Skip to main content
SpringerLink
Log in

Comprehensive identification, evolutionary patterns and the divergent response of PRX genes in Phaseolus vulgaris under biotic and abiotic interactions

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Peroxiredoxins (Prxs) are novel cysteine-based peroxidases which are involved in protecting cells from oxidative damage by catalyzing the reduction of different peroxides. The present study addressed, for the first time, genome-wide identification, evolutionary patterns and expression dynamics of Phaseolus vulgaris Prx gene family (PvPrx). Nine Prx proteins were identified in P. vulgaris based on homology searches. The phylogeny analysis of Prxs from seven plant species revealed that Prx proteins can be clustered into four groups (1C-Prx, 2C-Prxs, PrxQ and type II Prxs). Both tandem and segmental duplication contributed to PvPrx gene family expansion. Intragenic reorganizations including gain/loss of exon/intron and insertions/deletions have also contributed to PvPrx gene diversification. The collinearity analysis revealed the presence of some orthologous Prx gene pairs between A. thaliana and P. vulgaris genomes. The Ka/Ks ratio indicated that two of the three PvPrx duplicated gene pairs have undergone a purifying selection. Redundant stress-related cis-acting elements were also found in the promoters of most PvPrx genes. RT q-PCR analysis revealed an upregulation of key PvPrx members in response to symbiosis and different abiotic factors. The upregulation of targeted PvPrx members, particularly in leaves exposed to salinity or drought, was accompanied by an accumulation of hydrogen peroxide (H2O2). When exogenously applied, H2O2 modulated almost all PvPrx genes, suggesting a potential H2O2-scavenging role for these proteins. Collectively, our analysis provided valuable information for further functional analysis of key PvPrx members to improve common bean stress tolerance and/or its symbiotic performance.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Ahmad F, Kamal A, Singh A, Ashfaque F, Alamri S, Siddiqui MH (2022) Salicylic acid modulates antioxidant system, defense metabolites, and expression of salt transporter genes in Pisum sativum under salinity stress. J Plant Growth Regul 41:1905–1918

    Article  CAS  Google Scholar 

  • Boubakri H, Chihaoui SA, Najjar E, Gargouri M, Barhoumi F, Jebara M (2021) Genome-wide analysis and expression profiling of H-type Trx family in Phaseolus vulgaris revealed distinctive isoforms associated with symbiotic N2-fixing performance and abiotic stress response. J Plant Physiol 260:153410

    Article  CAS  Google Scholar 

  • Boubakri H, Najjar E, Jihnaoui N, Chihaoui S, Barhoumi F, Jebara M (2022) Genome-wide identification, characterization and expression analysis of glutaredoxin gene family (Grxs) in Phaseolus vulgaris. Gene 833:146591

    Article  CAS  Google Scholar 

  • Boubakri H, Saidi MN, Barhoumi F, Jebara M, Brini F (2019) Identification and characterization of thioredoxin h-type gene family in Triticum Turgidium ssp. durum in response to natural and environmental factor-induced oxidative stress. Plant Mol Biol Rep 37(5): 464–476

  • Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Bean (Phaseolus spp.)—model food legumes. Plant Soil 25:255–228

    Google Scholar 

  • Calderóna A, Ortiz-Espína A, Iglesias-Fernándezb R (2017) Thioredoxin (Trxo1) interacts with proliferating cell nuclear antigen (PCNA) and its overexpression affects the growth of tobacco cell culture. Redox Biol 11:688–700

    Article  Google Scholar 

  • Chen J, Yin H, Gu J, Li L, Liu Z, Jiang X, Zhou H, Wei S, Zhang S, Wu J (2015) Genomic characterization, phylogenetic comparison and differential expression of the cyclic nucleotide-gated channels gene family in pear (Pyrus bretchneideri Rehd.). Genomics 105(1):39–52

  • Derbali W, Manaa A, Goussi R, Derbali I, Abdelly C, Koyro HW (2021) Post-stress restorative response of two quinoa genotypes differing in their salt resistance after salinity release. Plant Physiol Biochem 164:222–236

    Article  CAS  Google Scholar 

  • Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1160

    Article  CAS  Google Scholar 

  • Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709

    Article  CAS  Google Scholar 

  • Dreyer A, Treffon P, Basiry D, Jozefowicz AM, Matros A, Mock HP, Dietz KJ (2021) Function and regulation of chloroplast peroxiredoxin IIE. Antioxidants 10(2):152

    Article  CAS  Google Scholar 

  • Frendo P, Matamoros MA, Alloing G, Becana M (2013) Thiol-based redox signaling in the nitrogen-fixing symbiosis. Front Plant Sci 4:376

    Article  Google Scholar 

  • Gho Y-S, Park SA, Kim SR, Nalini CAK, An G, Jung KH (2017) Comparative expression analysis of rice and arabidopsis peroxiredoxin genes suggests conserved or diversified roles between the two species and leads to the identification of tandemly duplicated rice peroxiredoxin genes differentially expressed in seeds. Rice 10:30

    Article  Google Scholar 

  • Guan C, Liu X, Song X, Wang G, Ji J, Jin C (2014) Overexpression of a peroxiredoxin Q gene, SsPrxQ, in Eustoma grandiflorum Shinn enhances its tolerance to salt and high light intensity. Mol Breed 33:657–667

    Article  CAS  Google Scholar 

  • Haslekas C, Viken MK, Grini PE, Nygaard V, Nordgard SH, Meza TJ, Aalen RB (2003) Seed 1-cysteine peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress. Plant Physiol 133:1148–1157

    Article  CAS  Google Scholar 

  • Heinekamp T, Kuhlmann M, Lenk A, Strathmann A, LaserW D (2002) The tobacco bZIP transcription factor BZI-1 binds to G-box elements in the promoters of phenylpropanoid pathway genes in vitro, but it is not involved in their regulation in vivo. Mol Genet Genomics 267:16–26

    Article  CAS  Google Scholar 

  • Hong SH, Lee SS, Chung JM, Jung HS, Singh S, Mondal S, Jang HH, Cho JY, Bae HJ, Chung BY (2017) Site-specific mutagenesis of yeast 2-Cys peroxiredoxin improves heat or oxidative stress tolerance by enhancing its chaperone or peroxidase function. Protoplasma 254(1):327–335

    Article  CAS  Google Scholar 

  • Horling F, Lamkemeyer P, König J, Finkemeier I, Kandlbinder A, Baier M, Dietz KJ (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol 131:317–325

    Article  CAS  Google Scholar 

  • Hornsveld M, Dansen TB (2016) The hallmarks of cancer from a redox perspective. Antioxid Redox Signal 25:300–325

    Article  CAS  Google Scholar 

  • Jardak R, Riahi J, Dallagi W, Planchon S, Boubakri H, Mejri S, Renaut J, Mock HP, Ghorbel A (2021) Proteomic analysis of salt-responsive proteins in the leaves of two contrasting Tunisian barley landraces. Plant Growth Regul 95:65–82

    Article  CAS  Google Scholar 

  • Jing LW, Chen SH, Guo XL, Zhang H, Zhao YX (2006) Overexpression of a chloroplast-located peroxiredoxin Q gene, SsPrxQ, increases the salt and low temperature tolerance of Arabidopsis. J Integr Plant Biol 48:1244–1249

    Article  CAS  Google Scholar 

  • Kapoor D, Sharma R, Handa N, Kaur H, Rattan A, Yadav P, Gautam V, Kaur R, Bhardwaj R (2015) Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front Environ Sci 3:13

    Article  Google Scholar 

  • Kim KH, Alam I, Lee KW, Sharmin SA, Kwak SS, Lee SY, Lee BH (2010) Enhanced tolerance of transgenic tall fescue plants overexpressing 2-Cys peroxiredoxin against methyl viologen and heat stresses. Biotechnol Lett 32:571–576

    Article  CAS  Google Scholar 

  • Kim IS, Kim YS, Yoon HS (2013) Expression of salt-induced 2-Cys peroxiredoxin from Oryza sativa increases stress tolerance and fermentation capacity in genetically engineered yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 97(8):3519–3533

    Article  CAS  Google Scholar 

  • Kong H, Landherr L, Frohlich MW, Leebens MJ, Ma H, DePamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885

    Article  CAS  Google Scholar 

  • Lallemand T, Leduc M, Landès C, Rizzon C, Lerat E (2020) An overview of duplicated gene detection methods: Why the duplication mechanism has to be accounted for in their choice. Genes 11:1046

    Article  CAS  Google Scholar 

  • Liebthal M, Maynard D, Dietz KJ (2018) Peroxiredoxins and redox signaling in plants. Antioxid Redox Signal 28(7)

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2–ΔΔCt method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Mhadhbi H, Jebara M, Limam F, Huguet T, Aouani ME (2005) Interaction between Medicago truncatula lines and Sinorhizobium meliloti strains for symbiotic efficiency and nodule antioxidant activities. Physiol Plant 124:4–11

    Article  CAS  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    Article  Google Scholar 

  • Ojeda V, Perez-Ruiz JM, Cejudo FJ (2018) 2-Cys peroxiredoxins participate in the oxidation of chloroplast enzymes in the dark. Mol Plant 11:1377–1388

    Article  CAS  Google Scholar 

  • O’Rourke JA, Iniguez LP, Fu F, Bucciarelli B, Miller SS, Jackson SA et al (2014) An RNA-Seq based gene expression atlas of the common bean. BMC Genomics 15:866

    Article  Google Scholar 

  • Pulido P, Spinola MC, Kirchsteiger K, Guinea M, Pascual MB, Sahrawy M, Sandalio LM, Dietz KJ, Gonzalez M, Cejudo FJ (2010) Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. J Exp Bot 61:4043–4054

    Article  CAS  Google Scholar 

  • Romero-Puertas MC, Laxa M, Matte A, Zaninotto F, Finkemeier I, Jones AM, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130

    Article  CAS  Google Scholar 

  • Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu SQ, Song QJ, Chavarro C (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713

    Article  CAS  Google Scholar 

  • Shaikhali J, Wingsle G (2017) Redox-regulated transcription in plants: emerging concepts. AIMS Molecular Science 4(3):301–338

    Article  CAS  Google Scholar 

  • Tovar-Méndez A, Matamoros MA, Bustos-Sanmamed P, Dietz KJ, Cejudo FJ, Rouhier N (2011) Peroxiredoxins and NADPHdependent thioredoxin systems in the model legume Lotus japonicus. Plant Physiol 156:1535–1547

    Article  Google Scholar 

  • Tripathi BN, Bhatt I, Dietz KJ (2009) Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. Protoplasma 235:3–15

    Article  CAS  Google Scholar 

  • Umate P (2010) Genome-wide analysis of thioredoxin fold superfamily peroxiredoxins in Arabidopsis and rice. Plant Signal Behav 5:1543–1546

    Article  CAS  Google Scholar 

  • Vidigal P, Carvalho R, Amâncio S, Carvalho L (2013) Peroxiredoxins are involved in two independent signaling pathways in the abiotic stress protection in Vitis vinifera. Biol Planta 57:675–683

    Article  CAS  Google Scholar 

  • Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X, Peng L (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10:282

    Article  CAS  Google Scholar 

  • Wang Y, Liu Z, Wang P, Jiang B, Lei X, Wu J, Dong W, Gao C (2020) A 2-Cys peroxiredoxin gene from Tamarix hispida improved salt stress tolerance in plants. BMC Plant Biol 20:360

    Article  CAS  Google Scholar 

  • Zhang HH, Xu N, Teng ZY, Wang JR, Ma S, Wu X, Li X, Sun GY (2019) 2-Cys Prx plays a critical role in scavenging H2O2 and protecting photosynthetic function in leaves of tobacco seedlings under drought stress. J Plant Interact 14(1):119–128

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Tunisian Ministry of Higher Education and Scientific Research for the financial support of this work. The authors are thankful to Prof. Ridha Mhamdi (Center of Biotechnology of Borj Cedria) for providing the Rhizobium strains used in the present study.

Author information

Authors and Affiliations

  1. Laboratory of Legumes and Sustainable Agrosystems, Centre of Biotechnology of Borj-Cedria, BP 901, 2050, Hammam-Lif, Tunisia

    Hatem Boubakri, Saif-Allah Chihaoui, Eya Najjar, Fathi Barhoumi & Moez Jebara

Authors
  1. Hatem Boubakri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saif-Allah Chihaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eya Najjar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fathi Barhoumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Moez Jebara
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HB designed this study, carried out the different stress treatments, bioinformatics and RT-qPCR analyses, and wrote the manuscript. SAC, EN and FB contributed to conducting plant hydroponic culture, inoculation and assessment of the physiological parameters. MJ supervised this work. All authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Hatem Boubakri.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1195 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boubakri, H., Chihaoui, SA., Najjar, E. et al. Comprehensive identification, evolutionary patterns and the divergent response of PRX genes in Phaseolus vulgaris under biotic and abiotic interactions. 3 Biotech 12, 175 (2022). https://doi.org/10.1007/s13205-022-03246-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-022-03246-8

Keywords

Search

Navigation