Advertisement

The Pollen Membrane Proteome

  • Heidi Pertl-ObermeyerEmail author
Chapter

Abstract

The male gametophyte (or pollen) is a highly specialized organ essential for sexual reproduction of higher plants. Their reduced complexity constitutes them as an ideal experimental system for analyses of biological processes maintaining tip growth. Rapid advances in proteomic technologies and a vast choice of metabolic labelling and label-free quantitation protocols as well as the availability of full genome sequences allow comprehensive analyses of various pollen proteomes. Pollen membrane proteome consists of integral and membrane-associated proteins involved in regulation of many cellular functions. In this chapter, novel insights into identification of membrane proteins by proteome analysis and how their dynamic subcellular localization contributes to the initiation of pollen grain germination and maintenance of tube growth are discussed.

Keywords

Mass spectrometry Membrane proteins Protein-protein interactions Proteomics 

Abbreviations

2D-PAGE

Two-dimensional polyacrylamide gel electrophoresis

2D DIGE

Two-dimensional difference in gel electrophoresis

ACA

Autoinhibited-type Ca2+ ATPase

BiFC

Bimolecular fluorescence complementation

CaM

Calmodulin

COP

Coat protein complex

ECA

Endoplasmic reticulum-type Ca2+ ATPase

ER

Endoplasmic reticulum

ESI Q-TOF MS/MS

Electrospray ionization quadrupole time-of-flight tandem mass spectrometry

GFP

Green fluorescent protein

IEF

Isoelectric focusing

LC-MSn

Liquid chromatography coupled with multistage accurate mass spectrometry

MALDI-TOF MS

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometer

mbSUS

Mating-based split-ubiquitin system

pI

Isoelectric point

PIP

Plasma membrane intrinsic proteins

PM

Plasma membrane

SNARE

Soluble N-ethylmaleimide-sensitive factor attachment protein receptor

TGN

Trans-Golgi network

VDAC

Voltage-dependent anion channel

References

  1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657PubMedCrossRefGoogle Scholar
  2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  3. Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101PubMedCrossRefGoogle Scholar
  4. Becker JD, Boavida LC, Carneiro J, Haury M, Feijo J (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G, Maurel C, Santoni V (2016) Novel aquaporin regulatory mechanisms revealed by interactomics. Mol Cell Proteomics. doi: 10.1074/mcp.M116.060087 PubMedGoogle Scholar
  6. Benkert R, Obermeyer G, Bentrup F-W (1997) The turgor pressure of growing lily pollen tubes. Protoplasma 198:1–8CrossRefGoogle Scholar
  7. Bibikova TN, Assmann S, Gilroy S (2004) Ca2+ and pH as integrated signals in transport control. In: Blatt MR (ed) Membrane transport in plants. Vol 15. Annual plant reviews. Blackwell, Oxford, pp 252-278Google Scholar
  8. Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25:1523–1530PubMedCrossRefGoogle Scholar
  9. Bücherl CA, van Esse GW, Kruis A, Luchtenberg J, Westphal AH, Aker J, van Hoek A, Albrecht C, Borst JW, de Vries SC (2013) Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol 162:1911–1925PubMedPubMedCentralCrossRefGoogle Scholar
  10. Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N, Michard E, Carneiro J, Rodriguez-Leon J, Wu H-M, Cheung AY, Feijo J (2008) Exclusion of a proton ATPase from the apical membrane is associated with cell polarity and tip growth in Nicotiana tabacum pollen tubes. Plant Cell 20:614–634PubMedPubMedCentralCrossRefGoogle Scholar
  11. 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 Physiol 160:1940–1955PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cheung AY, Wu H (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572PubMedCrossRefGoogle Scholar
  13. Cheung AY, Chen CY-h, Glaven RH, De Graaf BHJ, Vidali L, Hepler PK, Wu HM (2002) Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth. Plant Cell 14:945–962PubMedPubMedCentralCrossRefGoogle Scholar
  14. Dai S, Li L, Chen T, Chong K, Xue Y, Wang T (2006) Proteomic analysis of Oriza sativa pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6:2504–2529PubMedCrossRefGoogle Scholar
  15. Dai S, Chen T, Chong K, Xue Y, Liu S, Wang T (2007a) 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
  16. Dai S, Wang T, Yan X, Chen S (2007b) Proteomics of pollen development and germination. J Proteome Res 6:4556–4563PubMedCrossRefGoogle Scholar
  17. Dettmer J, Schubert D, Calvo-Weimar O, Stierhof Y-D, Schmidt R, Schumacher K (2005) Essential role of the V-ATPase in male gametophyte development. Plant J 41:117–124PubMedCrossRefGoogle Scholar
  18. Dunkley TPJ, Hester S, Shadford IP, Runions J, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, Watson RB, Dupree P, Lilley KS (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci U S A 103:6518–6523PubMedPubMedCentralCrossRefGoogle Scholar
  19. Feijó JA, Malhó R, Obermeyer G (1995) Ion dynamics and its possible role during in vitro pollen germination and tube growth. Protoplasma 187:155–167CrossRefGoogle Scholar
  20. Feijó JA, Sainhas J, Holdaway-Clarke T, Cordeiro S, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioessays 23:86–94PubMedCrossRefGoogle Scholar
  21. Ferreira F, Hirtenlehner K, Jilek A, Godnik-Cvar J, Breiteneder H, Grimm R, Hoffmann-Sommergruber K, Scheiner O, Kraft D, Breitenbach M, Rheinberger H-J, Ebner C (1996) Dissection of immunoglobulin E and T lymphocyte reactivity of isoforms of the major birch pollen allergen Bet v 1: potential use of hypoallergenic isoforms for immunotherapy. J Exp Med 183:599–609PubMedCrossRefGoogle Scholar
  22. Fricker MD, White NS, Obermeyer G (1997) pH gradients are not associated with tip growth in pollen tubes of Lilium longiflorum. J Cell Sci 110:1729–1740PubMedGoogle Scholar
  23. Frietsch S, Wang Y-F, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci U S A 104:14531–14536PubMedPubMedCentralCrossRefGoogle Scholar
  24. Fuglsang AT, Visconti S, Drumm K, Jahn T, Stensballe A, Mattei M, Jensen ON, Aducci P, Palmgren MG (1999) Binding of 14-3-3 protein to the plasma membrane H+ ATPase AHA2 involves the three C-terminal residues Tyr (946)-Thr-Val and requires phosphorylation of the THR (947). J Biol Chem 274:36774–36780PubMedCrossRefGoogle Scholar
  25. Gao QF, Gu LL, Wang HQ, Fei CF, Fang X, Hussain J, Sun SJ, Dong JY, Liu H, Wang YF (2016) Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. Proc Natl Acad Sci U S A 113:3096–3101PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gattolin S, Sorieul M, Hunter PR, Khonsari RH, Frigerio L (2009) In vivo imaging of the tonoplast intrinsic protein family in Arabidopsis roots. BMC Plant Biol 9:133. doi: 10.1186/1471-2229-9-133 PubMedPubMedCentralCrossRefGoogle Scholar
  27. 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
  28. Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun W-l, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  29. de Graaf BHJ, Cheung AY, Andreyeva T, Levasseur K, Kiesliszewski M, Wu H (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17:2564–2579PubMedPubMedCentralCrossRefGoogle Scholar
  30. Griessner M, Obermeyer G (2003) Characterization of whole-cell K+ currents across the plasma membrane of pollen grain and pollen tube protoplasts of Lilium longiflorum. J Membr Biol 193:99–108PubMedCrossRefGoogle Scholar
  31. Grobei MA, Qeli E, Brunner E, Rehrauer H, Zhang R, Roschitzki B, Basler K, Ahrens CH, Grossniklaus U (2009) Deterministic protein inference for shotgun proteomic data provides new insights into Arabidopsis pollen development and function. Genome Res 19:1786–1800PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gutermuth T, Lassig R, Portes MT, Maierhofer T, Romeis T, Borst JW, Hedrich R, Feijo JA, Konrad K (2013) Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 25:4525–4543PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE, Zarsky V (2008) An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20:1330–1345PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 form Lilium davidii. J Integr Plant Biol 52:1043–1058PubMedCrossRefGoogle Scholar
  35. Heslop-Harrison J (1987) Pollen germination and pollen-tube growth. Int Rev Cytol 107:1–78CrossRefGoogle Scholar
  36. Hoidn C, Puchner E, Pertl H, Holztrattner E, Obermeyer G (2005) Nondiffusional release of allergens from pollen grains of Artemisia vulgaris and Lilium longiflorum depends mainly on the type of the allergen. Int Arch Allergy Immunol 137:27–36PubMedCrossRefGoogle Scholar
  37. Holdaway-Clarke T, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563CrossRefGoogle Scholar
  38. Holmes-Davies R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5:4864–4884CrossRefGoogle Scholar
  39. Homblé F, Krammer E-M, Prévost M (2012) Plant VDAC: facts and speculations. Biochim Biophys Acta 1818:1486–1501PubMedCrossRefGoogle Scholar
  40. Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652PubMedPubMedCentralCrossRefGoogle Scholar
  41. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:85–97CrossRefGoogle Scholar
  42. Ischebeck T, Stenzel I, Heilmann I (2008) Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. Plant Cell 20:3312–3330PubMedPubMedCentralCrossRefGoogle Scholar
  43. Ischebeck T, Valledor L, Lyon D, Gingl S, Nagler M, Meijón 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
  44. Jiang L, Yang SF, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kim S-J, Brandizzi F (2014) The plant secretory pathway: an essential factory for building the plant cell wall. Plant Cell Physiol 55:687–689PubMedCrossRefGoogle Scholar
  46. van Kleeff PJM, Jaspert N, Li KW, Rauch S, Oecking C, de Boer AH (2014) Higher order Arabidopsis 14-3-3 mutants show 14-3-3 involvement in primary root growth both under control and abiotic stress conditions. J Exp Bot 65:5877–5888PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N-H (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kota U, Goshe MB (2011) Advances in qualitative and quantitative plant membrane proteomics. Phytochemistry 72:1040–1060PubMedCrossRefGoogle Scholar
  49. Ladwig F, Dahlke RI, Stührwohldt N, Hartmann J, Harter K, Sauter M (2015) Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+ ATPase, and BAK1. Plant Cell 27:1718–1729PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lang V, Pertl-Obermeyer H, Safiarian MJ, Obermeyer G (2014) Pump up the volume—a central role for the plasma membrane H+ pump in pollen grain germination and tube growth. Protoplasma 251:477–488PubMedCrossRefGoogle Scholar
  51. Larson C (1983) Partition in aqueous polymer two-phase systems: a rapid method for separation of membrane particles according to their surface properties. In: Hall JL, Moore AL (eds) Isolation of membranes and organelles from plant cells. Academic Press, London, pp 277–309Google Scholar
  52. Liu F, Rijkers DTS, Post H, Heck AJR (2015) Proteome-wide profiling of protein assemblies by cross-linking mass spectrometry. Nat Methods 12:1179–1184PubMedCrossRefGoogle Scholar
  53. Löcke S, Fricke I, Mucha E, Humpert M-L, Berken A (2010) Interactions in the pollen-specific receptor-like kinases-containing signaling network. Eur J Cell Biol 89:917–923PubMedCrossRefGoogle Scholar
  54. Loraine AE, McCormick S, Estrada A, Patel K, Qin P (2013) RNAseq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiol 162:1092–1109PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lucca N, León G (2012) Arabidopsis ACA7, encoding a putative auto-regulated Ca2+ ATPase, is required for normal pollen development. Plant Cell Rep 31:651–659PubMedCrossRefGoogle Scholar
  56. Ma L, Xu X, Cui S, Sun D (1999) The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. Plant Cell 11:1351–1363PubMedPubMedCentralCrossRefGoogle Scholar
  57. Mascarenhas JP (1975) The biochemistry of angiosperm pollen development. Bot Rev 41:259–314CrossRefGoogle Scholar
  58. Maudoux O, Batoko H, Oecking C, Gevaert K, Vandekerckhove J, Boutry M, Morsomme P (2000) A plant plasma membrane H+ ATPase expressed in yeast is activated by phosphorylation at its penultimate residue and binding of 14-3-3 regulatory proteins in the absence of fusicoccin. J Biol Chem 275:17762–17770PubMedCrossRefGoogle Scholar
  59. Mayfield JA, Preuss D (2000) Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat Cell Biol 2:128–130PubMedCrossRefGoogle Scholar
  60. Memon AR (2004) The role of ADP-ribosylation factor and SAR1 in vesicular trafficking in plants. Biochim Biophys Acta 1664:9–30PubMedCrossRefGoogle Scholar
  61. Michard E, Dias P, Feijo JA (2008) Tobacco pollen tubes as cellular models for ion dynamics: improved spatial and temporal resolution of extracellular flux and free cytosolic concentration of calcium and protons using pHluorin and YC3.1 CaMeleon. Sex Plant Reprod 21:169–181CrossRefGoogle Scholar
  62. Michard E, Alves F, Feijo J (2009) The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as an experimental paradigm. Int J Dev Biol 53:1609–1622PubMedCrossRefGoogle Scholar
  63. Michard E, Simon AA, Tavares B, Wudick MM, Feijó JA (2017) Signalling with ions: the keystone for apical cell growth and morphogenesis in pollen tubes. Plant Physiol 173:91–111PubMedCrossRefGoogle Scholar
  64. Mitsuda N, Enami K, Nakata M, Takeyasu K, Sato MH (2001) Novel type Arabidopsis thaliana H+ PPase is localized to the Golgi apparatus. FEBS Lett 488:29–33PubMedCrossRefGoogle Scholar
  65. Monteiro GA, Castanho-Coelho P, Rodrigues C, Camacho L, Quader H, Malhó R (2005) Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids. Protoplasma 226:31–38PubMedCrossRefGoogle Scholar
  66. Mouline K, Very A-A, Gaymard F, Boucherez J, Pilot G, Devic M, Bouchez D, Thibaud JB, Sentenac H (2002) Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Genes Dev 16:339–350PubMedPubMedCentralCrossRefGoogle Scholar
  67. Myers C, Romanowsky SM, Barron YD, Garg S, Azuse CL, Curran A, Davis RM, Hatton J, Harmon AC, Harper JF (2009) Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. Plant J 59:528–539PubMedCrossRefGoogle Scholar
  68. Nakamura R, Teshima R (2013) Proteomics-based allergen analysis in plants. J Proteomics 93:40–49PubMedCrossRefGoogle Scholar
  69. Nikolovski N, Rubtsov D, Segura MP, Miles GP, Stevens TJ, Dunkley TPJ, Munro S, Lilley KS, Dupree P (2012) Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol 160:1037–1051PubMedPubMedCentralCrossRefGoogle Scholar
  70. Noir S, Bräutigam 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
  71. Obermeyer G, Lützelschwab M, Heumann H-G, Weisenseel MH (1992) Immunolocalisation of H+ ATPases in the plasma membrane of pollen grains and pollen tubes of Lilium longiflorum. Protoplasma 171:55–63CrossRefGoogle Scholar
  72. Obermeyer G, Kriechbaumer R, Strasser D, Maschessnig A, Bentrup F-W (1996) Boric acid stimulates the plasma membrane H+ ATPase of ungerminated lily pollen grains. Physiol Plant 98:281–290CrossRefGoogle Scholar
  73. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64:445–458PubMedCrossRefGoogle Scholar
  74. Padmanaban S, Lin X, Perera I, Kawamura Y, Sze H (2004) Differential expression of vacuolar H+-ATPase subunit c genes in tissues active in membrane trafficking and their roles in plant growth as revealed by RNAi. Plant Physiol 134:1514–1526PubMedPubMedCentralCrossRefGoogle Scholar
  75. Palmgren MG (2001) Plant plasma membrane H+ ATPases: powerhouse for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845PubMedCrossRefGoogle Scholar
  76. Paul P, Chaturvedi P, Selymesi M, Ghatak A, Mesihovic A, Scharf K-D, Weckwerth W, Simm S, Schleiff E (2016) The membrane proteome of male gametophyte in Solanum lycopersicum. J Proteomics 131:48–60PubMedCrossRefGoogle Scholar
  77. Pertl H, Himly M, Gehwolf R, Kriechbaumer R, Strasser D, Michalke W, Richter K, Ferreira F, Obermeyer G (2001) Molecular and physiological characterisation of a 14-3-3 protein from lily pollen grains regulating the activity of the plasma membrane H+ ATPase during pollen grain germination and tube growth. Planta 213:132–141PubMedCrossRefGoogle Scholar
  78. Pertl H, Gehwolf R, Obermeyer G (2005) The distribution of membrane-bound 14-3-3 proteins in organelle-enriched fractions of germinating lily pollen. Plant Biol 7:140–147PubMedCrossRefGoogle Scholar
  79. 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
  80. Pertl H, Pöckl M, Blaschke C, Obermeyer G (2010) Osmoregulation in Lilium pollen grains occurs via modulation of the plasma membrane H+ATPase activity by 14-3-3 proteins. Plant Physiol 154:1921–1928PubMedPubMedCentralCrossRefGoogle Scholar
  81. Pertl H, Rittmann S, Schulze WX, Obermeyer G (2011) Identification of lily pollen 14-3-3 isoforms and their subcellular and time-dependent expression profile. Biol Chem 392:249–262PubMedCrossRefGoogle Scholar
  82. Pertl-Obermeyer H, Obermeyer G (2013) Pollen cultivation and preparation for proteome studies. Methods Mol Biol 1072:435–449CrossRefGoogle Scholar
  83. Pertl-Obermeyer H, Schulze WX, Obermeyer G (2014) In vivo cross-linking combined with mass spectrometry analysis reveals receptor-like kinases and Ca2+ signalling proteins as putative interaction partners of pollen plasma membrane H+ ATPases. J Proteomics 108:17–29PubMedCrossRefGoogle Scholar
  84. Petersen A, Dresselhaus T, Grobe K, Becker W-M (2006) Proteome analysis of maize pollen for allergy-relevant components. Proteomics 6:6317–6325PubMedCrossRefGoogle Scholar
  85. Pina C, Pinto F, Feijó 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
  86. Potocky M, Elias M, Profotova B, Novotna Z, Valentova O, Zarsky V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217:122–130PubMedGoogle Scholar
  87. Potocký M, Pleskot R, Pejchar P, Vitale N, Kost B, Žárský V (2014) Live-cell imaging of phosphatidic acid dynamics in pollen tubes visualized by Spo20p-derived biosensor. New Phytol 203:483–494PubMedCrossRefGoogle Scholar
  88. Rabilloud T (2014) How to use 2D gel electrophoresis in plant proteomics. Methods Mol Biol 1072:43–50PubMedCrossRefGoogle Scholar
  89. Rodriguez-Rosales MP, Roldán M, Belver A, Donaire JP (1989) Correlation between in vitro germination capacity and proton extrusion in olive pollen. Plant Physiol Biochem 27:23–728Google Scholar
  90. Safiarian MJ, Pertl-Obermeyer H, Lughofer P, Hude R, Bertl A, Obermeyer G (2015) Lost in traffic? The K+ channel of lily pollen, LilKT1, is detected at the endomembranes inside yeast cells, tobacco leaves, and lily pollen. Front Plant Sci 6:47. doi: 10.3389/fpls.2015.00047 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Sakurai N (1998) Dynamic function and regulation of apoplast in the plant body. J Plant Res 111:133–148CrossRefGoogle Scholar
  92. Schenk MF, Gilissen LJWJ, Smulders RJM, America THP (2010) Mass spectrometry and pollen allergies. Expert Rev Proteomics 7:627–630PubMedCrossRefGoogle Scholar
  93. Schiott M, Romanowski S, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci U S A 101:9502–9507PubMedPubMedCentralCrossRefGoogle Scholar
  94. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh C-T, Emrich SJ, Jia Y, Kalyanaraman A, Hsia A-P, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia J-M, Deragon J-M, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115PubMedCrossRefGoogle Scholar
  95. Schulze WX, Usadel B (2010) Quantitation in mass-spectrometry-based proteomics. Annu Rev Plant Biol 61:491–516PubMedCrossRefGoogle Scholar
  96. Shen P, Wang R, Jing W, Zhang W (2011) Rice phospholipase Dα is involved in salt tolerance by the mediation of H+ ATPase activity and transcription. J Integr Plant Biol 53:289–299PubMedCrossRefGoogle Scholar
  97. 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
  98. Sheoran IS, Ross ARS, Olson DJH, Sawhney VK (2007) Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J Exp Bot 58:3525–3535PubMedCrossRefGoogle Scholar
  99. Sheoran IS, Pedersen EJ, Ross ARS, Sawhney VK (2009) Dynamics of protein expression during pollen germination in canola (Brassica napus). Planta 230:779–793PubMedCrossRefGoogle Scholar
  100. Silva JC, Denny R, Dorschel CA, Gorenstein M, Kass IJ, Li G-Z, McKenna T, Nold MJ, Richardson K, Young P, Geromanos S (2005) Quantitative proteomic analysis by accurate mass retention time pairs. Anal Chem 77:2187–2200PubMedCrossRefGoogle Scholar
  101. Steinhorst L, Mähs A, Ischebeck T, Zhang C, TZhang X, Arendt S, Schültke S, Heilmann I, Kudla J (2015) Vacuolar CBL-CIPK12 Ca2+-sensor-kinase complexes are required for polarized pollen tube growth. Curr Biol 25:475–482CrossRefGoogle Scholar
  102. Sun W, Li S, Xu J, Liu T, Shang Z (2009) H+ ATPase in the plasma membrane of Arabidopsis pollen cells is involved in extracellular calmodulin-promoted pollen germination. Prog Nat Sci 19:1071–1078CrossRefGoogle Scholar
  103. Svennelid F, Olsson A, Piotroski M, Rosenquist M, Ottman C, Larsson C, Oecking C, Sommarin M (1999) Phosphorylation of Thr-948 at the C-terminus of the plasma membrane H+ ATPase creates a binding site for the regulatory 14-3-3 protein. Plant Cell 11:2379–2391PubMedPubMedCentralGoogle Scholar
  104. Sze H, Liang F, Hwang I, Curran AC, Harper JF (2000) Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433–462PubMedCrossRefGoogle Scholar
  105. Tateda C, Kusano T, Takahashi Y (2012) The Arabidopsis voltage-dependent anion channel 2 is required for plant growth. Plant Signal Behav 7:31–33PubMedPubMedCentralCrossRefGoogle Scholar
  106. The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641CrossRefGoogle Scholar
  107. Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR, Myers CT, Rato C, Poulsen LR, McDowell S, Miller G, Mittler R, Harper JF (2013) A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 161:1010–1020PubMedCrossRefGoogle Scholar
  108. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen G-L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé J-C, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C-J, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  109. Tyrrell M, Campanoni P, Sutter J-U, Pratelli R, Paneque M, Sokolovski S, Blatt MR (2007) Selective targeting of plasma membrane and tonoplast traffic by inhibitory (dominant-negative) SNARE fragments. Plant J 51:1099–1115PubMedCrossRefGoogle Scholar
  110. Van Aken O, Whelan J, Van Breusegem F (2010) Prohibitins: mitochondrial partners in development and stress response. Trends Plant Sci 15:275–282PubMedCrossRefGoogle Scholar
  111. 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
  112. Winship LJ, Obermeyer G, Geitmann A, Hepler PK (2010) Under pressure, cell walls set the pace. Trends Plant Sci 15:363–369PubMedPubMedCentralCrossRefGoogle Scholar
  113. Wu Y, Xu X, Li S, Liu T, Ma L, Shang Z (2007) Heterotrimeric G-protein participation in Arabidopsis pollen germination through modulation of a plasma membrane hyperpolarization-activated Ca2+-permeable channel. New Phytol 176:550–559PubMedCrossRefGoogle Scholar
  114. Young ND, Debelle F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KFX, Gouzy J, Schoof H, Van de Peer Y, Proost S, Cook DR, Meyers BC, Spannagl M, Cheung F, De Mita S, Krishnakumar V, Gundlach H, Zhou S, Mudge J, Bharti AK, Murray JD, Naoumkina MA, Rosen B, Silverstein KAT, Tang H, Rombauts S, Zhao PX, Zhou P, Barbe V, Bardou P, Bechner M, Bellec A, Berger A, Berges H, Bidwell S, Bisseling T, Choisne N, Couloux A, Denny R, Deshpande S, Dai X, Doyle JJ, Dudez A-M, Farmer AD, Fouteau S, Franken C, Gibelin C, Gish J, Goldstein S, Gonzalez AJ, Green PJ, Hallab A, Hartog M, Hua A, Humphray SJ, Jeong D-H, Jing Y, Jocker A, Kenton SM, Kim D-J, Klee K, Lai H, Lang C, Lin S, Macmil SL, Magdelenat G, Matthews L, McCorrison J, Monaghan EL, Mun J-H, Najar FZ, Nicholson C, Noirot C, O’Bleness M, Paule CR, Poulain J, Prion F, Qin B, Qu C, Retzel EF, Riddle C, Sallet E, Samain S, Samson N, Sanders I, Saurat O, Scarpelli C, Schiex T, Segurens B, Severin AJ, Sherrier DJ, Shi R, Sims S, Singer SR, Sinharoy S, Sterck L, Viollet A, Wang B-B, Wang K, Wang M, Wang X, Warfsmann J, Weissenbach J, White DD, White JD, Wiley GB, Wincker P, Xing Y, Yang L, Yao Z, Ying F, Zhai J, Zhou L, Zuber A, Denarie J, Dixon RA, May GD, Schwartz DC, Rogers J, Quetier F, Town CD, Roe BA (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yu J, Hu S, Wang J, Wong GK-S, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92PubMedCrossRefGoogle Scholar
  116. Zhang Y, Fonslos BR, Shan B, Baek M-C, Yates JR (2013) Protein analysis by shotgun/bottom-up proteomics. Chem Rev 113:2343–2394PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zou J, Song L, Zhang W, Wang Y, Ruan S, Wu WH (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

  1. 1.Molecular Plant Biophysics and Biochemistry, Department of Molecular BiologyUniversity of SalzburgSalzburgAustria

Personalised recommendations