Galacturonosyltransferase 4 silencing alters pectin composition and carbon partitioning in tomato

Journal of Experimental Botany

Volumn 64, Issue 8, 2013, Pages 2449-2466

  De Godoy, Fabiana ^a   Bermúdez, Luisa ^a   Lira, Bruno Silvestre ^a   De Souza, Amanda Pereira ^a   Elbl, Paula ^a   Demarco, Diego ^a   Alseekh, Saleh ^b   Insani, Marina ^c   Buckeridge, Marcos ^a   Almeida, Juliana ^a   Grigioni, Gabriela ^c   Fernie, Alisdair Robert ^b   Carrari, Fernando ^c   Rossi, Magdalena ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

Author keywords

fruit metabolism; galacturonic acid; galacturonosyltransferase; pectin; Solanum pennellii; tomato

Indexed keywords

ASCORBIC ACID; GALACTURONIC ACID; PECTIN; URONIC ACID; VEGETABLE PROTEIN;

ARTICLE; CELL WALL; CHEMISTRY; CONFOCAL MICROSCOPY; FRUIT; FRUIT METABOLISM; GALACTURONOSYLTRANSFERASE; GENETICS; MASS FRAGMENTOGRAPHY; METABOLISM; MOLECULAR CLONING; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT GENE; REAL TIME POLYMERASE CHAIN REACTION; SILENCER ELEMENT; SOLANUM PENNELLII; TOMATO; TOMATO.;

FRUIT METABOLISM; GALACTURONIC ACID; GALACTURONOSYLTRANSFERASE; PECTIN; SOLANUM PENNELLII; TOMATO.;

ASCORBIC ACID; CELL WALL; CLONING, MOLECULAR; FRUIT; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENES, PLANT; LYCOPERSICON ESCULENTUM; MICROSCOPY, CONFOCAL; PECTINS; PHOTOSYNTHESIS; PLANT PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SILENCER ELEMENTS, TRANSCRIPTIONAL; URONIC ACIDS;

EID: 84877994923     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert106     Document Type: Article

References (86)

1. Alim K, Hamant O, Boudaoud A. 2012. Regulatory role of cell division rules on tissue growth heterogeneity. Frontiers in Plant Science 3, 174.
2. Almeida J, Quadrana L, Asís R, et al. 2011. Genetic dissection of vitamin E biosynthesis in tomato. Journal of Experimental Botany 62, 3781-3798.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215, 403-410.
4. Arsovski AA, Popma TM, Haughn GW, Carpita NC, McCann MC, Western TL. 2009. AtBXL1 encodes a bifunctional α-d-xylosidase/α-l- arabinofuranosidase required for pectic arabinan modifcation in Arabidopsis mucilage secretory cells. Plant Physiology 150, 1219-1234.
5. Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood JA. 2011. Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturon an:galacturonosyltransferase complex. Proceedings of the National Academy of Sciences, USA 50, 20225-20230.
6. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S. 2002. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18, 298-305.
7. Barrett DM, Garcia E, Wayne JE. 1998. Textural modifcation of processing tomatoes. Critical Reviews in Food Science and Nutrition 38, 173-258.
8. Bermúdez L, Urias U, Milstein D, Kamenetzky L, Asis R, Fernie AR, Van Sluys MA, Carrari F, Rossi M. 2008. A candidate gene survey of quantitative trait loci affecting chemical composition in tomato fruit. Journal of Experimental Botany 59, 2875-2890.
9. Blanc G, Wolfe KH. 2004. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679-1691.
10. Bombarely A, Menda N, Tecle IY, Buels RM, Strickler S, Fischer-York T, Pujar A, Leto J, Gosselin J, Mueller LA. 2011. The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Research 39, D1149-D1155.
11. Bouton S, Leboeuf E, Mouille G, Leydecker MT, Talbotec J, Granier F, Lahaye M, Höfte H, Truong HN. 2002. QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14, 2577-2590.
12. Brummell D, Harpster M, Civello P, Palys J, Bennett A, Dunsmuir P. 1999a. Modifcation of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11, 2203-2216.
13. Brummell DA, Bird CR, Schuch W, Bennett AB. 1997. An endo-1, 4-β-glucanase expressed at high levels in rapidly expanding tissues. Plant Molecular Biology 33, 87-95.
14. Brummell DA, Hall BD, Bennett AB. 1999b. Antisense suppression of tomato endo-1, 4-β-glucanase Cel2 mRNA accumulation increases the force required to break fruit abscission zones but does not affect fruit softening. Plant Molecular Biology 40, 615-622.
15. Caffall KH, Mohnen D. 2009. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydrate Research 344, 1879-1900.
16. Caffall KH, Pattathil S, Phillips SE, Hahn MG, Mohnen D. 2009. Arabidopsis thaliana T-DNA mutants implicate GAUT genes in the biosynthesis of pectin and xylan in cell walls and seed testa. Molecular Plant 2, 1000-1014.
17. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Research 37, D233-D238.
18. Chaïb J, Lecomte L, Buret M, Causse M. 2006. Stability over genetic backgrounds, generations and years of quantitative trait locus (QTLs) for organoleptic quality in tomato. Theoretical and Applied Genetics 112, 934-944.
19. Chapman NH, Bonnet J, Grivet L, et al. 2012. High-resolution mapping of a fruit frmness-related quantitative trait locus in tomato reveals epistatic interactions associated with a complex combinatorial locus. Plant Physiology 159, 1644-1657.
20. Chou KC, Shen HB. 2010. Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5, e11335.
21. Corpet T. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 16, 10881-10890.
22. 2? Agricultural and Forest Meteorology 171-172, 82-92.
23. Di Rienzo JA. 2009. Statistical software for the analysis of experiments of functional genomics. RDNDA, Argentina. http://sites. google.com/site/ fgStatistics/
24. Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW. 2011. InfoStat versión 2011. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat. com.ar.
25. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP, and related tools. Nature Protocols 2, 953-971.
26. Fei Z, Joung JG, Tang X, Zheng Y, Huang M, Lee JM, McQuinn R, Tieman DM, Alba R, Klee HJ, Giovannoni JJ. 2011. Tomato Functional Genomics Database: a comprehensive resource and analysis package for tomato functional genomics. Nucleic Acids Research 39, 1156-1163.
27. Filisetti-Cozzi TMCC, Carpita NC. 1991. Measurement of uronic acids without interference from neutral sugars. Analytical Biochemstry 197, 157-162.
28. Fridman E, Carrari F, Liu Y, Fernie AR, Zamir D. 2004. Zooming in on a quantitative trait for tomato yield using interspecifc introgressions. Science 305, 1786-1789.
29. Gerrits PO. 1991. The application of glycol methacrylate in histotechnology; some fundamental principles. Department of Anatomy and Embryology, State University Groningen, Groningen, The Netherlands.
30. Giovannoni JJ, DellaPenna D, Bennett AB, Fischer RL. 1989. Expression of a chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening. Plant Cell 1, 53-63.
31. Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kühn C. 2006. Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. The Plant Journal 45, 180-192.
32. Harholt J, Suttangkakul A, Vibe Scheller H. 2010. Biosynthesis of pectin. Plant Physiology 153, 384-395.
33. Harker FR, Redgwell RJ, Hallett IC, Murray SH, Carter G. 1997. Texture of fresh fruit. Horticultural Reviews 20, 121-224.
34. Hoeglund A, Doennes P, Blum T, Adolph HW, Kohlbacher O. 2006. MultiLoc: prediction of protein subcellular localization using N-terminal targeting sequences, sequence motifs, and amino acid composition. Bioinformatics 22, 1158-1165.
35. Houben K, Jolie RP, Fraeye I, Van Loey AM, Hendrickx ME. 2011. Comparative study of the cell wall composition of broccoli, carrot, and tomato: structural characterization of the extractable pectins and hemicelluloses. Carbohydrate Research 346, 1105-1111.
36. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Computational Applied Biosciences 8, 275-282.
37. Karimi M, Inzé D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193-195.
38. Kong Y, Zhou G, Yin Y, Xu Y, Pattathil S, Hahn MG. 2011. Molecular analysis of a family of Arabidopsis genes related to galacturonosyltransferases. Plant Physiology 155, 1791-1805.
39. Kopka J, Schauer N, Krueger S, et al. 2005. GMD@CSB.DB: the GolmMetabolome Database. Bioinformatics 21, 1635-1638.
40. Lahaye M, Devaux MF, Poole M, Seymour GB, Causse M. 2013. Pericarp tissue microstructure and cell wall polysaccharide chemistry are differently affected in lines of tomato with contrasted frmness. Postharvest Biology and Technology 76, 83-90.
41. Lahaye M, Quemener B, Causse M, Seymour GB. 2012. Hemicellulose fne structure is affected differently during ripening of tomato lines with contrasted texture. International Journal of Biological Macromolecules 51, 462-470.
42. Leboeuf E, Guillon F, Thoiron S, Lahaye M. 2005. Biochemical and immunohistochemical analysis of pectic polysaccharides in the cell walls of Arabidopsis mutant QUASIMODO 1 suspension-cultured cells: implications for cell adhesion. Journal of Experimental Botany 56, 3171-3182.
43. Lillie RD. 1965. Histopathologic technic and practical histochemistry, 3rd edn. New York: McGraw-Hill.
44. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR. 2006. Gas chromatography mass spectrometry-based metabolite profling in plants. Nature Protocols 1, 387-396.
45. Lunn D, Phan TD, Tucker GA, Lycett GW. 2013. Cell wall composition of tomato fruit changes during development and inhibition of vesicle traffcking is associated with reduced pectin levels and reduced softening. Plant Physiology and Biochemistry 66, 91-97.
46. Maxwell K, Johnson GN. 2000. Chlorophyll fuorescence-a practical guide. Journal of Experimental Botany 51, 659-668.
47. Mohnen D. 2008. Pectin structure and biosynthesis. Current Opinion in Plant Biology 11, 266-277.
48. Nelson BK, Cai X, Nebenführ A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. The Plant Journal 51, 1126-1136.
49. Nguyen-Quoc B, Foyer CH. 2001. A role for 'futile cycles' involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. Journal of Experimental Botany 52, 881-889.
50. Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AMO, Loureiro ME, Ratcliffe RG, Sweetlove LJ, Fernie AR. 2005. Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiology 137, 611-622.
51. O'Brien TP, Feder N, McCully ME. 1964. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368-373.
52. Oms-Oliu G, Hertog MLATM, Van de Poel B, Ampofo-Asiama J, Geeraerd AH, Nicolaï BM. 2011. Metabolic characterization of tomato fruit during preharvest development, ripening, and postharvest shelf-life. Postharvest Biology and Technology 62, 7-16.
53. Oomen RJFJ, Doeswijk-Voragen CHL, Bush MS, et al. 2002. In muro fragmentation of the rhamnogalacturonan I backbone in potato (Solanum tuberosum L.) results in a reduction and altered location of the galactan and arabinan side-chains and abnormal periderm development. The Plant Journal 30, 403-413.
54. Orfla C, Sørensen SO, Harholt J, Geshi N, Crombie H, Truong HN, Reid JSG, Knox JP, Scheller HV. 2005. QUASIMODO1 is expressed in vascular tissue of Arabidopsis thaliana inforescence stems, and affects homogalacturonan and xylan biosynthesis. Planta 222, 613-622.
55. Osorio S, Alba R, Nikoloski Z, Kochevenko A, Fernie AR, Giovannoni JJ. 2012. Integrative comparative analyses of transcript and metabolite profles from pepper and tomato ripening and development stages uncovers species-specifc patterns of network regulatory behavior. Plant Physiology 159, 1713-1729.
56. Patrick JW, Offer CE. 1996. Post-sieve element transport of photoassimilates in sink regions. Journal of Experimental Botany 47, 1165-1177.
57. Peña M J, Zhong R, Zhou G, Richardson EA, O'Neill MA, Darvill AG, York WS, Ye Z. 2007. Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19, 549-563.
58. Persson S, Caffall KH, Freshour G, Hilley MT, Bauer S, Poindexter P, Hahn MG, Mohnen D, Somerville C. 2007. The Arabidopsis irregular xylem8 mutant is defcient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell 19, 237-255.
59. Rasband WS. 1997-2012. ImageJ. US National Institutes of Health, Bethesda, Maryland, USA. http://imagej.nih.gov/ij/.
60. Reiter WD. 2008. Biochemical genetics of nucleotide sugar interconversion reactions. Current Opinion in Plant Biology 11, 236-243.
61. Ridley BL, Neill MAO, Mohnen D. 2001. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57, 929-967.
62. Roessner U, Willmitzer L, Fernie AR. 2001. High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identifcation of phenocopies. Plant Physiology 127, 749-764.
63. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM. 2009. Amplifcation effciency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45.
64. Saeed AI, Sharov V, White J, et al. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378.
65. Saeman J F, Bulb JL, Harris EE. 1945. Quantitative saccharifcation of wood and cellulose. Industrial and Engineering Chemistry 17, 35-37.
66. Saladié M, Matas AJ, Isaacson T, et al. 2007. A reevaluation of the key factors that infuence tomato fruit softening and integrity. Plant Physiology 144, 1012-1028.
67. Schauer N, Semel Y, Roessner U, et al. 2006. Comprehensive metabolic profling and phenotyping of interspecifc introgression lines for tomato improvement. Nature Biotechnology 24, 447-454.
68. Schauer N, Steinhauser D, Strelkov S, et al. 2005. GC-MS libraries for the rapid identifcation of metabolites in complex biological samples. Federation of European Biochemical Societies Letters 579, 1332-1337.
69. Shackel KA, Greve C, Labavitch JM, Ahmadi H. 1991. Cell turgor changes associated with ripening in tomato pericarp tissue. Plant Physiology 97, 814-816.
70. Shatkay H, Höglund A, Brady S, Blum T, Dönnes P, Kohlbacher O. 2007. SherLoc: high-accuracy prediction of protein subcellular localization by integrating text and protein sequence data. Bioinformatics 23, 1410-1417.
71. Sienkiewicz-Porzucek A, Sulpice R, Osorio S, Krahnert I, Leisse A, Urbanczyk-Wochniak E, Hodges M, Fernie AR, Nunes-Nesi A. 2010. Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Molecular Plant 3, 156-173.
72. Sila DN, Buggenhout SV, Duvetter T, Fraeye I, Roeck AD, Loey AV, Hendrickx M. 2009. Pectins in processed fruits and vegetables: part II. Structure-function relationships. Comprehensive Reviews in Food Science and Food Safety 8, 86-104.
73. Smith DL, Abbott JA, Gross KC. 2002. Down-regulation of tomato β-galactosidase 4 results in decreased fruit softening. Plant Physiology 129, 1755-1762.
74. Song C, Guo J, Sun W, Wang Y. 2012. Whole genome duplication of intra-and inter-chromosomes in the tomato genome. Journal of Genetics and Genomics 39, 361-368.
75. Sterling JD, Atmodjo MA, Inwood SE, Kumar Kolli VS, Quigley HF, Hahn MG, Mohnen D. 2006. Functional identifcation of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. Proceedings of the National Academy of Sciences, USA 103, 5236-5241.
76. Szymanski DB, Cosgrove DJ. 2009. Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Current Biology 19, 800-811.
77. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731-2739.
78. The Tomato Genome Consortium. 2012. The tomato genome sequence provides insights into feshy fruit evolution. Nature 485, 635-641.
79. Thompson JD, Higgins DG, Gibson TJ. 1997. The CLUSTAL-X windows interface: fexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876-4882.
80. 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.
81. Unda F, Canam T, Preston L, Mansfeld SD. 2012. Isolation and characterization of galactinol synthases from hybrid poplar. Journal of Experimental Botany 63, 2059-2069.
82. Vincken JP, Schols HA, Oomen RJFJ, McCann MC, Ulvskov P, Voragen AGJ, Visser RGF. 2003. If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiology 132, 1781-1789.
83. Voorrips RE. 2002. MapChart: software for the graphical presentation of linkage maps and QTLs. Journal of Heredity 93, 77-78.
84. Wormit A, Butt SM, Chairam I, et al. 2012. Osmosensitive changes of carbohydrate metabolism in response to cellulose biosynthesis inhibition. Plant Physiology 159, 105-117.
85. Yin Y, Chen H, Hahn MG, Mohnen D, Xu Y. 2010. Evolution and function of the plant cell wall synthesis-related glycosyltransferase family 8. Plant Physiology 153, 1729-1746.
86. Zhou T, Zhang R, Guo S. 2011. Molecular cloning and characterization of GhGolS1, a novel gene encoding galactinol synthase from cotton (Gossypium hirsutum). Plant Molecular Biology Report 30, 699-709.