Skip to main content

In-silico evolutionary analysis of plant-OBERON proteins during compatible MYMV infection in respect of improving host resistance

Abstract

Yellow mosaic disease (YMD) of pulses caused by mungbean yellow mosaic virus is a major threat to crop production. An infection that is compatible with regulating and interacting host proteins and the virus causes YMD. Oberon families of proteins OBE1-4 and VIN1-4 are imperative for plants, functions in meristem and vascular development, and were also regulated during compatible disease infection. Furthermore, in-silico expression results suggested the involvement of OBE1 and OBE2 proteins during virus infection of Vigna, Arabidopsis and soybean. Moreover, a common ancestor for the meristem and virus movement related Oberons was inferred through phylogenetic analysis. Protein interaction studies showed three amino acids (Aspartate, glutamate and lysine) in the plant homeodomain (PHD), involved in interaction with the N-terminal region of the virus movement protein and were also conserved in both monocot and dicots. Additionally, major differences in the nuclear localization signal (NLS) showing clade specific conservation and significant variation between dicots and monocots were ascertained in meristem and virus movement related Oberons. Consequently, a combination of PHD, CCD and their interactions with the VPg viral domain increases the susceptibility to YMD. Further, modification in the NLS regions of the viral movement clade Oberons, to knock out allele generation in the OBE1 and OBE2 homologs through genome-editing approaches could be established as alternate strategies for the improvement of host resistance and control yellow mosaic disease in plants, especially in pulse crops.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Aasland R, Gibson TJ, Stewart AF (1995) The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem Sci 20(2):56–59

    CAS  PubMed  Article  Google Scholar 

  • Anand N (2010) Characterisation of the Potyvirus VPg Interacting Protein (PVIP) gene from Nicotiana benthamiana. Doctoral dissertation, Auckland University of Technology

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motifdiscovery and searching. Nucleic Acids Res 37(1):W202–W208

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Batra R, Agarwal P, Tyagi S, Saini DK, Kumar V, Kumar A et al (2019) A study of CCD8 genes/proteins in seven monocots and eight dicots. PLoS ONE 14(3):e0213531

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Betts MJ, Russell RB (2003) Amino acid properties and consequences of substitutions. Bioinform Genet 317(289):10–1002

    Google Scholar 

  • Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Ku A et al (2010) The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22(9):2943–2955

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Brodie J, Ball SG, Bouget FY, Chan CX, De Clerck O, Cock JM et al (2017) Biotic interactions as drivers of algal origin and evolution. New Phytol 216(3):670–681

    CAS  PubMed  Article  Google Scholar 

  • Casper Chater C, Caine RS, Fleming AJ, Gray JE (2017) Origins and evolution of stomatal development. Plant Physiol 174(2):624–638

    Article  CAS  Google Scholar 

  • Cayalvizhi B, Nagarajan P, Raveeendran M, Rabindran R, Selvam NJ, Bapu JK, Senthil N (2015) Unraveling the responses of mungbean (Vigna radiata) to mungbean yellow mosaic virus through 2D-protein expression. Physiol Mol Plant Pathol 90:65–77

    CAS  Article  Google Scholar 

  • Chen F, Zhang X, Liu X, Zhang L (2017) Evolutionary analysis of MIKCc-type MADS-box genes in gymnosperms and angiosperms. Front Plant Sci 8:895

    PubMed  PubMed Central  Article  Google Scholar 

  • Cheng J, Khan MA, Qiu WM, Li J, Zhou H, Zhang Q et al (2012) Diversification of genes encoding granule-bound starch synthase in monocots and dicots is marked by multiple genome-wide duplication events. PLoS ONE 7(1):e30088

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • De Vries SJ, Van Dijk M, Bonvin AM (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5(5):883–897

    PubMed  Article  CAS  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11(8):539–548

    CAS  PubMed  Article  Google Scholar 

  • Dunoyer P, Thomas C, Harrison S, Revers F, Maule A (2004) A cysteine-rich plant protein potentiates Potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol 78(5):2301–2309

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Garcia-Ruiz H (2018) Susceptibility genes to plant viruses. Viruses 10(9):484

    PubMed Central  Article  CAS  Google Scholar 

  • Greb T, Mylne JS, Crevillen P, Geraldo N, An H, Gendall AR et al (2007) The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr Biol 17(1):73–78

    CAS  PubMed  Article  Google Scholar 

  • Hake S, Smith HM, Holtan H, Magnani E, Mele G, Ramirez J (2004) The role of knox genes in plant development. Annu Rev Cell Dev Biol 20:125–151

    CAS  PubMed  Article  Google Scholar 

  • Han JD, Li X, Jiang CK, Wong GKS, Rothfels CJ, Rao GY (2017) Evolutionary analysis of the LAFL genes involved in the land plant seed maturation program. Front Plant Sci 8:439

    PubMed  PubMed Central  Google Scholar 

  • Haq QMI, Ali A, Malathi VG (2010) Engineering resistance against Mungbean yellow mosaic India virus using antisense RNA. Indian J Virol 21(1):82–85

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Harrison BD, Robinson DJ (1999) Natural genomic and antigenic variation in whitefly-transmitted geminiviruses (begomoviruses). Annu Rev Phytopathol 37(1):369–398

    CAS  PubMed  Article  Google Scholar 

  • Havelda Z, Várallyay É, Válóczi A, Burgyán J (2008) Plant virus infection-induced persistent host gene downregulation in systemically infected leaves. Plant J 55(2):278–288

    CAS  PubMed  Article  Google Scholar 

  • Hipper C, Brault V, Ziegler-Graff V, Revers F (2013) Viral and cellular factors involved in phloem transport of plant viruses. Front Plant Sci 4:154

    PubMed  PubMed Central  Article  Google Scholar 

  • Jiao Y, Paterson AH (2014) Polyploidy-associated genome modifications during land plant evolution. Philos Trans R Soc b Biol Sci 369(1648):20130355

    Article  Google Scholar 

  • Jin X, Ren J, Nevo E, Yin X, Sun D, Peng J (2017) Divergent evolutionary patterns of NAC transcription factors are associated with diversification and gene duplications in angiosperm. Front Plant Sci 8:1156

    PubMed  PubMed Central  Article  Google Scholar 

  • Kang BC, Yeam I, Jahn MM (2005) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621

    CAS  PubMed  Article  Google Scholar 

  • Krichevsky A, Kozlovsky SV, Citovsky YGV (2004) Nuclear import and export of plant virus proteins and genomes. Mol Plant Pathol 7(2):131–146

    Article  Google Scholar 

  • Kuhn M, Hyman AA, Beyer A (2014) Coiled-coil proteins facilitated the functional expansion of the centrosome. PLoS Comput Biol 10(6):e1003657

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Kumar BKP, Kanakala S, Malathi VG, Gopal P, Usha R (2017) Transcriptomic and proteomic analysis of yellow mosaic diseased soybean. J Plant Biochem Biotechnol 26(2):224–234

    Article  CAS  Google Scholar 

  • Laskowski RA (2001) PDBsum: summaries and analyses of PDB structures. Nucleic Acids Res 29(1):221–222

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Letunic I, Bork P (2017) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46(D1):D493–D496

    PubMed Central  Article  CAS  Google Scholar 

  • Li C, Li QG, Dunwell JM, Zhang YM (2012) Divergent evolutionary pattern of starch biosynthetic pathway genes in grasses and dicots. Mol Biol Evol 29(10):3227–3236

    PubMed  Article  CAS  Google Scholar 

  • Lin TF, Saiga S, Abe M, Laux T (2016) OBE3 and WUS interaction in shoot meristem stem cell regulation. PLoS ONE 11(5):e0155657

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Loriato VA, Martins LG, Euclydes NC, Reis PA, Duarte CE, Fontes EP (2020) Engineering resistance against geminiviruses: a review of suppressed natural defenses and the use of RNAi and the CRISPR/Cas system. Plant Sci 292:110410

    CAS  PubMed  Article  Google Scholar 

  • Lozano-Durán R, Rosas-Díaz T, Luna AP, Bejarano ER (2011) Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS ONE 6(7):e22383

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Mehta A, Brasileiro AC, Souza DS, Romano E, Campos MA, Grossi-de-Sá MF, Rocha TL (2008) Plant–pathogen interactions: what is proteomics telling us? FEBS J 275(15):3731–3746

    CAS  PubMed  Article  Google Scholar 

  • Meuzelaar H, Vreede J, Woutersen S (2016) Influence of Glu/Arg, Asp/Arg, and Glu/Lys salt bridges on α-helical stability and folding kinetics. Biophys J 110(11):2328–2341

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Morea EGO, da Silva EM, e Silva GFF, Valente GT, Rojas CHB, Vincentz M, Nogueira FTS (2016) Functional and evolutionary analyses of the miR156 and miR529 families in land plants. BMC Plant Biol 16(1):40

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Nair S (2013) Towards the analysis of Potyvirus VPg Interacting Protein (PVIP) gene expression in response to potyvirus infection. Doctoral dissertation, Auckland University of Technology

  • Nene YL (1973) Viral diseases of some warm weather pulse crops in India. Plant Dis Rep 57(5):463–467

    Google Scholar 

  • Ohtani M, Akiyoshi N, Takenaka Y, Sano R, Demura T (2016) Evolution of plant conducting cells: perspectives from key regulators of vascular cell differentiation. J Exp Bot 68(1):17–26

    Article  CAS  Google Scholar 

  • Pierce EJ, Rey MC (2013) Assessing global transcriptome changes in response to South African cassava mosaic virus [ZA-99] infection in susceptible Arabidopsis thaliana. PLoS ONE 8(6):e67534

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Piñeiro M, Gómez-Mena C, Schaffer R, Martínez-Zapater JM, Coupland G (2003) EARLY BOLTING IN SHORT DAYS is related to chromatin remodeling factors and regulates flowering in Arabidopsis by repressing FT. Plant Cell 15(7):1552–1562

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Pires ND, Dolan L (2012) Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc b Biol Sci 367(1588):508–518

    CAS  Article  Google Scholar 

  • Saiga S, Furumizu C, Yokoyama R, Kurata T, Sato S, Kato T, Komeda Y (2008) The Arabidopsis OBERON1 and OBERON2 genes encode plant homeodomain finger proteins and are required for apical meristem maintenance. Development 135(10):1751–1759

    CAS  PubMed  Article  Google Scholar 

  • Saiga S, Möller B, Watanabe-Taneda A, Abe M, Weijers D, Komeda Y (2012) Control of embryonic meristem initiation in Arabidopsis by PHD-finger protein complexes. Development 139(8):1391–1398

    CAS  PubMed  Article  Google Scholar 

  • Schenck S, Lehrer AT (2000) Factors affecting the transmission and spread of sugarcane yellow leaf virus. Plant Dis 84(10):1085–1088

    CAS  PubMed  Article  Google Scholar 

  • Smaczniak C, Immink RG, Angenent GC, Kaufmann K (2012) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139(17):3081–3098

    CAS  PubMed  Article  Google Scholar 

  • Sokalingam S, Raghunathan G, Soundrarajan N, Lee SG (2012) A study on the effect of surface lysine to arginine mutagenesis on protein stability and structure using green fluorescent protein. PLoS ONE 7(7):e40410

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Song W, Qin Y, Zhu Y, Yin G, Wu N, Li Y, Hu Y (2014) Delineation of plant caleosin residues critical for functional divergence, positive selection and coevolution. BMC Evol Biol 14(1):124

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Springer NM, Kaeppler SM (2005) Evolutionary divergence of monocot and dicot methyl-CpG-binding domain proteins. Plant Physiol 138(1):92–104

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Ito M (2005) Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc Natl Acad Sci 102(7):2436–2441

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wang X, Shi X, Chen S, Ma C, Xu S (2018) Evolutionary origin, gradual accumulation and functional divergence of heat shock factor gene family with plant evolution. Front Plant Sci 9:71

    PubMed  PubMed Central  Article  Google Scholar 

  • Xia R, Xu J, Meyers BC (2017) The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants. Plant Cell 29(6):1232–1247

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Yadav RK, Chattopadhyay D (2014) Differential soybean gene expression during early phase of infection with Mungbean yellow mosaic India virus. Mol Biol Rep 41(8):5123–5134

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

We acknowledge Bioinformatics lab of National Rice Research Institute for providing us Bioinformatics tools, software and hardware systems for our analysis. We acknowledge every person individually for helping us finish the analysis and manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cayalvizhi B. Sai.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

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.

Supplementary file1 (PDF 3606 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sai, C.B., Chidambaranathan, P. In-silico evolutionary analysis of plant-OBERON proteins during compatible MYMV infection in respect of improving host resistance. J Plant Res 135, 405–422 (2022). https://doi.org/10.1007/s10265-022-01372-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-022-01372-1

Keywords

  • Mungbean Yellow mosaic disease
  • Nuclear localization
  • Oberon protein
  • PHD and CC domain
  • Virus-host protein interaction and susceptibility