Pectic arabinan side chains are essential for pollen cell wall integrity during pollen development

Plant Biotechnology Journal

Volumn 12, Issue 4, 2014, Pages 492-502

  Cankar, Katarina ^a   Kortstee, Anne ^a   Toonen, Marcel A J ^a   Wolters Arts, Mieke ^b   Houbein, Rudolf ^a   Mariani, Celestina ^b   Ulvskov, Peter ^c   Jorgensen, Bodil ^c   Schols, Henk A ^a   Visser, Richard G F ^a   Trindade, Luisa M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Arabinan; Cell wall modification; Pectin; Pollen sterility; Potato; Solanum tuberosum

Indexed keywords

SOLANUM TUBEROSUM;

ARABAN; MONOSACCHARIDE; PECTIN; POLYSACCHARIDE;

ANATOMY AND HISTOLOGY; CELL WALL; CHROMOSOME SEGREGATION; CROSS BREEDING; CYTOLOGY; GENE DOSAGE; GENETIC TRANSFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE; PLANT INFERTILITY; PLANT TUBER; POLLEN; POTATO; TRANSGENE; TRANSGENIC PLANT; ULTRASTRUCTURE;

CELL WALL; CHROMOSOME SEGREGATION; CROSSES, GENETIC; GENE DOSAGE; MONOSACCHARIDES; PECTINS; PHENOTYPE; PLANT INFERTILITY; PLANT TUBERS; PLANTS, GENETICALLY MODIFIED; POLLEN; POLYSACCHARIDES; SOLANUM TUBEROSUM; TRANSFORMATION, GENETIC; TRANSGENES;

EID: 84899072713     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12156     Document Type: Article

References (54)

1. Arsovski, A.A., Popma, T.M., Haughn, G.W., Carpita, N.C., McCann, M.C. and Western, T.L. (2009) AtBXL1 encodes a bifunctional beta-D-Xylosidase/alpha-L-Arabinofuranosidase required for pectic arabinan modification in arabidopsis mucilage secretory cells. Plant Physiol. 150, 1219-1234.
2. Bush, M.S., Marry, M., Huxham, I.M., Jarvis, M.C. and McCann, M.C. (2001) Developmental regulation of pectic epitopes during potato tuberisation. Planta, 213, 69-880.
3. Caffall, K.H., Pattathil, S., Phillips, S.E., Hahn, M.G. and Mohnen, D. (2009) Arabidopsis thaliana T-DNA mutants implicate GAUT genes in the biosynthesis of pectin and xylan in cell walls and seed testa. Mol. Plant, 2, 1000-1014.
4. Chen, L., Carpita, N.C., Reiter, W.D., Wilson, R.H., Jeffries, C. and McCann, M.C. (1998) A rapid method to screen for cell-wall mutants using discriminant analysis of Fourier transform infrared spectra. Plant J. 16, 385-392.
5. Dardelle, F., Lehner, A., Ramdani, Y., Bardor, M., Lerouge, P., Driouich, A. and Mollet, J.C. (2010) Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol. 153, 1563-1576.
6. Gou, J.Y., Miller, L.M., Hou, G., Yu, X.H., Chen, X.Y. and Liu, C.J. (2012) Acetylesterase-mediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell, 24, 50-65.
7. Ha, M.A., Vietor, R.J., Jardine, G.D., Apperley, D.C. and Jarvis, M.C. (2005) Conformation and mobility of the arabinan and galactan side-chains of pectin. Phytochemistry, 66, 1817-1824.
8. Hansen, S.L., Ray, P.M., Karlsson, A.O., Jørgensen, B., Borkhardt, B., Petersen, B.L. and Ulvskov, P. (2011) Mechanical properties of plant cell walls probed by relaxation spectra. Plant Physiol. 155, 246-258.
9. Harholt, J., Kruger Jensen, J., Oxenboll Sorensen, S., Orfila, C., Pauly, M. and Scheller, H.V. (2006) Arabinan deficient 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol. 140, 49-58.
10. Hennegan, K.P. and Danna, K.J. (1998) pBIN20: an improved binary vector for agrobacterium-mediated transformation. Plant Mol. Biol. Rep. 16, 129-131.
11. Jones, L., Seymour, G.B. and Knox, J.P. (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1, -4)-β-D-galactan. Plant Physiol. 113, 1405-1412.
12. Jones, L., Milne, J.L., Ashford, D. and McQueen-Mason, S.J. (2003) Cell wall arabinan is essential for guard cell function. Proc. Natl Acad. Sci. USA, 100, 11783-11788.
13. Larsen, F.H., Byg, I., Damager, I., Diaz, J., Engelsen, S.B. and Ulvskov, P. (2011) Residue specific hydration of primary cell wall potato pectin identified by solid-state 13C single pulse MAS and CP/MAS NMR spectroscopy. Biomacromolecules, 12, 1844-1850.
14. Liepmann, A.H., Wigthman, R., Geshi, N., Turner, S.R. and Scheller, H.V. (2010) Arabidopsis-a powerful model system for plant cell wall research. Plant J. 61, 1107-1121.
15. Lindhout, P., Meijer, D., Schotte, T., Hutten, R.C.B., Visser, R.G.F. and van Eck, H.J. (2011) Towards F1 hybrid seed potato breeding. Potato Res. 54, 301-312.
16. Majewska-Sawka, A., Munster, A. and Wisniewska, E. (2004) Temporal and spatial distribution of pectin epitopes in differentiating anthers and microspores of fertile and sterile sugar beet. Plant Cell Physiol. 45, 560-572.
17. Martin, I., Dopico, B., Munoz, F.J., Esteban, R., Oomen, R.J., Driouich, A., Vincken, J.P., Visser, R. and Labrador, E. (2005) In vivo expression of a Cicer arietinum beta-galactosidase in potato tubers leads to a reduction of the galactan side-chains in cell wall pectin. Plant Cell Physiol. 46, 1613-1622.
18. Moore, J.P., Nguema-Ona, E., Chevalier, L., Lindsey, G.G., Brandt, W.F., Lerouge, P., Farrant, J.M. and Driouich, A. (2006) Response of the leaf cell wall to desiccation in the resurrection plant Myrothamnus flabellifolius. Plant Physiol. 141, 651-662.
19. Moore, J.P., Farrant, J.M. and Driouich, A. (2008) A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal. Behav. 3, 102-104.
20. Mouille, G., Robin, S., Lecomte, M., Pagant, S. and Höfte, H. (2003) Classification and identification of Arabidopsis cell wall mutants using Fourier-Transform InfraRed (FT-IR) microspectroscopy. Plant J. 35, 393-404.
21. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
22. Nicot, N., Hausman, J.F., Hoffmann, L. and Evers, D. (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J. Exp. Bot. 56, 2907-2917.
23. Øbro, J., Borkhardt, B., Harholt, J., Skjøt, M., Willats, W.G.T. and Ulvskov, P. (2009) Simultaneous in vivo truncation of pectic side chains. Transgenic Res. 18, 961-969.
24. Odell, J.T., Nagy, F. and Chua, N.H. (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature, 313, 810-812.
25. Olmedilla, A., Schrauwen, J.A.M. and Wullems, G.J. (1991) Visualization of starch-synthase expression by in situ hybridization during pollen development. Planta, 184, 182-186.
26. Oomen, R.J., Doeswijk-Voragen, C.H., Bush, M.S., Vincken, J.P., Borkhardt, B., van den Broek, L.A., Corsar, J., Ulvskov, P., Voragen, A.G., McCann, M.C. and Visser, R.G. (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. Plant J. 30, 403-413.
27. Oomen, R.J.F.J., Tzitzikas, E.N., Bakx, E.J., Straatman-Engelen, I., Bush, M.S., McCann, M.C., Schols, H.A., Visser, R.G.F. and Vincken, J.P. (2003) Modulation of the cellulose content of tuber cell walls by antisense expression of different potato (Solanum tuberosum L) CesA clones. Phytochemistry, 65, 535-546.
28. Oomen, R.J.F.J., Dao-Thi, B., Tzitzikas, E.N., Bakx, E.J., Schols, H.A., Visser, R.G.F. and Vincken, J.P. (2004) Overexpression of two different potato UDP-Glc 4-epimerases can increase the galactose content of potato tuber cell walls. Plant Sci. 166, 1097-1104.
29. Orfila, C., Dal Degan, F., Jørgensen, B., Scheller, H.V., Ray, P.M. and Ulvskov, P. (2012) Expression of mung bean pectin acetyl esterase in potato tubers: Effect on acetylation of cell wall polymers and tuber mechanical properties. Planta, 236, 185-196.
30. Oxenboll Sorensen, S., Pauly, M., Bush, M., Skjot, M., McCann, M.C., Borkhardt, B. and Ulvskov, P. (2000) Pectin engineering: modification of potato pectin by in vivo expression of an endo-1, 4-beta-D-galactanase. Proc. Natl Acad. Sci. USA, 97, 7639-7644.
31. Pacini, E., Guarnieri, M. and Nepi, M. (2006) Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma, 228, 73-77.
32. Peterson, R., Slovin, J.P. and Chen, C. (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int. J. Plant Biol. 1, 66-69.
33. Phan, T.D., Bo, W., West, G., Lycett, G.W. and Tucker, G.A. (2007) Silencing of the major salt-dependant isoform of pectin methyl esterase in tomato alters fruit softening. Plant Physiol. 144, 1960-1967.
34. Pina, C., Pinto, F., Feijo, J.A. and Decker, J.D. (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.
35. Reiter, W.D., Chapple, C.S. and Sommerville, C.R. (1993) Altered growth and cell walls in a fucose-deficient mutant of Arabidopsis. Science, 261, 1032-1035.
36. Reiter, W.D., Chapple, C.S. and Sommerville, C.R. (1997) Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. Plant J. 12, 335-345.
37. Ridley, B.L., O'Neill, M.A. and Mohnen, D. (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signalling. Phytochemistry, 57, 929-967.
38. Robert, P., Jamme, F., Barron, C., Bouchet, B., Saulnier, L., Dumas, P. and Guillon, F. (2011) Change in wall composition of transfer and aleurone cells during wheat grain development. Planta, 233, 393-406.
39. Rocha-Sosa, M., Sonnewald, U., Frommer, W., Stratmann, M., Schell, J. and Willmitzer, W. (1989) Both developmental and metabolic signals activate the promoter of a class I patatin gene. EMBO J. 8, 23-29.
40. Roger, S.O. and Bendich, A.J. (1988) Extraction of DNA from plant tissues. In Plant molecular Biology Manual (Gelvin, S.B. and Schilperoort, R.A. eds), sec A6, pp. 1-10. Dordrecht: Kluwer Academic Publishers.
41. Ross, H.A., McDougall, G.J., Vincent, J.F., Stewart, D., Verrall, S. and Taylor, M.A. (2010a) Discerning intra-tuber differences in textural properties in cooked Solanum tuberosum group Tuberosum and group Phureja tubers. J. Sci. Food Agric. 90, 1527-1532.
42. Ross, H.A., Wright, K.M., McDougall, G.J., Roberts, A.G., Chapmann, S.N., Morris, W.L., Hancock, R.D., Stewart, D., Tucker, G.A., James, E.K. and Taylor, M.A. (2010b) Potato tuber pectin structure is influenced by pectin methyl esterase activity and impacts on cooked potato tuber texture. J. Exp. Bot. 62, 371-381.
43. Ruiter, G.A., Schols, H.A., Voragen, A.G.J. and Rombouts, F.M. (1992) Carbohydrate analysis of water soluble uronic-acid containing polysaccharides with High-Performance-Anion-Exchange-Chromatography using methanolysis combined with TFA hydrolysis is superior to four other methods. Anal. Biochem. 207, 176-185.
44. Skjøt, M., Pauly, M., Bush, M.S., Borkhardt, B., McCann, M.C. and Ulvskov, P. (2002) Direct interference with rhamnogalacturonan I biosynthesis in Golgi vesicles. Plant Physiol. 129, 95-102.
45. 13C MAS NMR studies of the effects of hydration on the cell walls of potatoes and Chinese water chestnuts. J. Agric. Food Chem. 47, 510-517.
46. Taylor, L.R. and Hepler, P.K. (1997) Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 461-491.
47. Udea, K., Yoshimura, F., Miyao, A. and Hirochika, H. (2013) COLLAPSED ABNORMAL POLLEN gene encoding the arabinokinase-like protein is involved in pollen development in rice. Plant Physiol. 162, 858-871.
48. Ulskov, P., He, W., Bruce, D., Jorgensen, B., Bruun Qvist, K., Skjot, M., Hepwordh, D., Borkhardt, B. and Oxenboll Sorensen, S. (2005) Biophysical consequences of remodelling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potato. Planta, 220, 609-620.
49. Verhoeven, T., Feron, R., Wolters-Arts, M., Edqvist, J., Gerats, T., Derksen, J. and Mariani, C. (2005) STIG1 controls exudate secretion in the pistil of petunia and tobacco. Plant Physiol. 138, 153-160.
50. Visser, R.G.F. (1991) Regeneration and transformation of potato by Agrobacterium tumefaciens. In Plant Tissue Culture Manual (ed. Lindsey, K.) Sec. B5, 1-9. Dordrecht, Boston, London: Kluwer Academic Publishers.
51. Visser, R.G.F., Stolte, A. and Jacobsen, E. (1991) Expression of a chimaeric granule-bound starch synthase-GUS gene in transgenic potato plants. Plant Mol. Biol. 17, 691-699.
52. Willats, W.G.T., Marcus, S.E. and Knox, J.P. (1998) Generation of a monoclonal antibody specific to (1, -5)-alpha-L-arabinanan. Carbohydr. Res. 308, 149-152.
53. Willats, W.G.T., McCartney, L., Mackie, W. and Knox, J.P. (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol. Biol. 47, 9-27.
54. Zhu, S., Duwal, A., Su, Q., Vossen, J.H., Visser, R.G.F. and Jacobsen, E. (2013) Vector integration in triple R gene transformants and the clustered inheritance of resistance against potato late blight. Transgenic Res. 22, 315-325.