Skip to main content
Log in

Physiological and transcriptional response to heat stress in heat-resistant and heat-sensitive maize (Zea mays L.) inbred lines at seedling stage

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

To understand the molecular and physiological mechanism underlying the heat stress in maize, transcriptional and physiological response to heat stress in the heat-resistant Huangzaosi (HZS) and heat-sensitive Lv-9-Kuan (L9K) inbred lines at seedling stage were analyzed and compared at seedling stage. Our results indicated that MDA content of the two inbred lines increased significantly under heat stress; the values of MDA in L9K was significantly higher than that in HZS. The level of SOD, CAT, and POD enzyme activities in HZS was higher than those in L9K for both the heat-treated group and controls. The values of Fv/Fm, qP, and ФPSII reduced by heat stress in L9K were higher than the respective values in HZS. RNA-seq data showed that heat stress induced more heat stress-related genes in HZS (257 heat stress-related genes) than in L9K (224 heat stress-related genes). GO and KEGG enrichment analyses indicated that HZS and L9K changed their physiological and biochemical mechanisms in response to heat stress through different molecular mechanisms. Weighted Gene Co-expression Network Analysis showed that HZS might obtain stronger heat resistance than L9K through a unique transcriptional regulatory network. Our findings provide insights into the molecular networks that mediate the tolerance of maize heat stress and also help us to mine key heat stress-related genes.

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

Similar content being viewed by others

Abbreviations

SOD:

Superoxide dismutase

CAT:

Catalase

MDA:

Malondialdehyde

PRO:

Proline

GSH:

Glutathione

APX:

Ascorbate peroxidase

POD:

Peroxidase

GO:

Gene ontology

KEGG:

Kyoto Encyclopedia of Genes and Genome

DEG:

Differentially expressed gene

qPCR:

Quantitative PCR

FC:

Fold change

BP:

Biological process

CC:

Cellular component

MF:

Molecular function

MAPK:

Mitogen-activated protein kinase

CDPK:

Calcium-dependent protein kinase

TF:

Transcriptional factor

HSP:

Heat shock protein

ROS:

Reactive oxygen species

WGCNA:

Weighted gene co-expression network analysis

References

  • Battisti DS, Naylor RL (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323(5911):240–244. https://doi.org/10.1126/science.1164363

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Gu Z, Xin D, Hao L, Liu C, Huang J, Ma B, Zhang H (2011) Identification and characterization of putative CIPK genes in maize. J Genet Genomics 38(2):77–87. https://doi.org/10.1016/j.jcg.2011.01.005

    Article  CAS  PubMed  Google Scholar 

  • Crafts-Brandner JS (2002) Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiol 129(4):1773–1780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daisuke O, Kazuo Y, Takumi N (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 12:12

    Google Scholar 

  • Dewey CN, Li B (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12(1):323–323

    Google Scholar 

  • Ding Y, Robinson DG, Jiang L (2014) Unconventional protein secretion (UPS) pathways in plants. Curr Opin Cell Biol 29:107–115. https://doi.org/10.1016/j.ceb.2014.05.008

    Article  CAS  PubMed  Google Scholar 

  • Downs GS, Bi YM, Colasanti J, Wu W, Chen X, Zhu T, Rothstein SJ, Lukens LN (2013) A developmental transcriptional network for maize defines coexpression modules. Plant Physiol 161(4):1830–1843. https://doi.org/10.1104/pp.112.213231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng G, Huang C (2009) Improvement and utilization of the red bone germplasm of Luda. J Maize Sci 17(05):55–57

    Google Scholar 

  • Feng W, Xiaozhu W, Tongjian L, Mingliang J, Xinshen L, Peng L, Xiaojian Z, Xinxin J, Xiaomin Y, Keqiang W (2009) Genome-wide survey of heat shock factors and heat shock protein 70s and their regulatory network under abiotic stresses in Brachypodium distachyon. Plos One 12(7):e0180352

    Google Scholar 

  • Frey FP, Urbany C, Hüttel B, Reinhardt R, Stich B (2015) Genome-wide expression profiling and phenotypic evaluation of European maize inbreds at seedling stage in response to heat stress. BMC Genomics 16(1):123

    PubMed  PubMed Central  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophysi Acta 990(1):87–92

    CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14(5):9643–9684. https://doi.org/10.3390/ijms14059643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou K, Wu W, Gan S-S (2013) SAUR36, a SMALL AUXIN UP RNA gene, is involved in the promotion of leaf senescence in Arabidopsis. Plant Physiol 161(2):1002–1009

    CAS  PubMed  Google Scholar 

  • Hu X, Wu L, Zhao F, Zhang D, Li N, Zhu G, Li C, Wang W (2015a) Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress. Front Plant Sci 6:298. https://doi.org/10.3389/fpls.2015.00298

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu X, Yang Y, Gong F, Zhang D, Zhang L, Wu L, Li C, Wang W (2015b) Protein sHSP26 improves chloroplast performance under heat stress by interacting with specific chloroplast proteins in maize (Zea mays). J Proteomics 115:81–92

    CAS  PubMed  Google Scholar 

  • Jiang Y, Zheng Q, Chen L, Liang Y, Wu J (2018) Ectopic overexpression of maize heat shock transcription factor gene ZmHsf04 confers increased thermo and salt-stress tolerance in transgenic Arabidopsis. Acta Physiol Plant 40(1). https://doi.org/10.1007/s11738-017-2587-2

  • Kant S, Rothstein S (2009) Auxin-responsive SAUR39 gene modulates auxin level in rice. Plant Signal Behav 4(12):1174–1175

    PubMed  PubMed Central  Google Scholar 

  • Kim JH, Kim WT (2013) The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses. Plant Physiol 162(3):1733–1749. https://doi.org/10.1104/pp.113.220103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–U121. https://doi.org/10.1038/nmeth.3317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotak S, Larkindale J, Lee U, Koskull-Doring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10(3):310–316

    CAS  PubMed  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63(4):1593–1608. https://doi.org/10.1093/jxb/err460

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Gupta D, Nayyar H (2012) Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. Acta Physiol Plant 34(1):75–86

    CAS  Google Scholar 

  • Landry J, Chretien P, Lambert H, Hickey E, Weber LA (1989) Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J Cell Biol 109(1):7–15. https://doi.org/10.1083/jcb.109.1.7

    Article  CAS  PubMed  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinform 9:559. https://doi.org/10.1186/1471-2105-9-559

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–U354. https://doi.org/10.1038/nmeth.1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li HS, Sun Q, Zhao SJ (2000) The experiment principle and technique on plant physiology and biochemistry. Higher Education Press, Beijing

    Google Scholar 

  • Li C, Song W, Luo Y, Gao S, Zhang R, Shi Z, Wang X, Wang R, Wang F, Wang J, Zhao Y, Su A, Wang S, Li X, Luo M, Wang S, Zhang Y, Ge J, Zhao JR (2019a) The HuangZaoSi maize genome provides insights into genomic variation and improvement history of maize. Mol Plant 12(3):402–409

    CAS  PubMed  Google Scholar 

  • Li GL, Zhang HN, Shao H, Wang GY, Zhang YY, Zhang YJ, Zhao LN, Guo XL, Sheteiwy MS (2019b) ZmHsf05, a new heat shock transcription factor from Zea mays L. improves thermotolerance in Arabidopsis thaliana and rescues thermotolerance defects of the athsfa2 mutant. Plant Sci 283:375–384. https://doi.org/10.1016/j.plantsci.2019.03.002

    Article  CAS  PubMed  Google Scholar 

  • Liu HC, Charng YY (2013) Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol 163(1):276–290. https://doi.org/10.1104/pp.113.221168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu HC, Liao H-T, Charng Y-Y (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ 34(5):738–751

    CAS  PubMed  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. https://doi.org/10.1186/s13059-014-0550-8

  • Lu C (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J Exp Bot 54(383):851–860

    CAS  PubMed  Google Scholar 

  • Lund AA, Rhoads DM, Lund AL, Cerny RL, Elthon TE (2001) In vivo modifications of the maize mitochondrial small heat stress protein, HSP22. J Biol Chem 276(32):29924–29929

    CAS  PubMed  Google Scholar 

  • Lv W-T, Lin B, Zhang M, Hua X-J (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Amino Acids 41:S69–S69

    Google Scholar 

  • Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63(2):599–616. https://doi.org/10.1093/jxb/err310

    Article  CAS  PubMed  Google Scholar 

  • Mishra KS (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Develop 16(12):1555–1567

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra A, Heyer AG, Mishra KB (2014) Chlorophyll fluorescence emission can screen cold tolerance of cold acclimatedArabidopsis thalianaaccessions. Plant Methods 10(1):38

    PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149(1):88–95

    CAS  PubMed  PubMed Central  Google Scholar 

  • Patino LH, Ramírez JD (2017) RNA-seq in kinetoplastids: a powerful tool for the understanding of the biology and host-pathogen interactions. Infection Genet Evol 49:273–282

    CAS  Google Scholar 

  • Romeis T, Weckwerth P, Ehlert B (2015) ZmCPK1, a calcium-independent kinase member of the Zea mays CDPK gene family, functions as a negative regulator in cold stress signalling. Plant Cell Environ 38(3):544–558

    PubMed  Google Scholar 

  • Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, Goloubinoff P (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21(9):2829–2843. https://doi.org/10.1105/tpc.108.065318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savicka M, Škute N (2010) Effects of high temperature on malondialdehyde content, superoxide production and growth changes in wheat seedlings (Triticum aestivum L.). Ekologija 56:26–33

    CAS  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J, Yan B, Lou X, Ma H, Ruan S (2017) Comparative transcriptome analysis reveals the transcriptional alterations in heat-resistant and heat-sensitive sweet maize (Zea mays L.) varieties under heat stress. BMC Plant Biol 17(1):26

    PubMed  PubMed Central  Google Scholar 

  • Snider JL, Oosterhuis DM, Kawakami EM (2010) Genotypic differences in thermotolerance are dependent upon prestress capacity for antioxidant protection of the photosynthetic apparatus in Gossypium hirsutum. Physiol Plant 138(3):268–277

    CAS  PubMed  Google Scholar 

  • Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inze D, Peer WA, Murphy AS, Overvoorde PJ, Gray WM (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70(6):978–990. https://doi.org/10.1111/j.1365-313X.2012.04946.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suwa R, Hakata H, Hara H, El-Shemy HA, Adu-Gyamfi JJ, Nguyen NT, Kanai S, Lightfoot DA, Mohapatra PK, Fujita K (2010) High temperature effects on photosynthate partitioning and sugar metabolism during ear expansion in maize (Zea mays L.) genotypes. Plant Physiol Biochem 48(2-3):124–130

    CAS  PubMed  Google Scholar 

  • Torun H (2019) Time-course analysis of salicylic acid effects on ROS regulation and antioxidant defense in roots of hulled and hulless barley under combined stress of drought, heat and salinity. Physiol Plant 165(2):169–182. https://doi.org/10.1111/ppl.12798

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui T, Kato W, Asada Y, Sako K, Sato T, Sonoda Y, Kidokoro S, Yamaguchi-Shinozaki K, Tamaoki M, Arakawa K, Ichikawa T, Nakazawa M, Seki M, Shinozaki K, Matsui M, Ikeda A, Yamaguchi J (2009) DEAR1, a transcriptional repressor of DREB protein that mediates plant defense and freezing stress responses in Arabidopsis. J Plant Res 122(6):633–643. https://doi.org/10.1007/s10265-009-0252-6

    Article  CAS  PubMed  Google Scholar 

  • Wan B, Lin Y, Mou T (2007) Expression of rice Ca(2+)-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581(6):1179–1189

    CAS  PubMed  Google Scholar 

  • Wang G, Zhu Q, Meng Q, Wu C (2012) Transcript profiling during salt stress of young cotton (Gossypium hirsutum) seedlings via Solexa sequencing. Acta Physiol Plant 34(1):107–115

    Google Scholar 

  • Wang X, Jing XQ, Wang XJ (2015) Analysis of utilization potential of lvdahonggu germplasm in maize breeding in China. Liaoning Agricul Sci 2:42–45

    Google Scholar 

  • Wang H, Wang H, Shao H, Tang X (2016) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:67. https://doi.org/10.3389/fpls.2016.00067

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang CT, Ru JN, Liu YW, Li M, Zhao D, Yang JF, Fu JD, Xu ZS (2018) Maize WRKY transcription factor ZmWRKY106 confers drought and heat tolerance in transgenic plants. Int J Mol Sci 19(10). https://doi.org/10.3390/ijms19103046

  • Wu L, Zu X, Zhang H, Wu L, Chen Y (2015) Overexpression of ZmMAPK1 enhances drought and heat stress in transgenic Arabidopsis thaliana. Plant Mol Biol 88(4):429–443

    CAS  PubMed  Google Scholar 

  • Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56(3):274–285. https://doi.org/10.1016/j.envexpbot.2005.03.002

    Article  CAS  Google Scholar 

  • Yan N (2013) Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem Sci 38(3):151–159. https://doi.org/10.1016/j.tibs.2013.01.003

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P (2017) Temperature increase reduces global yields of major crops in four independent estimates. Proc Natl Acad Sci:201701762

  • Zheng J, Cui S, Li H (1995) Studies on feasibility for utilization of improved lines of maize Huangzao:4

  • Zheng J, Fu J, Gou M, Huai J, Liu Y, Jian M, Huang Q, Guo X, Dong Z, Wang H (2010) Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Mol Biol 72(4-5):407–421

    CAS  PubMed  Google Scholar 

Download references

Author contribution statement

DCW and GS conceived and designed research. JFZ, ZZS, WW, CY, and SBX conducted experiments. DW, CYW, and ZRD contributed new reagents or analytical tools. DCW and JFZ analyzed data and wrote the manuscript. GS edited the manuscript. All authors read and approved the manuscript.

Funding

This study was financially supported by the National Key Research and Development Program (2017YFD0300402-3, 2016YFD0300205-03), Anhui Natural Science Foundation (S202002b04020579), Anhui Province’s Fund for Introducing Leading Talents from Universities.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Genlou Sun.

Ethics declarations

Competing interests

This manuscript or substantial parts of it, submitted to the journal, has not be under consideration by any other journal. No material submitted as part of a manuscript infringes existing copyrights, or the rights of a third party. All authors have approved the manuscript. The authors declare that they have no conflict interest.

Additional information

Handling Editor: Bhumi Nath Tripathi

Publisher’s note

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

Electronic supplementary material

ESM 1

(XLS 217 kb)

ESM 2

(DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, DC., Zhu, JF., Shu, ZZ. et al. Physiological and transcriptional response to heat stress in heat-resistant and heat-sensitive maize (Zea mays L.) inbred lines at seedling stage. Protoplasma 257, 1615–1637 (2020). https://doi.org/10.1007/s00709-020-01538-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-020-01538-5

Keywords

Navigation