Skip to main content
SpringerLink
Log in

Positive Selection in the Chloroplastic ATP-Synthase β-Subunit and Its Relation to Virulence Factors

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The most paradigmatic examples of molecular evolution under positive selection involve genes related to the immune system. Recently, different chloroplastic factors have been shown to be important for plant defenses, among them, the α- and β-subunits of the ATP synthase. The β-subunit has been reported to interact with several viral proteins while both proteins have been implicated with sensitivity to tentoxin, a phytotoxin produced by the widespread fungus Alternaria alternata. Given the relation of both protein to virulence factors, we studied whether these proteins are evolving under positive selection. To this end, we used the dN/dS ratio to examine possible sites under positive selection in several Angiosperm clades. After examining 79 plant genera and 1232 species, we found three times more sites under pervasive diversifying selection in the N-terminal region of the β-subunit compared to the α-subunit, supporting previous results which identified this region as responsible for interacting with viral proteins. Moreover, we found the site 83 of β-subunit under positive selection in several plant genera, a site clearly related to the sensitivity to tentoxin according to biochemistry assays, which possibly reflects the selective pressure of the non-host specific tentoxin across various Angiosperm clades.

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

  • Akhtar KP, Saleem MY, Asghar M, Haq MA (2004) New report of Alternaria alternaria causing leaf blight of tomato in Pakistan. Plant Pathol 53:816

    Article  Google Scholar 

  • Ashkenazy H, Abadi S, Martz E, Chay O, Mayrose I, Pupko T, Ben-Tal N (2016) ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res 44:W344–W350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38:529–533

    Article  CAS  Google Scholar 

  • Avni A, Anderson JD, Holland N, Rochaix JD, Gromet-Elhanan Z, Edelman M (1992) Tentoxin sensitivity of chloroplasts determined by Codon 83 of β subunit of proton-ATPase. Science (80-) 257:1245–1247

    Article  CAS  Google Scholar 

  • Celniker G, Nimrod G, Ashkenazy H, Glaser F, Martz E, Mayrose I, Pupko T, Ben-Tal N (2013) ConSurf: using evolutionary data to raise testable hypotheses about protein function. Isr J Chem 53:199–206

    Article  CAS  Google Scholar 

  • D’Anatro A, Giorello F, Feijoo M, Lessa EP (2017) Testing for the occurrence of selective episodes during the divergence of otophysan fishes: insights from mitogenomics. J Mol Evol 84:162–173

    Article  PubMed  CAS  Google Scholar 

  • Daugherty MD, Malik HS (2012) Rules of engagement: molecular insights from host-virus arms races. Annu Rev Genet 46:677–700

    Article  CAS  PubMed  Google Scholar 

  • Durbin RD, Uchytil TF (1977) A survey of plant insensitivity to tentoxin. Phytopathology 77:602

    Article  Google Scholar 

  • Edgar RC (2004a) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004b) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:1–19

    Article  CAS  Google Scholar 

  • Fan WB, Wu Y, Yang J, Shahzad K, Li ZH (2018) Comparative chloroplast genomics of dipsacales species: Insights into sequence variation, adaptive evolution, and phylogenetic relationships. Front Plant Sci 9:1–13

    Article  Google Scholar 

  • Gellért Á, Pósa T, Fábián A, Szabó L, Bóka K, Forró B, Salánki K, Drahos L, Tóth E, Juhász A, Balázs E (2018) A single point mutation on the cucumber mosaic virus surface induces an unexpected and strong interaction with the F1 complex of the ATP synthase in Nicotiana clevelandii plants. Virus Res 251:47–55

    Article  PubMed  CAS  Google Scholar 

  • Gharib WH, Robinson-Rechavi M (2013) The branch-site test of positive selection is surprisingly robust but lacks power under synonymous substitution saturation and variation in GC. Mol Biol Evol 30:1675–1686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glaser F, Pupko T, Paz I, Bell RE, Bechor-Shental D, Martz E, Ben-Tal N (2003) ConSurf: Identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19:163–164

    Article  CAS  PubMed  Google Scholar 

  • González-Díaz JG, García-Velasco R, Camacho-Cerón G, Nieto-Ángel D (2011) CANKER IN Salix bonplandiana KUNTH TWIGS CAUSED BY Alternaria tenuissima (KUNZE EX PERS.) WILTSHIRE. Agrociencia 45:75–86

    Google Scholar 

  • Groth G (2002) Structure of spinach chloroplast F1-ATPase complexed with the phytopathogenic inhibitor tentoxin. Proc Natl Acad Sci USA 99:3464–3468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groth G, Pohl E (2001) The structure of the chloroplast F1-ATPase at 3.2 Å resolution. J Biol Chem 276:1345–1352

    Article  CAS  PubMed  Google Scholar 

  • Group TAP, Chase MW, Christenhusz MJM, Fay MF, Byng JW, Judd WS, Soltis DE, Mabberley DJ, Sennikov AN, Soltis PS, Stevens PF (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Article  Google Scholar 

  • Hermida-Carrera C, Fares MA, Fernández Á, Gil-Pelegrín E, Kapralov MV, Mir A, Molins A, Peguero-Pina JJ, Rocha J, Sancho-Knapik D, Galmés J (2017) Positively selected amino acid replacements within the RuBisCO enzyme of oak trees are associated with ecological adaptations. PLoS ONE 12:1–21

    Google Scholar 

  • Hosseinnia A, Mohammadi A (2018) Investigating the pathogenicity of Alternaria alternata on Lonicera japonica. Azarian J Agric 5:44–48

    Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, Von HA, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapralov MV, Filatov DA (2007) Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evol Biol 7:1–10

    Article  CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533

    Article  CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  CAS  Google Scholar 

  • Kretschmer M, Damoo D, Djamei A, Kronstad J (2020) Chloroplasts and plant immunity: Where are the fungal effectors? Pathogens 9:1–16

    Google Scholar 

  • Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, Pupko T, Ben-Tal N (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33:299–302

    Article  CAS  Google Scholar 

  • Larsson A (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30:3276–3278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leyva JA, Bianchet MA, Amzel LM (2003) Understanding ATP synthesis: structure and mechanism of the F1-ATPase (review). Mol Membr Biol 20:27–33

    Article  CAS  PubMed  Google Scholar 

  • Liu ML, Fan WB, Wang N, Bin DP, Zhang TT, Yue M, Li ZH (2018) Evolutionary analysis of plastid genomes of seven lonicera L. species: Implications for sequence divergence and phylogenetic relationships. Int J Mol Sci 19:1–17

    CAS  Google Scholar 

  • Meena M, Gupta SK, Swapnil P, Zehra A, Dubey MK, Upadhyay RS (2017) Alternaria toxins: potential virulence factors and genes related to pathogenesis. Front Microbiol 8:1451

    Article  PubMed  PubMed Central  Google Scholar 

  • Mirzwa-Mróz E, Kukula W, Frydrych I, Wit M, Wakulińsk W (2018) First report of Alternaria black spot caused by Alternaria Alternata on blue honeysuckle in Poland. Plant Dis 102:820

    Article  Google Scholar 

  • Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained bayesian AppRoximation for inferring selection. Mol Biol Evol 30:1196–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen LT, Schmidt HA, Von HA, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

    Article  CAS  PubMed  Google Scholar 

  • Oka K, Okubo A, Kodama M, Otani H (2006) Detoxification of α-tomatine by tomato pathogens Alternaria alternata tomato pathotype and Corynespora cassiicola and its role in infection. J Gen Plant Pathol 72:152–158

    Article  CAS  Google Scholar 

  • Qian J, Liu Y, Ma C, Chao N, Chen Q, Zhang Y, Luo Y, Cai D, Wu Y (2019) Positive selection of squalene synthase in Cucurbitaceae plants. Int J Genomics 2019:5913491

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ranwez V, Harispe S, Delsuc F, Douzery EJP (2011) MACSE: multiple alignment of coding sequences accounting for frameshifts and stop codons. PLoS ONE 6:e22594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Self RL, Zarko ML (1975) Control of Alternaria alternata on red maple (Acer palmatum). Proc SNA Res Conf Annu Rep South Nurserymen’s Assoc 20:57–58

    Google Scholar 

  • Seo EY, Nam J, Kim HS, Park YH, Hong SM, Lakshman D, Bae H, Hammond J, Lim HS (2014) Selective Interaction between chloroplast β-ATPase and TGB1L88 retards severe symptoms caused by Alternanthera mosaic virus infection. Plant Pathol J 30:58–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serrano I, Audran C, Rivas S (2016) Chloroplasts at work during plant innate immunity. J Exp Bot 67:3845–3854

    Article  CAS  PubMed  Google Scholar 

  • Shao-hua W, You-wei C, Zhi-ying L, Li-yuan Y, Shao-lan L (2011) Metabolites of the endophytic fungus Alternaria sp PR-14 of Paeonia delavayi. Nat Prod Res Dev 23:850

    Google Scholar 

  • Steele JA, Uchytil TF, Durbin RD (1977) The binding of tentoxin to a tryptic digest of chloroplast coupling factor 1. Biochim Biophys Acta 459:347–350

    Article  CAS  PubMed  Google Scholar 

  • Tu Y, Jin Y, Ma D, Li H, Zhang Z, Dong J, Wang T (2015) Interaction between PVY HC-Pro and the NtCF1 β-subunit reduces the amount of chloroplast ATP synthase in virus-infected tobacco. Sci Rep 5:1–14

    Google Scholar 

  • Tucker WC, Du Z, Hein R, Gromet-Elhanan Z, Richter ML (2001) Role of the ATP synthase α-subunit in conferring sensitivity to tentoxin. Biochemistry 40:7542–7548

    Article  CAS  PubMed  Google Scholar 

  • Wang JT, Ma ZH, Wang GK, Xu FQ, Chen L, Yu Y, Wang G, Liu JS (2019) Four meroterpenoids from Alternaria alternata isolated from Paeonia lactiflora. Phytochem Lett 31:1–4

    Article  CAS  Google Scholar 

  • Weaver S, Shank SD, Spielman SJ, Li M, Muse SV, Kosakovsky Pond SL (2018) Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 35:773–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Liu F, Yang DG, Li W, Zhou XJ, Pei XY, Liu YG, He KL, Zhang WS, Ren ZY, Zhou KH, Ma XF et al (2018) Comparative chloroplast genomics of Gossypium species: insights into repeat sequence variations and phylogeny. Front Plant Sci 9:1–14

    Article  Google Scholar 

  • Xia X (2018) DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Mol Biol Evol 35:1550–1552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Salemi M, Vandamme A-M, Lemey P (eds) The phylogenetic handbook: practical approach to phylogenetic analysis and hypothesis testing. Cambridge University Press, Cambridge, pp 615–630

    Chapter  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    Article  CAS  PubMed  Google Scholar 

  • Xie DF, Yu Y, Deng YQ, Li J, Liu HY, Zhou SD, He XJ (2018) Comparative analysis of the chloroplast genomes of the chinese endemic genus urophysa and their contribution to chloroplast phylogeny and adaptive evolution. Int J Mol Sci 19:1–20

    Google Scholar 

  • Yang Z, Nielsen R (2001) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19:908–917

    Article  Google Scholar 

  • Zhang Z, An M, Miao J, Gu Z, Liu C, Zhong B (2018) The Antarctic sea ice alga Chlamydomonas sp. ICE-L provides insights into adaptive patterns of chloroplast evolution. BMC Plant Biol 18:1–12

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Joaquina Farias and Facundo M. Giorello have contributed equally to this work.

Authors and Affiliations

  1. PDU Espacio de Biología Vegetal del Noreste, Centro Universitario de Tacuarembó (CUT), UdelaR, Ruta 5 km 386,200, 45000, Tacuarembó, Uruguay

    Joaquina Farias & Facundo M. Giorello

Authors
  1. Joaquina Farias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Facundo M. Giorello
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Facundo M. Giorello.

Ethics declarations

Competing 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

Handling Editor: David Alvarez-Ponce.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Tables (XLS 207 kb)

Supplementary File 1. Alignments of atpB and atpA for the intra-genus and global analysis (7Z 650 kb)

239_2020_9968_MOESM3_ESM.fasta

Supplementary File 2. Alignment of atpB showing the correspondence of the codon 117 with the spinach’ β83 site, related to tentoxin sensitivity (FASTA 787 kb)

239_2020_9968_MOESM4_ESM.png

Figure S1. Distribution of dN/dS values for atpB and atpA. The density for atpB is represented in red while the density for atpA is displayed in blue (PNG 144 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farias, J., Giorello, F.M. Positive Selection in the Chloroplastic ATP-Synthase β-Subunit and Its Relation to Virulence Factors. J Mol Evol 88, 703–713 (2020). https://doi.org/10.1007/s00239-020-09968-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-020-09968-8

Keywords

Search

Navigation