Nevo E, Chen G (2010) Drought and salt tolerances in wild relatives for wheat and barley improvement. Plant Cell Environ 33:670–685

    Article  CAS  Google Scholar 

  • Oyiga BC, Sharma RC, Baum M, Ogbonnaya FC, Léon J, Ballvora A (2017) Allelic variations and differential expressions detected at quantitative trait loci for salt stress tolerance in wheat. Plant, Cell Environ

  • Pandey N et al (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14:216

    Article  CAS  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time. PCR. Nucleic Acids Res 30:e36–e36

    Article  Google Scholar 

  • Pritchard D, Hollington P, Davies W, Gorham J, de Leon JD, Mujeeb-Kazi A (2002) K+/Na+ discrimination in synthetic hexaploid wheat lines: transfer of the trait for K+/Na+ discrimination from Aegilops tauschii into a Triticum turgidum background. Cereal Res Commun:261–267

  • Qian Y, Cheng Y, Cheng X, Jiang H, Zhu S, Cheng B (2011) Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep 30:1347–1363

    Article  CAS  Google Scholar 

  • Qiu Q-S, Guo Y, Dietrich MA, Schumaker KS, Zhu J-K (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci 99:8436–8441

    Article  CAS  Google Scholar 

  • Quarrie S et al (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring× SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110:865–880

    Article  CAS  Google Scholar 

  • Quintero FJ, Ohta M, Shi H, Zhu J-K, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proceedings of the Natl Acad Sci 99:9061–9066

  • Rahaie M, Xue G-P, Schenk PM (2013) The role of transcription factors in wheat under different abiotic stresses. In: Abiotic stress-plant responses and applications in agriculture. InTech

  • Riaño-Pachón DM, Ruzicic S, Dreyer I, Mueller-Roeber B (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinf 8(42)

  • Roitsch T, González M-C (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613

    Article  CAS  Google Scholar 

  • Roitsch T, Balibrea M, Hofmann M, Proels R, Sinha A (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524

    Article  CAS  Google Scholar 

  • Sanchez DH et al (2008) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J 53:973–987

    Article  CAS  Google Scholar 

  • Sathee L, Sairam RK, Chinnusamy V, Jha SK (2015) Differential transcript abundance of salt overly sensitive (SOS) pathway genes is a determinant of salinity stress tolerance of wheat. Acta Physiol Plant 37:169

    Article  Google Scholar 

  • Schachtman D, Munns R, Whitecross M (1991) Variation in sodium exclusion and salt tolerance in Triticum tauschii. Crop Sci 31:992–997

    Article  CAS  Google Scholar 

  • Schachtman D, Lagudah E, Munns R (1992) The expression of salt tolerance from Triticum tauschii in hexaploid wheat. Theor Appl Genet 84:714–719

    Article  CAS  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu J-K (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  CAS  Google Scholar 

  • Sohail Q, Inoue T, Tanaka H, Eltayeb AE, Matsuoka Y, Tsujimoto H (2011) Applicability of Aegilops tauschii drought tolerance traits to breeding of hexaploid wheat. Breed Sci 61:347

    Article  CAS  Google Scholar 

  • Thimm O et al (2004) MapMan: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  Google Scholar 

  • Tran L-SP et al (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

    Article  CAS  Google Scholar 

  • Tran L-SP, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1:32–39

    Article  Google Scholar 

  • Wang B, Lüttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52:2355–2365

    Article  CAS  Google Scholar 

  • Wang S et al (2014) Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796

    Article  CAS  Google Scholar 

  • Weinl S, Kudla J (2009) The CBL–CIPK Ca2+−decoding signaling network: function and perspectives. New Phytol 184:517–528

    Article  CAS  Google Scholar 

  • Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H, Wobus U (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33:395–411

    Article  CAS  Google Scholar 

  • Witcombe JR, Hollington PA, Howarth CJ, Reader S, Steele KA (2008) Breeding for abiotic stresses for sustainable agriculture. Philos Trans R Soc B: Biol Sci 363:703–716. https://doi.org/10.1098/rstb.2007.2179

    Article  CAS  Google Scholar 

  • Xie W, Nevo E (2008) Wild emmer: genetic resources, gene mapping and potential for wheat improvement. Euphytica 164:603–614

    Article  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  CAS  Google Scholar 

  • Yang T, Poovaiah B (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058

    Article  CAS  Google Scholar 

  • Yang O, Popova OV, Süthoff U, Lüking I, Dietz K-J, Golldack D (2009) The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436:45–55

    Article  CAS  Google Scholar 

  • Yoo JH et al (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem 280:3697–3706

    Article  CAS  Google Scholar 

  • Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  Google Scholar 

  • Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247

    Article  CAS  Google Scholar 

  • Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  Google Scholar 

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Funding

This study was supported by a grant from the Iran National Foundation Science (project number: 90003984).

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MM, MRN, HA, and GM-N conceived and designed the research. MM and SAM performed the experiments and analyzed the data. MM, MRN, HA, SAM, and YT interpreted the results and wrote the manuscript. MRN, HA, GM-N, and GHS supervised the study. All authors read and approved the manuscript.

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Correspondence to Mohammad Reza Naghavi or Yuichi Tada.

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Mansouri, M., Naghavi, M.R., Alizadeh, H. et al. Transcriptomic analysis of Aegilops tauschii during long-term salinity stress. Funct Integr Genomics 19, 13–28 (2019). https://doi.org/10.1007/s10142-018-0623-y

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