A Single Amino-acid Substitution Allows Endo-polygalacturonase of Fusarium Verticillioides to Acquire Recognition by PGIP2 from Phaseolus Vulgaris

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 Nov 22

PMID 24260434

Citations 14

Authors

Manuel Benedetti

Federico Andreani

Claudia Leggio

Luciano Galantini

Adele Di Matteo

Nicolae Viorel Pavel

Giulia De Lorenzo

Felice Cervone

Luca Federici

Francesca Sicilia

Affiliations

Soon will be listed here.

Abstract

Polygalacturonases (PGs) are secreted by phytopathogenic fungi to degrade the plant cell wall homogalacturonan during plant infection. To counteract Pgs, plants have evolved polygalacturonase-inhibiting proteins (PGIPs) that slow down fungal infection and defend cell wall integrity. PGIPs favour the accumulation of oligogalacturonides, which are homogalacturonan fragments that act as endogenous elicitors of plant defence responses. We have previously shown that PGIP2 from Phaseolus vulgaris (PvPGIP2) forms a complex with PG from Fusarium phyllophilum (FpPG), hindering the enzyme active site cleft from substrate. Here we analyse by small angle X-ray scattering (SAXS) the interaction between PvPGIP2 and a PG from Colletotrichum lupini (CluPG1). We show a different shape of the PG-PGIP complex, which allows substrate entry and provides a structural explanation for the different inhibition kinetics exhibited by PvPGIP2 towards the two isoenzymes. The analysis of SAXS structures allowed us to investigate the basis of the inability of PG from Fusarium verticilloides (FvPG) to be inhibited by PvPGIP2 or by any other known PGIP. FvPG is 92.5% identical to FpPG, and we show here, by both loss- and gain-of-function mutations, that a single amino acid site acts as a switch for FvPG recognition by PvPGIP2.

Citing Articles

Plant polygalacturonase structures specify enzyme dynamics and processivities to fine-tune cell wall pectins.

Safran J, Tabi W, Ung V, Lemaire A, Habrylo O, Bouckaert J Plant Cell. 2023; 35(8):3073-3091.

PMID: 37202370 PMC: 10396364. DOI: 10.1093/plcell/koad134.

The potential of plant proteins as antifungal agents for agricultural applications.

Chiu T, Poucet T, Li Y Synth Syst Biotechnol. 2022; 7(4):1075-1083.

PMID: 35891944 PMC: 9305310. DOI: 10.1016/j.synbio.2022.06.009.

New Players in the Interaction Between Beetle Polygalacturonases and Plant Polygalacturonase-Inhibiting Proteins: Insights From Proteomics and Gene Expression Analyses.

Haeger W, Wielsch N, Shin N, Gebauer-Jung S, Pauchet Y, Kirsch R Front Plant Sci. 2021; 12:660430.

PMID: 34149758 PMC: 8213348. DOI: 10.3389/fpls.2021.660430.

Interaction between Brassica napus polygalacturonase inhibition proteins and Sclerotinia sclerotiorum polygalacturonase: implications for rapeseed resistance to fungal infection.

Wang Z, Wan L, Zhang X, Xin Q, Song Y, Hong D Planta. 2021; 253(2):34.

PMID: 33459878 DOI: 10.1007/s00425-020-03556-2.

Direct evidence for a new mode of plant defense against insects via a novel polygalacturonase-inhibiting protein expression strategy.

Haeger W, Henning J, Heckel D, Pauchet Y, Kirsch R J Biol Chem. 2020; 295(33):11833-11844.

PMID: 32611768 PMC: 7450104. DOI: 10.1074/jbc.RA120.014027.

References

Hammel M . Validation of macromolecular flexibility in solution by small-angle X-ray scattering (SAXS). Eur Biophys J. 2012; 41(10):789-99. PMC: 3462898. DOI: 10.1007/s00249-012-0820-x. View

Cervone F, Hahn M, De Lorenzo G, Darvill A, Albersheim P . Host-Pathogen Interactions : XXXIII. A Plant Protein Converts a Fungal Pathogenesis Factor into an Elicitor of Plant Defense Responses. Plant Physiol. 1989; 90(2):542-8. PMC: 1061758. DOI: 10.1104/pp.90.2.542. View

Rambo R, Tainer J . Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law. Biopolymers. 2011; 95(8):559-71. PMC: 3103662. DOI: 10.1002/bip.21638. View

Rodriguez-Palenzuela P, Burr T, Collmer A . Polygalacturonase is a virulence factor in Agrobacterium tumefaciens biovar 3. J Bacteriol. 1991; 173(20):6547-52. PMC: 208991. DOI: 10.1128/jb.173.20.6547-6552.1991. View

Joubert D, Slaughter A, Kemp G, Becker J, Krooshof G, Bergmann C . The grapevine polygalacturonase-inhibiting protein (VvPGIP1) reduces Botrytis cinerea susceptibility in transgenic tobacco and differentially inhibits fungal polygalacturonases. Transgenic Res. 2006; 15(6):687-702. DOI: 10.1007/s11248-006-9019-1. View

Svergun D, Aldag I, Sieck T, Altendorf K, Koch M, Kane D . A model of the quaternary structure of the Escherichia coli F1 ATPase from X-ray solution scattering and evidence for structural changes in the delta subunit during ATP hydrolysis. Biophys J. 1998; 75(5):2212-9. PMC: 1299895. DOI: 10.1016/S0006-3495(98)77665-9. View

Sicilia F, Fernandez-Recio J, Caprari C, De Lorenzo G, Tsernoglou D, Cervone F . The polygalacturonase-inhibiting protein PGIP2 of Phaseolus vulgaris has evolved a mixed mode of inhibition of endopolygalacturonase PG1 of Botrytis cinerea. Plant Physiol. 2005; 139(3):1380-8. PMC: 1283773. DOI: 10.1104/pp.105.067546. View

Schneidman-Duhovny D, Kim S, Sali A . Integrative structural modeling with small angle X-ray scattering profiles. BMC Struct Biol. 2012; 12:17. PMC: 3427135. DOI: 10.1186/1472-6807-12-17. View

Firoz A, Malik A, Afzal O, Jha V . ContPro: A web tool for calculating amino acid contact distances in protein from 3D -structures at different distance threshold. Bioinformation. 2011; 5(2):55-7. PMC: 3039989. DOI: 10.6026/97320630005055. View

10.

Koch M, Vachette P, Svergun D . Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q Rev Biophys. 2003; 36(2):147-227. DOI: 10.1017/s0033583503003871. View

11.

DOvidio R, Mattei B, Roberti S, Bellincampi D . Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Biochim Biophys Acta. 2004; 1696(2):237-44. DOI: 10.1016/j.bbapap.2003.08.012. View

12.

Galantini L, Leggio C, Pavel N . Human serum albumin unfolding: a small-angle X-ray scattering and light scattering study. J Phys Chem B. 2008; 112(48):15460-9. DOI: 10.1021/jp806821e. View

13.

Sella L, Castiglioni C, Roberti S, DOvidio R, Favaron F . An endo-polygalacturonase (PG) of Fusarium moniliforme escaping inhibition by plant polygalacturonase-inhibiting proteins (PGIPs) provides new insights into the PG-PGIP interaction. FEMS Microbiol Lett. 2004; 240(1):117-24. DOI: 10.1016/j.femsle.2004.09.019. View

14.

Raiola A, Sella L, Castiglioni C, Balmas V, Favaron F . A single amino acid substitution in highly similar endo-PGs from Fusarium verticillioides and related Fusarium species affects PGIP inhibition. Fungal Genet Biol. 2008; 45(5):776-89. DOI: 10.1016/j.fgb.2007.11.003. View

15.

Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G . A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci U S A. 2010; 107(20):9452-7. PMC: 2889104. DOI: 10.1073/pnas.1000675107. View

16.

Oeser B, Heidrich P, Muller U, Tudzynski P, Tenberge K . Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet Biol. 2002; 36(3):176-86. DOI: 10.1016/s1087-1845(02)00020-8. View

17.

Ferrari S, Galletti R, Vairo D, Cervone F, De Lorenzo G . Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonase-inhibiting protein accumulation and enhances susceptibility to Botrytis cinerea. Mol Plant Microbe Interact. 2006; 19(8):931-6. DOI: 10.1094/MPMI-19-0931. View

18.

Federici L, Caprari C, Mattei B, Savino C, di Matteo A, De Lorenzo G . Structural requirements of endopolygalacturonase for the interaction with PGIP (polygalacturonase-inhibiting protein). Proc Natl Acad Sci U S A. 2001; 98(23):13425-30. PMC: 60887. DOI: 10.1073/pnas.231473698. View

19.

Boller T, Felix G . A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009; 60:379-406. DOI: 10.1146/annurev.arplant.57.032905.105346. View

20.

De Lorenzo G, Brutus A, Savatin D, Sicilia F, Cervone F . Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett. 2011; 585(11):1521-8. DOI: 10.1016/j.febslet.2011.04.043. View