Cutinsomes and lipotubuloids appear to participate in cuticle formation in Ornithogalum umbellatum ovary epidermis: EM-immunogold research

Protoplasma

Volumn 251, Issue 5, 2014, Pages 1151-1161

  Kwiatkowska, Maria ^a   Wojtczak, Agnieszka ^a   Popłońska, Katarzyna ^a   Polit, Justyna Teresa ^a   Stepiński, Dariusz ^a   Domnguez, Eva ^b   Heredia, Antonio ^b  

^a UNIVERSITY OF LODZ   (Poland)

^b UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

Cuticle; Cutinsomes; Electron microscopy immunogold technique; Lipotubuloids; Ornithogalum umbellatum ovary epidermis

Indexed keywords

LYCOPERSICON ESCULENTUM; ORNITHOGALUM; ORNITHOGALUM UMBELLATUM;

CUTIN; FATTY ACID; MEMBRANE LIPID; PALMITIC ACID;

BIOSYNTHESIS; CELL WALL; CYTOLOGY; ELECTRON MICROSCOPY; FLOWER; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; MICROTUBULE; ORNITHOGALUM; PLANT EPIDERMIS;

CELL WALL; FATTY ACIDS; FLOWERS; IMMUNOHISTOCHEMISTRY; MEMBRANE LIPIDS; MICROSCOPY, ELECTRON; MICROTUBULES; ORNITHOGALUM; PALMITIC ACID; PLANT EPIDERMIS;

EID: 84905687776     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-014-0623-2     Document Type: Article

References (71)

1. Apel CL, Deamer DW, Mautner MN (2002) Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for the encapsulation of biopolymers. Biochim Biophys Acta Biomembr 1559: 1-9.
2. Barnes JD, Percy KE, Paul ND, Jones P, McLaughlin CK, Mullineaux PM, Creissen G, Wellburn AR (1996) The influence of UV-B radiation on the physicochemical nature of tobacco (Nicotiana tabacum L.) leaf surfaces. J Exp Bot 47: 99-109.
3. Bendayan M, Zollinger M (1983) Ultrastructural localization of antigenic sites on osmium fixed tissues applying the protein A-gold technique. J Histochem Cytochem 31: 101-109.
4. Benveniste I, Tijet N, Adas F, Philipps G, Salaün JP, Durst F (1998) CYP86A1 from Arabidopsis thaliana encodes a cytochrome P450-dependet fatty acid omega-hydroxylase. Biochem Biophys Res Commun 243: 688-693.
5. Benίtez JJ, Garcίa-Seguraq R, Heredia A (2004) Plant biopolyester cutin: a tough way to its chemical synthesis. Biochim Biophys Acta 1674: 1-3.
6. Benίtez JJ, Heredia-Guerrero JA, Heredia A (2007) Self-assembly of carboxylic acids and hydroxyl derivatives on mica. A qualitative AFM study. J Phys Chem C 111: 9465-9470.
7. Benίtez JJ, Heredia-Guerrero JA, Serrano FM, Heredia A (2008) The role of hydroxyl groups in the self-assembly of long chain alkylhydroxyl carboxylic acids on mica. J Phys Chem 112: 16968-16972.
8. Bessire M, Chassot C, Jacquat AC, Humphry M, Borel S, Petétot JMC, Metraux JP, Nawrath C (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botritis cinerea. EMBO J 26: 2158-2168.
9. Bird DA (2008) The role of ABC transporter in cuticular lipid secretion. Plant Sci 174: 563-569.
10. Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu X, Yephremov A, Samuels L (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52: 485-498.
11. Bonaventure G, Bao X, Ohlrogge J, Pollard M (2004) Metabolic responses to the reduction in palmitate caused by disruption of the FATB gene in Arabidopsis. Plant Physiol 135: 1269-1279.
12. Chen G, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu Y-G, Sameri M, Li X, Zhao X, Liu Y, Li C, Ma X, Wang A, Nair S, Wang N, Miyao A, Sakuma S, Yamaji N, Zheng X, Nevo E (2011) An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad Sci U S A 108: 12354-12359.
13. D'Angeli S, Falasca G, Matteucci M, Altamura MM (2013) Cold perception and gene expression differ in Olea europaea seed coat and embryo during drupe cold acclimation. New Phytol 197: 123-138.
14. DeBono A, Yeats TH, Rose JKC, Bird D, Jetter R, Kunst L, Samuels L (2009) Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21: 1230-1238.
15. Domίnguez E, Heredia-Guerrero JA, Benίtez JJ, Heredia A (2010) Self-assembly of supramolecular lipid nanoparticles in the formation of plant biopolyester cutin. Mol BioSyst 6: 948-950.
16. Domίnguez E, Heredia-Guerrero JA, Heredia A (2011) The biophysical design of plant cuticles: an overview. New Phytol 189: 938-984.
17. Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, Nawrath C, Schreiber L (2005) Apoplastic polyesters in Arabidopsis surface tissues-a typical suberin and particular cutin. Phytochemistry 66: 2643-2658.
18. Girard A-L, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J, Runavot J-L, Quemener B, Petit J, Germain V, Rothan C, Marion D, Bakan B (2012) Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24: 3119-3134.
19. Heredia A (2003) Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochim Biophys Acta 1620: 1-7.
20. Heredia-Guerrero JA, Benίtez JJ, Heredia A (2008) Self-assembled polyhydroxy fatty acids vesicles: a mechanism for plant cutin synthesis. BioEssays 30: 273-277.
21. Heredia-Guerrero JA, San-Miguel MA, Sansom MSP, Heredia A, Benίtez JJ (2009) Chemical reaction 2D: self-assembly and self-esterification of 9(10), 16-dihydroxypalmitic acid on mica surface. Langmuir 25: 6869-6874.
22. Heredia-Guerrero JA, San-Miguel MA, Luna M, Domίnguez E, Heredia A, Benίtez JJ (2011) Structure and support induced structure disruption of soft nanoparticles obtained from hydroxylated fatty acids. Soft Matter. doi: 10. 1039/c0sm01545h.
23. Jenks MA, Joly RJ, Peters PJ, Rich PJ, Axtell JD, Ashworth E (1994) Chemically induced cuticle mutation affecting epidermal conductance to water vapor and disease susceptibility in Sorghum bicolor (L.) Moench. Plant Physiol 105: 1239-1245.
24. Kolattukudy PE (2001) Polyesters in higher plants. Adv Biochem Engin/Biotechnol 71: 1-49.
25. Kolattukudy PE (2005) Cutin from plants. Biopolymers Online. Wiley-VCH. doi: 10. 1002/3527600035. bpol3a01.
26. Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci U S A 107: 2361-2366.
27. 3H-palmitic acid into lipotubuloids of Ornithogalum umbellatum L. Fol Histoch Cytochem 10: 121-124.
28. Kwiatkowska M (1972b) Changes in the diameter of microtubules connected with the autonomous rotary motion of lipotubuloids (elaiopolasts). Protoplasma 75: 345-357.
29. Kwiatkowska M (1973) Half unit membrane surrounding osmiophilic granules (lipid droplets) of so-called lipotubuloid in Ornithogalum umbellatum. Proc Natl Acad Sci U S A 77: 473-476.
30. 3H-palmitic acid into Ornithogalum umbellatum lipotubuloids, which are a cytoplasmic domain rich in lipid bodies and microtubules: light and EM authoradiography. Acta Soc Bot Pol 73: 181-186.
31. Kwiatkowska M, Popłońska K, Ste{ogonek}piński D (2005) Actin filaments connected with microtubules of lipotubuloids: cytoplasmic domains rich in lipid bodies and microtubules. Protoplasma 226: 163-167.
32. Kwiatkowska M, Popłońska K, Kaźmierczak A, Ste{ogonek}piński D, Rogala K, Polewczyk K (2007) Role of DNA endoreduplication, lipotubuloids, and gibberellic acid in epidermal cell growth during fruit development of Ornithogalum umbellatum. J Exp Bot 58: 2023-2031.
33. Kwiatkowska M, Popłońska K, Ste{ogonek}piński D (2009) Diameters of microtubules change during rotation of the lipotubuloids of Ornithogalum umbellatum stipule epidermis as result of varying protofilament monomers sizes and distance between them. Cell Biol Int 33: 1245-1252.
34. Kwiatkowska M, Ste{ogonek}piński D, Popłońska K, Wojtczak A, Polit J (2010) "Elaioplasts" of Haemanthus albiflos are true lipotubuloids: cytoplasmic domains rich in lipid bodies entwined by microtubules. Acta Physiol Plant 32: 1189-1196.
35. 3H-palmitic acid and are connected with cuticle synthesis. Trends Cell Mol Biol 6: 97-108.
36. Kwiatkowska M, Ste{ogonek}piński D, Popłońska K, Wojtczak A, Polit JT (2011b) "Elaioplasts" identified as lipotubuloids in Althaea rosea, Funkia sieboldiana and Vanilla planifolia contain lipid bodies connected with microtubules. Acta Soc Bot Pol 80: 211-219.
37. Kwiatkowska M, Popłońska K, Wojtczak A, Ste{ogonek}piński D, Polit JT (2012a) Lipid body biogenesis and the role of microtubules in lipid synthesis in Ornithogalum umbellatum lipotubuloids. Cell Biol Int. doi: 10. 1042/CBI20100638.
38. Kwiatkowska M, Popłońska K, Ste{ogonek}piński D, Wojtczak A, Polit JT, Paszak K (2012b) Lipotubuloids-structure and function. In: Montanaro G, Dichio B (eds) Advances in selected plant physiology aspects. InTech, Rijeka, pp 365-388.
39. Kwiatkowska M, Polit JT, Popłońska K, Ste{ogonek}piński D, Wojtczak A (2013) Immunogold method evidences that kinesin and myosin bind to and couple microtubules and actin filaments in lipotubuloids of Ornithogalum umbellatum ovary epidermis. Acta Physiol Plant 35: 1967-1977.
40. Lam P, Zhao L, McFarlane HE, Aiga M, Lam V, Hooker TS, Kunst L (2012) RDR1 and SGS3, components of RNA-mediated gene silencing, are required for the regulation of cuticular wax biosynthesis in developing inflorescence stems of Arabidopsis. Plant Physiol 159: 1385-1395.
41. Lev S (2010) Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat Rev Mol Cell Biol 11: 739-750.
42. Li X-C, Zhu J, Yang J, Zhang G-R, Xing W-F, Zhang S, Yang Z-N (2012) Glycerol-3-phosphate acyltransferase 6 (GPAT6) is important for tapetum development in Arabidopsis and plays multiple roles in plant fertility. Mol Plant 5: 131-142.
43. Li-Beisson Y, Pollard M, Saveplane V, Pinot F, Ohlrogge J, Beisson F (2009) Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc Natl Acad Sci U S A 106: 22008-22013.
44. Lü S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA (2009) Arabidopsis CER8 encodes long-chain acyl-CoA synthetase 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 59: 553-564.
45. Lü S, Zhao H, Des Marais DJ, Parsons EP, Wen X, Xu X, Bangarusamy DK, Wang G, Rowland O, Juenger T, Bressan RA, Jenks MA (2012) Arabidopsis ECERIFERUM9 involvement in cuticle formation and maintenance of plant water status. Plant Physiol 159: 930-944.
46. Luo B, Xue XY, Hu WL, Wang LJ, Chen XY (2007) An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant Cell Physiol 48: 1790-1802.
47. Matas AJ, Yeats TH, Buda GJ, Zheng Y, Chatterjee S, Tohge T, Ponnala L, Adato A, Aharoni A, Stark R, Fernie AR, Fei Z, Giovannoni JJ, Rose JKC (2011) Tissue- and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 23: 3893-3910.
48. Molina I, Bonaventure G, Ohlrogge J, Pollard M (2006) The lipid polyester composition of Arabidopsis thaliana and Brassica napus seeds. Phytochemistry 67: 2597-2610.
49. Molina I, Ohlrogge JB, Pollard M (2008) Deposition and localization of lipid polyester in developing seeds of Brassica napus and Arabidopsis thaliana. Plant J 55: 437-449.
50. Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Hoifer R, Schreiber L, Chory J, Aharoni A (2007) The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 145: 1345-1360.
51. Pollard M, Beisson F, Li YH, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13: 236-246.
52. Prinz WA (2010) Lipid trafficking sans vesicles: where, why, how? Cell 143: 870-874.
53. Pulsifer IP, Kluge S, Rowland O (2012) Arabidopsis long-chain acyl-CoA synthetase 1 (LACS1), LACS2, and LACS3 facilitate fatty acid uptake in yeast. Plant Physiol Biochem 51: 31-39.
54. Rautengarten C, Ebert B, Ouellet M, Nafisi M, Baidoo EEK, Benke P, Stranne M, Mukhopadhyay A, Keasling JD, Sakuragi Y, Scheller HV (2012) Arabidopsis Deficient in Cutin Ferulate encodes a transferase required for feruloylation of ω-hydroxy fatty acids in cutin polyester. Plant Physiol 158: 654-665.
55. Reynolds ES (1963) The use of lead citrate of high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208-212.
56. Samuels L, McFarlane HE (2012) Plant cell wall secretion and lipid traffic at membrane contact sites of the cell cortex. Protoplasma 249: S19-S23.
57. Schnurr J, Shockey J, Browse J (2004) The acyl-CoA synthetase encoded by LCS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16: 629-642.
58. Seo PJ, Lee SB, Suh MC, Park M-J, Go YS, Park C-M (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23: 1138-1152.
59. Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy P, Métraux J-P, Nawrath C (2000) Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12: 721-737.
60. Ukitsu H, Kuromori T, Toyooka K, Goto Y, Matsuoka K, Sakuradani E, Shimizu S, Kamiya A, Imura Y, Yuguchi M, Wada T, Hirayama T, Shinozaki K (2007) Cytological and biochemical analysis of COF1, an Arabidopsis mutant of an ABC transporter gene. Plant Cell Physiol 48: 1524-1533.
61. Villena JF, Domίnguez E, Stewart D, Heredia A (1999) Characterization and biosynthesis of non-degradable polymers in plant cuticles. Planta 208: 181-187.
62. Wakker LCH (1888) Studien über die Inhaltskörper der Pflanzenzelle. Jahrb wiss Bot 19: 423-496.
63. Wang HW, Hwang SG, Karuppanapandian T, Liu A, Kim W, Jang CS (2012) Insight into the molecular evolution of non-specific lipid transfer protein via comparative analysis between rice and sorghum. DNA Res 19: 179-194.
64. Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, Wisman E, Steiner-Lange S, Saedler H, Zephremov A (2001) Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different robes of fatty acid omega-hydroxylation in development. Proc Natl Acad Sci U S A 98: 9694-9699.
65. Weng H, Molina I, Shockey J, Browse J (2010) Organ fusion and defective cuticle function in a lacs1 lacs2 double mutant of Arabidopsis. Planta 231: 1089-1100.
66. Wu RH, Li SB, He S, Wassmann F, Yu CH, Qin GJ, Schreiber L, Qu LJ, Gu HY (2011) CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. Plant Cell 23: 3392-3411.
67. Xiao FM, Goodwin SM, Xiao IM, Sun ZY, Baker D, Tang XY, Jenks MA, Zhou JM (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type II genes and required for cuticle development. EMBO J 23: 2903-2913.
68. Yang W, Pollard M, Li-Beisson Y, Beisson F, Feig M, Ohlrogge J (2010) A distinct type of glycerol-3-phosphatase acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc Natl Acad Sci U S A 107: 12040-12045.
69. Yeats T, Rose JKC (2013) The formation and function of plant cuticles. Plant Physiol. doi: 10. 1104/pp. 113. 222737.
70. Yeats T, Howe KJ, Matas AJ, Buda GJ, Thannhauser TW, Rose JKC (2010) Mining the surface proteome of tomato (Solanum lycopersicum) fruit for proteins associated with cuticle biogenesis. J Exp Bot 61: 3759-3771.
71. Yeats TH, Martin LBB, Viart HM-F, Isaacson T, He Y, Zhao L, Matas A, Buda JG, Domozych DS, Clausen MH, Rose JKC (2012) The identification of cutin synthase: formation of the plant polyester cutin. Nat Chem Biol 8: 609-611.