Abstract
The major events of male reproductive development and function have been known for years, but the molecular and cellular bases of these processes are still poorly understood. Recent advances in cell biology coupled with molecular genetics and functional genomics are poised to offer tremendous opportunities to understand how membrane transport is integrated with male gametophyte development and physiology. Here we first propose the type of transporters necessary to affect the dynamics of Ca 2+, K+, pH and others ions observed in polarized tip growth, and then show how pollen transcriptomics and molecular genetic tools are beginning to reveal the roles of specific transporters in microgametogenesis, pollen tube growth and male fertility.
Preview
Unable to display preview. Download preview PDF.
References
Becker D, Geiger D, Dunkel M, Roller A, Bertl A, Latz A, Carpaneto A, Dietrich P, Roelfsema MR, Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K, Hedrich R (2004) AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner. Proc Natl Acad Sci USA 101:15621–15626
Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500
Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating Membrane Transport with Male Gametophyte Development and Function through Transcriptomics. Plant Physiol. (accepted)
Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI (2000) At-ACA8encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol 123:1495–1506
Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865
Busch W, Saier MH Jr (2004) The IUBMB-endorsed transporter classification system. Mol Biotechnol 27:253–262
Cho MH, Spalding EP (1996) An anion channel in Arabidopsis hypocotyls activated by blue light. Proc Natl Acad Sci USA 93:8134–8138
Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 defense, no death gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328
Dettmer J, Schubert D, Calvo-Weimar O, Stierhof YD, Schmidt R, Schumacher K (2005) Essential role of the V-ATPase in male gametophyte development. Plant J 41:117–124
Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406
Fan LM, Wang YF, Wang H, Wu WH (2001) In vitro Arabidopsis pollen germination and characterization of the inward potassium currents in Arabidopsis pollen grain protoplasts. J Exp Bot 52:1603–1614
Fan LM, Wang YF, Wu WH (2003) Outward K+ channels in Brassica chinensis pollen protoplasts are regulated by external and internal pH. Protoplasma 220:143–152
Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK (1999) Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 144:483–496
Fricker MD, White NS, Obermeyer G (1997) pH gradients are not associated with tip growth in pollen tubes of Lilium longoflorum. J Cell Sci 110:1729–1740
Garrill A, Jackson SL, Lew RR, Heath IB (1993) Ion channel activity and tip growth: tip-localized stretch-activated channels generate an essential Ca2+ gradient in the oomycete Saprolegnia ferax. Eur J Cell Biol 60:358–365
Graham RD (1975) Male sterility in wheat plants deficient in copper. Nature 254:514–515
Griessner M, Obermeyer G (2003) Characterization of whole-cell K+ currents across the plasma membrane of pollen grain and tube protoplasts of Lilium longiflorum. J Membr Biol 193:99–108
Hicks GR, Rojo E, Hong S, Carter DG, Raikhel NV (2004) Geminating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol 134:1227–1239
Holdaway-Clarke TI, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563
Holdaway-Clarke TL, Feijó JA, Hackett GR, Kunkel JG, Hepler PK (1997) Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx Is delayed. Plant Cell 9:1999–2010
Holdaway-Clarke TL, Weddle NM, Kim S, Robi A, Parris C, Kunkel JG, Hepler PK (2003) Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. J Exp Bot 380:65–72
Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85
Hua BG, Mercier RW, Leng Q, Berkowitz GA (2003) Plants do it differently. A new basis for potassium/sodium selectivity in the pore of an ion channel. Plant Physiol 132:1353–1361
Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339
Iwano M, Shiba H, Miwa T, Che FS, Takayama S, Nagai T, Miyawaki A, Isogai A (2004) Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 136:3562–3571
Jaffe LA, Weisenseel MH, Jaffe LF (1975) Calcium accumulations within the growing tips of pollen tubes. J Cell Biol 67:488–492
Johnson MA, von Besser K, Zhou Q, Smith E, Aux G, Patton D, Levin JZ, Preuss D (2004) Arabidopsis hapless mutations define essential gametophytic functions. Genetics 168:971–982
Kuhtreiber WM, Jaffe LF (1990) Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. J Cell Biol 110:1565–1573
Leng Q, Mercier RW, Hua BG, Fromm H, Berkowitz GA (2002) Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol 128:400–410
Malhó R, Camacho L, Moutinho A (2000) Signalling pathways in pollen tube growth and reorientation. Ann Bot 85(suppl A):59–68
Malhó R, Read ND, Trewavas AJ, Pais MS (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7:1173–1184
Malhó R, Trewavas AJ (1996) Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8:1935–1949
Matveyeva NP, Andreyuk DS, Yermakov IP (2003) Transport of Cl− across the plasma membrane during pollen grain germination in tobacco. Biochemistry (Mosc) 68:1247–1251
Messerli M, Robinson KR (1997) Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum. J Cell Sci 110(Pt 11):1269–1278
Messerli MA, Robinson KR (1998) Cytoplasmic acidification and current influx follow growth pulses of Lilium longiflorum pollen tubes. Plant Journal 16:87–91
Messerli MA, Smith PJ, Lewis RC, Robinson KR (2004) Chloride fluxes in lily pollen tubes: a critical reevaluation. Plant J 40:799–812
Mouline K, Very AA, 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 16:339–350
Moutinho A, Hussey PJ, Trewavas AJ, Malhó R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci USA 98:10481–10486
O'Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849
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 134:1514–1526
Palmgren MG (2001) Plant plasma membrane H+-ATPases: Powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845
Parton RM, Fischer S, Malhó R, Papasouliotis O, Jelitto T, Leonard T, Read ND (1997) Pronounced cytoplasmic pH gradients are not required for tip growth in plant and fungal cells. J Cell Sci 110:1187–1198
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 138:744–756
Reiss HD, Herth W (1978) Visualization of the Ca2+ gradient in growing pollen tubes of Lilium longiflorum with chlorotetraceycline fluorescence. Protoplasma 97:373–377
Robertson WR, Clark K, Young JC, Sussman MR (2004) An Arabidopsis thaliana plasma membrane proton pump is essential for pollen development. Genetics 168:1677–1687
Rudd JJ, Franklin-Tong VE (2000) Unravelling response-specificity in Ca2+ signaling pathways in plant cells. New Phytol 151:7–33
Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L (2004) The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279:15348–15355
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14 Suppl:S401–S417
Schiott M, Romanowsky SM, 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 USA 101:9502–9507
Schneidereit A, Scholz-Starke J, Buttner M (2003) Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis. Plant Physiol 133:182–190
Schneidereit A, Scholz-Starke J, Sauer N, Buttner M (2005) AtSTP11, a pollen tube-specific monosaccharide transporter in Arabidopsis. Planta 221:48–55
Scholz-Starke J, Buttner M, Sauer N (2003) AtSTP6, a new pollen-specific H+-monosaccharide symporter from Arabidopsis. Plant Physiol 131:70–77
Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flugge UI, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131:16–26
Shang ZL, Ma LG, Zhang HL, He RR, Wang XC, Cui SJ, Sun DY (2005) Ca2+ influx into lily pollen grains through a hyperpolarization-activated Ca2+-permeable channel which can be regulated by extracellular CaM. Plant Cell Physiol 46:598–608
Stadler R, Truernit E, Gahrtz M, Sauer N (1999) The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis. Plant J 19:269–278
Steer MW, Steer JM (1989) Pollen tube tip growth. New Phytol 111:323–358
Sze H (1985) H+-translocating ATPases: Advances using membrane vesicles. Annu Rev Plant Physiol 36:175–208
Sze H, Li X, Palmgren MG (1999) Energization of plant cell membranes by H+-pumping ATPases. Regulation and biosynthesis. Plant Cell 11:677–690
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 51:433–462
Sze H, Padmanaban S, Cellier F, Honys D, Cheng NH, Bock KW, Conejero G, Li X, Twell D, Ward JM, Hirschi KD (2004) Expression patterns of a novel AtCHX gene family highlight potential roles in osmotic adjustment and K+ homeostasis in pollen development. Plant Physiol 136:2532–2547
Sze H, Schumacher K, Muller ML, Padmanaban S, Taiz L (2002) A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H(+)-ATPase. Trends Plant Sci 7:157–161
Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420:337–340
Talke IN, Blaudez D, Maathuis FJ, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293
Truernit E, Stadler R, Baier K, Sauer N (1999) A male gametophyte-specific monosaccharide transporter in Arabidopsis. Plant J 17:191–201
Tschieu JH, Fana F, Fink JL, Harper J, Nair TM, Niedner RH, Smith DW, Steube K, Tam TM, Veretnik S, Wang D, Gribskov M (2003) The PlantsP and PlantsT Functional Genomics Databases. Nucleic Acids Res 31:342–344
Very AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci USA 97:9801–9806
Very AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54:575–603
Wang Q, Lu L, Wu X, Li Y, Lin J (2003) Boron influences pollen germination and pollen tube growth in Picea meyeri. Tree Physiol 23:345–351
Wang YF, Fan LM, Zhang WZ, Zhang W, Wu WH (2004) Ca2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments. Plant Physiol 136:3892–3904
Ward JM (2001) Identification of novel families of membrane proteins from the model plant Arabidopsis thaliana. Bioinformatics 17:560–563
Ward JM, Pei ZM, Schroeder JI (1995) Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 7:833–844
Weisenseel MH, Nuccitelli R, Jaffe LF (1975) Large electrical currents traverse growing pollen tubes. J Cell Biol 66:556–567
Woeste KE, Kieber JJ (2000) A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12:443–455
Zonia L, Cordeiro S, Tupy J, Feijó JA (2002) Oscillatory chloride efflux at the pollen tube apex has a role in growth and cell volume regulation and is targeted by inositol 3,4,5,6-tetrakisphosphate. Plant Cell 14:2233–2249
Author information
Authors and Affiliations
Corresponding author
Editor information
Rights and permissions
About this chapter
Cite this chapter
Sze, H., Frietsch, S., Li, X., Bock, K.W., Harper, J.F. Genomic and Molecular Analyses of Transporters in the Male Gametophyte. In: Malhó, R. (eds) The Pollen Tube. Plant Cell Monographs, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_044
Download citation
DOI: https://doi.org/10.1007/7089_044
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-31121-8
Online ISBN: 978-3-540-34276-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)