Abstract
Bcl-2-associated anthogenes (BAGs), chaperone regulators are known to regulate programmed cell death in plants. In the present study, we have identified eight BAG genes in the rice (Oryza sativa) genome. Subsequently, to understand the evolution, 78 BAG homologs were identified in other nine Oryza species. In addition to the signature ubiquitin-like domain, an additional conserved sequence of 12 amino acids was found in all the class I BAG genes except few exceptions in wild species. A significantly variable number of BAG genes was identified in different Oryza species indicates the expansion of BAG genes due to segmental duplication. Based on whole genome resequencing information available for 4726 rice genotypes, haplotype diversity and the functional effect of variations in BAG genes were predicted. Transcriptomic analyses further suggested the multifunctional roles of BAG genes during both developmental and defense response in Oryza species. Differential expression of BAG genes particularly BAG3 and BAG5 was observed under heavy metal stress. Similarly, higher expression of OsBAG1 and OsBAG2 were found in resistant rice cultivar in response to Magnaporthe oryzae infection and OsBAG2 showed upregulation in response to Xanthomonas oryzae infection as well. A similar expression of BAG genes was observed in the qRT-PCR analysis. Furthermore, heterologous transient expression of OInBAG6 protein tagged with yellow fluorescent protein in tobacco leaves showed the subcellular localization in both nucleus and plasma membrane. This study will help to understand the evolution of BAG genes and their role in cell death under stress conditions in rice.
Similar content being viewed by others
References:
Alberti S et al (2002) Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J Biol Chem 277(48):45920–45927
Arif M et al (2020) The BAG2 and BAG6 genes are involved in multiple abiotic stress tolerance in Arabidopsis Thaliana. Int J Mol Sci 22(11):5856
Arvidsson S et al (2008) QuantPrime–a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinform 9(1):465
Bailey TL et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(suppl_2):W202–W208
Bansal R et al (2020) Evolutionary understanding of metacaspase genes in cultivated and wild Oryza species and its role in disease resistance mechanism in rice. Genes 11(12):1412
Briknarová K et al (2001) Structural analysis of BAG1 cochaperone and its interactions with Hsc70 heat shock protein. Nat Struct Biol 8(4):349–352
Callis J (2014) The ubiquitination machinery of the ubiquitin system. Arabidopsis Book/am Soc Plant Biol 12:e0174
Choi Y et al (2012) Predicting the functional effect of amino acid substitutions and indels. PLoS ONE 7(10):e46688
Doukhanina EV et al (2006) Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem 281(27):18793–18801
El-Gebali S et al (2018) The Pfam protein families database in 2019. Nucleic Acids Res 47(D1):D427–D432
Fang S et al (2013) Structural insight into plant programmed cell death mediated by BAG proteins in Arabidopsis thaliana. Acta Crystallogr D Biol Crystallogr 69(6):934–945
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series. Information Retrieval Ltd., London, c1979-c2000
Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67(1):425–479
Higo K et al (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27(1):297–300
Hirokawa T et al (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics (oxf, Engl) 14(4):378–379
Höhfeld J et al (2001) From the cradle to the grave: molecular chaperones that may choose between folding and degradation. EMBO Rep 2(10):885–890
Hruz T et al (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747
Hu B et al (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297
Kabbage M, Dickman M (2008) The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci 65(9):1390–1402
Kabbage M et al (2016) A plant Bcl-2-associated athanogene is proteolytically activated to confer fungal resistance. Microbial Cell 3(5):224
Kozlowski LP (2016) IPC—isoelectric point calculator. Biol Direct 11(1):55
Krogh A et al (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580
Krzywinski M et al (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645
Kumar S et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549
Lockshin RA et al (1998) When cells die: a comprehensive evaluation of apoptosis and programmed cell death. Wiley, New York
Lu S et al (2020) CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 48(D1):D265–D268
Monaco MK et al (2013) Gramene 2013: comparative plant genomics resources. Nucleic Acids Res 42(D1):D1193–D1199
Nawkar GM et al (2017) In silico study on Arabidopsis BAG gene expression in response to environmental stresses. Protoplasma 254(1):409–421
Pagliuca MG et al (2003) Regulation by heavy metals and temperature of the human BAG-3 gene, a modulator of Hsp70 activity. FEBS Lett 541(1–3):11–15
Rana RM et al (2012) Identification and characterization of the Bcl-2-associated athanogene (BAG) protein family in rice. Afr J Biotechnol 11(1):88–98
Rodrigues CHM et al (2018) DynaMut: predicting the impact of mutations on protein conformation, flexibility, and stability. Nucleic Acids Res 46(W1):W350–W355
Sato Y et al (2012) RiceXPro Version 3.0: expanding the informatics resource for rice transcriptome. Nucleic Acids Res 41:D1206–D1213
Sievers F, Higgins DG (2018) Clustal Omega for making accurate alignments of many protein sequences. Protein Sci 27(1):135–145
Takayama S, Reed JC (2001) Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol 3(10):E237–E241
Takayama S et al (1995) Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell 80(2):279–284
Van Bel M et al (2017) PLAZA 4.0: an integrative resource for functional, evolutionary and comparative plant genomics. Nucleic Acids Res 46(D1):D1190–D1196
Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78
Waese J et al (2017) ePlant: visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell 29:1806–1821
Williams B et al (2010) AtBAG7, an Arabidopsis Bcl-2–associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc Natl Acad Sci USA 107(13):6088–6093
Xia L et al (2017) Rice expression database (RED): an integrated RNA-Seq-derived gene expression database for rice. J Genet Genomics 44:235–241
Yan J et al (2003) The BAG-family proteins in Arabidopsis thaliana. Plant Sci 165(1):1–7
Yang J et al (2015) The I-TASSER suite: protein structure and function prediction. Nat Methods 12(1):7–8
Yang J et al (2019) The crosstalks between jasmonic acid and other plant hormone signaling highlight the involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses. Front Plant Sci 10:1349
Yu CS et al (2006) Prediction of protein subcellular localization. Proteins Struct Funct Bioinform 64(3):643–651
Zhao H et al (2015) RiceVarMap: a comprehensive database of rice genomic variations. Nucleic Acids Res 43(D1):D1018–D1022
Acknowledgements
The authors are thankful to the Department of Biotechnology, Government of India, for the Ramalingaswami Fellowship Award to H.S. and R.D., and for grants BT/PR32853/AGIII/103/1159/2019 and BTINIGPER/Flagship-Prog/2018-19 to H.S., R.D., and T.R.S.; Council of Scientific and Industrial Research (CSIR) for granting senior research fellowship to R.B.; and the Department of Science and Technology for JC Bose Fellowship to T.R.S., and research grant (CRG/2019/006599) to R.D., H.S., and T.R.S.; authors are also thankful to Ganesh Prakashan, Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, India for sharing Magnaporthe oryzae isolate and valuable inputs.
Funding
This research was funded by the Department of Biotechnology (DBT) and Science and Engineering Research Board (SERB), Department of Science and Technology, Government of India.
Author information
Authors and Affiliations
Contributions
Data curation: RB and SK; Cloning and Transient expression analysis: RJ; Formal analysis: RB, PD, and SK; Funding acquisition: HS, RD, and TRS; Methodology: RB, SK, PD, SS, and AK; Software: AK and SS; Supervision: HS, RD, and TRS; Validation: RB and PD; Visualization: RB, AK, PD, and SK; Writing—original draft: RB; Writing—review & editing: HS, RD, and TRS. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare no conflict of interest.
Additional information
Handling Editor: Anket Sharma.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
344_2021_10552_MOESM14_ESM.txt
Supplementary File 1 The Multiple sequence alignment file of 78 BAG genes retrieved by clustal omega (clustal O (1.2.4) multiple sequence alignment) online tool in both wild and cultivated Oryza species. (TXT 93 kb)
344_2021_10552_MOESM15_ESM.docx
Supplementary File 2 Gene expression of OsJaBAGs genes under different stress conditions constructed by Bio-Analytic Resource for Plant Biology (https://ricexpro.dna.affrc.go.jp/data-set.html) (DOCX 2389 kb)
Rights and permissions
About this article
Cite this article
Bansal, R., Kumawat, S., Dhiman, P. et al. Evolution of Bcl-2 Anthogenes (BAG) as the Regulators of Cell Death in Wild and Cultivated Oryza Species. J Plant Growth Regul 42, 348–364 (2023). https://doi.org/10.1007/s00344-021-10552-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-021-10552-7