Cutinsomes and CUTIN SYNTHASE1 Function Sequentially in Tomato Fruit Cutin Deposition1[OPEN]

In tomato fruit development, cutinsomes participate in procuticle deposition and CUTIN SYNTHASE1 in cutin synthesis during the later cell expansion period. The aerial parts of plants, including the leaves, fruits and non-lignified stems, are covered with a protective cuticle, largely composed of the polyester cutin. Two mechanisms of cutin deposition have been identified in tomato (Solanum lycopersicum) fruit. The contribution of each mechanism to cutin synthesis and deposition has shown a temporal and coordinated sequence that correlates with the two periods of organ growth, cell division and cell expansion. Cutinsomes, self-assembled particles composed of esterified cutin monomers, are involved in the synthesis of the procuticle during cell division and provide a template for further cutin deposition. CUTIN SYNTHASE1 (CUS1), an acyl transferase enzyme that links cutin monomers, contributes to massive cuticle deposition during the early stages of the cell expansion period by incorporating additional cutin to the procuticle template. However, cutin deposition and polymerization appear to be part of a more complex biological scenario, which is yet not fully understood. CUS1 is also associated with the coordinated growth of the cutinized and non-cutinized domains of the outer epidermal wall, and affects cell size. A dynamic and complex interplay linking cutin synthesis with cell wall development and epidermal cell size has been identified.

[1]  B. Bakan,et al.  Assembly of tomato fruit cuticles: a cross-talk between the cutin polyester and cell wall polysaccharides. , 2019, The New phytologist.

[2]  Synthesis and Oligomerization of 10,16‐Dihydroxyhexadecanoyl Esters with Different Head‐Groups for the Study of CUS1 Selectivity , 2019, European Journal of Organic Chemistry.

[3]  E. Domínguez,et al.  Cutinsomes as building-blocks of Arabidopsis thaliana embryo cuticle. , 2017, Physiologia plantarum.

[4]  B. Bakan,et al.  Assembly of the Cutin Polyester: From Cells to Extracellular Cell Walls , 2017, Plants.

[5]  J. Rose,et al.  CUTIN SYNTHASE 2 Maintains Progressively Developing Cuticular Ridges in Arabidopsis Sepals. , 2017, Molecular plant.

[6]  A. Aharoni,et al.  MYB107 and MYB9 Homologs Regulate Suberin Deposition in Angiosperms , 2016, Plant Cell.

[7]  F. Beisson,et al.  BODYGUARD is required for the biosynthesis of cutin in Arabidopsis. , 2016, The New phytologist.

[8]  A. Heredia,et al.  Cutinsomes and cuticle enzymes GPAT6 and DGAT2 seem to travel together from a lipotubuloid metabolon (LM) to extracellular matrix of O. umbellatum ovary epidermis. , 2016, Micron.

[9]  L. Gil,et al.  Cuticle Structure in Relation to Chemical Composition: Re-assessing the Prevailing Model , 2016, Front. Plant Sci..

[10]  OeFAD8, OeLIP and OeOSM expression and activity in cold-acclimation of Olea europaea, a perennial dicot without winter-dormancy , 2016, Planta.

[11]  B. Bakan,et al.  Ester Cross-Link Profiling of the Cutin Polymer of Wild-Type and Cutin Synthase Tomato Mutants Highlights Different Mechanisms of Polymerization1 , 2015, Plant Physiology.

[12]  E. Domínguez,et al.  Ultrastructure of the Epidermal Cell Wall and Cuticle of Tomato Fruit (Solanum lycopersicum L.) during Development1[OPEN] , 2015, Plant Physiology.

[13]  E. Domínguez,et al.  Plant cutin genesis: unanswered questions. , 2015, Trends in plant science.

[14]  E. Domínguez,et al.  Transcriptional Activity of the MADS Box ARLEQUIN/TOMATO AGAMOUS-LIKE1 Gene Is Required for Cuticle Development of Tomato Fruit1 , 2015, Plant Physiology.

[15]  Ilker S. Bayer,et al.  Pectin-Lipid Self-Assembly: Influence on the Formation of Polyhydroxy Fatty Acids Nanoparticles , 2015, PloS one.

[16]  A. Heredia,et al.  Lipotubuloids in ovary epidermis of Ornithogalum umbellatum act as metabolons: suggestion of the name 'lipotubuloid metabolon'. , 2015, Journal of experimental botany.

[17]  J. Ayad,et al.  Over-Expression of SlSHN1 Gene Improves Drought Tolerance by Increasing Cuticular Wax Accumulation in Tomato , 2014, International journal of molecular sciences.

[18]  E. Domínguez,et al.  Transient Silencing of CHALCONE SYNTHASE during Fruit Ripening Modifies Tomato Epidermal Cells and Cuticle Properties1[C][W] , 2014, Plant Physiology.

[19]  E. Domínguez,et al.  Biomechanical properties of the tomato (Solanum lycopersicum) fruit cuticle during development are modulated by changes in the relative amounts of its components. , 2014, The New phytologist.

[20]  A. Heredia,et al.  Cutinsomes and lipotubuloids appear to participate in cuticle formation in Ornithogalum umbellatum ovary epidermis: EM–immunogold research , 2014, Protoplasma.

[21]  J. Rose,et al.  Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. , 2014, The Plant journal : for cell and molecular biology.

[22]  J. Ohlrogge,et al.  Golgi- and Trans-Golgi Network-Mediated Vesicle Trafficking Is Required for Wax Secretion from Epidermal Cells1[W][OPEN] , 2014, Plant Physiology.

[23]  B. Bakan,et al.  Analyses of Tomato Fruit Brightness Mutants Uncover Both Cutin-Deficient and Cutin-Abundant Mutants and a New Hypomorphic Allele of GDSL Lipase[C][W][OPEN] , 2013, Plant Physiology.

[24]  M. Kwiatkowska,et al.  Immunogold method evidences that kinesin and myosin bind to and couple microtubules and actin filaments in lipotubuloids of Ornithogalum umbellatum ovary epidermis , 2013, Acta Physiologiae Plantarum.

[25]  A. Adato,et al.  The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. , 2013, The New phytologist.

[26]  S. D'Angeli,et al.  Cold perception and gene expression differ in Olea europaea seed coat and embryo during drupe cold acclimation. , 2013, The New phytologist.

[27]  E. Domínguez,et al.  Tomato fruit continues growing while ripening, affecting cuticle properties and cracking. , 2012, Physiologia plantarum.

[28]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[29]  B. Bakan,et al.  Tomato GDSL1 Is Required for Cutin Deposition in the Fruit Cuticle[C][W] , 2012, Plant Cell.

[30]  J. Rose,et al.  The identification of cutin synthase: formation of the plant polyester cutin , 2012, Nature chemical biology.

[31]  Zhijin Zhang,et al.  An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice , 2011, Plant Molecular Biology.

[32]  Asaph Aharoni,et al.  SHINE Transcription Factors Act Redundantly to Pattern the Archetypal Surface of Arabidopsis Flower Organs , 2011, PLoS genetics.

[33]  Eva Domínguez,et al.  The biophysical design of plant cuticles: an overview. , 2011, The New phytologist.

[34]  M. Kwiatkowska The incorporation of 3H-palmitic acid into Ornithogalum umbellatum lipotubuloids, which are a cytoplasmic domain rich in lipid bodies and microtubules. Light and EM autoradiography , 2011 .

[35]  G. Ingram,et al.  Epidermis: the formation and functions of a fundamental plant tissue. , 2011, The New phytologist.

[36]  A. Negi,et al.  Defective in Cuticular Ridges (DCR) of Arabidopsis thaliana, a Gene Associated with Surface Cutin Formation, Encodes a Soluble Diacylglycerol Acyltransferase* , 2010, The Journal of Biological Chemistry.

[37]  E. Domínguez,et al.  Self-assembly of supramolecular lipid nanoparticles in the formation of plant biopolyester cutin. , 2010, Molecular Biosystems.

[38]  E. Domínguez,et al.  Structural characterization of polyhydroxy fatty acid nanoparticles related to plant lipid biopolyesters. , 2010, Chemistry and physics of lipids.

[39]  Olivier Hamant,et al.  The mechanics behind plant development. , 2010, The New phytologist.

[40]  A. Aharoni,et al.  The Arabidopsis DCR Encoding a Soluble BAHD Acyltransferase Is Required for Cutin Polyester Formation and Seed Hydration Properties1[C][W][OA] , 2009, Plant Physiology.

[41]  J. Rose,et al.  Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. , 2009, The Plant journal : for cell and molecular biology.

[42]  K. Matsuoka,et al.  A Mobile Secretory Vesicle Cluster Involved in Mass Transport from the Golgi to the Plant Cell Exterior[W][OA] , 2009, The Plant Cell Online.

[43]  A. Casadevall,et al.  Vesicular transport across the fungal cell wall. , 2009, Trends in microbiology.

[44]  C. Werner,et al.  Charging and structure of zwitterionic supported bilayer lipid membranes studied by streaming current measurements, fluorescence microscopy, and attenuated total reflection Fourier transform infrared spectroscopy , 2009, Biointerphases.

[45]  E. Domínguez,et al.  Cutin synthesis: A slippery paradigm , 2009, Biointerphases.

[46]  A. A. Borges,et al.  Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process , 2008, BMC Plant Biology.

[47]  E. Domínguez,et al.  Development of fruit cuticle in cherry tomato (Solanum lycopersicum). , 2008, Functional plant biology : FPB.

[48]  U. Kutschera The growing outer epidermal wall: design and physiological role of a composite structure. , 2008, Annals of botany.

[49]  A. Heredia,et al.  Self-assembled polyhydroxy fatty acids vesicles: a mechanism for plant cutin synthesis. , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[50]  C. Jeffree,et al.  The Fine Structure of the Plant Cuticle , 2007 .

[51]  Jesús Cuartero,et al.  Biomechanics of isolated tomato (Solanum lycopersicum L.) fruit cuticles: the role of the cutin matrix and polysaccharides. , 2007, Journal of experimental botany.

[52]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[53]  A. Heredia,et al.  Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. leaf epidermis. , 2007, Journal of experimental botany.

[54]  Markus Riederer,et al.  Biology of the plant cuticle , 2006 .

[55]  H. Saedler,et al.  The Epidermis-Specific Extracellular BODYGUARD Controls Cuticle Development and Morphogenesis in Arabidopsis[W] , 2006, The Plant Cell Online.

[56]  M. Bret-Harte,et al.  Changes in composition of the outer epidermal cell wall of pea stems during auxin-induced growth , 1993, Planta.

[57]  H. Heide-Jørgensen Cuticle development and ultrastructure: evidence for a procuticle of high osmium affinity , 1991, Planta.

[58]  P. Schopfer,et al.  Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles , 1987, Planta.

[59]  A. Heredia,et al.  Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. , 2003, Biochimica et biophysica acta.

[60]  F. Speleman,et al.  Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes , 2002, Genome Biology.

[61]  A. Heredia,et al.  Water permeability of isolated cuticular membranes: a structural analysis. , 1995, Archives of biochemistry and biophysics.

[62]  J. Massié,et al.  Relationship between interchain spacing of amorphous polymers and blend miscibility as determined by wide‐angle X‐ray scattering , 1991 .

[63]  R. Croteau,et al.  Biosynthesis of hydroxyfatty acid polymers. Enzymatic synthesis of cutin from monomer acids by cell-free preparations from the epidermis of Vicia faba leaves. , 1974, Biochemistry.

[64]  N. D. Hallam Leaf wax fine structure and ontogeny in Eucalyptus demonstrated by means of a specialized fixation technique , 1970 .

[65]  A. Frey-wyssling,et al.  Ultrastructural plant cytology : with an Introduction to molecular biology , 1965 .