The cell wall pectic polymer rhamnogalacturonan-II is required for proper pollen tube elongation: Implications of a putative sialyltransferase-like protein

Annals of Botany

Volumn 114, Issue 6, 2014, Pages 1177-1188

  Dumont, Marie ^a   Lehner, Arnaud ^a   Bouton, Sophie ^b   Kiefer Meyer, Marie Christine ^a   Voxeur, Aline ^a,c   Pelloux, Jérôme ^b   Lerouge, Patrice ^a   Mollet, Jean Claude ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

^c INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

Arabidopsis thaliana; Dha; Kdo; pectin motif; plant cell wall; pollen tube; RG II; Rhamnogalacturonan II; sialyltransferase like protein

Indexed keywords

ANATOMY; BIOLOGICAL DEVELOPMENT; BIOLOGICAL PRODUCTION; CELL ORGANELLE; DICOTYLEDON; ENZYME ACTIVITY; FUNCTIONAL ROLE; GENE EXPRESSION; MUTATION; PHYTOCHEMISTRY; POLYSACCHARIDE; PROTEIN;

ARABIDOPSIS THALIANA;

2-KETO-3-DEOXYOCTONATE; ARABIDOPSIS PROTEIN; PECTIN; POLYMER; RHAMNOGALACTURONAN II; SIA2 PROTEIN, ARABIDOPSIS; SIALYLTRANSFERASE; SUGAR ACID;

ANTIBODY SPECIFICITY; ARABIDOPSIS; CELL WALL; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; POLLEN; POLLEN TUBE; REPORTER GENE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; MUTATION; ORGAN SPECIFICITY; PECTINS; PHENOTYPE; POLLEN; POLLEN TUBE; POLYMERS; SIALYLTRANSFERASES; SUGAR ACIDS;

EID: 84910658784     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu093     Document Type: Article

References (87)

1. Abramoff MD, Magalhães PJ, Ram SJ. 2004. Image processing with Image J. Biophotonics International 11: 36-42.
2. Audry M, Jeanneau C, Imberty A, Harduin-Lepers A, Delannoy P, Breton C. 2011. Current trends in the structure-activity relationships of sialyltrans-ferases. Glycobiology 21: 716-726.
3. Bakker H, Routier F, Ashikov A, Neumann D, Bosch D, Gerardy-Schahn R. 2008. A CMP-sialic acid transporter cloned from Arabidopsis thaliana. Carbohydrate Research 343: 2148-2152.
4. Bar-Peled M, Urbanowicz BR, O'Neill MA. 2012. The synthesis and origin of thepectic polysacchariderhamnogalacturonanII-Insightsfrom nucleotide sugar formation and diversity. Frontiers in Plant Science 3: 1-12.
5. Belunis CJ, Clementz T, Carty SM, Raetz CRH. 1995. Inhibition of lipopolysaccharide biosynthesis and cell growth following inactivation of the kdtA gene in Escherichia coli. Journal of Biological Chemistry 270: 27646-27652.
6. Blevins DG, Lukaszewski KM. 1998. Boron in plant structure and function. Annual Review of Plant Physiology and Plant Molecular Biology 49: 481-500.
7. Boavida LC, McCormick S. 2007. Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. The Plant Journal 52: 570-582.
8. Brewbaker JL, Kwack BH. 1963. The essentialroleofcalcium ioninpollenger-mination and pollen tube growth. American Journal of Botany 50: 859.
9. Chebli Y, Kaneda M, Zerzour R, Geitmann A. 2012. The cell wall of the Arabidopsis pollen tube-spatial distribution, recycling, and network formation of polysaccharides. Plant Physiology 160: 1940-1955.
10. Cheng C, McComb JA, Rerkasem B. 1992. Techniques to study the anther in wheat. In: Mann CE, Rerkasem B, eds. Wheat Special Report No. 11. Boron deficiency in wheat. Mexico: CIMMYT, 32-33.
11. Covey PA, Subbaiah CC, Parsons RL, et al. 2010. Apollen-specific RALFfrom tomato that regulates pollen tube elongation. Plant Physiology 153: 703-715.
12. Dai S, Chen T, Chong K, Xue Y, Liu S, Wang T. 2006. Proteomicsidentification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Molecular and Cellular Proteomics 6: 207-230.
13. Dardelle F, Lehner A, Ramdani Y, et al. 2010. Biochemical and immunocyto-logical characterizations of Arabidopsis pollen tube cell wall. Plant Physiology 153: 1563-1576.
14. Darvill AG, McNeil M, Albersheim P. 1978. Structureof plant cell walls. Plant Physiology 62: 418-422.
15. Daskalova SM, Pah AR, Baluch DP, Lopez LC. 2009. The Arabidopsis thali-ana putative sialyltransferase resides in the Golgi apparatus but lacks the ability to transfer sialic acid. Plant Biology 11: 284-299.
16. Delmas F, Séveno M, Northey JGB, et al. 2008. The synthesis of the rhamno-galacturonan II component 3-deoxy-d-manno-2-octulosonic acid (Kdo) is required for pollen tube growth and elongation. Journal of Experimental Botany 59: 2639-2647.
17. Deng Y, Wang W, Li W-Q, et al. 2010. MALEGAMETOPHYTEDEFECTIVE2, encoding a sialyltransferase-like protein, is required for normal pollen germination and pollen tube growth in Arabidopsis. Journal of Integrative Plant Biology 52: 829-843.
18. Doco T, O'Neill MA, Pellerin P. 2001. Determination of the neutral and acidic glycosyl-residue compositions of plant polysaccharides by GC-EI-MS analysis of the trimethylsilyl methyl glycoside derivatives. Carbohydrate Polymers 46: 249-259.
19. Dunkley TPJ, Hester S, Shadforth IP, et al. 2006. Mapping the Arabidopsis or-ganelle proteome. Proceedings of the National Academy of Sciences, USA 103: 6518-6523.
20. Edashige Y, Ishii T. 1998. Rhamnogalacturonan II from cell walls of Cryptomeria japonica. Phytochemistry 49: 681-690.
21. Egelund J, Petersen BL, Motawia MS, et al. 2006. Arabidopsis thaliana RGXT1 and RGXT2 encode Golgi-localized (1, 3)-alpha-d-xylosyltransferases involved in the synthesis of pectic rhamnogalacturonan-II. The Plant Cell 18: 2593-2607.
22. Egelund J, Damager I, Faber K, Olsen C-E, Ulvskov P, Petersen BL. 2008. Functional characterisation of a putative rhamnogalacturonan II specific xylosyltransferase. FEBS Letters 582: 3217-3222.
23. Fang K, Wang Y, Yu T, et al. 2008. Isolationofde-exined pollen and cytological studies of the pollen intines of Pinus bungeana Zucc. Ex Endl. and Picea wilsonii Mast. Flora 203: 332-340.
24. Ganie MA, Akhter F, Bhat MA, et al. 2013. Boron-a critical nutrient element for plant growth and productivity with referenceto temperate fruits. Current Science 104: 76-85.
25. García-Hernández ER, Cassab López GI. 2005. Structural cell wall proteins from five pollen species and their relationship with boron. Brazilian Journal of Plant Physiology 17: 375-381.
26. Goldbach HE, Wimmer MA. 2007. Boron in plants and animals: is there a role beyond cell wall structure? Journalof Plant Nutrition and Soil Science 170: 39-48.
27. Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C. 2009. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. The Plant Cell 21: 3119-3132.
28. Holdaway-Clarke TL, Weddle NM, Kim S, et al. 2003. Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. Journal of Experimental Botany 54: 65-72.
29. Ishii T, Matsunaga T. 1996. Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp. Carbohydrate Research 284: 1-9.
30. Jayaprakash P, Sarla N. 2001. Development of an improved medium for germination of Cajanus cajan (L.) Millsp. pollen in vitro. Journal of Experimental Botany 52: 851-855.
31. Jiang L, Yang S-L, Xie L-F, et al. 2005. VANGUARD1 encodes a pectin methy-lesterase that enhancespollentube growthintheArabidopsisstyle and transmitting tract. The Plant Cell 17: 584-596.
32. Johnson MA, Lord E. 2006. Extracellular guidance cues and intracellular signalling pathways that direct pollen tube growth. In: Malhó R, ed. Plant Cell Monographs. The pollen tube. Berlin: Springer, 223-242.
33. Johnson-Brousseau SA, McCormick S. 2004. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. The Plant Journal 39: 761-775.
34. Kakani VG, Reddy KR, Koti S, et al. 2005. Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. Annals of Botany 96: 59-67.
35. Kaneko S, Ishii T, Matsunaga T. 1997. A boron-rhamnogalacturonan-II complex from bamboo shoot cell walls. Phytochemistry 44: 243-248.
36. Kobayashi M, Kouzu N, Inami A, et al. 2011. Characterization of Arabidopsis CTP:3-deoxy-d-manno-2-octulosonate cytidylyltransferase (CMP-KDO synthetase), the enzyme that activates KDO during rhamnogalacturonan II biosynthesis. Plant and Cell Physiology 52: 1832-1843.
37. Lazzaro MD, Donohue JM, Soodavar FM. 2003. Disruption of cellulose synthesisbyisoxaben causestip swelling and disorganizes cortical microtu-bules in elongating conifer pollen tubes. Protoplasma 220: 201-207.
38. Lee S-H, Kim W-S, Han T-H. 2009. Effects of post-harvest foliar boron and calcium applications on subsequent season's pollen germination and pollen tube growth of pear (Pyrus pyrifolia). Scientia Horticulturae 122: 77-82.
39. Lehner A, Dardelle F, Soret-Morvan O, Lerouge P, Driouich A, Mollet J-C. 2010. Pectins in the cell wall of Arabidopsis thaliana pollen tube and pistil. Plant Signaling and Behavior 5: 1282-1285.
40. Li T, Choi W-G, Wallace IS, Baudry J, Roberts DM. 2011. Arabidopsis thaliana NIP7. 1: an anther-specific boric acid transporter of the aquaporin superfamily regulated by an unusual tyrosine in helix 2 of the transport pore. Biochemistry 50: 6633-6641.
41. Liu L, Huang L, Li Y. 2013. Influence of boric acid and sucrose on the germination and growth of Areca pollen. American Journal of Plant Sciences 4: 1669-1674.
42. Liu X-L, Liu L, Niu Q-K, et al. 2011. MALE GAMETOPHYTE DEFECTIVE 4 encodes a rhamnogalacturonan II xylosyltransferase and is important for growth of pollen tubes and roots in Arabidopsis. The Plant Journal 65: 647-660.
43. Loraine AE, McCormick S, Estrada A, Patel K, Qin P. 2013. RNA-Seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiology 162: 1092-1109.
44. Matoh T, Takasaki M, Takabe K, Kobayashi M. 1998. Immunocytochemistry of rhamnogalacturonan II in cell walls of higher plants. Plant and Cell Physiology 39: 483-491.
45. Matsunaga T, Ishii T, Matsumoto S, et al. 2004. Occurrenceof the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiology 134: 339-351.
46. Mc Gee RJ, Baggett JR. 1992. Unequal growth rate of pollen tubes from normal and stringless pea genotypes. Hort Science 27: 833-834.
47. Mc Kenna ST, Kunkel JG, Bosch M, et al. 2009. Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. The Plant Cell 21: 3026-3040.
48. Missihoun TD, Kirch H-H, Bartels D. 2012. T-DNA insertion mutants reveal complex expression patterns of the aldehyde dehydrogenase 3H1 locus in Arabidopsis thaliana. Journal of Experimental Botany 63: 3887-3898.
49. Mohnen D. 2008. Pectin structure and biosynthesis. Current Opinion in Plant Biology 11: 266-277.
50. Mollet J-C, Faugeron C, Morvan H. 2007. Cell adhesion, separation and guidance in compatible plant reproduction. Annual Plant Reviews 25: 69-90.
51. Mollet J-C, Leroux C, Dardelle F, Lehner A. 2013. Cell wall composition, biosynthesisandremodelling duringpollen tube growth. Plants 2:107-147.
52. Noguchi K, Yasumori M, Imai T, et al. 1997. bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron. Plant Physiology 115: 901-906.
53. O'Neill MA, Warrenfeltz D, Kates K, et al. 1996. Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester. In vitro conditions for the formation and hydrolysis of the dimer. Journal of Biological Chemistry 271: 22923-22930.
54. O'Neill MA, Eberhard S, Albersheim P, Darvill AG. 2001. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294: 846-849.
55. O'Neill MA, Ishii T, Albersheim P, Darvill AG. 2004. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysacchar-ide. Annual Review of Plant Biology 55: 109-139.
56. Pabst M, Fischl RM, et al. 2013. Rhamnogalacturonan II structure shows vari-ationin the side chains monosaccharide composition and methylation status within and across different plant species. The Plant Journal 76: 61-72.
57. Palanivelu R, Tsukamoto T. 2012. Pathfinding in angiosperm reproduction: pollen tube guidance by pistils ensures successful double fertilization. Developmental Biology 1: 96-113.
58. Parre E, Geitmann A. 2005a. More than a leak sealant. The mechanical properties of callose in pollen tubes. Plant Physiology 137: 274-286.
59. Parre E, Geitmann A. 2005b. Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220: 582-592.
60. Paynel F, Leroux C, Surcouf O, Schaumann A, Pelloux J, Driouich A, Mollet JC, Lerouge P, Lehner A, Mareck A. 2014. Kiwi fruit PMEI inhi-bitsPMEactivity, modulatesroot elongationand inducespollentubeburstin Arabidopsis thaliana. Plant Growth Regulation. doi:10.1007/s10725-014-9919-7.
61. Pérez S, Rodríguez-Carvajal MA, Doco T. 2003. A complex plant cell wall polysaccharide: rhamnogalacturonan II. A structure in quest of a function. Biochimie 85: 109-121.
62. Persia D, Cai G, Casino CD, Faleri C, Willemse MTM, Cresti M. 2008. Sucrose synthase is associated with the cell wall of tobacco pollen tubes. Plant Physiology 147: 1603-1618.
63. Pina C. 2005. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiology 138: 744-756.
64. Potts B, Marsden-Smedley J. 1989. In vitro germination of Eucalyptus pollen: responsetovariationinboric acid and sucrose. Australian Journalof Botany 37: 429-441.
65. Prajapati PP, Jain BK. 2010. Effect of sucrose, boron, calcium, magnesium and nitrate during in vitro pollen germination in Luffa aegyptica Mill. Prajna 18: 5-8
66. Rhee SY, Somerville CR. 1998. Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysacchar-ides of the pollen mother cell wall. The Plant Journal 15: 79-88.
67. Roberts IN, Gaude TC, Harrod G, Dickinson HG. 1983. Pollen-stigma interactions in Brassica oleracea; a new pollen germination medium and its use in elucidating the mechanism of self incompatibility. Theoretical and Applied Genetics 65: 231-238.
68. Rounds CM, Winship LJ, Hepler PK. 2011. Pollentube energetics:respiration, fermentation and the race to the ovule. Ao B Plants 2011: plr019.
69. Schreiber DN, Dresselhaus T. 2003. In vitro pollen germination and transient transformation of Zea mays and other plant species. Plant Molecular Biology Reporter 21: 31-41.
70. Séveno M, Bardor M, Paccalet T, Gomord V, Lerouge P, Faye L. 2004. Glycoprotein sialylation in plants? Nature Biotechnology 22: 1351-1352.
71. Shimokawa T, Ishii T, Matsunaga T. 1999. Isolationandstructural characterization of rhamnogalacturonan II-borate complex from Pinus densiflora. Journal of Wood Science 45: 435-439.
72. Takashima S, Seino J, Nakano T, et al. 2009. Analysis of CMP-sialic acid transporter-like proteins in plants. Phytochemistry 70: 1973-1981.
73. Tian G-W, Chen M-H, Zaltsman A, Citovsky V. 2006. Pollen-specific pectin methylesterase involved in pollen tube growth. Developmental Biology 294: 83-91.
74. Ulker B, Peiter E, Dixon DP, et al. 2008. Getting the most out of publicly available T-DNA insertion lines. The Plant Journal 56: 665-677.
75. Vandesompele J, De Preter K, Pattyn F, et al. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: research0034.
76. Vidal S, Williams P, O'Neill MA, Pellerin P. 2001. Polysaccharides from grape berry cell walls. Part I: tissue distribution and structural characterization of the pectic polysaccharides. Carbohydrate Polymers 45: 315-323.
77. Vizintin L, Bohanec B. 2004. In vitro manipulation of cucumber (Cucumis sativus L.) pollen and microspores: isolation procedures, viability tests, germination, maturation. Acta Biologica Cracoviensia Series Botanica 46: 177-183.
78. Voxeur A, Gilbert L, Rihouey C, et al. 2011. Silencing of the GDP-d-mannose 3, 5-epimerase affects the structure and cross-linking of the pectic polysac-charide rhamnogalacturonan II and plant growth in tomato. Journal of Biological Chemistry 286: 8014-8020.
79. Voxeur A, André A, Breton C, Lerouge P. 2012. Identification of putative rhamnogalacturonan-II specific glycosyltransferases in Arabidopsis using a combination of bioinformatics approaches. PLoS One 7: e51129.
80. Wang L, Wang W, Wang Y-Q, et al. 2013. Arabidopsis galacturonosyltransfer-ase (GAUT) 13 and GAUT14 have redundant functions in pollen tube growth. Molecular Plant 6: 1131-1148.
81. Wang Q, Lu L, Wu X, Li Y, Lin J. 2003. Boron influences pollen germination and pollen tube growth in Picea meyeri. Tree Physiology 23: 345-351.
82. Wang W, Wang L, Chen C, et al. 2011. Arabidopsis CSLD1 and CSLD4 are required for cellulose deposition and normal growth of pollen tubes. Journal of Experimental Botany 62: 5161-5177.
83. Wang YH. 2008. How effective is T-DNA insertional mutagenesis in Arabidopsis? Journal of Biochemical Technology 1: 11-20.
84. Warrington K. 1923. The effect of boric acid and borax on the broad bean and certain other plants. Annals of Botany 37: 629-672.
85. Whitcombe AJ, O'Neill MA, Steffan W, Albersheim P, Darvill AG. 1995. Structural characterization of the pectic polysaccharide, rhamnogalacturonan-II. Carbohydrate Research 271: 15-29.
86. White KA, Kaltashov IA, Cotter RJ, Raetz CR. 1997. A mono-functional 3-deoxy-d-manno-octulosonic acid (Kdo) transferase and a Kdo kinase in extracts of Haemophilus influenzae. Journal of Biological Chemistry 272: 16555-16563.
87. Woriedh M, Wolf S, Márton ML, et al. 2013. External application of gametophyte-specific Zm PMEI1 induces pollen tube burst in maize. Plant Reproduction 26: 255-266.