Advertisement

When Simple Meets Complex: Pollen and the -Omics

  • Jan Fíla
  • Lenka Záveská Drábková
  • Antónia Gibalová
  • David Honys
Chapter

Abstract

Pollen, an extremely reduced bi-cellular or tri-cellular male reproductive structure of flowering plants, serves as a model for numerous studies covering a wide range of developmental and physiological processes. The pollen development and subsequent progamic phase represent two fragile and vital phases of plant ontogenesis, and pollen was among the first singular plant tissues thoroughly characterised at the transcriptomic level. Here we present an overview of high-throughput tools applied in pollen research on numerous plant species. Transcriptomics, being the first experimental approach used, has provided and continues providing valuable information about global and specific gene expression and its dynamics. However, the proteome does not fully reflect the transcriptome, namely, because post-transcriptional regulatory levels, especially translation, mRNA storage and protein modifications, are active during male gametophyte development and during progamic phase. Transcriptomics therefore should be complemented by other -omic tools to get more realistic insight, most importantly proteomics and other specialised approaches mapping the involvement of regulatory RNAs and protein post-translational modifications as well as experiments designed to identify the subsets of total -omes like translatome, secretome or allergome.

Keywords

Pollen development Gene expression Regulation -Omics Transcriptome Proteome 

Abbreviations

2-D DIGE

two dimensional fluorescence difference gel electrophoresis

2-DE

two dimensional gel electrophoresis

bHLH

basic helix-loop-helix transcription factor

bZIP TF

basic leucine zipper transcription factor

cAMP

cyclic adenosine monophosphate

CAGE

cap analysis of gene expression

cGMP

cyclic guanosine monophosphate

DEFL protein

defensin-like family protein

EAR motif

ethylene-responsive element binding factor-associated amphiphilic repression motif

EPP

EDTA/puromycin-resistant particle

GO

gene ontology

IMAC

immobilized metal affinity chromatography

LC–MS/MS

liquid chromatography–tandem mass spectrometry

MADS-box TF

family of transcription factors containing conserved MADS DNA-binding domain

MALDI–TOF/TOF

matrix-assisted laser desorption/ionization–time-of-flight tandem mass spectrometry

MIKC* type proteins

subfamily of MADS-box proteins with conserved domain structure, where the MADS (M) domain is followed by Intervening (I), Keratin-like (K) and C-terminal domains

MOAC

metal oxide/hydroxide affinity chromatography

MPSS

massively parallel signature sequencing

mRNP

messenger ribonucleoprotein particle

MYB family proteins

transcription factor protein family characterised by the presence of MYB (myeloblastosis) DNA-binding domain

PKA

cAMP-dependent protein kinase

PKC

protein kinase C

PKG

cGMP-dependent protein kinase

R2R3-MYB

MYB-protein subfamily characterised by the R2R3-type MYB domain

RNAseq

RNA deep sequencing technologies

RPM

reads per million

SAGE

serial analysis of gene expression

SIMAC

sequential elution from IMAC

TCTP

translationally controlled tumour protein

TF

transcription factor

Notes

Acknowledgements

The authors gratefully acknowledge the financial support from the Czech Science Foundation (grants no. 15–16050S and 17-23183S).

References

  1. Abiko M, Furuta K, Yamauchi Y, Fujita C, Taoka M, Isobe T, Okamoto T (2013) Identification of proteins enriched in rice egg or sperm cells by single-cell proteomics. PLoS One 8:e69578. doi: 10.1371/journal.pone.0069578 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Abou Chakra OR, Sutra JP, Demey Thomas E, Vinh J, Lacroix G, Poncet P, Senechal H (2012) Proteomic analysis of major and minor allergens from isolated pollen cytoplasmic granules. J Proteome Res 11:1208–1216PubMedCrossRefGoogle Scholar
  3. Adamczyk BJ, Fernandez DE (2009) MIKC* MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol 149:1713–1723PubMedPubMedCentralCrossRefGoogle Scholar
  4. Anderson SN, Johnson CS, Jones DS, Conrad LJ, Gou X, Russell SD, Sundaresan V (2013) Transcriptomes of isolated Oryza sativa gametes characterized by deep sequencing: evidence for distinct sex-dependent chromatin and epigenetic states before fertilization. Plant J 76:729–741PubMedCrossRefGoogle Scholar
  5. Aya K, Suzuki G, Suwabe K, Hobo T, Takahashi H, Shiono K, Yano K, Tsutsumi N, Nakazono M, Nagamura Y, Matsuoka M, Watanabe M (2011) Comprehensive network analysis of anther-expressed genes in rice by the combination of 33 laser microdissection and 143 spatiotemporal microarrays. PLoS One 6:e26162. doi: 10.1371/journal.pone.0026162 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Barranca M, Fontana S, Taverna S, Duro G, Zanella-Cleon I, Becchi M, De Leo G, Alessandro R (2010) Proteomic analysis of Parietaria judaica pollen and allergen profiling by an immunoproteomic approach. Biotechnol Lett 32:565–570PubMedCrossRefGoogle Scholar
  7. Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725PubMedPubMedCentralCrossRefGoogle Scholar
  8. Becker JD, Takeda S, Borges F, Dolan L, Feijó JA (2014) Transcriptional profiling of Arabidopsis root hairs and pollen defines an apical cell growth signature. BMC Plant Biol 14. doi: 10.1186/s12870-014-0197-3
  9. Berger F, Twell D (2011) Germline specification and function in plants. Annu Rev Plant Biol 62:461–484PubMedCrossRefGoogle Scholar
  10. Boavida LC, Borges F, Becker JD, Feijo JA (2011) Whole genome analysis of gene expression reveals coordinated activation of signaling and metabolic pathways during pollen-pistil interactions in Arabidopsis. Plant Physiol 155:2066–2080PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bokvaj P, Hafidh S, Honys D (2015) Transcriptome profiling of male gametophyte development Nicotiana tabacum. Genomics Data 3:106–111PubMedCrossRefGoogle Scholar
  12. Bonhomme L, Valot B, Tardieu F, Zivy M (2012) Phosphoproteome dynamics upon changes in plant water status reveal early events associated with rapid growth adjustment in maize leaves. Mol Cell Proteomics 11:957–972PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bordas-Le Floch V, Le Mignon M, Bouley J, Groeme R, Jain K, Baron-Bodo V, Nony E, Mascarell L, Moingeon P (2015) Identification of novel short ragweed pollen allergens using combined transcriptomic and immunoproteomic approaches. PLoS One 10:e0136258PubMedPubMedCentralCrossRefGoogle Scholar
  14. Borg M, Twell D (2010) Life after meiosis: patterning the angiosperm male gametophyte. Biochem Soc Trans 38:577–582PubMedCrossRefGoogle Scholar
  15. Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23:534–549PubMedPubMedCentralCrossRefGoogle Scholar
  16. Borg M, Rutley N, Kagale S, Hamamura Y, Gherghinoiu M, Kumar S, Sari U, Esparza-Franco MA, Sakamoto W, Rozwadowski K, Higashiyama T, Twell D (2014) An EAR-dependent regulatory module promotes male germ cell division and sperm fertility in Arabidopsis. Plant Cell 26:2098–2113PubMedPubMedCentralCrossRefGoogle Scholar
  17. Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148:1168–1181PubMedPubMedCentralCrossRefGoogle Scholar
  18. Borges F, Pereira PA, Slotkin RK, Martienssen RA, Becker JD (2011) MicroRNA activity in the Arabidopsis male germline. J Exp Bot 62:1611–1620PubMedCrossRefGoogle Scholar
  19. Brewbaker JL (1967) Distribution and phylogenetic significance of binucleate and trinucleate pollen grains in angiosperms. Am J Bot 54:1069–1083CrossRefGoogle Scholar
  20. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190PubMedCrossRefGoogle Scholar
  21. Bryce M, Drews O, Schenk MF, Menzel A, Estrella N, Weichenmeier I, Smulders MJ, Buters J, Ring J, Gorg A, Behrendt H, Traidl-Hoffmann C (2010) Impact of urbanization on the proteome of birch pollen and its chemotactic activity on human granulocytes. Int Arch Allergy Immunol 151:46–55PubMedCrossRefGoogle Scholar
  22. Calarco JP, Borges F, Donoghue MTA, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijó J, Becker JD, Martienssen RA (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205PubMedPubMedCentralCrossRefGoogle Scholar
  23. Campbell BC, Gilding EK, Timbrell V, Guru P, Loo D, Zennaro D, Mari A, Solley G, Hill MM, Godwin ID, Davies JM (2015) Total transcriptome, proteome, and allergome of Johnson grass pollen, which is important for allergic rhinitis in subtropical regions. J Allergy Clin Immunol 135:133–142PubMedCrossRefGoogle Scholar
  24. Carmona R, Zafra A, Seoane P, Castro AJ, Guerrero-Fernández D, Castillo-Castillo T, Medina-García A, Cánovas FM, Aldana-Montes JF, Navas-Delgado I, Alché JD, Claros MG (2015) ReprOlive: a database with linked data for the olive tree (Olea europaea L.) reproductive transcriptome. Front Plant Sci 6. doi: 10.3389/fpls.2015.00625
  25. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655PubMedPubMedCentralCrossRefGoogle Scholar
  26. Caruso M, Merelo P, Distefano G, La Malfa S, Lo Piero AR, Tadeo FR, Talon M, Gentile A (2012) Comparative transcriptome analysis of stylar canal cells identifies novel candidate genes implicated in the self-incompatibility response of Citrus clementina. BMC Plant Biol 12:20. doi: 10.1186/1471-2229-12-20 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chalivendra SC, Lopez-Casado G, Kumar A, Kassenbrock AR, Royer S, Tovar-Mendez A, Covey PA, Dempsey LA, Randle AM, Stack SM, Rose JK, McClure B, Bedinger PA (2013) Developmental onset of reproductive barriers and associated proteme changes in stigma/styles of Solanum pennellii. J Exp Bot 64:265–279PubMedCrossRefGoogle Scholar
  28. Chambers C, Shuai B (2009) Profiling microRNA expression in Arabidopsis pollen using microRNA array and real-time PCR. BMC Plant Biol 9. doi: 10.1186/1471-2229-9-87
  29. Chao Q, Gao ZF, Wang YF, Li Z, Huang XH, Wang YC, Mei YC, Zhao BG, Li L, Jiang YB, Wang BC (2016) The proteome and phosphoproteome of maize pollen uncovers fertility candidate proteins. Plant Mol Biol 91:287–304PubMedCrossRefGoogle Scholar
  30. Chaturvedi P, Ischebeck T, Egelhofer V, Lichtscheidl I, Weckwerth W (2013) Cell-specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. J Proteome Res 12:4892–4903PubMedCrossRefGoogle Scholar
  31. Chen T, Wu X, Chen Y, Li X, Huang M, Zheng M, Baluška F, Šamaj J, Lin J (2009) Combined proteomic and cytological analysis of Ca2+-calmodulin regulation in Picea meyeri pollen tube growth. Plant Physiol 149:1111–1126PubMedPubMedCentralCrossRefGoogle Scholar
  32. Chen C, Farmer AD, Langley RJ, Mudge J, Crow JA, May GD, Huntley J, Smith AG, Retzel EF (2010) Meiosis-specific gene discovery in plants: RNAseq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol 10:280. doi: 10.1186/1471-2229-10-280 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chen Y, Liu P, Hoehenwarter W, Lin J (2012) Proteomic and phosphoproteomic analysis of Picea wilsonii pollen development under nutrient limitation. J Proteome Res 11:4180–4190PubMedCrossRefGoogle Scholar
  34. Chen Y, Zou M, Cao Y (2014) Transcriptome analysis of the Arabidopsis semi-in vivo pollen tube guidance system uncovers a distinct gene expression profile. J Plant Biol 57(2):93–105CrossRefGoogle Scholar
  35. Chettoor AM, Givan SA, Cole RA, Coker CT, Unger-Wallace E, Vejlupkova Z, Vollbrecht E, Fowler JE, Evans MS (2014) Discovery of novel transcripts and gametophytic functions via RNAseq analysis of maize gametophytic transcriptomes. BMC Plant Biol 15:414Google Scholar
  36. Collins LJ (2011) Spliceosomal RNA infrastructure: the network of splicing components and their regulation by miRNAs. Adv Exp Med Biol 722:86–102PubMedCrossRefGoogle Scholar
  37. Costa M, Nobre MS, Becker JD, Masiero S, Amorim MI, Pereira LG, Coimbra S (2013) Expression-based and co-localization detection of arabinogalactan protein 6 and arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes. BMC Plant Biol 13. doi: 10.1186/1471-2229-13-7
  38. Dai S, Li L, Chen T, Chong K, Xue Y, Wang T (2006) Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6:2504–2529PubMedCrossRefGoogle Scholar
  39. Dai S, Chen T, Chong K, Xue Y, Liu S, Wang T (2007) Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Mol Cell Proteomics 6:207–230PubMedCrossRefGoogle Scholar
  40. Davidson RM, Hansey CN, Gowda M, Childs KL, Lin H, Vaillancourt B, Sekhon RS, de Leon N, Kaeppler SM, Jiang N, Buell CR (2011) Utility of RNA sequencing for analysis of maize reproductive transcriptomes. Plant Genome J 4:191CrossRefGoogle Scholar
  41. de Groot MJ, Daran-Lapujade P, van Breukelen B, Knijnenburg TA, de Hulster EA, Reinders MJ, Pronk JT, Heck AJ, Slijper M (2007) Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes. Microbiology 153:3864–3878PubMedCrossRefGoogle Scholar
  42. Der JP, Barker MS, Wickett NJ, de Pamphilis CW, Wolf PG (2011) De novo characterization of the gametophyte transcriptome in bracken fern, Pteridium aquilinum. BMC Genomics 12. doi: 10.1186/1471-2164-12-99
  43. Du H, Feng B-R, Yang S-S, Huang Y-B, Tang Y-X (2012) The R2R3-MYB transcription factor gene family in maize. PLoS One 7:e37463. doi: 10.1371/journal.pone.0037463 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Du H, Liang Z, Zhao S, Nan MG, Tran LS, Lu K, Huang YB, Li JN (2015) The evolutionary history of R2R3-MYB proteins across 50 eukaryotes: new insights into subfamily classification and expansion. Sci Rep 5:11037. doi: 10.1038/srep11037 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Dukowic-Schulze S, Sundararajan A, Mudge J, Ramaraj T, Farmer AD, Wang M, Sun Q, Pillardy J, Kianian SF, Retzel EF, Pawloski WP, Chen C (2014) The transcriptome landscape of early maize meiosis. BMC Plant Biol 14:18. doi: 10.1186/1471-2229-14-118 CrossRefGoogle Scholar
  46. Durbarry A, Vizir I, Twell D (2005) Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol 137(1):297–307PubMedPubMedCentralCrossRefGoogle Scholar
  47. El Kelish A, Zhao F, Heller W, Dumer J, Winkler JB, Behdendt H, Traidl-Hoffmann C, Horres R, Pfeiffer M, Ernst D (2014) Ragweed (Ambrosia artemisiifolia) pollen allergenicity: SuperSAGE transcriptomic analysis upon elevated CO2 and drought stress. BMC Plant Biol 14:176PubMedPubMedCentralCrossRefGoogle Scholar
  48. Elfving F (1879) Studien über die Pollenkörner der Angiospermen. Jenaische Zeitschrift für Naturwissenschaft 13:1–28Google Scholar
  49. Engel ML, Chaboud A, Dumas C, McCormick S (2003) Sperm cells of Zea mays have a complex complement of mRNAs. Plant J 34:697–707PubMedCrossRefGoogle Scholar
  50. Fasoli M, Dal Santo S, Zenoni S, Tornielli GB, Farina L, Zamboni A, Porceddu A, Venturini L, Bicego M, Murino V, Ferrarini A, Delledonne M, Pezzotti M (2012) The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24:3489–3505PubMedPubMedCentralCrossRefGoogle Scholar
  51. Feng J, Chen X, Yuan Z, He T, Zhang L, Wu Y, Liu W, Liang Q (2006) Proteome comparison following self- and across-pollination in self-incompatible apricot (Prunus armeniaca L.) Protein J 25:328–335PubMedCrossRefGoogle Scholar
  52. Fernando DD (2005) Characterization of pollen cube development in Pinus strobus (Eastern white pine) through proteomic analysis of differentially expressed proteins. Proteomics 5:4917–4926PubMedCrossRefGoogle Scholar
  53. Fíla J, Honys D (2012) Enrichment techniques employed in phosphoproteomics. Amino Acids 43:1025–1047PubMedCrossRefGoogle Scholar
  54. Fíla J, Čapková V, Feciková J, Honys D (2011) Impact of homogenization and protein extraction conditions on the obtained tobacco pollen proteomic patterns. Biol Plant 55:499–506CrossRefGoogle Scholar
  55. Fíla J, Matros A, Radau S, Zahedi RP, Čapková V, Mock H-P, Honys D (2012) Revealing phosphoproteins playing role in tobacco pollen activated in vitro. Proteomics 12:3229–3250PubMedCrossRefGoogle Scholar
  56. Fíla J, Radau S, Matros A, Hartmann A, Scholz U, Feciková J, Mock HP, Čapková V, Zahedi RP, Honys D (2016) Phosphoproteomics profiling of tobacco mature pollen and pollen activated in vitro. Mol Cell Proteomics 15:1338–1350PubMedPubMedCentralCrossRefGoogle Scholar
  57. Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908PubMedPubMedCentralCrossRefGoogle Scholar
  58. Futamura N, Ujino-Ihara T, Nishiguchi M, Kanamori H, Yoshimura K, Sakaguchi M, Shinohara K (2006) Analysis of expressed sequence tags from Cryptomeria japonica pollen reveals novel pollen-specific transcripts. Tree Physiol 26:1517–1528PubMedCrossRefGoogle Scholar
  59. Ge W, Song Y, Zhang C, Zhang Y, Burlingame AL, Guo Y (2011) Proteomic analyses of apoplastic proteins from germinating Arabidopsis thaliana pollen. Biochim Biophys Acta 1814:1964–1973PubMedPubMedCentralCrossRefGoogle Scholar
  60. Ghosh N, Sircar G, Saha B, Pandey N, Gupta Bhattacharya S (2015) Search for allergens from the pollen proteome of sunflower (Helianthus annuus L.): a major sensitizer for respiratory allergy patients. PLoS One 10:e0138992. doi: 10.1371/journal.pone.0138992 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Gibalová A, Reňák D, Matczuk K, Dupl’áková N, Cháb D, Twell D, Honys D (2009) AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen. Plant Mol Biol 70:581–601PubMedCrossRefGoogle Scholar
  62. Gou X, Yuan T, Wei X, Russell SD (2009) Gene expression in the dimorphic sperm cells of Plumbago zeylanica: transcript profiling, diversity, and relationship to cell type. Plant J 60:33–47PubMedCrossRefGoogle Scholar
  63. Grant-Downton R, Hafidh S, Twell D, Dickinson HG (2009a) Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol Plant 2:500–512PubMedCrossRefGoogle Scholar
  64. Grant-Downton R, Le Trionnaire G, Schmid R, Rodriguez-Enriquez J, Hafidh S, Mehdi S, Twell D, Dickinson H (2009b) MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genomics 10. doi: 10.1186/1471-2164-10-643
  65. Grobei MA, Qeli E, Brunner E, Rehrauer H, Zhang R, Roschitzki B, Basler K, Ahrens CH, Grossniklaus U (2009) Deterministic protein inference for shotgun proteomics data provides new insights into Arabidopsis pollen development and function. Genome Res 19:1786–1800PubMedPubMedCentralCrossRefGoogle Scholar
  66. Haerizadeh F, Wong CE, Bhalla PL, Gresshoff PM, Singh MB (2009) Genomic expression profiling of mature soybean (Glycine max) pollen. BMC Plant Biol 9. doi: 10.1186/1471-2229-9-25
  67. Hafidh S, Čapková V, Honys D (2011) Safe keeping the message: mRNP complexes tweaking after transcription. Adv Exp Med Biol 722:118–136PubMedCrossRefGoogle Scholar
  68. Hafidh S, Breznenová K, Honys D (2012a) De novo post-pollen mitosis II tobacco pollen tube transcriptome. Plant Signal Behav 7:918–921PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hafidh S, Breznenová K, Růžička P, Feciková J, Čapková V, Honys D (2012b) Comprehensive analysis of tobacco pollen transcriptome unveils common pathways in polar cell expansion and underlying heterochronic shift during spermatogenesis. BMC Plant Biol 12:24. doi: 10.1186/1471-2229-12-24 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Hafidh S, Potěšil D, Fíla J, Feciková J, Čapková V, Zdráhal Z, Honys D (2014) In search of ligands and receptors of the pollen tube: the missing link in pollen tube perception. Biochem Soc Trans 42:388–394PubMedCrossRefGoogle Scholar
  71. Hafidh S, Fíla J, Honys D (2016a) Male gametophyte development and function in angiosperms: a general concept. Plant Reprod 29:31–51PubMedCrossRefGoogle Scholar
  72. Hafidh S, Potěšil D, Fíla J, Čapková V, Zdráhal Z, Honys D (2016b) Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization. Genome Biol 17:81. doi: 10.1186/s13059-016-0928-x PubMedPubMedCentralCrossRefGoogle Scholar
  73. Han B, Chen S, Dai S, Yang N, Wang T (2010) Isobaric tags for relative and absolute quantification-based comparative proteomics reveals the features of plasma membrane-associated proteomes of pollen grains and pollen tubes from Lilium davidii. J Integrative Plant Biol 52:1043–1058CrossRefGoogle Scholar
  74. Higashiyama T (2015) The mechanism and key molecules involved in pollen tube guidance. Annu Rev Plant Biol 66:393–413PubMedCrossRefGoogle Scholar
  75. Higo A, Niwa M, Yamato KT, Yamada L, Sawada H, Sakamoto T, Kurata T, Shirakawa M, Endo M, Shigenobu S, Yamaguchi K, Ishizaki K, Nishihama R, Kohchi T, Araki T (2016) Transcriptional framework of male gametogenesis in the liverwort Marchantia polymorpha L. Plant Cell Physiol 57:325–338PubMedCrossRefGoogle Scholar
  76. Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguchi-Tanaka M, Matsuoka M (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol 49:1429–1450PubMedPubMedCentralCrossRefGoogle Scholar
  77. Hobo T, Suwabe K, Aya K, Suzuki G, Yano K, Ishimizu T, Fujita M, Kikuchi S, Hamada K, Miyano M, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Takahashi H, Shiono K, Nakazono M, Tsutsumi N, Nagamura Y, Kurata N, Watanabe M, Matsuoka M (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant Cell Physiol 49:1417–1428PubMedPubMedCentralCrossRefGoogle Scholar
  78. Hollender CA, Kang C, Darwish O, Geretz A, Matthews BF, Slovin J, Alkharouf N, Liu Z (2014) Floral transcriptomes in woodland strawberry uncover developing receptacle and anther gene networks. Plant Physiol 165:1062–1075PubMedPubMedCentralCrossRefGoogle Scholar
  79. Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5:4864–4884PubMedCrossRefGoogle Scholar
  80. Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652PubMedPubMedCentralCrossRefGoogle Scholar
  81. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5. doi: 10.1186/gb-2004-5-11-r85
  82. Honys D, Combe JP, Twell D, Čapková V (2000) The translationally repressed pollen-specific ntp303 mRNA is stored in non-polysomal mRNPs during pollen maturation. Sex Plant Reprod 13:135–144CrossRefGoogle Scholar
  83. Honys D, Reňák D, Feciková J, Jedelský PL, Nebesářova J, Dobrev P, Čapková V (2009) Cytoskeleton-associated large RNP complexes in tobacco male gametophyte (EPPs) are associated with ribosomes and are involved in protein synthesis, processing, and localization. J Proteome Res 8:2015–2031PubMedCrossRefGoogle Scholar
  84. Huang J-C, Chang L-C, Wang M-L, Guo C-L, Chung M-C, Jauh G-Y (2011) Identification and exploration of pollen tube small proteins encoded by pollination-induced transcripts. Plant Cell Physiol 52:1546–1559PubMedCrossRefGoogle Scholar
  85. Iaria D, Chiappetta A, Muzzalupo I (2016) De novo transcriptome sequencing of Olea europaea L. to identify genes involved in the development of the pollen tube. Sci World J 2016:4305252. doi: 10.1155/2016/4305252 CrossRefGoogle Scholar
  86. Ibarra CA, Feng X, Schoft VK, Hsieh TF, Uzawa R, Rodrigues JA, Zemach A, Chumak N, Machlicova A, Nishimura T, Rojas D, Fischer RL, Tamaru H, Zilberman D (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:1360–1364PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ikram S, Durandet M, Vesa S, Pereira S, Guerche P, Bonhomme S (2014) Functional redundancy and/or ongoing pseudogenization among F-box protein genes expressed in Arabidopsis male gametophyte. Plant Reprod 27:95–107PubMedCrossRefGoogle Scholar
  88. Ischebeck T, Valledor L, Lyon D, Gingl S, Nagler M, Meijon M, Egelhofer V, Weckwerth W (2014) Comprehensive cell-specific protein analysis in early and late pollen development from diploid microsporocytes to pollen tube growth. Mol Cell Proteomics 13:295–310PubMedCrossRefGoogle Scholar
  89. Kagale S, Rozwadowski K (2011) EAR motif-mediated transcriptional repression in plants. Epigenetics 6:141–146PubMedPubMedCentralCrossRefGoogle Scholar
  90. Kanter U, Heller W, Durner J, Winkler JB, Engel M, Behrendt H, Holzinger A, Braun P, Hauser M, Ferreira F, Mayer K, Pfeifer M, Ernst D (2013) Molecular and immunological characterization of ragweed (Ambrosia artemisiifolia L.) pollen after exposure of the plants to elevated ozone over a whole growing season. PLoS One 8. doi: 10.1371/journal.pone.0061518
  91. Kao SH, Su SN, Huang SW, Tsai JJ, Chow LP (2005) Sub-proteome analysis of novel IgE-binding proteins from Bermuda grass pollen. Proteomics 5:3805–3813PubMedCrossRefGoogle Scholar
  92. Kazan K (2003) Alternative splicing and proteome diversity in plants: the tip of the iceberg has just emerged. Trends Plant Sci 8:468–471PubMedCrossRefGoogle Scholar
  93. Keene JD (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8:533–543PubMedCrossRefGoogle Scholar
  94. Kessler SA, Grossniklaus U (2011) She’s the boss: signaling in pollen tube reception. Curr Opin Plant Biol 14:622–627PubMedCrossRefGoogle Scholar
  95. Lang V, Usadel B, Obermeyer G (2015) De novo sequencing and analysis of the lily pollen transcriptome: an open access data source for an orphan plant species. Plant Mol Biol 87:69–80PubMedCrossRefGoogle Scholar
  96. Lee JY, Lee DH (2003) Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 132:517–529PubMedPubMedCentralCrossRefGoogle Scholar
  97. Lee TY, Bretana NA, Lu CT (2011) PlantPhos: using maximal dependence decomposition to identify plant phosphorylation sites with substrate site specificity. BMC Bioinformatics 12:13. doi: 10.1186/1471-2105-12-261 CrossRefGoogle Scholar
  98. Leydon AR, Beale KM, Woroniecka K, Castner E, Chen J, Horgan C, Palanivelu R, Johnson MA (2013) Three MYB transcription factors control pollen tube differentiation required for sperm release. Curr Biol 23:1209–1214PubMedPubMedCentralCrossRefGoogle Scholar
  99. Li J, Chen J, Zhang Z, Pan Y (2008) Proteome analysis of tea pollen (Camellia sinensis) under different storage conditions. Agric Food Chem 56:7535–7544CrossRefGoogle Scholar
  100. Li M, Sha A, Zhou X, Yang P (2012) Comparative proteomic analyses reveal the changes of metabolic features in soybean (Glycine max) pistils upon pollination. Sex Plant Reprod 25:281–291PubMedCrossRefGoogle Scholar
  101. Li XM, Sang YL, Zhao XY, Zhang XS (2013) High-throughput sequencing of small RNAs from pollen and silk and characterization of miRNAs as candidate factors involved in pollen-silk interactions in maize. PLoS One 8:e72852. doi: 10.1371/journal.pone.0072852 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Li M, Wang K, Wang X, Yang P (2014) Morphological and proteomic analysis reveal the role of pistil under pollination in Liriodendron chinense (Hemsl.) Sarg. PLoS One 9:e99970. doi: 10.1371/journal.pone.0099970 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Li M, Wang K, Li S, Yang P (2016) Exploration of rice pistil responses during early post-pollination through a combined proteomic and transcriptomic analysis. J Proteomics 131:214–226PubMedCrossRefGoogle Scholar
  104. Liang Y, Tan Z-M, Zhu L, Niu Q-K, Zhou J-J, Li M, Chen L-Q, Zhang X-Q, Ye D (2013) MYB97, MYB101 and MYB120 function as male factors that control pollen tube-synergid interaction in Arabidopsis thaliana fertilization. PLoS Genet 9. doi: 10.1371/journal.pgen.1003933
  105. Lin S-Y, Chen P-W, Chuang M-H, Juntawong P, Bailey-Serres J, Jauh G-Y (2014) Profiling of translatomes of in vivo-grown pollen tubes reveals genes with roles in micropylar guidance during pollination in Arabidopsis. Plant Cell 26:602–618PubMedPubMedCentralCrossRefGoogle Scholar
  106. Liu Y, Cui S, Wu F, Yan S, Lin X, Du X, Chong K, Schilling S, Theissen G, Meng Z (2013) Functional conservation of MIKC*-type MADS box genes in Arabidopsis and rice pollen maturation. Plant Cell 25:1288–1303PubMedPubMedCentralCrossRefGoogle Scholar
  107. Liu Y, Joly V, Dorion S, Rivoal J, Matton DP (2015) The plant ovule secretome: a different view toward pollen-pistil interactions. J Proteome Res 14:4763–4775PubMedCrossRefGoogle Scholar
  108. Lopez-Casado G, Covey PA, Bedinger PA, Mueller LA, Thannhauser TW, Zhang S, Fei Z, Giovannoni JJ, Rose JK (2012) Enabling proteomic studies with RNA-Seq: the proteome of tomato pollen as a test case. Proteomics 12:761–774PubMedCrossRefGoogle Scholar
  109. Lora J, Herrero M, Hormaza JI (2009) The coexistence of bicellular and tricellular pollen in Annona cherimola (Annonaceae): implications for pollen evolution. Am J Bot 96:802–808PubMedCrossRefGoogle Scholar
  110. Loraine AE, McCormick S, Estrada A, Patel K, Qin P (2013) RNA-Seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiol 162(2):1092–1109PubMedPubMedCentralCrossRefGoogle Scholar
  111. Loraine AE, Blakley IC, Jagadeesan S, Harper J, Miller G, Firon N (2015) Analysis and visualization of RNAseq expression data using RStudio, Bioconductor, and Integrated Genome Browser. Methods Mol Biol 1284:481–501PubMedPubMedCentralCrossRefGoogle Scholar
  112. Lorkovic ZJ, Barta A (2004) Compartmentalization of the splicing machinery in plant cell nuclei. Trends Plant Sci 9:565–568PubMedCrossRefGoogle Scholar
  113. Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, Russell S, Singh M, Koltunow A (2011) A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet 7:e1002125. doi: 10.1371/journal.pgen.1002125 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Ma J, Skibbe DS, Fernandes J, Walbot V (2008) Male reproductive development: gene expression profiling of maize anther and pollen ontogeny. Genome Biol 9. doi: 10.1186/gb-2008-9-12-r181
  115. Mani BM, Huerta-Ocampo JA, Garcia-Sanchez JR, Barrera-Pacheco A, de la Rosa AP, Teran LM (2015) Identification of Ligustrum lucidum pollen allergens using a proteomics approach. Biochem Biophys Res Commun 468:788–792PubMedCrossRefGoogle Scholar
  116. Matsuda T, Matsushima M, Nabemoto M, Osaka M, Sakazono S, Masuko-Suzuki H, Takahashi H, Nakazono M, Iwano M, Takayama S, Shimizu KK, Okumura K, Suzuki G, Watanabe M, Suwabe K (2014) Transcriptional characteristics and differences in Arabidopsis stigmatic papilla cells pre- and post-pollination. Plant Cell Physiol 56:663–673PubMedCrossRefGoogle Scholar
  117. Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83. doi: 10.1186/1471-2229-8-83 PubMedPubMedCentralCrossRefGoogle Scholar
  118. Mayank P, Grossman J, Wuest S, Boisson-Dernier A, Roschitzki B, Nanni P, Nuehse T, Grossniklaus U (2012) Characterization of the phosphoproteome of mature Arabidopsis pollen. Plant J 72:89–101PubMedCrossRefGoogle Scholar
  119. McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275PubMedPubMedCentralCrossRefGoogle Scholar
  120. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834PubMedPubMedCentralCrossRefGoogle Scholar
  121. Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19:1327–1331PubMedCrossRefGoogle Scholar
  122. Nazemof N, Couroux P, Rampitsch C, Xing T, Robert LS (2014) Proteomic profiling reveals insights into Triticeae stigma development and function. J Exp Bot 65:6069–6080PubMedPubMedCentralCrossRefGoogle Scholar
  123. Noir S, Brautigam A, Colby T, Schmidt J, Panstruga R (2005) A reference map of the Arabidopsis thaliana mature pollen proteome. Biochem Biophys Res Commun 337:1257–1266PubMedCrossRefGoogle Scholar
  124. O’Donoghue MT, Chater C, Wallace S, Gray JE, Beerling DJ, Fleming AJ (2013) Genome-wide transcriptomic analysis of the sporophyte of the moss Physcomitrella patens. J Exp Bot 64:3567–3581PubMedPubMedCentralCrossRefGoogle Scholar
  125. Obermeyer G, Fragner L, Lang V, Weckwerth W (2013) Dynamic adaption of metabolic pathways during germination and growth of lily pollen tubes after inhibition of the electron transport chain. Plant Physiol 162:1822–1833PubMedPubMedCentralCrossRefGoogle Scholar
  126. Oh SA, Johnson A, Smertenko A, Rahman D, Park SK, Hussey PJ, Twell D (2005) A divergent cellular role for the FUSED kinase family in the plant-specific cytokinetic phragmoplast. Curr Biol 15:2107–2111PubMedCrossRefGoogle Scholar
  127. Ohr H, Bui AQ, Le BH, Fischer RL, Choi Y (2007) Identification of putative Arabidopsis DEMETER target genes by GeneChip analysis. Biochem Biophys Res Commun 364:856–860PubMedPubMedCentralCrossRefGoogle Scholar
  128. Okada T, Bhalla PL, Singh MB (2006) Expressed sequence tag analysis of Lilium longiflorum generative cells. Plant Cell Physiol 47:698–705PubMedCrossRefGoogle Scholar
  129. Okada T, Singh MB, Bhalla PL (2007) Transcriptome profiling of Lilium longiflorum generative cells by cDNA microarray. Plant Cell Rep 26:1045–1052PubMedCrossRefGoogle Scholar
  130. Oliver MJ, Dowd SE, Zaragoza J, Mauget SA, Payton PR (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5:89. doi: 10.1186/1471-2164-5-89 PubMedPubMedCentralCrossRefGoogle Scholar
  131. Ortiz-Ramirez C, Hernandez-Coronado M, Thamm A, Catarino B, Wang M, Dolan L, Feijo JA, Becker JD (2016) A transcriptome atlas of Physcomitrella patens provides insights into the evolution and development of land plants. Mol Plant 9:205–220PubMedCrossRefGoogle Scholar
  132. Osaka M, Matsuda T, Sakazono S, Masuko-Suzuki H, Maeda S, Sewaki M, Sone M, Takahashi H, Nakazono M, Iwano M, Takayama S, Shimizu KK, Yano K, Lim YP, Suzuki G, Suwabe K, Watanabe M (2013) Cell type-specific transcriptome of Brassicaceae stigmatic papilla cells from a combination of laser microdissection and RNA sequencing. Plant Cell Physiol 54:1894–1906PubMedPubMedCentralCrossRefGoogle Scholar
  133. Palanivelu R, Preuss D (2000) Pollen tube targeting and axon guidance: parallels in tip growth mechanisms. Trends Cell Biol 10:517–524PubMedCrossRefGoogle Scholar
  134. Palanivelu R, Preuss D (2006) Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 6:7. doi: 10.1186/1471-2229-6-7 PubMedPubMedCentralCrossRefGoogle Scholar
  135. Palanivelu R, Tsukamoto T (2012) Pathfinding in angiosperm reproduction: pollen tube guidance by pistils ensures successful double fertilization. Wiley Interdiscip Rev Dev Biol 1:96–113PubMedCrossRefGoogle Scholar
  136. Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D, Carrington JC, Weigel D (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13:115–125PubMedCrossRefGoogle Scholar
  137. Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799PubMedGoogle Scholar
  138. Paul P, Chaturvedi P, Selymesi M, Ghatak A, Mesihovic A, Scharf KD, Weckwerth W, Simm S, Schleiff E (2016) The membrane proteome of male gametophyte in Solanum lycopersicum. J Proteomics 131:48–60PubMedCrossRefGoogle Scholar
  139. Pearce LR, Komander D, Alessi DR (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11:9–22PubMedCrossRefGoogle Scholar
  140. Peng H, Chun J, Ai TB, Tong YA, Zhang R, Zhao MM, Chen F, Wang SH (2012) MicroRNA profiles and their control of male gametophyte development in rice. Plant Mol Biol 80:85–102PubMedCrossRefGoogle Scholar
  141. Pertl H, Schulze WX, Obermeyer G (2009) The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen. J Proteome Res 8:5142–5152PubMedCrossRefGoogle Scholar
  142. Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756PubMedPubMedCentralCrossRefGoogle Scholar
  143. Pirone-Davies C, Prior N, von Aderkas P, Smith D, Hardie D, Friedman WE, Mathews S (2016) Insights from the pollination drop proteome and the ovule transcriptome of Cephalotaxus at the time of pollination drop production. Ann Bot 117:973–984PubMedPubMedCentralCrossRefGoogle Scholar
  144. Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5. doi: 10.1371/journal.pgen.1000621
  145. Qiu YL, Taylor AB, McManus HA (2012) Evolution of the life cycle in land plants. J Syst Evol 50:171–194CrossRefGoogle Scholar
  146. Quinn CR, Iriyama R, Fernando DD (2014) Expression patterns of conserved microRNAs in the male gametophyte of loblolly pine (Pinus taeda). Plant Reprod 27:69–78PubMedCrossRefGoogle Scholar
  147. Raghavan V (2003) Some reflections on double fertilization, from its discovery to the present. New Phytol 159:565–583CrossRefGoogle Scholar
  148. Reddy AS, Day IS, Gohring J, Barta A (2012) Localization and dynamics of nuclear speckles in plants. Plant Physiol 158:67–77PubMedCrossRefGoogle Scholar
  149. Reiser L, Fischer RL (1993) The ovule and the embryo sac. Plant Cell 5:1291–1301PubMedPubMedCentralCrossRefGoogle Scholar
  150. Rejon JD, Delalande F, Schaeffer-Reiss C, Carapito C, Zienkiewicz K, de Dios AJ, Isabel Rodriguez-Garcia M, Van Dorsselaer A, Jesus Castro A (2013) Proteomics profiling reveals novel proteins and functions of the plant stigma exudate. J Exp Bot 64:5695–5705PubMedPubMedCentralCrossRefGoogle Scholar
  151. Reňák D, Dupľáková N, Honys D (2012) Wide-scale screening of T-DNA lines for transcription factor genes affecting male gametophyte development in Arabidopsis. Sex Plant Reprod 25:39–60PubMedCrossRefGoogle Scholar
  152. Rodriguez de Francisco L, Romero-Rodriguez MC, Navarro-Cerrillo RM, Minino V, Perdomo O, Jorrin-Novo JV (2016) Characterization of the orthodox Pinus occidentalis seed and pollen proteomes by using complementary gel-based and gel-free approaches. J Proteomics 143:382–389PubMedCrossRefGoogle Scholar
  153. Röhrig H, Colby T, Schmidt J, Harzen A, Facchinelli F, Bartels D (2008) Analysis of desiccation-induced candidate phosphoproteins from Craterostigma plantagineum isolated with a modified metal oxide affinity chromatography procedure. Proteomics 8:3548–3560PubMedCrossRefGoogle Scholar
  154. Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15:244–248PubMedCrossRefGoogle Scholar
  155. Russell SD, Bhalla PL, Singh MB (2008) Transcriptome-based examination of putative pollen allergens of rice (Oryza sativa ssp. japonica). Mol Plant 1:751–759PubMedCrossRefGoogle Scholar
  156. Russell SD, Gou X, Wong CE, Wang X, Yuan T, Wei X, Bhalla PL, Singh MB (2012) Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage. New Phytol 195:560–573PubMedCrossRefGoogle Scholar
  157. Rutley N, Twell D (2015) A decade of pollen transcriptomics. Plant Reprod 28:73–89PubMedPubMedCentralCrossRefGoogle Scholar
  158. Saha B, Sircar G, Pandey N, Gupta Bhattacharya S (2015) Mining novel allergens from coconut pollen employing manual de novo sequencing and homology-driven proteomics. J Proteome Res 14:4823–4833PubMedCrossRefGoogle Scholar
  159. Šamaj J, Muller J, Beck M, Böhm N, Menzel D (2006) Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci 11:594–600PubMedCrossRefGoogle Scholar
  160. Sanchez SE, Petrillo E, Kornblihtt AR, Yanovsky MJ (2011) Alternative splicing at the right time. RNA Biol 8:954–959PubMedPubMedCentralCrossRefGoogle Scholar
  161. Sanetomo R, Hosaka K (2013) Pollen transcriptome analysis of Solanum tuberosum (2n=4x=48), S-demissum (2n=6x=72), and their reciprocal F-1 hybrids. Plant Cell Rep 32:623–636PubMedCrossRefGoogle Scholar
  162. Sang YL, Xu M, Ma FF, Chen H, Xu XH, Gao XQ, Zhang XS (2012) Comparative proteomic analysis reveals similar and distinct features of proteins in dry and wet stigmas. Proteomics 12:1983–1998PubMedCrossRefGoogle Scholar
  163. Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470PubMedCrossRefGoogle Scholar
  164. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506PubMedCrossRefGoogle Scholar
  165. Schmidt H, Gelhaus C, Nebendahl M, Janssen O, Petersen A (2010) Characterization of Phleum pratense pollen extracts by 2-D DIGE and allergen immunoreactivity. Proteomics 10:4352–4362PubMedCrossRefGoogle Scholar
  166. Schreiber DN, Bantin J, Dresselhaus T (2004) The MADS box transcription factor ZmMADS2 is required for anther and pollen maturation in maize and accumulates in apoptotic bodies during anther dehiscence. Plant Physiol 134:1069–1079PubMedPubMedCentralCrossRefGoogle Scholar
  167. Schulten V, Greenbaum JA, Hauser M, McKinney DM, Sidney J, Kolla R, Lindestam Arlehamn CS, Oseroff C, Alam R, Broide DH, Ferreira F, Grey HM, Sette A, Peters B (2013) Previously undescribed grass pollen antigens are the major inducers of T helper 2 cytokine-producing T cells in allergic individuals. Proc Natl Acad Sci U S A 110:3459–3464PubMedPubMedCentralCrossRefGoogle Scholar
  168. Shen Y, Venu RC, Nobuta K, Wu X, Notibala V, Demirci C, Meyers BC, Wang GL, Ji G, Li QQ (2011) Transcriptome dynamics through alternative polyadenylation in developmental and environmental responses in plants revealed by deep sequencing. Genome Res 21:1478–1486PubMedPubMedCentralCrossRefGoogle Scholar
  169. Sheoran IS, Sproule KA, Olson DJH, Ross ARS, Sawhney VK (2006) Proteome profile and functional classification of proteins in Arabidopsis thaliana (Landsberg erecta) mature pollen. Sex Plant Reprod 19:185–196CrossRefGoogle Scholar
  170. Sheoran IS, Ross ARS, Olson DJH, Sawhney VK (2007) Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J Exp Bot 58:3525–3535PubMedCrossRefGoogle Scholar
  171. Sheoran IS, Pedersen EJ, Ross ARS, Sawhney VK (2009a) Dynamics of protein expression during pollen germination in canola (Brassica napus). Planta 230:779–793PubMedCrossRefGoogle Scholar
  172. Sheoran IS, Ross ARS, Olson DJH, Sawhney VK (2009b) Differential expression of proteins in the wild type and 7B-1 male-sterile mutant anthers of tomato (Solanum lycopersicum): a proteomic analysis. J Proteomics 71:624–636PubMedCrossRefGoogle Scholar
  173. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472PubMedPubMedCentralCrossRefGoogle Scholar
  174. Sousa R, Osório H, Duque L, Ribeiro H, Cruz A, Anbreu I (2014) Identification of Plantago lanceolata pollen allergens using an immunoproteomic approach. J Investig Allergol Clin Immunol 24:177–183PubMedGoogle Scholar
  175. Strasburger E (1884) Neue Untersuchungen uber den Befruchtungsvorgang bei den Phanerogamen als Grundlage fur eine Theorie der Zeugung. Gustav Fischer, JenaCrossRefGoogle Scholar
  176. Suwabe K, Suzuki G, Takahashi H, Shiono K, Endo M, Yano K, Fujita M, Masuko H, Saito H, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Kawagishi-Kobayashi M, Tsutsumi N, Kurata N, Nakazono M, Watanabe M (2008) Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray. Plant Cell Physiol 49:1407–1416PubMedPubMedCentralCrossRefGoogle Scholar
  177. Tang X, Zhang ZY, Zhang WJ, Zhao XM, Li X, Zhang D, Liu QQ, Tang WH (2010) Global gene profiling of laser-captured pollen mother cells indicates molecular pathways and gene subfamilies involved in rice meiosis. Plant Physiol 154:1855–1870PubMedPubMedCentralCrossRefGoogle Scholar
  178. Tran F, Penniket C, Patel RV, Provart NJ, Laroche A, Rowland O, Robert LS (2013) Developmental transcriptional profiling reveals key insights into Triticeae reproductive development. Plant J 74:971–988PubMedCrossRefGoogle Scholar
  179. Tsubomura M, Kurita M, Watanabe A (2016) Determination of male strobilus developmental stages by cytological and gene expression analyses in Japanese cedar (Cryptomeria japonica). Tree Physiol 36:653–666PubMedPubMedCentralCrossRefGoogle Scholar
  180. Twell D, Oh S-A, Honys D (2006) Pollen development, a genetic and transcriptomic view. In: Malhó R (ed) Plant cell monographs: the pollen tube, vol 3. Springer, Berlin, pp 15–45Google Scholar
  181. Valero Galvan J, Valledor L, Gonzalez Fernandez R, Navarro Cerrillo RM, Jorrin-Novo JV (2012) Proteomic analysis of Holm oak (Quercus ilex subsp. ballota [Desf.] Samp.) pollen. J Proteomics 75:2736–2744PubMedCrossRefGoogle Scholar
  182. Verelst W, Saedler H, Muenster T (2007a) MIKC* MADS-protein complexes bind motifs enriched in the proximal region of late pollen-specific Arabidopsis promoters. Plant Physiol 143:447–460PubMedPubMedCentralCrossRefGoogle Scholar
  183. Verelst W, Twell D, de Folter S, Immink R, Saedler H, Muenster T (2007b) MADS-complexes regulate transcriptome dynamics during pollen maturation. Genome Biol 8. doi: 10.1186/gb-2007-8-11-r249
  184. Vogler F, Konrad SSA, Sprunck S (2015) Knockin’ on pollen’s door: live cell imaging of early polarization events in germinating Arabidopsis pollen. Front Plant Sci 6. doi: 10.3389/fpls.2015.00246
  185. Wang Y, Zhang W-Z, Song L-F, Zou J-J, Su Z, Wu W-H (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211PubMedPubMedCentralCrossRefGoogle Scholar
  186. Wang Z, Gerstein M, Snyder M (2009) RNAseq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63PubMedPubMedCentralCrossRefGoogle Scholar
  187. Wang W, Sheng X, Shu Z, Li D, Pan J, Ye X, Chang P, Li X, Wang Y (2016) Combined cytological and transcriptomic analysis reveals a nitric oxide signaling pathway involved in cold-inhibited Camellia sinensis pollen tube growth. Front Plant Sci 7:456. doi: 10.3389/fpls.2016.00456 PubMedPubMedCentralGoogle Scholar
  188. Wei LQ, Xu WY, Deng ZY, Su Z, Xue Y, Wang T (2010) Genome-scale analysis and comparison of gene expression profiles in developing and germinated pollen in Oryza sativa. BMC Genomics 11:338. doi: 10.1186/1471-2164-11-338 PubMedPubMedCentralCrossRefGoogle Scholar
  189. Wei LQ, Yan LF, Wang T (2011) Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol 12. doi: 10.1186/gb-2011-12-6-r53
  190. Whittle CA, Malik MR, Li R, Krochko JE (2010) Comparative transcript analyses of the ovule, microspore, and mature pollen in Brassica napus. Plant Mol Biol 72:279–299PubMedCrossRefGoogle Scholar
  191. Williams JH, Taylor ML, O’Meara BC (2014a) Repeated evolution of tricellular (and bicellular) pollen. Am J Bot 101:559–571PubMedCrossRefGoogle Scholar
  192. Williams JS, Der JP, de Pamphilis CW, Kao TH (2014b) Transcriptome analysis reveals the same 17 S-locus F-box genes in two haplotypes of the self-incompatibility locus of Petunia inflata. Plant Cell 26:2873–2888PubMedPubMedCentralCrossRefGoogle Scholar
  193. Wu J, Shahid MQ, Guo H, Yin W, Chen Z, Wang L, Liu X, Lu Y (2014) Comparative cytological and transcriptomic analysis of pollen development in autotetraploid and diploid rice. Plant Reprod 27:181–196PubMedCrossRefGoogle Scholar
  194. Xiao L, Wang H, Wan P, Kuang T, He Y (2011) Genome-wide transcriptome analysis of gametophyte development in Physcomitrella patens. BMC Plant Biol 11:177PubMedPubMedCentralCrossRefGoogle Scholar
  195. Xin H-P, Peng X-B, Ning J, Yan T-T, Ma L-G, Sun M-X (2011) Expressed sequence-tag analysis of tobacco sperm cells reveals a unique transcriptional profile and selective persistence of paternal transcripts after fertilization. Sex Plant Reprod 24:37–46PubMedCrossRefGoogle Scholar
  196. Xing D, Li QQ (2011) Alternative polyadenylation and gene expression regulation in plants. Wiley Interdiscip Rev RNA 2:445–458PubMedCrossRefGoogle Scholar
  197. Xu XH, Chen H, Sang YL, Wang F, Ma JP, Gao X-Q, Zhang XS (2012) Identification of genes specifically or preferentially expressed in maize silk reveals similarity and diversity in transcript abundance of different dry stigmas. BMC Genomics:13. doi: 10.1186/1471-2164-13-294
  198. Yang H, Yang N, Wang T (2016) Proteomic analysis reveals the differential histone programs between male germline cells and vegetative cells in Lilium davidii. Plant J 85:660–674PubMedCrossRefGoogle Scholar
  199. Zhang X-M, Zhao L, Larson-Rabin Z, Li D-Z, Guo Z-H (2012) De novo sequencing and characterization of the floral transcriptome of Dendrocalamus latiflorus (Poaceae: Bambusoideae). PLoS One 7. doi: 10.1371/journal.pone.0042082
  200. Zhang H, Egger RL, Kelliher T, Morrow D, Fernandes J, Nan GL, Walbot V (2014) Transcriptomes and proteomes define gene expression progression in pre-meiotic maize anthers. G3 (Bethesda) 4:993–1010CrossRefGoogle Scholar
  201. Zhao X, Yang N, Wang T (2013) Comparative proteomic analysis of generative and sperm cells reveals molecular characteristics associated with sperm development and function specialization. J Proteome Res 12:5058–5071PubMedCrossRefGoogle Scholar
  202. Zhao P, Zhang L, Zhao L (2015) Dissection of the style’s response to pollination using transcriptome profiling in self-compatible (Solanum pimpinellifolium) and self-incompatible (Solanum chilense) tomato species. BMC Plant Biol 15:119. doi: 10.1186/s12870-015-0492-7 PubMedPubMedCentralCrossRefGoogle Scholar
  203. Zhao F, Elkelish A, Durner J, Lindermayr C, Winkler JB, Ruёff F, Behrendt H, Traidl-Hoffmann C, Holzinger A, Kofler W, Braun P, von Toerne C, Hauck SM, Ernst D, Frank U (2016) Common ragweed (Ambrosia artemisiifolia L.): allergenicity and molecular characterization of pollen after plant exposure to elevated NO2. Plant Cell Environ 39:147–164PubMedCrossRefGoogle Scholar
  204. Zhou H, Yin H, Chen J, Liu X, Gao Y, Wu J, Zhang S (2016) Gene-expression profile of developing pollen tube of Pyrus bretschneideri. Gene Expr Patterns 20:11–21PubMedCrossRefGoogle Scholar
  205. Zou J, Song L, Zhang W, Wang Y, Ruan S, Wu W-H (2009) Comparative proteomic analysis of Arabidopsis mature pollen and germinated pollen. J Integr Plant Biol 51:438–455PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Jan Fíla
    • 1
  • Lenka Záveská Drábková
    • 1
  • Antónia Gibalová
    • 1
  • David Honys
    • 1
  1. 1.Laboratory of Pollen Biology, Institute of Experimental BotanyAcademy of Sciences of the Czech RepublicPraha 6Czech Republic

Personalised recommendations