Skip to main content
Log in

Comparative transcriptome analysis of salt-sensitive and salt-tolerant maize reveals potential mechanisms to enhance salt resistance

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Background

Salt stress is a devastating environmental stress that causes plant growth inhibition and yield reduction.

Objective

The identification of salt-tolerant genes brings hope for the generation of salinity-tolerant crop plants through molecular breeding.

Methods

In this study, one salt-sensitive and one salt-tolerant maize inbred line were screened from 242 maize inbred lines. Reactive oxygen species (ROS)-related enzyme activities were detected and salt-responsive comparative transcriptome analysis was performed for control and 220 mM NaCl treated maize leaves.

Results

Salt-tolerant maize inbred line (L87) showed higher ROS-related enzyme (SOD, POD, APX and CAT) activities and accumulated relatively lower levels of ROS under salt stress. Of the total DEGs, 1856 upregulated DEGs were specific to L87, including stress tolerance-related members of the 70kDa family of heat shock proteins (Hsp70s) and aquaporins. The DEGs involved in the abscisic acid (ABA), ethylene, jasmonic acid (JA) and salicylic acid (SA) signal transduction pathways may determine the difference in salt tolerance between the two varieties, especially one central component SnRK2, that positively regulates ABA signaling and was only upregulated in L87. Analysis of DEGs related to ROS scavenging showed that some peroxidase (POD), glutathione S-transferase (GST), catalase (CAT) and superoxide dismutase (SOD) genes specific to L87 probably enhanced its salt tolerance. The analysis of differentially expressed transcription factors (TFs) suggested that WRKY TFs could contribute to the difference in salt tolerance between the two maize lines.

Conclusion

Compared with Salt-sensitive maize inbred line (L29), L87 exhibits specific regulatory mechanisms related to salt tolerance, including plant hormone interactions, ROS scavenging and the regulation of TFs. Our study identifies new candidate genes that may regulate maize tolerance to salt stress and provides useful information for breeding maize with high salt resistance.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S, Tran LS (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347

    PubMed  PubMed Central  Google Scholar 

  • Ahrazem O, Rubio-Moraga A, Trapero-Mozos A, Climent MF, Gomez-Cadenas A, Gomez-Gomez L (2015) Ectopic expression of a stress-inducible glycosyltransferase from saffron enhances salt and oxidative stress tolerance in Arabidopsis while alters anchor root formation. Plant Sci 234:60–73

    Article  CAS  PubMed  Google Scholar 

  • Alavilli H, Awasthi JP, Rout GR, Sahoo L, Lee BH, Panda SK (2016) Overexpression of a barley aquaporin gene, HvPIP2;5 confers salt and osmotic stress tolerance in yeast and plants. Front Plant Sci 7:1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Alexa A, Rahnenfuhrer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22:1600–1607

    Article  CAS  PubMed  Google Scholar 

  • Ali MA, Azeem F, Nawaz MA, Acet T, Abbas A, Imran QM, Shah KH, Rehman HM, Chung G, Yang SH, Bohlmann H (2018) Transcription factors WRKY11 and WRKY17 are involved in abiotic stress responses in Arabidopsis. J Plant Physiol 226:12–21

    Article  CAS  PubMed  Google Scholar 

  • Andjelkovic V, Thompson R (2006) Changes in gene expression in maize kernel in response to water and salt stress. Plant Cell Rep 25:71–79

    Article  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  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 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai J, Qin Y, Liu J, Wang Y, Sa R, Zhang N, Jia R (2017) Proteomic response of oat leaves to long-term salinity stress. Environ Sci Pollut Res Int 24:3387–3399

    Article  CAS  PubMed  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  Google Scholar 

  • Barrs H, Weatherley P (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Article  Google Scholar 

  • Cai R, Dai W, Zhang C, Wang Y, Wu M, Zhao Y, Ma Q, Xiang Y, Cheng B (2017) The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants. Planta 246:1215–1231

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Zhang J, Hu J, Xiong W, Du C, Lu M (2017) Integrated regulatory network reveals the early salt tolerance mechanism of Populus euphratica. Sci Rep 7:6769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng C, Wang Z, Ren Z, Zhi L, Yao B, Su C, Liu L, Li X (2017) SCFAtPP2-B11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana. PLoS Genet 13:e1006947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu X, Wang C, Chen X, Lu W, Li H, Wang X, Hao L, Guo X (2015) The cotton WRKY gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana benthamiana. PLoS One 10:e0143022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Ding L, Li Y, Wang Y, Gao L, Wang M, Chaumont F, Shen Q, Guo S (2016) Root ABA accumulation enhances rice seedling drought tolerance under ammonium supply: interaction with aquaporins. Front Plant Sci 7:1206

    PubMed  PubMed Central  Google Scholar 

  • Fernandes J, Morrow DJ, Casati P, Walbot V (2008) Distinctive transcriptome responses to adverse environmental conditions in Zea mays L. Plant Biotechnol J 6:782–798

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Y, Jiang W, Dai Y, Xiao N, Zhang C, Li H, Lu Y, Wu M, Tao X, Deng D, Chen J (2015) A maize phytochrome-interacting factor 3 improves drought and salt stress tolerance in rice. Plant Mol Biol 87:413–428

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Cui Y, Long R, Sun Y, Zhang T, Yang Q, Kang J (2019) Salt-stress induced proteomic changes of two contrasting alfalfa cultivars during germination stage. J Sci Food Agric 99:1384–1396

    Article  CAS  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gondim FA, Gomes-Filho E, Costa JH, Alencar M, N.L. and Prisco JT (2012) Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. Plant Physiol Biochem 56:62–71

    Article  CAS  PubMed  Google Scholar 

  • Guan Q, Liao X, He M, Li X, Wang Z, Ma H, Yu S, Liu S (2017) Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO3 stress. PLoS One 12:e0186052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Shi G, Guo X, Zhang L, Xu W, Wang Y, Su Z, Hua J (2015) Transcriptome analysis reveals that distinct metabolic pathways operate in salt-tolerant and salt-sensitive upland cotton varieties subjected to salinity stress. Plant Sci 238:33–45

    Article  CAS  PubMed  Google Scholar 

  • Hayashi H, Murata N (1998) Genetically engineered enhancement of salt tolerance in higher plants, stress responses of photosynthetic organisms. Elsevier, Amsterdam, pp 133–148

    Book  Google Scholar 

  • Hichri I, Muhovski Y, Zizkova E, Dobrev PI, Gharbi E, Franco-Zorrilla JM, Lopez-Vidriero I, Solano R, Clippe A, Errachid A, Motyka V, Lutts S (2017) The Solanum lycopersicum WRKY3 transcription factor SlWRKY3 is involved in salt stress tolerance in tomato. Front Plant Sci 8:1343

    Article  PubMed  PubMed Central  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hückelhoven R, Fodor J, Preis C, Kogel K-H (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol 119:1251–1260

    Article  PubMed  PubMed Central  Google Scholar 

  • Ji C, Mao X, Hao J, Wang X, Xue J, Cui H, Li R (2018) Analysis of bZIP transcription factor family and their expressions under salt stress in Chlamydomonas reinhardtii. Int J Mol Sci 19:2800

    Article  CAS  PubMed Central  Google Scholar 

  • Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  PubMed  Google Scholar 

  • Karanja BK, Xu L, Wang Y, Muleke EM, Jabir BM, Xie Y, Zhu X, Cheng W, Liu L (2017) Genome-wide characterization and expression profiling of NAC transcription factor genes under abiotic stresses in radish (Raphanus sativus L.). PeerJ 5, e4172

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leah R, Tommerup H, Svendsen I, Mundy J (1991) Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J Biol Chem 266:1564–1573

    CAS  PubMed  Google Scholar 

  • Li P, Cao W, Fang H, Xu S, Yin S, Zhang Y, Lin D, Wang J, Chen Y, Xu C, Yang Z (2017) Transcriptomic profiling of the maize (Zea mays L.) leaf response to abiotic stresses at the seedling stage. Front Plant Sci 8:290

    PubMed  PubMed Central  Google Scholar 

  • Li P, Yang H, Liu G, Ma W, Li C, Huo H, He J, Liu L (2018) PpSARK regulates moss senescence and salt tolerance through ABA related pathway. Int J Mol Sci. https://doi.org/10.3390/ijms19092609

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang MH, Jiang JG (2017) Analysis of carotenogenic genes promoters and WRKY transcription factors in response to salt stress in Dunaliella bardawil. Sci Rep 7:37025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci 98:4782–4787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu X, Zhang X, Duan H, Lian C, Yin W, Xia X (2018) Three stress-responsive NAC transcription factors from Populus euphratica differentially regulate salt and drought tolerance in transgenic plants. Physiol Plant 162:73–97

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Molina A, Görlach J, Volrath S, Ryals J (1999) Wheat genes encoding two types of PR-1 proteins are pathogen inducible, but do not respond to activators of systemic acquired resistance. Mol Plant Microbe Interact 12:53–58

    Article  CAS  PubMed  Google Scholar 

  • Mostek A, Borner A, Weidner S (2016) Comparative proteomic analysis of beta-aminobutyric acid-mediated alleviation of salt stress in barley. Plant Physiol Biochem 99:150–161

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970

    Article  CAS  PubMed  Google Scholar 

  • Natali L, Vangelisti A, Guidi L, Remorini D, Cotrozzi L, Lorenzini G, Nali C, Pellegrini E, Trivellini A, Vernieri P, Landi M, Cavallini A, Giordani T (2018) How Quercus ilex L. saplings face combined salt and ozone stress: a transcriptome analysis. BMC Genom 19:872

    Article  CAS  Google Scholar 

  • Peng Z, He S, Gong W, Sun J, Pan Z, Xu F, Lu Y, Du X (2014) Comprehensive analysis of differentially expressed genes and transcriptional regulation induced by salt stress in two contrasting cotton genotypes. BMC Genom 15:760

    Article  CAS  Google Scholar 

  • Pilarska M, Wiciarz M, Jajic I, Kozieradzka-Kiszkurno M, Dobrev P, Vankova R, Niewiadomska E (2016) A different pattern of production and scavenging of reactive oxygen species in halophytic Eutrema salsugineum (Thellungiella salsuginea) plants in comparison to arabidopsis thaliana and its relation to salt stress signaling. Front Plant Sci 7:1179

    Article  PubMed  PubMed Central  Google Scholar 

  • Qing DJ, Lu HF, Li N, Dong HT, Dong DF, Li YZ (2009) Comparative profiles of gene expression in leaves and roots of maize seedlings under conditions of salt stress and the removal of salt stress. Plant Cell Physiol 50:889–903

    Article  CAS  PubMed  Google Scholar 

  • Rong L, Li Q, Li S, Tang L, Wen J (2016) De novo transcriptome sequencing of Acer palmatum and comprehensive analysis of differentially expressed genes under salt stress in two contrasting genotypes. Mol Genet Genom 291:575–586

    Article  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Shen Z, Yao J, Sun J, Chang L, Wang S, Ding M, Qian Z, Zhang H, Zhao N, Sa G, Hou P, Lang T, Wang F, Zhao R, Shen X, Chen S (2015) Populus euphratica HSF binds the promoter of WRKY1 to enhance salt tolerance. Plant Sci 235:89–100

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Liu W, Yao Y, Wei Y, Chan Z (2017) Alcohol dehydrogenase 1 (ADH1) confers both abiotic and biotic stress resistance in Arabidopsis. Plant Sci 262:24–31

    Article  CAS  PubMed  Google Scholar 

  • Swarup R, Kargul J, Marchant A, Zadik D, Rahman A, Mills R, Yemm A, May S, Williams L, Millner P, Tsurumi S, Moore I, Napier R, Kerr ID, Bennett MJ (2004) Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16:3069–3083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang N, Zhang H, Li X, Xiao J, Xiong L (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang T, Yu A, Li P, Yang H, Liu G, Liu L (2016) Sequence analysis of the Hsp70 family in moss and evaluation of their functions in abiotic stress responses. Sci Rep 6:33650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Miyazaki S, Kawai K, Deyholos M, Galbraith DW, Bohnert HJ (2003) Temporal progression of gene expression responses to salt shock in maize roots. Plant Mol Biol 52:873–891

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Bai Y, Shen C, Wu Y, Zhang S, Jiang D, Guilfoyle TJ, Chen M, Qi Y (2010) Auxin-related gene families in abiotic stress response in Sorghum bicolor. Funct Integr Genom 10:533–546

    Article  CAS  Google Scholar 

  • Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang R, Yang T, Zhang H, Qi Y, Xing Y, Zhang N, Li R, Weeda S, Ren S, Ouyang B, Guo YD (2014) Hormone profiling and transcription analysis reveal a major role of ABA in tomato salt tolerance. Plant Physiol Biochem 77:23–34

    Article  CAS  PubMed  Google Scholar 

  • Ying S, Zhang DF, Fu J, Shi YS, Song YC, Wang TY, Li Y (2012) Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta 235:253–266

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Ni Z, Chen Q, Qu Y (2017) The wheat salinity-induced R2R3-MYB transcription factor TaSIM confers salt stress tolerance in Arabidopsis thaliana. Biochem Biophys Res Commun 491:642–648

    Article  CAS  PubMed  Google Scholar 

  • Zaharieva T, Yamashita K, Matsumoto H (1999) Iron deficiency induced changes in ascorbate content and enzyme activities related to ascorbate metabolism in cucumber roots. Plant Cell Physiol 40:273–280

    Article  CAS  Google Scholar 

  • Zhang D, Jiang S, Pan J, Kong X, Zhou Y, Liu Y, Li D (2014) The overexpression of a maize mitogen-activated protein kinase gene (ZmMPK5) confers salt stress tolerance and induces defence responses in tobacco. Plant Biol (Stuttg) 16:558–570

    Article  CAS  Google Scholar 

  • Zhang F, Li L, Jiao Z, Chen Y, Liu H, Chen X, Fu J, Wang G, Zheng J (2016) Characterization of the calcineurin B-Like (CBL) gene family in maize and functional analysis of ZmCBL9 under abscisic acid and abiotic stress treatments. Plant Sci 253:118–129

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Li X, He Y, Zhang J, Yan T, Liu X (2017) Physiological investigation of C4-phosphoenolpyruvate-carboxylase-introduced rice line shows that sucrose metabolism is involved in the improved drought tolerance. Plant Physiol Biochem 115:328–342

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Jiang J, Li K, Liu G (2017) Populus simonii × Populus nigra WRKY70 is involved in salt stress and leaf blight disease responses. Tree Physiol 37:827–844

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The materials were collected from the Maize Research Institute of Heilongjiang Academy of Agricultural Sciences. This work was partially supported by Grants from the National Science and Technology Support Plan of China (2013BAD07B01); the Innovation Project of Heilongjiang Academy of Agricultural Science (2014ZD003); the Open Project of the Experimental Station of Crop Cultivation and Observation in Northeast China, Northeast Agricultural University of China; Heilongjiang Acamedy of Agricultural Sciences Postdoctoral Programme; the Ministry of Agriculture Genetically Modified Major Project of China (SQ2016ZD080034); and the National Key Research and Development Plan of China (2016YFD0100103, 2017YFD0300502 and 2017YFD0300506).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kejun Yang.

Additional information

Publisher’s Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1. Sequences of eight gene-specific primers and primers for one internal reference gene (18S rDNA) (DOCX 17 KB)

13258_2019_793_MOESM2_ESM.xls

Table S2. Morphological indexes from the assay of 242 maize inbred lines under salty and normal conditions at the germination stage (XLS 157 KB)

13258_2019_793_MOESM3_ESM.xls

Table S3. Morphological indexes from the assay of 242 maize inbred lines under salty and normal conditions at the seedling stage (XLS 166 KB)

Table S4. DEGs in the salt-sensitive maize variety (L29) in response to salt stress (XLSX 1016 KB)

Table S5. DEGs in the salt-tolerant maize variety (L87) in response to salt stress (XLSX 1763 KB)

13258_2019_793_MOESM6_ESM.xlsx

Table S6. GO enrichment of upregulated DEGs of the salt-sensitive maize variety (L29) in response to salt stress (XLSX 161 KB)

13258_2019_793_MOESM7_ESM.xlsx

Table S7. GO enrichment of downregulated DEGs of the salt-sensitive maize variety (L29) in response to salt stress (XLSX 138 KB)

13258_2019_793_MOESM8_ESM.xlsx

Table S8. GO enrichment of upregulated DEGs of the salt-tolerant maize variety (L87) in response to salt stress (XLSX 283 KB)

13258_2019_793_MOESM9_ESM.xlsx

Table S9. GO enrichment of downregulated DEGs of the salt-tolerant maize variety (L87) in response to salt stress (XLSX 257 KB)

13258_2019_793_MOESM10_ESM.xlsx

Table S10. KEGG enrichment of upregulated DEGs of the salt-sensitive maize variety (L29) in response to salt stress (XLSX 28 KB)

13258_2019_793_MOESM11_ESM.xlsx

Table S11. KEGG enrichment of downregulated DEGs of the salt-sensitive maize variety (L29) in response to salt stress (XLSX 23 KB)

13258_2019_793_MOESM12_ESM.xlsx

Table S12. KEGG enrichment of upregulated DEGs of the salt-tolerant maize variety (L87) in response to salt stress (XLSX 38 KB)

13258_2019_793_MOESM13_ESM.xlsx

Table S13. KEGG enrichment of downregulated DEGs of the salt-tolerant maize variety (L87) in response to salt stress (XLSX 30 KB)

Table S14. The DEGs involved in phytohormone biosynthesis in the two cultivars (XLSX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, M., Wang, Y., Zhang, Y. et al. Comparative transcriptome analysis of salt-sensitive and salt-tolerant maize reveals potential mechanisms to enhance salt resistance. Genes Genom 41, 781–801 (2019). https://doi.org/10.1007/s13258-019-00793-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-019-00793-y

Keywords

Navigation