Skip to main content
SpringerLink
Log in

Transcriptome analysis reveals translational regulation in barley microspore-derived embryogenic callus under salt stress

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Transcriptome analysis of barley embryogenic callus from isolated microspore culture under salt stress uncovered a role of translation inhibition and selective activation of stress-specific proteins in cellular defense.

Abstract

Soil salinity is one of the major abiotic stresses which constrains the plant growth and reduces the productivity of field crops. In this study, it was observed that the salt stress in barley isolated microspore culture impacted not only on the quantity of embryogenic callus but also on the quality for later differentiation. The barley microspore-derived embryogenic callus, a transient intermediate form linked cells and plants, was employed for a global transcriptome analysis by RNA sequencing to provide new insights into the cellular adaptation or acclimation to stress. A total of 596 differentially expressed genes (DEGs) were identified, in which 123 DEGs were up-regulated and 473 DEGs were down-regulated in the embryogenic callus produced from microspore culture under salt stress as compared to the control conditions. KEGG pathway analysis identified ‘translation’ (27 DEGs; 12.56 %) as the largest group and followed by ‘folding, sorting and degradation’ (25 DEGs; 11.63 %) in 215 mapped metabolic pathways. The results of RNA-Seq data and quantitative real-time polymerase chain reaction validation showed that the genes related to translation regulation (such as eIF1A, RPLP0, RPLP2, VARS) were down-regulated to control general protein synthesis, and the genes related to endoplasmic reticulum stress response (such as small heat shock protein genes) were selectively up-regulated against protein denaturing during microspore embryogenesis under continuous salt stress. These transcriptional remodeling might affect the essential protein synthesis for the cell development to fulfill totipotency under salt stress.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ashraf M, Athar HR, Harris PJC, Kwon TR (2008) Some prospective strategies for improving crop salt tolerance. Adv Agron 97:45–110

    Article  CAS  Google Scholar 

  • Berg M, Rogers R, Muralla R, Meinke D (2005) Requirement of aminoacyl—tRNA synthetases for gametogenesis and embryo development in Arabidopsis. Plant J 44:866–878

    Article  CAS  PubMed  Google Scholar 

  • Chang F, Wang Y, Wang S, Ma H (2011) Molecular control of microsporogenesis in Arabidopsis. Curr Opin Plant Biol 14:66–73

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Lin S, Liu Q, Huang J, Zhang W, Lin J, Wang Y, Ke Y, He H (2014) Expression and interaction of small heat shock proteins (sHsps) in rice in response to heat stress. Biochim Biophys Acta 1844:818–828

    Article  CAS  PubMed  Google Scholar 

  • Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodall AJ, Kumar P, Tobin AK (2013) Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.). Plant Cell Physiol 54:492–505

    Article  CAS  PubMed  Google Scholar 

  • Haslbeck M, Vierling E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 427:1537–1548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosp J, Tashpulatov A, Roessner U, Barsova E, Katholnigg H, Steinborn R, Melikant B, Lukyanov S, Heberle-Bors E, Touraev A (2007) Transcriptional and metabolic profiles of stress-induced, embryogenic tobacco microspores. Plant Mol Biol 63:137–149

    Article  CAS  PubMed  Google Scholar 

  • Islam SMS, Tuteja N (2012) Enhancement of androgenesis by abiotic stress and other pretreatments in major crop species. Plant Sci 182:134–144

    Article  CAS  PubMed  Google Scholar 

  • Jain SM (2001) Tissue culture-derived variation in crop improvement. Euphytica 118:153–166

    Article  CAS  Google Scholar 

  • Lavania D, Dhingra A, Siddiqui MH, Al-Whaibi MH, Grover A (2015) Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant Physiol Biochem 86:100–108

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lu R, Wang YF, Sun YF, Shan LL, Chen PD, Huang JH (2008) Improvement of isolated microspore culture of barley (Hordeum vulgare L.): the effect of floret co-culture. Plant Cell Tissue Organ 93:21–27

    Article  Google Scholar 

  • Maraschin SF, de Priester W, Spaink HP, Wang M (2005) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56:1711–1726

    Article  CAS  PubMed  Google Scholar 

  • Maraschin SF, Caspers M, Potokina E, Wülfert F, Graner A, Spaink HP, Wang M (2006) cDNA array analysis of stress-induced gene expression in barley androgenesis. Physiol Plantarum 127:535–550

    Article  CAS  Google Scholar 

  • Mayer KF, Waugh R, Brown JW, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, Wise RP, Stein N, International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716

    CAS  PubMed  Google Scholar 

  • Mohammad AO, Nooshin O, Farajollah SA, Zoran N, Bernd MR (2012) Effect of salt stress on genes encoding translation-associated proteins in Arabidopsis thaliana. Plant Signal Behav 7:1095–1102

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Exp Bot 71:89–98

    Article  Google Scholar 

  • Rausell A, Kanhonou R, Yenush L, Serrano R, Ros R (2003) The translation initiation factor eIF1A is an important determinant in the tolerance to NaCl stress in yeast and plants. Plant J 34:257–267

    Article  CAS  PubMed  Google Scholar 

  • Rout G, Senapati S, Panda J (2008) Selection of salt tolerant plants of Nicotiana tabacum L. through in vitro and its biochemical characterization. Acta Biol Hung 59(1):77–92

    Article  CAS  PubMed  Google Scholar 

  • Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124

    Article  CAS  PubMed  Google Scholar 

  • Ruibal C, Castro A, Carballo V, Szabados L, Vidal S (2013) Recovery from heat, salt and osmotic stress in Physcomitrella patens requires a functional small heat shock protein PpHsp16.4. BMC Plant Biol 13:56–60

    Article  Google Scholar 

  • Sánchez-Díaz RA, Castillo AM, Vallés MP (2013) Microspore embryogenesis in wheat: new marker genes for early, middle and late stages of embryo development. Plant Reprod 26:287–296

    Article  PubMed  Google Scholar 

  • Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genom 10:1–18

    Article  Google Scholar 

  • Seguí-Simarro JM, Corral-Martínez P, Corredor E, Raska I, Testillano PS, Risueño MC (2011) A change of developmental program induces the remodeling of the interchromatin domain during microspore embryogenesis in Brassica napus L. J Plant Physiol 168:746–757

    Article  PubMed  Google Scholar 

  • Shankhdhar D, Shankhdhar SC, Mani RC (2000) In vitro selection for salt tolerance in rice. Biol Plantarum 43:477–480

    Article  CAS  Google Scholar 

  • Shannon MC (1998) Adaptation of plants to salinity. Adv Agron 60:75–119

    Article  Google Scholar 

  • Soriano M, Li H, Boutilier K (2013) Microspore embryogenesis: establishment of embryo identity and pattern in culture. Plant Reprod 26:181–196

    Article  PubMed  PubMed Central  Google Scholar 

  • Touraev A, Vicente O, Heberle-Bors E (1997) Initiation of microspore embryogenesis by stress. Trends Plant Sci 2:297–302

    Article  Google Scholar 

  • Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J 274:1152–1171

    Article  CAS  PubMed  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Biol 42:579–620

    Article  CAS  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Lan P, Gao H, Zheng L, Li W, Schmidt W (2013) Expression changes of ribosomal proteins in phosphate-and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genom 14:783

    Article  CAS  Google Scholar 

  • Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64:391–403

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  CAS  PubMed  Google Scholar 

  • Zhang JL, Shi HZ (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115:1–22

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Shono M, Sun A, Yi S, Li M, Liu J (2007) Constitutive expression of an endoplasmic reticulum small heat shock protein alleviates endoplasmic reticulum stress in transgenic tomato. J Plant Physiol 164:835–841

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Natural Science Foundation of Shanghai (15ZR1436600) and China Agriculture Research System (CARS-05).

Author information

Authors and Affiliations

  1. Biotech Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, 201106, China

    Cheng-hong Liu, Rui-ju Lu, Gui-mei Guo, Ting He, Ying-bo Li, Hong-wei Xu, Run-hong Gao, Zhi-wei Chen & Jian-hua Huang

  2. Shanghai Key Laboratory of Agricultural Genetics and Breeding, Shanghai, 201106, China

    Cheng-hong Liu, Rui-ju Lu, Gui-mei Guo, Ting He, Ying-bo Li, Hong-wei Xu, Run-hong Gao, Zhi-wei Chen & Jian-hua Huang

Authors
  1. Cheng-hong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rui-ju Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gui-mei Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ting He
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ying-bo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hong-wei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Run-hong Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhi-wei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jian-hua Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian-hua Huang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by N. Sreenivasulu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Ch., Lu, Rj., Guo, Gm. et al. Transcriptome analysis reveals translational regulation in barley microspore-derived embryogenic callus under salt stress. Plant Cell Rep 35, 1719–1728 (2016). https://doi.org/10.1007/s00299-016-1986-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-1986-y

Keywords

Search

Navigation