Skip to main content
Log in

Abiotic stress-related genes governing signal transduction cascades in wild plants with emphasis to those in Hordeum spontaneum

  • Review Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The study aims at discussing abiotic stress-related genes and metabolites in the crosstalking signal transduction pathways with emphasis to those in leaves of wild barley Hordeum spontaneum. Selected pathways involve tryptophan and target of rapamycin (or TOR) complex as core metabolites. In H. spontaneum, route towards tryptophan production seems to be mediated via anthranilate synthase acting as a master switch. Downstream auxin-related factors and proteins can secure plant’s ability to maintain proper growth rates and stress tolerance. Detected TOR in H. spontaneum participates in several signal transduction related pathways with a central role in nutrient starvation, ribosome biogenesis and protein synthesis and in standing oxidative and other abiotic stresses. TOR also participates as a master regulator of lifespan, aging and autophagy in H. spontaneum to regulate growth and maintain plant yield and its attributes under stress conditions. In conclusion, the present study emphasizes some mechanisms by which wild plant species, e.g., H. spontaneum, utilize to cope with abiotic stresses.

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

Similar content being viewed by others

Data availability

Supplemental data can be accessed at: https://drive.google.com/drive/folders/1yVB2zFSwacYCB5_2wrP34skSxD7GoxET?usp=sharing.

Abbreviations

AMPK:

AMP-activated protein kinase

ARFs:

Auxin response factors

AUX:

Auxin

eIF3:

Eukaryotic translation initiation factor 3 h

eIF4E:

Eukaryotic initiation factor 4E

ETC:

Electron transport chain

GH3:

Gretchen Hagen 3

H. spontaneum :

Hordeum spontaneum

HEAT:

Huntington, elongation factor 3 regulatory

IAA:

Indole acetic acid

JA:

Jasmonic acid

KEGG:

Kyoto encyclopedia of genes and genomes

PA:

Phosphatidic acid

PIKK:

Phosphatidylinositol 3-kinase-related kinase

PLD:

Phospholipase D

RAPTOR:

Regulatory-associated protein of TOR

RICTOR:

Rapamycin-insensitive companion of TOR

RPF:

Reinitiation-promoting factor

S6K:

S6 kinase

SA:

Salicylic acid

SnRK1:

Snf1-related kinase 1

TOR:

Target of rapamycin

UCP1:

Uncoupling protein 1

WMV:

Watermelon mosaic virus

References

  • Abulfaraj (2020) Stepwise signal transduction cascades under salt stress in leaves of wild barley (Hordeum spontaneum). Biotechnol Biotechnol Equip 34(1):860–872

    Google Scholar 

  • Aznar NR, Consolo VF, Salerno GL, Martínez-Noël GMA (2018) TOR signaling downregulation increases resistance to the cereal killer Fusarium graminearum. Plant Signal Behav 13:e1414120

    PubMed  PubMed Central  Google Scholar 

  • Baena-González E, Hanson J (2017) Shaping plant development through the SnRK1-TOR metabolic regulators. Curr Opin Plant Biol 35:152–157

    PubMed  Google Scholar 

  • Bahieldin A, Atef A, Sabir JSM et al (2015) RNA-seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress. C R Biol 338:285–297

    PubMed  Google Scholar 

  • Bakshi A, Moin M, Kumar MU et al (2017) Ectopic expression of Arabidopsis target of rapamycin (AtTOR) improves water-use efficiency and yield potential in rice. Sci Rep 7:42835

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caldana C, Martins MCM, Mubeen U, Urrea-Castellanos R (2019) The magic ‘hammer’ of TOR: the multiple faces of a single pathway in the metabolic regulation of plant growth and development. J Exp Bot 70:2217–2225

    CAS  PubMed  Google Scholar 

  • De Vleesschauwer D, Filipe O, Hoffman G et al (2018) Target of rapamycin signaling orchestrates growth-defense trade-offs in plants. New Phytol 217:305–319

    PubMed  Google Scholar 

  • Deprost D, Yao L, Sormani R et al (2016) TOR signaling and nutrient sensing. Annu Rev Plant Biol 67:261–285

    Google Scholar 

  • Du, W., Hu, H., Zhang, J., et al. (2019): The mechanism of MAPK signal transduction pathway involved with electro-acupuncture treatment for different diseases. Evid Based Complement Alternat Med Article ID: 8138017.

  • Ebrahim F, Arzani A, Rahimmalek M, Sun D, Peng J (2020) Salinity tolerance of wild barley Hordeum vulgare ssp. spontaneum. Plant Breeding 139(2):304–316

    CAS  Google Scholar 

  • Ellis R, Foster B, Handley L et al (2000) Wild barley: a source of genes for crop improvement in the 21st century? J Exp Bot 51:9–17

    CAS  PubMed  Google Scholar 

  • FAO (2019) Crop prospects and food situation. Quarterly Global Report no. 3, Rome.

  • Gray WM, Kepinski S, Rouse D et al (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    CAS  PubMed  Google Scholar 

  • Gunaskera D, Santakumari M, Glinka Z, Berkowitz GA (1994) Wild and cultivated barley genotypes demonstrate varying ability to acclimate to plant water deficits. Plant Sci 99:125–134

    Google Scholar 

  • Heitman J, Movva NR, Hall MN (1991) Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905–909

    CAS  PubMed  Google Scholar 

  • Herzig S, Shaw RJ (2018) AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 19:121–135

    CAS  PubMed  Google Scholar 

  • Hosokawa N, Hara T, Kaizuka T et al (2009) Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20:1981–1991

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inaba JI, Nagy PD (2018) Tombusvirus RNA replication depends on the TOR pathway in yeast and plants. Virol 519:207–222

    CAS  Google Scholar 

  • Knauss S, Rohrmeier T, Lehle L (2003) The auxin-induced maize gene ZmSAUR2 encodes a short-lived nuclear protein expressed in elongating tissues. J Biol Chem 237:23936–23943

    Google Scholar 

  • Krejci A, Tennessen JM (2017) Metabolism in time and space-exploring the frontier of developmental biology. Development 144:3193–3198

    CAS  PubMed  Google Scholar 

  • Li G, Xue HW (2007) Arabidopsis PLDzeta2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125

    PubMed  PubMed Central  Google Scholar 

  • Li X, Cai W, Liu Y et al (2017) Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes. Proc Natl Acad Sci USA 114:2765–2770

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhang C, Wei C et al (2016) The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice. Plant Physiol 170:429–443

    CAS  PubMed  Google Scholar 

  • Liu M, Li Y, Ma Y et al (2019) The draft genome of a wild barley genotype reveals its enrichment in genes related to biotic and abiotic stresses compared to cultivated barley. Plant Biotechnol J 18:443–456

    PubMed  PubMed Central  Google Scholar 

  • Liu TK, Song XM, Duan WK et al (2014) Genome-wide analysis and expression patterns of NAC transcription factor family under different developmental stages and abiotic stresses in Chinese cabbage. Plant Mol Biol Rep 32:1041–1056

    Google Scholar 

  • Liu Y, Bassham DC (2010) TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS ONE 5:e11883

    PubMed  PubMed Central  Google Scholar 

  • Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63:215–237

    CAS  PubMed  Google Scholar 

  • Liu Y, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5:954–963

    CAS  PubMed  Google Scholar 

  • Ma Q, Dai X, Xu Y et al (2009) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol 150:244–256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Magnuson B, Ekim B, Fingar DC (2012) Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 441:1–21

    CAS  PubMed  Google Scholar 

  • Margalha L, Confraria A, Baena E (2019) SnRK1 and TOR: modulating growth-defense trade-offs in plant stress responses. J Exp Bot 70:2261–2274

    CAS  PubMed  Google Scholar 

  • Mehta RH, Ponnuchamy M, Kumar J, Reddy NR (2017) Exploring drought stress-regulated genes in senna (Cassia angustifolia Vahl.): a transcriptomic approach. Funct Integr Genomics 17:1–25

    CAS  PubMed  Google Scholar 

  • Menand B, Desnos T, Nussaume L et al (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99:6422–6427

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meteignier LV, El Oirdi M, Cohen M et al (2017) Translatome analysis of an NB-LRR immune response identifies important contributors to plant immunity in Arabidopsis. J Exp Bot 68:2333–2344

    CAS  PubMed  Google Scholar 

  • Montané M-H, Menand B (2019) TOR inhibitors: from mammalian outcomes to pharmacogenetics in plant and algae. J Exp Bot 70:2297–2312

    PubMed  Google Scholar 

  • Mossmann D, Park S, Hall MN (2018) mTOR signalling and cellular metabolism are mutual determinants in cancer. Nat Rev Cancer 18:744–757

    CAS  PubMed  Google Scholar 

  • Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nukarinen E, Nägele T, Pedrotti L (2016) Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation. Sci. Rep. 6:31697

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oğuz AC (2019) Resistance of wild barley (Hordeum spontaneum) and barley landraces to leaf stripe (Drechslera graminea). Phytopathol Mediterr 58:485–495

    Google Scholar 

  • Oğuz AC, Karakaya A, Duran RM, Özbek K (2019) Identification of Hordeum spontaneum genotypes resistant to net blotch disease. J Agric Sci 25:115–122

    Google Scholar 

  • Ouibrahim L, Rubio AG, Moretti A et al (2015) Potyviruses differ in their requirement for TOR signalling. J Gen Virol 96:2898–2903

    CAS  PubMed  Google Scholar 

  • Paponov IA, Paponov M, Teale W et al (2008) Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant 1:321–337

    CAS  PubMed  Google Scholar 

  • Pfeiffer A, Janocha D, Dong Y et al (2016) Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. eLife 5:e17023

    PubMed  PubMed Central  Google Scholar 

  • Puente C, Hendrickson RC, Jiang X (2016) Nutrient-regulated phosphorylation of ATG13 inhibits starvation-induced autophagy. J Biol Chem 291:6026–6035

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quilichini TD, Gao P, Pandey PK et al (2019) A role for TOR signaling in every stage of plant life. J Exp Bot 70:2285–2296

    CAS  PubMed  Google Scholar 

  • Raney JA, Reynolds DJ, Elzinga DB et al (2014) Transcriptome analysis of drought induced stress in Chenopodium quinoa. Am J Plant Sci 5:338–357

    CAS  Google Scholar 

  • Ren M, Qiu S, Venglat P et al (2011) Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol 155:1367–1382

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roustan V, Weckwerth W (2018) Quantitative phosphoproteomic and system-level analysis of TOR inhibition unravel distinct organellar acclimation in Chlamydomonas reinhardtii. Front Plant Sci 9:1590

    PubMed  PubMed Central  Google Scholar 

  • Saxton RA, Sabatini DM (2017) mTOR signaling in growth, metabolism, and disease. Cell 168:960–976

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schepetilnikov M, Dimitrova M, Mancera-Martínez E et al (2013) TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h. The EMBO J 32:1087–1102

    CAS  PubMed  Google Scholar 

  • Schepetilnikov M, Ryabova LA (2018) Recent discoveries on the role of TOR (Target of Rapamycin) signaling in translation in plants. Plant Physiol 176:1095–1105

    CAS  PubMed  Google Scholar 

  • Schepetilnikov M, Makarian J, Srour O et al (2017) GTPase ROP2 binds and promotes activation of target of rapamycin, TOR, in response to auxin. EMBO J 36:886–903

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi L, Wu Y, Sheen J (2018) TOR signaling in plants: conservation and innovation. Development. https://doi.org/10.1242/dev.160887

    Article  PubMed  PubMed Central  Google Scholar 

  • Soprano AS, Smetana JHC, Benedetti CE (2018) Regulation of tRNA biogenesis in plants and its link to plant growth and response to pathogens. BBA Gene Regul Mech 1861:344–353

    CAS  Google Scholar 

  • Soto-Burgos J, Bassham DC (2017) SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana. PLoS ONE 12:e0182591

    PubMed  PubMed Central  Google Scholar 

  • Stacey SN, Jordan D, Williamson, et al (2000) Leaky scanning is the predominant mechanism for translation of human papillomavirus type 16 E7 oncoprotein from E6/E7 bicistronic mRNA. J Virol 74:7284–7297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tatebe H, Shiozaki K (2017) Evolutionary conservation of the components in the TOR signaling pathways. Biomolecules 7:77

    PubMed Central  Google Scholar 

  • Ulmasov T, Hagen G, Guibal O (1997a) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868

    CAS  PubMed  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997b) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin responsive elements. Plant Cell 9:1963–1971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Li H, Zhao C et al (2017) The inhibition of protein translation mediated by AtGCN1 is essential for cold tolerance in Arabidopsis thaliana. Plant Cell Environ 40:56–68

    PubMed  Google Scholar 

  • Wang P, Zhao Y, Li Z et al (2018) Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol Cell 69:100–112

    CAS  PubMed  Google Scholar 

  • Weichhart T (2018) mTOR as regulator of lifespan, aging, and cellular senescence: a mini-review. Gerontol 64:127–134

    CAS  Google Scholar 

  • Werth EG, McConnell EW, Couso Lianez I et al (2019) Investigating the effect of target of rapamycin kinase inhibition on the Chlamydomonas reinhardtii phosphoproteome: from known homologs to new targets. New Phytol 221:247–260

    CAS  PubMed  Google Scholar 

  • Wu Y, Shi L, Li L et al (2019) Integration of nutrient, energy, light, and hormone signalling via TOR in plants. J Exp Bot 70:2227–2238

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wurzinger B, Nukarinen E, Nägele T et al (2018) The SnRK1 kinase as central mediator of energy signalling between different organelles. Plant Physiol 176:1085–1094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong Y, McCormack M, Li L et al (2013) Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496:181–186

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong Y, Sheen J (2012) Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J Biol Chem 287:2836–2842

    CAS  PubMed  Google Scholar 

  • Yang X, Bassham DC (2015) New insight into the mechanism and function of autophagy in plant cells. In: Jeon Kwang W (ed) International review of cell and molecular biology. Academic Press, Burlington, pp 1–40

    Google Scholar 

  • Zhang J, Ruhlman TA, Mower JP, Jansen RK (2013) Comparative analyses of two Geraniaceae transcriptomes using next-generation sequencing. BMC Plant Biol 13:228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Zhu J-Y, Roh J et al (2016) TOR signaling promotes accumulation of BZR1 to balance growth with carbon availability in Arabidopsis. Curr Biol 26:1854–1860

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Wu A, Yue Y, Zhao Y (2020) uORFs: important cis-regulatory elements in plants. Intl J Mol Sci 21:6238

    CAS  Google Scholar 

  • Ziemann M, Kamboj A, Hove RM et al (2013) Analysis of the barley leaf transcriptome under salinity stress using mRNA-Seq. Acta Physiol Plant 35:1915–1924

    CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge Prof. Dr. Ahmed Bahieldin for providing physical and logistic supports for this study.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: AAA, SHQ, DAA, SAH, Editing manuscript: AAA, SHQ, DAA, SAH, Review & correspondence: AAA.

Corresponding author

Correspondence to Aala A. Abulfaraj.

Ethics declarations

Conflict of interest

Authors declare no conflict of interest including grants, membership, employment, ownership of stock or any other interest or non‐financial interest.

Additional information

Publisher's Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abulfaraj, A.A., Qari, S.H., Abuljadayel, D.A. et al. Abiotic stress-related genes governing signal transduction cascades in wild plants with emphasis to those in Hordeum spontaneum. J. Plant Biochem. Biotechnol. 31, 12–21 (2022). https://doi.org/10.1007/s13562-021-00660-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-021-00660-6

Keywords

Navigation