Pollen Transcriptome and Proteome: Molecular and Functional Analysis

Open access


The pollen grain, because of its unique structural organization, is an extremely useful experimental model in cytological, molecular as well as in genetic studies. Due to the ease of pollen grain isolation, their sorting as well as simple extraction of their DNA, RNA and proteins, male gametophyte cells of angiosperms are presently one of the most intensively studied plant cells. Important and rapid progress in the development of experimental tools for genome exploration caused a significant increase in the number of reports concerning different aspects of gene expression during microsporogenesis and microgametogenesis in angiosperm plants. In this review we present the current knowledge of the pollen transcriptome and proteome during different stages of male gametophyte development, especially in Arabidopsis thaliana. Most of the results presented here were obtained in experiments carried out using microarrays, which were designed on the basis of the known sequence of the Arabidopsis genome.

[1] ALFIERI JA, MARTIN AD, TAKEDA J, KONDOH G, MYLES DG, PRIMAKOFF P. Infertility in female mice with an oocyte-specific knock-out of GPI-anchored proteins. J Cell Sci 2003; 116: 2149-2155.

[2] ALVES-FERREIRA M, WELLMER F, BANHARA A, KUMAR V, RIECHMANN JL, MEYEROWITZ EM. Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol 2007; 145: 745-762.

[3] ARAKI S, ITO M, SOYANO T, NISHIHAMA R, MACHIDA Y. Mitotic cyclins stimulate the activity of c-myb-like factors for transactivation of G2/M phase-specific genes in tobacco. J Biol Chem 2004; 279: 32979-32988.

[4] BECKER D, GEIGER D, DUNKEL M, ROLLER A, BERTL A, LATZ A, CARPANETO A, DIETRICH P, ROELFSEMA MRG, VOELKER C, SCHMIDT D, MUELLER-ROEBER B, CZEMPIŃSKI K, HEDRICH R. AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane volatage in pH- and Ca2+-dependent manner. Proc Natl Acad Sci USA 2004; 101: 15621-15626

[5] BECKER JD, BOAVIDA LC, CARNEIRO J, HAURY M, FEIJÓ JA. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristic of the pollen transcriptome. Plant Physiol 2003; 133: 713-725.

[6] BECKER JD, FEIJÓ JA. How many genes are needed to make pollen tube? Lessons from transcriptomics. Ann Bot 2007; 100: 1117-1123.

[7] BEDNARSKA E, LENARTOWSKA M. Rola wapniowego systemu przekazywania sygnałów w regulacji wzrostu łagiewek pyłkowych. Post Biol Kom 2000; 27: 467-479.

[8] BELOSTOTSKY DA. Unexpected complexity of poly(A)-binding protein gene families in flowering plants: three conserved lineages that are at least 200 million years old and possible autoand cross-regulation. Genetics 2003; 163: 311-319.

[9] BOAVIDA LC, BECKER JD, FEIJÓ JA. The making of gametes in higher plants. Int J Dev Biol 2005; 49: 595-614.

[10] BOCK KW, HONYS D, WARD JM, PADMANABAM S, NAWROCKI EP, HIRSCHI KD, TWELL D, SZE H. Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 2006; 140: 1151-1168.

[11] BOLLE C. The role of GRAS proteins in plant signal transduction and development. Planta 2004; 218: 683-692.

[12] BORGES F, GOMES G, GARDNER R, MORENO N, McCORMICK S, FEIJÓ JA, BECKER JD. Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 2008; 148: 1168-1181.

[13] BORNER GH, SHERRIER DJ, STEVENS TJ, ARKIN IT, DUPREE P. Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A genomic analysis. Plant Physiol 2002; 129: 486-499.

[14] BOSCH M, CHEUNG AY, HEPLER PK. Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 2005; 138: 1334-1346.

[15] CARLAND FM, NELSON T. Cotyledon vascular pattern2-mediated inositol (1,4,5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs. Plant Cell 2004; 16: 1263-1275.

[16] CHÉREL I. Regulation of K+ channel activities in plants: from physiological to molecular aspects. J Exp Bot 2004; 55: 337-351.

[17] CHEUNG AY, CHEN CY, GLAVEN RH, DE GRAAF BH, VIDALI L, HEPLER PK, WU HM. Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth. Plant Cell 2002; 14: 945-962.

[18] CHEVALIER F, MARTIN O, ROFIDAL V, DEVAUCHELLE AD, BARTEAU S, SOMMERER N, ROSSIGNOL M. Proteomic investigation of natural variation between Arabidopsis ecotypes. Proteomics 2004; 4: 1372-1381.

[19] DA COSTA-NUNES JA, GROSSNIKLAUS U. Unveiling the gene-expression profile of pollen. Genome Biol 2003; 5: 205.

[20] DAI S, CHEN T, CHONG K, XUE Y, LIU S, WANG T. Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Mol Cell Proteomics 2007; 6: 207-230.

[21] DEWITTE W, MURRAY JA. The plant cell cycle. Annu Rev Plant Biol 2003; 54: 235-264.

[22] DRESSELHAUS T, SRILUNCHANG KO, LELJAK-LEVANIC D, SCHREIBER DN, GARG P. The fertilization induced-DNA replication factor MCM6 of maize shuttles between cytoplasm and nucleus, and is essential for plant growth and development. Plant Physiol 2006; 140: 512-527.

[23] EBBS ML, BENDER J. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 2006; 18: 1166-1176.

[24] ENGEL ML, CHABOUD A, DUMAS C, McCORMICK S. Sperm cells of Zea mays have a complex complement of mRNAs. Plant J 2003; 34: 697-707.

[25] ENGEL ML, HOLMES-DAVIS R, McCORMICK S. Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 2005; 138: 2124-2133.

[26] FAN X, HOU J, CHEN X, CHAUDHRY F, STAIGER CJ, REN H. Identification and characterization of Ca2+-dependent actin filament-severing protein from lily pollen. Plant Physiol 2004; 136: 3979-3989.

[27] FEIJÓ JA, SAINHAS J, HOLDAWAY-CLARKE T, CORDEIRO MS, KUNKEL JG, HEPLER PK. Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioessays 2001; 23: 86-94.

[28] FRIEDMAN WE. Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development 1999; 126: 1065-1075.

[29] GIOVANE A, SERVILLO L, BALESTRIERI C, RAIOLA A, D’AVINO R, TAMBURRINI M, CIARDIELLO MA, CAMARDELLA L. Pectin methylesterase inhibitor. Biochim Biophys Acta 2004; 1696: 245-252.

[30] GORGONI B, GRAY NK. The roles of cytoplasmic poly(A)-binding proteins in regulating gene expression: a developmental perspective. Brief Funct Genomic Proteomic 2004; 3: 125-141.

[31] GOUBET F, MISRAHI A, PARK SK, ZHANG Z, TWELL D, DUPREE P. AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol 2003; 131: 547-557.

[32] HEIDSTRA R, WELCH D, SCHERES B. Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev 2004; 18: 1964-1969

[33] HEPLER PK, VIDALI L, CHEUNG AY. Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 2001; 17: 159-187.

[34] HOLMES-DAVIS R, TANAKA CK, VENSEL WH, HURKMAN WJ, McCORMICK S. Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 2005; 5: 4864-4884.

[35] HONYS D, COMBE JP, TWELL D, ČAPKOVÁ V. The translationally repressed pollen-specific ntp303 mRNA is stored in non-polysomal mRNPs during maturation. Sex Plant Reprod 2000; 13: 135-144.

[36] HONYS D, TWELL D. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 2003; 132: 640-652.

[37] HONYS D, TWELL D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 2004; 5: R85.

[38] JAKOBSEN MK, POULSEN LR, SCHULZ A, FLEURAT-LESSARD P, MØLLER A, HUSTED S, SCHIØTT M, AMTMANN A, PALMGREN MG. Pollen development and fertilization in Arabidopsis is dependent on the male gametogenesis impaired anthers gene encoding a type V Ptype ATP-ase. Genes Dev 2005; 19: 2757-2769.

[39] JOHNSON MA, VON BESSER K, ZHOU Q, SMITH E, AUX G, PATTON D, LEVIN JZ, PREUSS D. Arabidopsis hapless mutations define essential gametophytic functions. Genetics 2004; 168: 971-982.

[40] KAOTHIEN P, OK SH, SHUAI B, WENGIER D, COTTER R, KELLEY D, KIRIAKOPOLOS S, MUSCHIETTI J, McCORMICK S. Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. Plant J 2005; 42: 492-503.

[41] KERIM T, IMIN N, WEINMAN JJ, ROLFE BG. Proteome analysis of male gametophyte development in rice anthers. Proteomics 2003; 3: 738-751.

[42] KIM HU, COTTER R, JOHNSON S, SENDA M, DODDS P, KULIKAUSKAS R, TANG W, EZCURRA I, HERZMARK P, McCORMICK S. New pollen-specific receptor kinases identified in tomato, maize and Arabidopsis: the tomato kinases show overlapping but distinct localization patterns on pollen tubes. Plant Mol Biol 2002: 50: 1-16.

[43] LALANNE E, HONYS D, JOHNSON A, BORNER GH, LILLEY KS, DUPREE P, GROSSNIKLAUS N, TWELL D. SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabodopsis. Plant Cell 2004; 16: 229-240.

[44] LATHROP WF, CARMICHAEL PE, MYLES DG, PRIMAKOFF P. cDNA cloning reveals the molecular structure of sperm surface protein, PH-20, involved in sperm-egg adhesion and the wide distribution of its gene among mammals. J Cell Biol 1990; 111: 2939-2949.

[45] LEE JY, LEE DH. Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 2003; 132: 517-529.

[46] LENARTOWSKA M, MICHALSKA A. Actin filament organization and polarity in pollen tubes revealed by myosin II subfragment 1 decoration. Planta 2008; 228: 891-896.

[47] LIMMONGKON A, GIULIANI C, VALENTA R, MITTERMANN I, HEBERLE-BORS E, WILSON C. MAP kinase phosphorylation of plant profilin. Biochem Biophys Res Commun 2004; 324: 382-386.

[48] LUO K, DENG W, XU S, PEI Y. Functional analysis of the Arabidopsis thaliana poly(A)binding protein PAB5 gene promoter in Nicotiana tabacum. Plant Cell Rep 2008; 27: 1811-1819.

[49] MALHÓ R, LIU Q, MONTEIRO D, RATO C, CAMACHO L, DINIS A. Signalling pathways in pollen germination and tube growth. Protoplasma 2006; 228: 21-30.

[50] MARICONTI L, PELLEGRINI B, CANTONI R, STEVENS R, BERGOUNIOUX C, CELLA R, ALBANI D. The E2F family of transcription factors from Arabidopsis thaliana. Novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 2002; 277: 9911-9919.

[51] MASCARENHAS JP. The male gametophyte of flowering plants. Plant Cell 1989; 1: 657-664.

[52] MATZKE M, KANNO T, HUETTEL B, DAXINGER L, MATZKE AJ. Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 2007; 10: 512-519.

[53] MOULINE K, VÉRY AA, GAYMARD F, BOUCHEREZ J, PILOT G, DEVIC M, BOUCHEZ D, THIBAUD JB, SENTENAC H. Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Genes Dev 2002; 16: 339-350.

[54] MUSCHIETTI J, EYAL Y, MCCORMICK S. Pollen tube localization implies a role in pollenpistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell 1998; 10: 319-330.

[55] NOIR S, BRÄUTIGAM A, COLBY T, SCHMIDT J, PANSTRUGA R. A reference map of the Arabidopsis thaliana mature pollen proteome. Biochem Biophys Res Commun 2005; 337: 1257-1266.

[56] OKADA T, SINGH MB, BHALLA PL. Transcriptome profiling of Lilium longiflorum generative cells by cDNA microarray. Plant Cell Rep 2007; 26: 1045-1052.

[57] PARENICOVÁ L, DE FOLTER S, KIEFFER M, HORNER DS, FAVALLI C, BUSSCHER J, COOK HE, INGRAM RM, KATER MM, DAVIES B, ANGENENT GC, COLOMBO L. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 2003; 15: 1538-1551.

[58] PINA C, PINTP F, FEIJO JA, BECKER JD. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 2005; 138: 744-756.

[59] POPŁOŃSKA K, WOJTCZAK A, KWIATKOWSKA M, KAŹMIERCZAK A. Cytochemical and immunocytochemical studies of the localization of histones and protamine-type proteins in spermatids of Chara vulgaris and Chara tomentosa. Folia Histochem Cytobiol 2007; 45: 367-374.

[60] RATO C, MONTEIRO D, HEPLER PK, MALHÓ R. Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes. Plant J 2004; 38: 887-897.

[61] ROBERTSON WR, CLARCK K, YOUNG JC, SUSSMAN MR. An Arabidopsis thaliana plasma membrane proton pump is essential for pollen development. Genetics 2004; 168: 1677-1687.

[62] RODRIGUEZ-PEÑA JM, RODRIGUEZ C, ALVAREZ A, NOMBELA C, ARROYO J. Mechanisms for targeting of the Saccharomyces cerevisiae GPI-anchored cell wall protein Crh2p to polarized growth sites. J Cell Sci 2002; 115: 2549-2558.

[63] ROTMAN N, DURBARRY A, WARDLE A, YANG WC, CHABOUD A, FAURE JE, BERGER F, TWELL D. A novel class of MYB factors controls sperm cell formation in plants. Curr Biol 2005; 15: 244-248.

[64] ROUDIER F, FERNANDEZ AG, FUJITA M, HIMMELSPACH R, BORNER GHH, SCHINDELMAN G, SONG S, BASKIN TI, DUPREE P, WASTENEYS GO, Benfey PN. COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 2005; 17: 1749-1763.

[65] ŠAMAJ J, MÜLLER J, BECK M, BÖHM N, MENZEL D. Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci 2006; 11: 594-600.

[66] SAUTER M, VON WIEGEN P, LÖRZ H, KRANZ E. Cell cycle regulatory genes from maize are differentially controlled during fertilization and first embryonic cell division. Sex Plant Reprod 1998; 11: 41-48.

[67] SCHINDELMAN G, MORIKAMI A, JUNG J, BASKIN TI, CARPITA NC, DERBYSHIRE P, MCCANN MC, BENFEY PN. COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 2001; 15: 115-1127.

[68] SCHIØTT M, ROMANOWSKY SM, BAEKGAARD L, JAKOBSEN MK, PALMGREN MG, HARPER JF. A plant plasma membrane Ca2+ pump is required for normal tube growth and fertilization. Proc Natl Acad Sci USA 2004; 101: 9502-9507.

[69] SCHMID M, UHLENHAUT NH, GODARD F, DEMAR M, BRESSAN R, WEIGEL D, LOHMANN JU. Dissection of floral induction pathways using global expression analysis. Development 2003; 130: 6001-6012.

[70] SCHNEIDEREIT A, SCHOLZ-STARKE J, BÜTTNER M, Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis. Plant Physiol 2003; 133: 182-190.

[71] SCHNEIDEREIT A, SCHOLZ-STARKE J, SAUER N, BÜTTNER M. AtST11, a pollen tube specific monosaccharide transporter in Arabidopsis. Planta 2005; 221: 48-55.

[72] SHEORAN IS, ROSS AR, OLSON DJ, SAWHNEY VK. Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J Exp Bot 2007; 58: 3525-3535.

[73] SIVITZ AB, REINDERS A, WARD JM. Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation. Plant Physiol 2008; 147: 92-100.

[74] SUEN DF, WU SSH, CHANG CHANG H, DHUGGA KS, HUANG AHC. Cell wall reactive proteins in the coat and wall of maize pollen. J Biol Chem 2003; 278: 43673-43681.

[75] TAKAHASHI T, MU JH, GASCH A, CHUA NH. Identification by PCR of receptor-like protein kinases from Arabidopsis flower. Plant Mol Biol 1998; 37: 587-596

[76] TANG W, KELLEY D, EZCURRA I, COTTER R, MCCORMICK S. LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant J 2004; 39: 343-353.

[77] TWELL D, OH SA, HONYS D. Pollen development, a genetic and transcriptomic review. [w] Malhó R [red.] The pollen tube. A cellular and molecular perspective. Berlin, Springer-Verlag, Plant Cell Monographs 2006; 3: 15-45.

[78] VAILLANT I, SCHUBERT I, TOURMENTE S, MATHIEU O. MOM1 mediates DNAmethylation- independent silencing of repetitive sequence is Arabidopsis. EMBO Rep 2006; 7: 1273-1278.

[79] VANDEPOELE K, RAES J, DE VEYLDER L, ROUZÉ P, ROMBAUTS S, INZÉ D. Genomewide analysis of core cell cycle genes in Arabidopsis. Plant Cell 2002; 14: 903-916.

[80] VANTARD M, BLANCHOIN L. Actin polymerization processes in plant cells. Curr Opin Plant Biol 2002; 5: 502-506.

[81] VAZQUEZ F. Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci 2006; 11: 460-468.

[82] VERELST W, TWELL D, DE FOLTER S, IMMINK R, SAEDLER H, MÜNSTER T. MADScomplexes regulate transcriptome dynamics during pollen maturation. Genome Biol 2007; 8: R249.

[83] WANG ML, HSU CM, CHANG LC, WANG CS, SU TH, HUANG YJ, JIANG L, JAUH GY, Gene expression profiles of cold-stored and fresh pollen to investigate pollen germination and growth. Plant Cell Physiol 2004; 45: 1519-1528.

[84] WANG Y, ZHANG WZ, SONG LF, ZOU JJ, SU Z, WU WH. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 2008; 148: 1201-1211.

[85] WENGIER D, VALSECCHI I, CABANAS ML, TANG WH, McCORMICK S, MUSCHIETTI J. The receptor kinases LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract. Proc Natl Acad Sci USA 2003; 100: 6860-6865.

[86] ZIENKIEWICZ K, SMOLIŃSKI DJ, BEDNARSKA E. Distribution of poly(A)RNA and splicing machinery elements in Hyacinthus orietalis L. pollen grains and pollen tubes growing in vitro. Protoplasma 2006; 227: 95-103.

[87] ZIENKIEWICZ K, ZIENKIEWICZ A, SMOLIŃSKI DJ, RAFIŃSKA K, ŚWIDZIŃSKI M, BEDNARSKA E. Transcriptional state and distribution of poly(A) RNA and RNA polymerase II in differentiating Hyacinthus orientalis L. pollen grains. Sex Plant Rep 2008; 21: 233-245.

Medical Journal of Cell Biology

The Journal of Foundation for Cell Biology and Molecular Biology

Journal Information


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 230 230 44
PDF Downloads 68 68 18