Dr. Lionetti has a proven track record in the field of plant pathogen interactions, specifically in the area of plant cell wall involvement in these processes. Cell Wall Degrading Enzymes (CWDEs) are expressed by pathogens during host invasion to penetrate the cell wall barrier and colonize the tissue. Plants have evolved the ability to sense loss of cell wall integrity produced by pathogen attack and trigger defence responses leading to an improved resistance to disease. Dr Lionetti, togheter with his collaborators, significantly contributed to understanding the molecular bases of plant defence to biotic stresses. He demonstrated that the modulation of the expression of CWDEs or their inhibitors in planta represents a useful tool to improve plant resistance to pathogens and to investigate the role of altered structure and integrity of wall polysaccharides in plant-pathogen interactions. For example, by overexpressing a fungal endo-polygalacturonase in tobacco and Arabidopsis he contributed to dissect the signalling triggered by oligogalacturonides (OGs), the degradation products of pectin with elicitor activity ad inducers of plant protection from pests. The same approach was applied to dissect the plant responses to a fungal acetylesterase and a feruloylesterase. Moreover, he demonstrated that alterations of pectin esterification can lead to significant impact on cell wall degradability and, as a result of it, on plant susceptibility to pathogens. In more recent work, Dr. Lionetti applying his competence in glycomics of cell wall polysaccharides acquired in his experiences abroad, uncovered specific cell wall components responsible for susceptibility in Arabidopsis and wheat to fungal necrotrophs. He also proposed biotechnological applications of the CWDEs and their inhibitors to improve saccharification of cell wall polysaccharides, the quality of plant derived products, and protoplast isolation. He developed new methodologies to investigate plant defence mechanisms against biotic stresses.
Cell wall dynamics during necrotrophs invasion. (A) Necrotrophic fungi secrete a large arsenal of CWDEs like PGs, hemicellulases and cellulases, assisted by PMEs and AEs in the apoplastic space to degrade cell wall polymers and facilitate the availability of nutrients. PGs and EIXs have been proposed to function as PAMPs recognized by the membrane receptors RBPG1 and Eix1 or 2 respectively. (B) As first line of defense, plants produce a variety of CWDE inhibitors to hinder degradation by microbial CWDEs. For instance, the inhibition of PG degrading activity by PGIPs induce the accumulation of elicitor-active pectin fragments (OGs) perceived by WAK1 receptors. It cannot be excluded the presence of other not yet identified receptors sensing damage of other cell wall components. The perception of cell wall damage triggers specific signaling pathways activating defence responces aimed to reinforce cell wall structure. The more evident defense strategies are callose and lignin deposition, induction of peroxidases/ROS-mediated crosslinks between cell wall structural proteins and polysaccharides. (C) Necrotrophs force plants to cooperate in disease exploiting plant cellulases, expansins, PGs and PMEs as susceptibility factors. PM, plasma membrane; CW, cell wall; Cyt, cytoplasm; OGs, oligogalacturonides; WAK1, wall associated kinase 1; AEs, acetyl esterases; PGs, polygalacturonases; EIX, ethylen induced xylanase; PME, pectin methylesterases; PMEI, pectin methylesterase inhibitor; FA, ferulic acid; FAE, ferulic acid esterase; XI, xylanase inhibitor; PRR, pattern recognition receptor; POX, peroxidase; ROS, reactive oxygen species
1: Lionetti V, Fabri E, De Caroli M, Hansen AR, Willats WG, Piro G, Bellincampi D. Three Pectin Methylesterase Inhibitors Protect Cell Wall Integrity for Arabidopsis Immunity to Botrytis. Plant Physiol. 2017 Mar;173(3):1844-1863. doi: 10.1104/pp.16.01185. Epub 2017 Jan 12. PubMed PMID: 28082716; PubMed Central PMCID: PMC5338656. 2: Tundo S, Kalunke R, Janni M, Volpi C, Lionetti V, Bellincampi D, Favaron F, D'Ovidio R. Pyramiding PvPGIP2 and TAXI-III But Not PvPGIP2 and PMEI Enhances Resistance Against Fusarium graminearum. Mol Plant Microbe Interact. 2016 Aug;29(8):629-39. doi: 10.1094/MPMI-05-16-0089-R. Epub 2016 Jul 27. PubMed PMID: 27366923. 3: Reem NT, Pogorelko G, Lionetti V, Chambers L, Held MA, Bellincampi D, Zabotina OA. Decreased Polysaccharide Feruloylation Compromises Plant Cell Wall Integrity and Increases Susceptibility to Necrotrophic Fungal Pathogens. Front Plant Sci. 2016 May 10;7:630. doi: 10.3389/fpls.2016.00630. eCollection 2016. PubMed PMID: 27242834; PubMed Central PMCID: PMC4862258. 4: Lionetti V, Raiola A, Mattei B, Bellincampi D. The Grapevine VvPMEI1 Gene Encodes a Novel Functional Pectin Methylesterase Inhibitor Associated to Grape Berry Development. PLoS One. 2015 Jul 23;10(7):e0133810. doi: 10.1371/journal.pone.0133810. eCollection 2015. PubMed PMID: 26204516; PubMed Central PMCID: PMC4512722. 5: Lionetti V. PECTOPLATE: the simultaneous phenotyping of pectin methylesterases, pectinases, and oligogalacturonides in plants during biotic stresses. Front Plant Sci. 2015 May 13;6:331. doi: 10.3389/fpls.2015.00331. eCollection 2015. PubMed PMID: 26029230; PubMed Central PMCID: PMC4429564. 6: Lionetti V, Cervone F, De Lorenzo G. A lower content of de-methylesterified homogalacturonan improves enzymatic cell separation and isolation of mesophyll protoplasts in Arabidopsis. Phytochemistry. 2015 Apr;112:188-94. doi: 10.1016/j.phytochem.2014.07.025. Epub 2014 Aug 13. PubMed PMID: 25128920. 7: Lionetti V, Giancaspro A, Fabri E, Giove SL, Reem N, Zabotina OA, Blanco A, Gadaleta A, Bellincampi D. Cell wall traits as potential resources to improve resistance of durum wheat against Fusarium graminearum. BMC Plant Biol. 2015 Jan 19;15:6. doi: 10.1186/s12870-014-0369-1. PubMed PMID: 25597920; PubMed Central PMCID: PMC4298115. 8: Lionetti V, Métraux JP. Plant cell wall in pathogenesis, parasitism and symbiosis. Front Plant Sci. 2014 Nov 6;5:612. doi: 10.3389/fpls.2014.00612. eCollection 2014. PubMed PMID: 25414718; PubMed Central PMCID: PMC4222219. 9: Bellincampi D, Cervone F, Lionetti V. Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Front Plant Sci. 2014 May 28;5:228. doi: 10.3389/fpls.2014.00228. eCollection 2014. Review. PubMed PMID: 24904623; PubMed Central PMCID: PMC4036129. 10: Lionetti V, Raiola A, Cervone F, Bellincampi D. Transgenic expression of pectin methylesterase inhibitors limits tobamovirus spread in tobacco and Arabidopsis. Mol Plant Pathol. 2014 Apr;15(3):265-74. doi: 10.1111/mpp.12090. Epub 2013 Dec 5. Erratum in: Mol Plant Pathol. 2014 Aug;15(6):646. PubMed PMID: 24127644. 11: Lionetti V, Raiola A, Cervone F, Bellincampi D. How do pectin methylesterases and their inhibitors affect the spreading of tobamovirus? Plant Signal Behav. 2014;9(12):e972863. doi: 10.4161/15592316.2014.972863. PubMed PMID: 25482766; PubMed Central PMCID: PMC4623000. 12: Francocci F, Bastianelli E, Lionetti V, Ferrari S, De Lorenzo G, Bellincampi D, Cervone F. Analysis of pectin mutants and natural accessions of Arabidopsis highlights the impact of de-methyl-esterified homogalacturonan on tissue saccharification. Biotechnol Biofuels. 2013 Nov 18;6(1):163. doi: 10.1186/1754-6834-6-163. PubMed PMID: 24245704; PubMed Central PMCID: PMC3843582. 13: Pogorelko G, Lionetti V, Bellincampi D, Zabotina O. Cell wall integrity: targeted post-synthetic modifications to reveal its role in plant growth and defense against pathogens. Plant Signal Behav. 2013 Sep;8(9). pii: e25435. doi: 10.4161/psb.25435. Epub 2013 Jun 20. Review. PubMed PMID: 23857352; PubMed Central PMCID: PMC4002593. 14: Pogorelko G, Lionetti V, Fursova O, Sundaram RM, Qi M, Whitham SA, Bogdanove AJ, Bellincampi D, Zabotina OA. Arabidopsis and Brachypodium distachyon transgenic plants expressing Aspergillus nidulans acetylesterases have decreased degree of polysaccharide acetylation and increased resistance to pathogens. Plant Physiol. 2013 May;162(1):9-23. doi: 10.1104/pp.113.214460. Epub 2013 Mar 5. PubMed PMID: 23463782; PubMed Central PMCID: PMC3641233. 15: Lionetti V, Cervone F, Bellincampi D. Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. J Plant Physiol. 2012 Nov 1;169(16):1623-30. doi: 10.1016/j.jplph.2012.05.006. Epub 2012 Jun 18. Review. PubMed PMID: 22717136. 16: Reca IB, Lionetti V, Camardella L, D'Avino R, Giardina T, Cervone F, Bellincampi D. A functional pectin methylesterase inhibitor protein (SolyPMEI) is expressed during tomato fruit ripening and interacts with PME-1. Plant Mol Biol. 2012 Jul;79(4-5):429-42. doi: 10.1007/s11103-012-9921-2. Epub 2012 May 19. PubMed PMID: 22610346. 17: Volpi C, Janni M, Lionetti V, Bellincampi D, Favaron F, D'Ovidio R. The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant Microbe Interact. 2011 Sep;24(9):1012-9. doi: 10.1094/MPMI-01-11-0021. PubMed PMID: 21585271. 18: Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G, Cervone F, Bellincampi D. Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe Interact. 2011 Apr;24(4):432-40. doi: 10.1094/MPMI-07-10-0157. PubMed PMID: 21171891.
19: Lionetti V, Francocci F, Ferrari S, Volpi C, Bellincampi D, Galletti R, D'Ovidio R, De Lorenzo G, Cervone F. Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):616-21. doi: 10.1073/pnas.0907549107. Epub 2009 Dec 22. PubMed PMID: 20080727; PubMed Central PMCID: PMC2818903. 20: Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G. Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol. 2008 Feb;146(2):669-81. Epub 2007 Dec 7. PubMed PMID: 18065558; PubMed Central PMCID: PMC2245817. 21: Lionetti V, Raiola A, Camardella L, Giovane A, Obel N, Pauly M, Favaron F, Cervone F, Bellincampi D. Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol. 2007 Apr;143(4):1871-80. Epub 2007 Feb 2. PubMed PMID: 17277091; PubMed Central PMCID: PMC1851811.