Abstract
Sexual plant reproduction necessitates proper development of pollen, pollen germination and tube growth through various tissues of the pistil, the female organ of the flower. Finally, sperm cells are released to fertilize the female gametophyte. These processes require high metabolic activities of all tissues involved and rely on the delivery of nitrogen assimilates for success. However, transporters mediating nitrogen fluxes are mostly unknown. The presented work provides an expression analysis of members of the LHT amino acid transporter family in relation to pollen development and pollen–pistil interaction. Expression of Arabidopsis LHTs was analyzed during flower development and the location of LHT function resolved by transporter-GFP and promoter-GUS studies. GFP-LHT localization in onion cells indicates that all LHTs analyzed are targeted to the plasma membrane. We further showed that LHTs are expressed in anthers and male gametophytes where they are proposed to function in transport of amino acids for pollen development and maturation. Expression in germinating pollen, pollen tubes and transmitting tissue of the pistil points to a role of LHTs in support of the fertilization process. Overall, our study suggests that LHT function in flowers is cell or tissue specific, developmentally regulated and highly coordinated between male and female tissue.
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References
Becker D, Kemper E, Schell J, Masterson R (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol Biol 20:1195–1197
Bhadula SK, Sawhney VK (1991) Protein analysis during the ontogeny of normal and male sterile stamenless-2 mutant stamens of tomato (Lycopersicon esculentum Mill.). Biochem Genet 29:29–41
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 140:1151–1168
Chen L, Bush DR (1997) LHT1, a lysine- and histidine-specific amino acid transporter in Arabidopsis. Plant Physiol 115:1127–1134
Cheung AY (1996) Pollen–pistil interactions during pollen tube growth. Trends Plant Sci 1:45–51
Cheung AY, Wang H, Wu H-M (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82:383–393
Chiang H-H, Dandekar AM (1995) Regulation of proline accumulation in Arabidopsis thaliana (L.) Heynh during development and in response to desiccation. Plant Cell Environ 18:1280–1290
Clément C, Laporte P, Audran JC (1998) The loculus content and tapetum during pollen development in Lilium. Sex Plant Reprod 11:94–106
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta Plant Physiol 133:462–469
Dickinson HG, Lewis D (1973) The formation of the tryphine coating the pollen grains of Raphanus, and its properties relating to the self-incompatibility system. Proc R Soc London Ser B184:149–165
Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138:778–789
Elleman CJ, Franklin-Tong V, Dickinson HG (1992) Pollination in species with dry stigmas: The nature of the early stigmatic response and the pathway taken by pollen tubes. New Phytol 121:413–424
Evans JJ, Pressey R, Reger BJ (1987) Amino acids in stigmas of Pennisetum americanum. Phytochemistry 26:2661–2663
Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, Neuhaus JM, Rentsch D (2005) The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol 137:117–126
Hammes UZ, Nielsen E, Honaas LA, Taylor CG, Schachtman DP (2006) AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J 48:414–426
Hess MW, Hesse M (1994) Ultrastructural observations on anther tapetum development of freeze-fixed Ledebouria socialis Roth (Hyacinthaceae). Planta 192:421–430
Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946
Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85
Horner M, Pratt ML (1979) Amino acid analysis of in vivo and androgenic anthers of Nicotiana tabacum. Protoplasma 98:279–282
Knox RB (1984) Pollen–pistil interactions. Encyclop Plant Physiol 17:508–608
Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396
Krichevsky A, Kozlovsky SV, Tian G-W, Chen M-H, Zaltsman A, Citovsky V (2007) How pollen tubes grow. Dev Biol 303:405–420
Krogaard H, Andersen AS (1983) Free amino acids of Nicotiana alata anthers during development in vivo. Physiol Plantarum 57:527–531
Labarca C, Loewus F (1973) The nutritional role of pistil exudates in pollen tube wall formation in Lilium longiflorum. Plant Physiol 52:87–92
Lalanne E, Mathieu C, Roche O, Vedel F, De Pape R (1997) Structure and specific expression of a Nicotiana sylvestris putative amino-acid transporter gene in mature and in vitro germinating pollen. Plant Mol Biol 35:855–864
Latz A, Becker D, Hekman M, Muller T, Beyhl D, Marten I, Eing C, Fischer A, Dunkel M, Bertl A, Rapp UR, Hedrich R (2007) TPK1, a Ca(2+)-regulated Arabidopsis vacuole two-pore K(+) channel is activated by 14-3-3 proteins. Plant J 52:449–459
Lee YH, Tegeder M (2004) Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers. Plant J 40:60–74
Lennon KA, Roy S, Hepler PK, Lord EM (1998) The structure of the transmitting tissue of Arabidopsis thaliana (L.) and the path of pollen tube growth. Sex Plant Reprod 11:49–59
Lévesque-Lemay M, Albani D, Aldcorn D, Hammerlindl J, Keller W, Robert LS (2003) Expression of CCAAT-binding factor antisense transcripts in reproductive tissues affects plant fertility. Plant Cell Rep 21:804–808
Liu X, Bush DR (2006) Expression and transcriptional regulation of amino acid transporters in plants. Amino acids 30:113–120
Lord EM, Russell SD (2002) The mechanisms of pollination and fertilization in plants. Annu Rev Cell Dev Biol 18:81–105
Meyer A, Eskandari S, Grallath S, Rentsch D (2006) AtGAT1, a high affinity transporter for gamma-aminobutyric acid in Arabidopsis thaliana. J Biol Chem 281:7197–7204
Minet M, Dufour ME, Lacroute F (1992) Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J 2:417–422
Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T (2006) A specific transporter for iron(III)-phytosiderophore in barley roots. Plant J 46:563–572
Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114:47–59
Palanivelu R, Preuss D (2006) Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 6:7
Pélissier HC, Frerich A, Desimone M, Schumacher K, Tegeder M (2004) PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiol 134:664–675
Pélissier HC, Tegeder M (2007) PvUPS1 plays a role in source-sink transport of allantoin in French bean (Phaseolus vulgaris). Funct Plant Biol 34:282–291
Peña-Valdivia CB, Rodriguez-Gracia R (1999) Free amino acids in maize (Zea mays L.) anthers during microsporogenesis. Cereal Res Comm 27:395–402
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 138:744–756
Pineros MA, Cancado GM, Maron LG, Lyi SM, Menossi M, Kochian LV (2008) Not all ALMT1-type transporters mediate aluminum-activated organic acid responses: the case of ZmALMT1 – an anion-selective transporter. Plant J 53:352–367
Platt KA, Huang AHC, Thomson WW (1998) Ultrastructural study of lipid accumulation in tapetal cells of Brassica napus L. Cv. Westar during microsporogenesis. Int J Plant Sci 159:724–737
Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett 581:2281–2289
Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C (2004) Pistil factors controlling pollination. Plant Cell 16:S98–S106
Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu Y-C, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322
Sangwan RS (1978) Change in the amino acid content during male gametophyte formation of Datura metel in situ. Theor Appl Genet 52:221–225
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 37:501–506
Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and γ-amino butyric acid in tomato pollen. Plant Cell 11:377–392
Sivitz AB, Reinders A, Johnson ME, Krentz AD, Grof CP, Perroux JM, Ward JM (2007) Arabidopsis sucrose transporter AtSUC9. High-affinity transport activity, intragenic control of expression, and early flowering mutant phenotype. Plant Physiol 143:188–198
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767
Steer MW (1977) Differentiation of the tapetum in Avena. J Cell Sci 25:125–138
Taylor PE, Glover JA, Lavithis M, Craig S, Singh MB, Knox RB, Dennis ES, Chaudhury AM (1998) Genetic control of male fertility in Arabidopsis thaliana: structural analyses of postmeiotic developmental mutants. Planta 205:492–505
Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J 43:153–163
Tupý J (1961) Investigation of free amino acids in cross-, self- and non-pollinated pistils of Nicotiana alata. Biol Plantarum 3:47–64
Wang H, Wu HM, Cheung AY (1993) Development and pollination regulated accumulation and glycosylation of a stylar transmitting tissue-specific proline-rich protein. Plant Cell 5:1639–1650
Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28:27–39
Xie JH, Gao MW, Liang ZQ, Shu QY, Cheng XY, Xue QZ (1997) The effect of cool-pretreatment on the isolated microspore culture and the free amino acid change of anthers in Japonica rice (Oryza sativa L.). J Plant Physiol 151:79–82
Yang S-L, Xie L-F, Mao H-Z, Puah CS, Yang W-C, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinent1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804
Zhang H-Q, Croes AF, Linskens HF (1982) Protein synthesis in germinating pollen of Petunia: role of proline. Planta 154:199–203
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This work was supported by the National Science Foundation (grant IBN 0135344 to M.T.).
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Communicated by Scott Russell.
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Foster, J., Lee, YH. & Tegeder, M. Distinct expression of members of the LHT amino acid transporter family in flowers indicates specific roles in plant reproduction. Sex Plant Reprod 21, 143–152 (2008). https://doi.org/10.1007/s00497-008-0074-z
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DOI: https://doi.org/10.1007/s00497-008-0074-z