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Comparative Transcriptome Analysis of Seedling Stage of Two Sorghum Cultivars Under Salt Stress

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Abstract

Soil salinity is one of the major abiotic stresses restricting crop production. Mechanisms of salt response have been intensively studied in model plants such as Arabidopsis and rice, but are rarely known in sorghum. In this study, we compared the transcriptome profiles between two cultivars with different salt tolerance under salt treatment (0.8% NaCl) for 0, 48, and 72 h. On average, about 243.9 million clean reads, representing 32.4 thousand transcripts and 26.4 thousand unigenes with 829 new genes were detected in each library. Also, over 112,000 single nucleotide polymorphisms were identified, which may supply useful resources for marker development. In total, 5647 differentially expressed genes (DEGs) were identified from all of the comparisons. Functional annotation analysis indicated that expression of genes in transcriptional regulation, signal transduction, and secondary metabolism changed significantly between the two varieties under salt stress, and hundreds of genes involved in the salt stress response were differentially expressed, especially genes encoding receptors like kinases and transcription factors. Besides, qRT-PCR analysis of expression profiles of the selected DEGs was in keeping with the results from RNA-seq analysis. Based on the findings, we proposed several candidate genes that might be used to improve salt tolerance in sorghum. The transcriptional profiles presented here provide further understanding of the salt-tolerance mechanism in sorghum.

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References

  • Abogadallah GM, Nada RM, Malinowski R, Quick P (2011) Overexpression of HARDY, an AP2/ERF gene from Arabidopsis, improves drought and salt tolerance by reducing transpiration and sodium uptake in transgenic Trifolium alexandrinum L. Planta 233(6):1265–1276

    Article  PubMed  CAS  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285(5431):1256–1258

    Article  PubMed  CAS  Google Scholar 

  • Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O’Donovan C, Redaschi N, Yeh LS (2004) UniProt: the universal protein knowledge base. Nucleic Acids Res 32(Database issue):D115–D119

    Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25(1):25–29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Calvino M, Messing J (2012) Sweet sorghum as a model system for bioenergy crops. Curr Opin Biotechnol 23(3):323–329

    Article  PubMed  CAS  Google Scholar 

  • Carpita NC, McCann MC (2008) Maize and sorghum: genetic resources for bioenergy grasses. Trends Plant Sci 13(8):415–420

    Article  PubMed  CAS  Google Scholar 

  • Chopra R, Burow G, Hayes C, Emendack Y, Xin Z, Burke J (2015) Transcriptome profiling and validation of gene based single nucleotide polymorphisms (SNPs) in sorghum genotypes with contrasting responses to cold stress. BMC Genom 16(1):1040

    Article  CAS  Google Scholar 

  • Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong K (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol 143(4):1739–1751

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dugas DV, Monaco MK, Olsen A, Klein RR, Kumari S, Ware D, Klein PE (2011) Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid. BMC Genom 12:514

    Article  CAS  Google Scholar 

  • Gelli M, Duo Y, Konda AR, Zhang C, Holding D, Dweikat I (2014) Identification of differentially expressed genes between sorghum genotypes with contrasting nitrogen stress tolerance by genome-wide transcriptional profiling. BMC Genom 15:179

    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(8):1383–1391

    Article  PubMed  CAS  Google Scholar 

  • Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68(2):302–313

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103(35):12987–12992

    Article  PubMed  CAS  Google Scholar 

  • Johnson SM, Lim FL, Finkler A, Fromm H, Slabas AR, Knight MR (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genom 15:456

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32(Database issue):D277–D280

    Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14(4):R36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lease K, Ingham E, Walker JC (1998) Challenges in understanding RLK function. Curr Opin Plant Biol 1(5):388–392

    Article  PubMed  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199(3):639–649

    Article  PubMed  CAS  Google Scholar 

  • Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA, Hu XH, Ren ZH, Chao DY (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theor Appl Genet 108(2):253–260

    Article  PubMed  CAS  Google Scholar 

  • Mace ES, Tai S, Gilding EK, Li Y, Prentis PJ, Bian L, Campbell BC, Hu W, Innes DJ, Han X, Cruickshank A, Dai C, Frere C, Zhang H, Hunt CH, Wang X, Shatte T, Wang M, Su Z, Li J, Lin X, Godwin ID, Jordan DR, Wang J (2013) Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nat Commun 4:2320

    Article  PubMed  PubMed Central  Google Scholar 

  • Monreal JA, Arias-Baldrich C, Pérez-Montaño F, Gandullo J, Echevarría C, García-Mauriño S (2013) Factors involved in the rise of phosphoenolpyruvate carboxylase-kinase activity caused by salinity in sorghum leaves. Planta 237(5):1401–1413

    Article  PubMed  CAS  Google Scholar 

  • Munns R, Gilliham M (2015) Salinity tolerance of crops—what is the cost? New Phytol 208(3):668–673

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64(2):445–458

    Article  PubMed  CAS  Google Scholar 

  • Ouyang SQ, Liu YF, Liu P, Lei G, He SJ, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62(2):316–329

    Article  PubMed  CAS  Google Scholar 

  • Park S, Moon JC, Park YC, Kim JH, Kim DS, Jang CS (2014) Molecular dissection of the response of a rice leucine-rich repeat receptor-like kinase (LRR-RLK) gene to abiotic stresses. J Plant Physiol 171(17):1645–1653

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556

    Article  PubMed  CAS  Google Scholar 

  • Platten JD, Cotsaftis O, Berthomieu P, Bohnert H, Davenport RJ, Fairbairn DJ, Horie T, Leigh RA, Lin HX, Luan S, Mäser P, Pantoja O, Rodríguez-Navarro A, Schachtman DP, Schroeder JI, Sentenac H, Uozumi N, Véry AA, Zhu JK, Dennis ES, Tester M (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci 11:372–374

    Article  PubMed  CAS  Google Scholar 

  • Pruitt KD, Tatusova T, Maglott DR (2005) Ncbi reference sequence (refseq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33(Database issue):D501–D504

    Google Scholar 

  • Rong W, Qi L, Wang A, Ye X, Du L, Liang H, Xin Z, Zhang Z (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol J 12(4):468–479

    Article  PubMed  CAS  Google Scholar 

  • Sayyad-Amin P, Jahansooz MR, Borzouei A, Ajili F (2016) Changes in photosynthetic pigments and chlorophyll-a fluorescence attributes of sweet-forage and grain sorghum cultivars under salt stress. J Biol Phys 42(4):601–620

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97(12):6896–6901

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21(1):81–85

    Article  PubMed  CAS  Google Scholar 

  • Sui N, Yang Z, Liu M, Wang B (2015) Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genom 16:534

    Article  CAS  Google Scholar 

  • Sun X, Sun M, Luo X, Ding X, Cai H, Bai X, Liu X, Zhu Y (2013a) A Glycine soja ABA-responsive receptor-like cytoplasmic kinase, GsRLCK, positively controls plant tolerance to salt and drought stresses. Planta 237(6):1527–1545

    Article  PubMed  CAS  Google Scholar 

  • Sun XL, Yu QY, Tang LL, Ji W, Bai X, Cai H, Liu XF, Ding XD, Zhu YM (2013b) GsSRK, a G-type lectin S-receptor-like serine/threonine protein kinase, is a positive regulator of plant tolerance to salt stress. J Plant Physiol 170(5):505–515

    Article  PubMed  CAS  Google Scholar 

  • Surender Reddy P, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kavi Kishor PB (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113

    Article  PubMed  CAS  Google Scholar 

  • Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28(1):33–36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Google Scholar 

  • Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63(7):2541–2556

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang QS, Gao J, He WD, Dou TX, Ding LJ, Wu JH, Li CY, Peng XX, Zhang S, Yi GJ (2015) Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress. BMC Genom 16:446

    Article  CAS  Google Scholar 

  • Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30(5):529–539

    Article  PubMed  CAS  Google Scholar 

  • Zahaf O, Blanchet S, de Zelicourt A, Alunni B, Plet J, Laffont C, de Lorenzo L, Imbeaud S, Ichante JL, Diet A, Badri M, Zabalza A, Gonzalez EM, Delacroix H, Gruber V, Frugier F, Crespi M (2012) Comparative transcriptomic analysis of salt adaptation in roots of contrasting Medicago truncatula genotypes. Mol Plant 5(5):1068–1081

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Guo G, Hu X, Zhang Y, Li Q, Li R, Zhuang R, Lu Z, He Z, Fang X, Chen L, Tian W, Tao Y, Kristiansen K, Zhang X, Li S, Yang H, Wang J, Wang J (2010) Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res 20(5):646–654

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang WD, Wang P, Bao Z, Ma Q, Duan LJ, Bao AK, Zhang JL, Wang SM (2017) SOS1, HKT1;5, and NHX1 synergistically modulate Na+ homeostasis in the halophytic grass Puccinellia tenuiflora. Front Plant Sci 8:576

    PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6(2):66–71

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study was supported by grants from Hebei Province Key Basic Research Foundation (15962905D).

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Authors and Affiliations

  1. North China Key Laboratory for Crop, Key Laboratory for Crop Germplasm Resources of Hebei, College of Agronomy, Agricultural University of Hebei, No. 2596 LeKai South Street, Baoding, Hebei, China

    Jianghui Cui, Genzeng Ren, Haiyu Qiao, Xiaodong Xiang & Jinhua Chang

  2. Beijing Biomics Tech Co.Ltd, Beijing, China

    Lisha Huang

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  1. Jianghui Cui
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  2. Genzeng Ren
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  3. Haiyu Qiao
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  4. Xiaodong Xiang
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  5. Lisha Huang
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  6. Jinhua Chang
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Contributions

Conceived and designed the experiments: JC, JC. Performed the experiments: JC, GR, HQ, XX, JC. Analyzed the data: JC, GR, LH, and JC. Contributed reagents/materials/analysis tools: GR, HQ, and XX.

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Correspondence to Jinhua Chang.

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Cui, J., Ren, G., Qiao, H. et al. Comparative Transcriptome Analysis of Seedling Stage of Two Sorghum Cultivars Under Salt Stress. J Plant Growth Regul 37, 986–998 (2018). https://doi.org/10.1007/s00344-018-9796-9

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  • DOI: https://doi.org/10.1007/s00344-018-9796-9

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