CoChat
Sign Up
Cited by 76Polysaccharides and Plant Cell WallsPostharvest Quality and Shelf Life ManagementPlant Surface Properties and Treatments

The DOI matches its Crossref record.

A functional pectin methylesterase inhibitor protein (SolyPMEI) is expressed during tomato fruit ripening and interacts with PME-1

Reca, Ida Barbara, Lionetti, Vincenzo, Camardella, Laura, D’Avino, Rossana, Giardina, Thierry, Cervone, Felice, Bellincampi, Daniela·2012·Plant Molecular Biology
DOI 10.1007/s11103-012-9921-2
Open this paper in CoChat — free account

Abstract

A pectin methylesterase inhibitor (SolyPMEI) from tomato has been identified and characterised by a functional genomics approach. SolyPMEI is a cell wall protein sharing high similarity with Actinidia deliciosa PMEI (AdPMEI), the best characterised inhibitor from kiwi. It typically affects the activity of plant pectin methylesterases (PMEs) and is inactive against a microbial PME. SolyPMEI transcripts were mainly expressed in flower, pollen and ripe fruit where the protein accumulated at breaker and turning stages of ripening. The expression of SolyPMEI correlated during ripening with that of PME-1, the major fruit specific PME isoform. The interaction of SolyPMEI with PME-1 was demonstrated in ripe fruit by gel filtration and by immunoaffinity chromatography. The analysis of the zonal distribution of PME activity and the co-localization of SolyPMEI with high esterified pectins suggest that SolyPMEI regulates the spatial patterning of distribution of esterified pectins in fruit.

Overview

Integrity signals

Registry

Crossref · 10.1007/s11103-012-9921-2

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Still being checked.

Research works printed but not linked: 84

  1. An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78 · DOI
  2. Atkinson RG, Bolitho KM, Wright MA, Iturriagagoitia-Bueno T, Reid SJ, Ross GS (1998) Apple ACC-oxidase and polygalacturonase: ripening-specific gene expression and promoter analysis in transgenic tomato. Plant Mol Biol 38:449–460 · DOI
  3. Balestrieri C, Castaldo D, Giovane A, Quagliuolo L, Servillo L (1990) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit (Actinidia chinensis). Eur J Biochem 193:183–187 · DOI
  4. Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37:859–869 · DOI
  5. Blumer JM, Clay RP, Bergmann CW, Albersheim P, Darvill A (2000) Characterization of changes in pectin methylesterase expression and pectin esterification during tomato fruit ripening. Can J Bot 78:607–618
  6. Bordenave M, Goldberg R (1993) Purification and characterization of pectin methylesterases from Mung bean hypocotyl cell walls. Phytochemistry 33:999–1003 · DOI
  7. Bosch M, Cheung AY, Hepler PK (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138:1334–1346 · DOI
  8. Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340 · DOI
  9. Camardella L, Carratore V, Ciardiello MA, Servillo L, Balestrieri C, Giovane A (2000) Kiwi protein inhibitor of pectin methylesterase amino-acid sequence and structural importance of two disulfide bridges. Eur J Biochem 267:4561–4565 · DOI
  10. Cervone F, De Lorenzo G, Degrà L, Salvi G, Bergami M (1987) Purification and characterization of a polygalacturonase- inhibiting protein from Phaseolus vulgaris L. Plant Physiol 85:631–637 · DOI
  11. Chen M-H, Citovsky V (2003) Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant J 35:386–392 · DOI
  12. Ciardiello MA, D’Avino R, Amoresano A, Tuppo L, Carpentieri A, Carratore V, Tamburrini M, Giovane A, Pucci P, Camardella L (2008) The peculiar structural features of kiwi fruit pectin methylesterase: Amino acid sequence, oligosaccharides structure, and modeling of the interaction with its natural proteinaceous inhibitor. Proteins 71:195–206 · DOI
  13. De Caroli M, Lenucci MS, Di Sansebastiano GP, Dalessandro G, De Lorenzo G, Piro G (2011) Protein trafficking to the cell wall occurs through mechanisms distinguishable from default sorting in tobacco. Plant Journal 65:295–308 · DOI
  14. Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, Cervone F, Bellincampi D, Tsernoglou D (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17:849–858 · DOI
  15. Di Sansebastiano GP, Paris N, Marc-Martin S, Neuhaus JM (1998) Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting pathway. Plant Journal 15:449–457 · DOI
  16. Dorokhov YL, Makinen K, Frolova OY, Merits A, Saarinen J, Kalkkinen N, Atabekov JG, Saarma M (1999) A novel function for a ubiquitous plant enzyme pectin methylesterase: the host-cell receptor for the tobacco mosaic virus movement protein. FEBS Lett 461:223–228 · DOI
  17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 · DOI
  18. Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G (2008) Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol 146:669–681 · DOI
  19. Futamura N, Mori H, Kouchi H, Shinohara K (2000) Male flower-specific expression of genes for polygalacturonase, pectin methylesterase and beta-1,3-glucanase in a dioecious willow (Salix gilgiana Seemen). Plant Cell Physiol 41:16–26 · DOI
  20. Gaffe J, Tiznado ME, Handa AK (1997) Characterization and functional expression of a ubiquitously expressed tomato pectin methylesterase. Plant Physiol 114:1547–1556 · DOI
  21. Giovane A, Balestrieri C, Quagliuolo L, Castaldo D, Servillo L (1995) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit - Purification by affinity chromatography and evidence of a ripening-related precursor. Eur J Biochem 233:926–929 · DOI
  22. Greer J (1990) Comparative modeling of proteins in the design of novel renin inhibitors. Biophys J 57:A207 · DOI
  23. Grsic-Rausch S, Rausch T (2004) A coupled spectrophotometric enzyme assay for the determination of pectin methylesterase activity and its inhibition by proteinaceous inhibitors. Anal Biochem 333:14–18 · DOI
  24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
  25. Hall LN, Bird CR, Picton S, Tucker GA, Seymour GB, Grierson D (1994) Molecular characterization of cDNA clones representing pectin esterase isozymes from tomato. Plant Mol Biol 25:313–318 · DOI
  26. Hao YL, Huang XY, Mei XH, Li RY, Zhai ZY, Yin S, Huang Y, Luo YB (2008) Expression, purification and characterization of pectin methylesterase inhibitor from kiwi fruit in Escherichia coli. Protein Expr Purif 60:221–224 · DOI
  27. Harriman RW, Tieman DM, Handa AK (1991) Molecular cloning of tomato pectin methylesterase gene and its expression in Rutgers, ripening inhibitor, nonripening, and never ripe tomato fruits. Plant Physiol 97:80–87 · DOI
  28. Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci USA 94:2122–2127 · DOI
  29. Hasunuma T, Fukusaki E, Kobayashi A (2004) Expression of fungal pectin methylesterase in transgenic tobacco leads to alteration in cell wall metabolism and a dwarf phenotype. J Biotechnol 111:241–251 · DOI
  30. Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093 · DOI
  31. Hong MJ, Kim DJ, Lee TG, Jeon WB, Seo YW (2010) Functional characterization of pectin methylesterase inhibitor (PMEI) in wheat. Genes Genet Syst 85:97–106 · DOI
  32. Hothorn M, Van den Ende W, Lammens W, Rybin V, Scheffzek K (2010) Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein. Proc Nat Acad Sci USA 107:17427–17432 · DOI
  33. Irifune K, Nishida T, Egawa H, Nagatani A (2004) Pectin methylesterase inhibitor cDNA from kiwi fruit. Plant Cell Rep 22:333–338 · DOI
  34. Jolie RP, Duvetter T, Van Loey AM, Hendrickx ME (2010) Pectin methylesterase and its proteinaceous inhibitor: a review. Carbohydr Res 345:2583–2595 · DOI
  35. Juge N (2006) Plant protein inhibitors of cell wall degrading enzymes. Trends Plant Sci 11:359–367 · DOI
  36. Koch JL, Nevins DJ (1989) Tomato fruit cell wall. I. Use of purified tomato polygalacturonase and pectinmethylesterase to identify developmental changes in pectins. Plant Physiol 91:816–822 · DOI
  37. Kojima K, Sakurai N, Kuraishi S, Yamamoto R, Nevins DJ (1991) Novel technique for measuring tissue firmness within tomato (Lycopersicon-Esculentum Mill) fruit. Plant Physiol 96:545–550 · DOI
  38. Limberg G, Korner R, Buchholt HC, Christensen TM, Roepstorff P, Mikkelsen JD (2000) Analysis of different de-esterification mechanisms for pectin by enzymatic fingerprinting using endopectin lyase and endopolygalacturonase II from A. niger. Carbohydr Res 327:293–307 · DOI
  39. Lionetti V, Raiola A, Camardella L, Giovane A, Obel N, Pauly M, Favaron F, Cervone F, Bellincampi D (2007) Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol 143:1871–1880 · DOI
  40. Lionetti V, Francocci F, Ferrari S, Volpi C, Bellincampi D, Galletti R, D’Ovidio R, De Lorenzo G, Cervone F (2010) Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc Natl Acad Sci USA 107:616–621 · DOI
  41. Lohaus G, Pennewiss K, Sattelmacher B, Hussmann M, Hermann MK (2001) Is the infiltration-centrifugation technique appropriate for the isolation of apoplastic fluid? A critical evaluation with different plant species. Physiol Plant 111:457–465 · DOI
  42. Markovic O, Janecek S (2001) Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution. Protein Eng 14:615–631 · DOI
  43. Markovic O, Janecek S (2004) Pectin methylesterases: sequence-structural features and phylogenetic relationships. Carbohydr Res 339:2281–2295 · DOI
  44. Markovic O, Jörnvall H (1986) Pectinesterase - the Primary Structure of the Tomato Enzyme. Eur J Biochem 158:455–462 · DOI
  45. Matsudaira P (1987) Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem 262:10035–10038 · DOI
  46. McCartney L, Ormerod AP, Gidley MJ, Knox JP (2000) Temporal and spatial regulation of pectic (1-4)-beta-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J 22:105–113 · DOI
  47. Mei XH, Hao YL, Zhu HL, Gao HY, Luo YB (2007) Cloning of pectin methylesterase inhibitor from kiwi fruit and its high expression in Pichia pastoris. Enzyme Microbial Technol 40:1001–1005 · DOI
  48. Mohnen D (2008) Pectin structure and biosynthesis. Curr Op Plant Biol 11:266–277 · DOI · Paper page
  49. Montgomery J, Goldman S, Deikman J, Margossian L, Fischer RL (1993) Identification of an ethylene-responsive region in the promoter of a fruit ripening gene. Proc Natl Acad Sci USA 90:5939–5943 · DOI
  50. Orfila C, Huisman MM, Willats WG, van Alebeek GJ, Schols HA, Seymour GB, Knox JP (2002) Altered cell wall disassembly during ripening of Cnr tomato fruit: implications for cell adhesion and fruit softening. Planta 215:440–447 · DOI
  51. Peaucelle A, Louvet R, Johansen JN, Hofte H, Laufs P, Pelloux J, Mouille G (2008) Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr Biol 18:1943–1948 · DOI
  52. Pelletier S, Van Orden J, Wolf S, Vissenberg K, Delacourt J, Ndong YA, Pelloux J, Bischoff V, Urbain A, Mouille G, Lemonnier G, Renou JP, Hofte H (2010) A role for pectin de-methylesterification in a developmentally regulated growth acceleration in dark-grown Arabidopsis hypocotyls. New Phytol 188:726–739 · DOI
  53. Pelloux J, Rusterucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277 · DOI
  54. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45 · DOI · Paper page
  55. Phan TD, Bo W, West G, Lycett GW, Tucker GA (2007) Silencing of the major salt-dependent isoform of pectinesterase in tomato alters fruit softening. Plant Physiol 144:1960–1967 · DOI
  56. Pilling J, Willmitzer L, Bucking H, Fisahn J (2004) Inhibition of a ubiquitously expressed pectin methyl esterase in Solanum tuberosum L. affects plant growth, leaf growth polarity, and ion partitioning. Planta 219:32–40 · DOI
  57. Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756 · DOI
  58. Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena—an overview. Crit Rev Food Sci Nutr 47:1–19 · DOI
  59. Pressey R, Avants JK (1972) Multiple forms of pectinesterase in tomatoes. Phytochemistry 11:3139–3142 · DOI
  60. Raiola A, Camardella L, Giovane A, Mattei B, De Lorenzo G, Cervone F, Bellincampi D (2004) Two Arabidopsis thaliana genes encode functional pectin methylesterase inhibitors. FEBS Lett 557:199–203 · DOI
  61. Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G, Cervone F, Bellincampi D (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant-Microbe Interact 24:432–440 · DOI
  62. Ray J, Knapp J, Grierson D, Bird C, Schuch W (1988) Identification and sequence determination of a cDNA clone for tomato pectin esterase. Eur J Biochem 174:119–124 · DOI
  63. Reca IB, Brutus A, D’Avino R, Villard C, Bellincampi D, Giardina T (2008) Molecular cloning, expression and characterization of a novel apoplastic invertase inhibitor from tomato (Solanum lycopersicum) and its use to purify a vacuolar invertase. Biochimie 90:1611–1623 · DOI
  64. Ren C, Kermode AR (2000) An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant Physiol 124:231–242 · DOI
  65. Rockel N, Wolf S, Kost B, Rausch T, Greiner S (2008) Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J 53:133–143 · DOI
  66. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
  67. Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234:779–815 · DOI · Paper page
  68. Scognamiglio MA, Ciardiello MA, Tamburrini M, Carratore V, Rausch T, Camardella L (2003) The plant invertase inhibitor shares structural properties and disulfide bridges arrangement with the pectin methylesterase inhibitor. J Prot Chem 22:363–369 · DOI
  69. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal Chem 68:850–858 · DOI
  70. Sicilia F, Mattei B, Cervone F, Bellincampi D, De Lorenzo G (2005) Characterization of a membrane-associated apoplastic lipoxygenase in Phaseolus vulgaris L. Biochim Biophys Acta 1748:9–19 · DOI
  71. Steele NM, McCann MC, Roberts K (1997) Pectin modification in cell walls of ripening tomatoes occurs in distinct domains. Plant Physiol 114:373–381 · DOI
  72. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599 · DOI
  73. Tieman DM, Harriman RW, Ramamohan G, Handa AK (1992) An antisense pectin methylesterase gene alters pectin chemistry and soluble solids in tomato fruit. Plant Cell 4:667–679 · DOI
  74. Tucker GA, Robertson NG, Grierson D (1982) Purification and changes in activities of tomato pectinesterase isoenzymes. J Sci Fd Agric 33:396–400 · DOI
  75. Vandevenne E, Van Buggenhout S, Duvetter T, Brouwers E, Declerck PJ, Hendrickx ME, Van Loey A, Gils A (2009) Development and evaluation of monoclonal antibodies as probes to assess the differences between two tomato pectin methylesterase isoenzymes. J Immunol Meth 349:18–27 · DOI
  76. Vandevenne E, Christiaens S, Van Buggenhout S, Jolie RP, Gonzalez-Vallinas M, Duvetter T, Declerck PJ, Hendrickx ME, Gils A, Van Loey A (2011) Advances in understanding pectin methylesterase inhibitor in kiwi fruit: an immunological approach. Planta 233:287–298 · DOI
  77. Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862 · DOI
  78. Volpi C, Janni M, Lionetti V, Bellincampi D, Favaron F, D’Ovidio R (2011) The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant-Microbe Interact 24:1012–1019 · DOI
  79. Wakabayashi K, Hoson T, Huber DJ (2003) Methyl de-esterification as a major factor regulating the extent of pectin depolymerization during fruit ripening: a comparison of the action of avocado (Persea americana) and tomato (Lycopersicon esculentum) polygalacturonases. J Plant Physiol 160:667–673 · DOI
  80. Wakeley PR, Rogers HJ, Rozycka M, Greenland AJ, Hussey PJ (1998) A maize pectin methylesterase-like gene, ZmC5, specifically expressed in pollen. Plant Mol Biol 37:187–192 · DOI
  81. Wolf S, Grsic-Rausch S, Rausch T, Greiner S (2003) Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis. FEBS Lett 555:551–555 · DOI
  82. Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851–860 · DOI
  83. Yin XR, Allan AC, Chen KS, Ferguson IB (2010) Kiwifruit EIL and ERF Genes Involved in Regulating Fruit Ripening. Plant Physiol 153:1280–1292 · DOI
  84. Zhang GY, Feng J, Wu J, Wang XW (2010) BoPMEI1, a pollen-specific pectin methylesterase inhibitor, has an essential role in pollen tube growth. Planta 231:1323–1334 · DOI

Cited by

Sorted by citations

Metadata

Authors
Reca, I. B., Lionetti, V., Camardella, L., D’Avino, R., Giardina, T., Cervone, F., & Bellincampi, D.
Affiliations
  • Sapienza University of Rome (IT)
  • Institute of Protein Biochemistry (IT)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
Bellincampi, Daniela
ORCID
Venue
Plant Molecular Biology
Publisher
Springer Science and Business Media LLC
Published
2012-05-19
Volume
79
Issue
4-5
Pages
429-442
ISSN
  • 0167-4412 (ISSN-L)
  • 1573-5028
DOI
10.1007/s11103-012-9921-2
OpenAlex
W2006382769
Cited by
76
References
0
Citations by year
2026: 3 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 9 · 2021: 6 · 2020: 3 · 2019: 3 · 2018: 6 · 2017: 6 · 2016: 5 · 2015: 7 · 2014: 7 · 2013: 7
FWCI
7.67
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)
Locations
  • Plant Molecular Biology (publishedVersion)
  • PubMed (publishedVersion)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Polysaccharides and Plant Cell Walls
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Postharvest Quality and Shelf Life Management
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Surface Properties and Treatments
Keywords
pectin methylesterase inhibitor, tomato, fruit ripening, PME-1, pectin methylesterase, cell wall proteins, protein-protein interaction, gene expression
MeSH terms
Amino Acid Sequence, Base Sequence, Carboxylic Ester Hydrolases, Enzyme Inhibitors, Esterification, Fruit, Molecular Sequence Data, Pectins, Phylogeny, Pichia, Plant Proteins, Recombinant Proteins, Nicotiana, Transformation, Genetic, Genes, Plant, Arabidopsis, Sequence Homology, Amino Acid, Solanum lycopersicum, DNA, Plant, Plants, Genetically Modified

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review