Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Plant extracellular matrix metalloproteinases

Barry S. Flinn
+ Author Affiliations
- Author Affiliations

A The Institute for Advanced Learning and Research, Institute for Sustainable and Renewable Resources, 150 Slayton Avenue, Danville, VA 24540, USA.

B Departments of Horticulture and Forestry, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
Email: barry.flinn@ialr.org

Functional Plant Biology 35(12) 1183-1193 https://doi.org/10.1071/FP08182
Submitted: 27 June 2008  Accepted: 18 September 2008   Published: 16 December 2008

Abstract

The plant extracellular matrix (ECM) includes a variety of proteins with critical roles in the regulation of plant growth, development, and responses to pests and pathogens. Several studies have shown that various ECM proteins undergo proteolytic modification. In mammals, the extracellular matrix metalloproteinases (MMPs) are known modifiers of the ECM, implicated in tissue architecture changes and the release of biologically active and/or signalling molecules. Although plant MMPs have been identified, little is known about their activity and function. Plant MMPs show structural similarity to mammalian MMPs, including the presence of an auto-regulatory cysteine switch domain and a zinc-binding catalytic domain. Plant MMPs are differentially expressed in cells and tissues during plant growth and development, as well as in response to several biotic and abiotic stresses. The few gene expression and mutant analyses to date indicate their involvement in plant growth, morphogenesis, senescence and adaptation and response to stress. In order to gain a further understanding of their function, an analysis and characterisation of MMP proteins, their activity and their substrates during plant growth and development are still required. This review describes plant MMP work to date, as well as the variety of genomic and proteomic methodologies available to characterise plant MMP activity, function and potential substrates.

Additional keywords: proteolysis, substrate, tissue inhibitor of metalloproteinase.


Acknowledgements

Research in the author’s laboratory has been supported through a grant from the United States Department of Agriculture (2003–38891–02112), and operating funds from the Commonwealth of Virginia.


References


Amano T, Kwak O, Fu L, Marshak A, Shi Y-B (2005) The matrix metalloproteinase stromelysin-3 cleaves laminin receptor at two distinct sites between the transmembrane domain and laminin binding sequence within the extracellular domain. Cell Research 15, 150–159.
CrossRef | CAS | PubMed |

Berger D, Altmann T (2000) A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes & Development 14, 1119–1131.
CAS | PubMed |


Bodet C, Chandad F, Grenier D (2007) Inhibition of host extracellular matrix destructive enzyme production and activity by a high-molecular-weight cranberry fraction. Journal of Periodontal Research 42, 159–168.
CrossRef | CAS | PubMed |

Boudart G, Jamet E, Rossignol M, Lafitte C, Borderies G, Jauneau A, Esquerré-Tugayé M-T, Pont-Lezica R (2005) Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: identification by mass spectrometry and bioinformatics. Proteomics 5, 212–221.
CrossRef | CAS | PubMed |

Brewin NJ (2004) Plant cell wall remodelling in the rhizobium–legume symbiosis. Critical Reviews in Plant Sciences 23, 293–316.
CrossRef | CAS |

Brownlee C (2002) Role of the extracellular matrix in cell–cell signaling; paracrine paradigms. Current Opinion in Plant Biology 5, 396–401.
CrossRef | CAS | PubMed |

Carlile AJ, Bindschedler LV, Bailey AM, Bowyer P, Clarkson JM, Cooper RM (2000) Characterization of SNP1, a cell wall-degrading trypsin, produced during infection by Stagonospora nodorum. Molecular Plant-Microbe Interactions 13, 538–550.
CrossRef | CAS | PubMed |

Carvalho A de O, Gomes VM (2007) Role of lipid transfer proteins in plant cell physiology – a concise review. Peptides 28, 1144–1153.
CrossRef | CAS | PubMed |

Cauwe B, Van den Steen PE, Opdenakker G (2007) The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Critical Reviews in Biochemistry and Molecular Biology 42, 113–185.
CrossRef | CAS | PubMed |

Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T (2003) Regulation of matrix metalloproteinases: an overview. Molecular and Cellular Biochemistry 253, 269–285.
CrossRef | CAS | PubMed |

Clark IM , Thomas MD , de Vos S (2004) Plant matrixins. In ‘Handbook of proteolytic enzymes’. (2nd edn) (Eds AJ Barrett, ND Rawlings, JF Woessner) pp. 570–572. (Elsevier: London)

Combier J-P, Vernié T, de Billy F, El Yahyaoui F, Mathis R, Gamas P (2007) The MtMMPL1 early nodulin is a novel member of the matrix metalloendoproteinase family with a role in Medicago truncatula infection by Sinorhizobium meliloti. Plant Physiology 144, 703–716.
CrossRef | CAS | PubMed |

Dani V, Simon WJ, Duranti M, Croy RRD (2005) Changes in the tobacco leaf apoplast proteome in response to salt stress. Proteomics 5, 737–745.
CrossRef | CAS | PubMed |

Das S, Mandal M, Chakraborti T, Mandal A, Chakraborti S (2003) Structure and evolutionary aspects of matrix metalloproteinases: a brief overview. Molecular and Cellular Biochemistry 253, 31–40.
CrossRef | CAS | PubMed |

Delorme VGR, McCabe PF, Kim D-J, Leaver CJ (2000) A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber. Plant Physiology 123, 917–927.
CrossRef | CAS | PubMed |

Deng SJ, Bickett DM, Mitchell JL, Lambert MH, Blackburn RK, Carter HL, Neugebauer J, Pahel G, Weiner MP, Moss ML (2000) Substrate specificity of human collagenase 3 assessed using a phage-displayed peptide library. Journal of Biological Chemistry 275, 31422–31427.
CrossRef | PubMed |

Dow JW, Davies HA, Daniels MJ (1998) A metalloprotease from Xanthomonas campestris that specifically degrades proline/hydroxyproline- rich glycoproteins of the plant extracellular matrix. Molecular Plant-Microbe Interactions 11, 1085–1093.
CrossRef | CAS | PubMed |

Farrokhi N, Whitelegge JP, Brusslan JA (2008) Plant peptides and peptidomics. Plant Biotechnology Journal 6, 105–134.
CrossRef | CAS | PubMed |

Golldack D, Popova OV, Dietz K-J (2002) Mutation of the matrix metalloproteinase At2-MMP inhibits growth and causes late flowering and early senescence in Arabidopsis. Journal of Biological Chemistry 277, 5541–5547.
CrossRef | CAS | PubMed |

Goujon T, Minic Z, El Amrani A, Lerouxel O, Aletti E, Lapierre C, Joseleau JP, Jouanin L (2003) AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. The Plant Journal 33, 677–690.
CrossRef | CAS | PubMed |

Graham JS, Xiong J, Gillikin JW (1991) Purification and developmental analysis of a metalloendoproteinase from the leaves of Glycine max. Plant Physiology 97, 786–792.
CAS | PubMed |


Hristova K, Lam M, Field T, Sage TL (2005) Transmitting tissue ECM distribution and composition, and pollen germinability in Sarcandra glabra and Chloranthus japonicus (Chloranthaceae). Annals of Botany 96, 779–791.
CrossRef | CAS | PubMed |

Humphrey TV, Bonetta DT, Goring DR (2007) Sentinels at the wall: cell wall receptors and sensors. New Phytologist 176, 7–21.
CrossRef | CAS | PubMed |

Ii M, Yamamoto H, Adachi Y, Maruyama Y, Shinomura Y (2006) Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Experimental Biology and Medicine 231, 20–27.
CAS | PubMed |


Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. The Plant Cell 17, 584–596.
CrossRef | CAS | PubMed |

Jin UH, Lee JY, Kang SK, Kim JK, Park WH, Kim JG, Moon SK, Kim CH (2005) A phenolic compound, 5-caffeoylquinic acid (chlorogenic acid), is a new type and strong matrix metalloproteinase-9 inhibitor: isolation and identification from methanol extract of Euonymus alatus. Life Sciences 77, 2760–2769.
CrossRef | CAS | PubMed |

Katembe WJ, Swatzell LJ, Makaroff CA, Kiss JZ (1997) Immunolocalization of integrin–like proteins in Arabidopsis and Chara. Physiologia Plantarum 99, 7–14.
CrossRef | CAS | PubMed |

Kim MM, Ta QV, Mendis E, Rajapakse N, Jung WK, Byun HG, Jeon YJ, Kim SK (2006) Phlorotannins in Ecklonia cava extract inhibit matrix metalloproteinase activity. Life Sciences 79, 1436–1443.
CrossRef | CAS | PubMed |

Lid SE, Gruis D, Jung R, Lorentzen JA, Ananiev E, Chamberlin M, Niu X, Meeley R, Nichols S, Olsen OA (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proceedings of the National Academy of Sciences of the United States of America 99, 5460–5465.
CrossRef | CAS | PubMed |

Liu Y, Dammann C, Bhattacharyya MK (2001) The matrix metalloproteinase gene GmMMP2 is activated in response to pathogenic infections in soybean. Plant Physiology 127, 1788–1797.
CrossRef | CAS | PubMed |

Lombard C, Saulnier J, Wallach J (2005) Assays of matrix metalloproteinases (MMPs) activities: a review. Biochimie 87, 265–272.
CrossRef | CAS | PubMed |

Maidment JM, Moore D, Murphy GP, Murphy G, Clark IM (1999) Matrix metalloproteinase homologues from Arabidopsis thaliana. Journal of Biological Chemistry 274, 34706–34710.
CrossRef | CAS | PubMed |

Marmagne A, Rouet M-A, Ferro M, Rolland N, Alcon C, Joyard J, Garin J, Barbier-Brygoo H, Ephritikhine G (2004) Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome. Molecular & Cellular Proteomics 3, 675–691.
CrossRef | CAS |

Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology 54, 23–61.
CrossRef | CAS | PubMed |

Massova I, Kotra LP, Fridman R, Mobashery S (1998) Matrix metalloproteinases: structures, evolution, and diversification. The FASEB Journal 12, 1075–1095.
CAS | PubMed |


McGeehan G, Burkhart W, Anderegg R, Becherer JD, Gillikin JW, Graham JS (1992) Sequencing and characterization of the soybean leaf metalloproteinase. Plant Physiology 99, 1179–1183.
CAS | PubMed |


Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovascular Research 69, 562–573.
CrossRef | CAS | PubMed |

Napier R (2004) Plant hormone binding sites. Annals of Botany 93, 227–233.
CrossRef | CAS | PubMed |

Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Current Opinion in Plant Biology 9, 281–287.
CrossRef | CAS | PubMed |

Ohkubo S, Miyadera K, Sugimoto Y, Matsuo K, Wierzba K, Yamada Y (2001) Substrate phage as a tool to identify novel substrate sequences of proteases. Combinatorial Chemistry & High Throughput Screening 4, 573–583.
CAS | PubMed |


Overall CM, McQuibban GA, Clark-Lewis I (2002) Discovery of chemokine substrates for matrix metalloproteinases by exosite scanning: a new tool for degradomics. Biological Chemistry 383, 1059–1066.
CrossRef | CAS | PubMed |

Overall CM, Tam EM, Kappelhoff R, Connor A, Ewart T, Morrison CJ, Puente X, López-Otin C, Seth A (2004) Protease degradomics: mass spectrometry discovery of protease substrates and the CLIP-CHIP, a dedicated DNA microarray of all human proteases and inhibitors. Biological Chemistry 385, 493–504.
CrossRef | CAS | PubMed |

Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodeling. Nature Reviews. Molecular Cell Biology 8, 221–233.
CrossRef | CAS | PubMed |

Pak JH, Liu CY, Huangpu J, Graham JS (1997) Construction and characterization of the soybean leaf metalloproteinase cDNA. FEBS Letters 404, 283–288.
CrossRef | CAS | PubMed |

Pellenc D, Schmitt E, Gallet O (2004) Purification of a plant cell wall fibronectin-like adhesion protein involved in plant response to salt stress. Protein Expression and Purification 34, 208–214.
CrossRef | CAS | PubMed |

Ragster L, Chrispeels MJ (1979) Azocoll-digesting proteinases in soybean leaves. Plant Physiology 64, 857–862.
CAS | PubMed |


Ringli C, Keller B, Ryser U (2001) Glycine-rich proteins as structural components of plant cell walls. Cellular and Molecular Life Sciences 58, 1430–1441.
CrossRef | CAS | PubMed |

Ropke CD, da Silva VV, Kera CZ, Miranda DV, de Almeida RL, Sawada TC, Barros SB (2006) In vitro and in vivo inhibition of skin matrix metalloproteinases by Pothomorphe umbellata root extract. Photochemistry and Photobiology 82, 439–442.
CrossRef | CAS | PubMed |

Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH , et al. (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. The Plant Cell 17, 1749–1763.
CrossRef | CAS | PubMed |

Rowsell S, Hawtin P, Minshull CA, Jepson H, Brockbank SM , et al. (2002) Crystal structure of human MMP9 in complex with a reverse hydroxamate inhibitor. Journal of Molecular Biology 319, 173–181.
CrossRef | CAS | PubMed |

Sanders LC, Wang C-S, Walling LL, Lord EM (1991) A homolog of the substrate adhesion molecule vitronectin occurs in four species of flowering plants. The Plant Cell 3, 629–635.
CrossRef | CAS | PubMed |

Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annual Review of Plant Biology 58, 137–161.
CrossRef | CAS | PubMed |

Simossis VA, Heringa J (2005) PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Research 33, W289–W294.
CrossRef | CAS | PubMed |

Snoek-van Beurden PAM, Von den Hoff JW (2005) Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors. BioTechniques 38, 73–83.
CrossRef | CAS | PubMed |

Stamenkovic I (2003) Extracellular matrix remodelling: the role of matrix metalloproteinases. Journal of Pathology 200, 448–464.
CrossRef | CAS | PubMed |

Stawowy P, Meyborg H, Stibenz D, Borges N, Stawowy P , et al. (2005) Furin-like proprotein convertases are central regulators of the membrane type matrix metalloproteinase-pro-matrix metalloproteinase-2 proteolytic cascade in atherosclerosis. Circulation 111, 2820–2827.
CrossRef | CAS | PubMed |

Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annual Review of Cell and Developmental Biology 17, 463–516.
CrossRef | CAS | PubMed |

Suzuki H, Xia Y, Cameron R, Shadle G, Blount J, Lamb C, Dixon RA (2004) Signals for local and systemic responses of plants to pathogen attack. Journal of Experimental Botany 55, 169–179.
CrossRef | CAS | PubMed |

Tam EM, Morrison CJ, Wu YI, Stack S, Overall CM (2004) Membrane protease proteomics: isotope-coded affinity tag MS identification of undescribed MT-1 matrix metalloproteinase substrates. Proceedings of the National Academy of Sciences of the United States of America 101, 6917–6922.
CrossRef | CAS | PubMed |

Tanaka H, Onouchi H, Kondo M, Hara-Nishimura I, Nishimura M, Machida C, Machida Y (2001) A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development 128, 4681–4689.
CAS | PubMed |


Tang W, Kelley D, Ezcurra I, Cotter R, McCormick S (2004) LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. The Plant Journal 39, 343–353.
CrossRef | CAS | PubMed |

Tao TY, Ouellet T, Dadej K, Miller SS, Johnson DA, Singh J (2006) Characterization of a novel glycine-rich protein from the cell wall of maize silk tissues. Plant Cell Reports 25, 848–858.
CrossRef | CAS | PubMed |

Tornero P, Mayda E, Gómez MD, Cañas L, Conejero V, Vera P (1996) Characterization of LRP, a leucine-rich repeat (LRR) protein from tomato plants that is processed during pathogenesis. The Plant Journal 10, 315–330.
CrossRef | CAS | PubMed |

Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The Botany Array Resource: e-Northerns, expression angling, and promoter analyses. The Plant Journal 43, 153–163.
CrossRef | CAS | PubMed |

Turk BE, Huang LL, Piro ET, Cantley LC (2001) Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nature Biotechnology 19, 661–667.
CrossRef | CAS | PubMed |

van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, van Kammen A, de Vries SC (2001) N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiology 125, 1880–1890.
CrossRef | CAS | PubMed |

van Wart HE, Birkedal-Hansen H (1990) The cysteine switch: a principal of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proceedings of the National Academy of Sciences of the United States of America 87, 5578–5582.
CrossRef | CAS | PubMed |

Vu TH, Werb Z (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes & Development 14, 2123–2133.
CrossRef | CAS | PubMed |

Ye Y, Fortini ME (2000) Proteolysis and developmental signal transduction. Seminars in Cell & Developmental Biology 11, 211–221.
CrossRef | CAS | PubMed |

Yu W-H, Woessner F (2001) Heparin-enhanced zymographic detection of matrilysin and collagenases. Analytical Biochemistry 293, 38–42.
CrossRef | CAS | PubMed |

Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology 136, 2621–2632.
CrossRef | CAS | PubMed |








Rent Article (via Deepdyve) Export Citation Cited By (12)