Abstract
Although gene expression profile of pollen has been described, there is limited information regarding a particular phase during anther/pollen development. This work characterizes gene expression pattern at desiccation in lily (Lilium longiflorum Thunb. cv Snow Queen) anthers. We have applied a suppression-subtractive hybridization (SSH) strategy, through which 90 clones were identified and sequenced. These clones resulted in the identification of 42 individual cDNAs among which 33 genes were specifically expressed at the desiccation phase of anthers of >150-mm buds. Fourteen cDNAs were chosen for further examination. Six genes were both dehydration- and abscisic acid (ABA)-inducible whereas the other eight genes were apparently dehydration-irrelevant. The group of dehydration- and ABA-induced genes was also induced by desiccation that developmentally occurs in the anther. The application of fluridone has a significant effect of inhibition on mRNA accumulation of these genes in maturing anthers during which desiccation occurs. Pollen germination analysis indicated that, of those dehydration-irrelevant genes, three were ABA-responsive and the other five were not. Thus, three separate signal pathways that function in the activation of late genes at desiccation during anther development are established. The first is the ABA-dependent pathway induced by environmental stress of dehydration. The other two pathways of signaling triggered by developmental cues, through which one is ABA-dependent and another is ABA-independent. The 14 gene proteins showed spatial and temporal expression patterns and may participate in membrane/cell wall synthesis, cytoskeletal organization, signaling, RNA binding, ubiquitin-mediated degradation and transportation during germination and tube growth.
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Abbreviations
- ABA:
-
Abscisic acid
- MOPS:
-
3-[N-Morpholino]propanesulfonic acid
- PCR:
-
Polymerase chain reaction
- SDS:
-
Sodium dodecyl sulfate
- SSH:
-
Suppression-subtractive hybridization
References
Altschul SF, Madden TL, Schafer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
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 133:713–725
Chiang J-Y, Hsu S-W, Ko C-W, Wang C-S (2006) Biochemical characterization of a pollen-specific cDNA encoding polygalacturonase in Lilium longiflorum. Plant Sci 170:433–440
Dawson PJ, Hulme JS, Lloyd CW (1985) Monoclonal antibody to intermediate filament antigen cross-reacts with higher plant cells. J Cell Biol 100:1793–1798
Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030
Dickinson DB (1978) Influence of borate and pentaerythritol concentrations on germination and tube growth of Lilium longiflorum pollen. J Am Soc Horti Sci 103:413–416
Dopico B, Lowe AL, Wilson ID, Merodio C, Grierson D (1993) Cloning and characterization of avocado fruit mRNAs and their expression during ripening and low-temperature storage. Plant Mol Biol 21:437–449
Dudareva1 N, Evrard JL, Pillay DTN, Steinmetz A (1994) Nucleotide sequence of a pollen-specific cDNA from Helianthus annuus L. encoding a highly basic protein (accession noX74772). Plant Physiol 106:403–404
Filichkin SA, Leonard JM, Monteros A, Liu PP, Nonogaki H (2004) A novel endo-beta-mannanase gene in tomato LeMAN5 is associated with anther and pollen development. Plant Physiol 134:1080–1087
Frankis R, Mascarenhas JP (1980) Messenger RNA in the ungerminated pollen grains: a direct demonstration of its presence. Ann Bot 45:595–599
Gupta R, Ting JT, Sokolov LN, Johnson SA, Luan S (2002) A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell 10:2495–2507
Gurskaya NG, Diatchenko L, Chenchik A, Siebert PD, Khaspekov GL, Lukyanov KA, Vagner LL, Ermolaeva OD, Lukyanov SA, Sverdlov ED (1996) Equalizing cDNA subtraction based on selective suppression of polymerase chain reaction: cloning of Jurkat cell transcripts induced by phytohemaglutinin and phorbol 12-myristate 13-acetate. Anal Biochem 240:90–97
Guyon VN, Astwood JD, Garner EC, Dunker AK, Taylor LP (2000) Isolation and characterization of cDNAs expressed in the early stages of flavonol-induced pollen germination in petunia. Plant Physiol 123:699–710
Halperin T, Zheng B, Itzhaki H, Clarke AK, Adam Z (2001) Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease. Plant Mol Biol 45:461–468
Hiwasa K, Kinugasa Y, Amano S, Hashimoto A, Nakano R, Inaba A, Kubo Y (2003) Ethylene is required for both the initiation and progression of softening in pear (Pyrus communis L.) fruit. J Exp Bot 54:771–779
Hoekstra FA (1984) Imbibitional chilling injury in pollen: involvement of the respiratory chain. Plant Physiol 74:815–821
Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5:4864–4884
Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652
Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85.1–R85.13
Huang J, Chen F, Casino CD, Autino A, Shen M, Yuan S, Peng J, Shi H, Wang C, Cresti M, Li Y (2006) An ankyrin repeat-containing protein, characterized as a ubiquitin ligase, is closely associated with membrane-enclosed organelles and required for pollen germination and pollen tube growth in lily. Plant Physiol 140:1374–1383
Huang J-C, Lin S-M, Wang C-S (2000) A pollen-specific and desiccation-associated transcript in Lilium longiflorum during development and stress. Plant Cell Physiol 41:477–485
Kagan-Zur V, Tieman DM, Marlow SJ, Handa AK (1995) Differential regulation of polygalacturonase and pectin methylesterase gene expression during and after heat stress in ripening tomato (Lycopersicon esculentum Mill.) fruits, Plant Mol Biol 29:1101–1110
Lubkowitz MA, Barnes D, Breslav M, Burchfield A, Naider F, Becker JM (1998) Schizosaccharomyces pombe isp4 encodes a transporter representing a novel family of oligopeptide transporters. Mol Microbiol 28:729–741
McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275
Miki-Hirosige H, Yamanaka Y, Nakamura S, Kurata S, Hirano H (2004) Changes of protein profiles during pollen development in L. longiflorum. Sex Plant Reprod 16:209–214
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
Rothan C, Duret S, Chevalier C, Raymond P (1997) Suppression of ripening-associated gene expression in tomato fruits subjected to a high CO2 concentration. Plant Physiol 114:255–263
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Scholz-Starke J, Buttner M, Sauer N (2003) AtSTP6, a new pollen-specific H+-monosaccharide symporter from Arabidopsis. Plant Physiol 131:70–77
Shary S, Kumar R, Guha-Mukherjee S (2006) Isolation of pollen early genes and analysis of expression pattern during the development of male gametophyte. Plant Sci 170:417–425
Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334
Steiner C, Bauer J, Amrhein N, Bucher M (2003) Two novel genes are differentially expressed during early germination of the male gametophyte of Nicotiana tabacum. Biochem Biophys Acta 1625:123–133
Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30
Suen DF, Wu SS, Chang HC, Dhugga KS, Huang AH (2003) Cell-wall reactive proteins in the coat and wall of maize pollen: potential role in pollen tube growth on the stigma and through the style. J Biol Chem 278:43672–43681
Wang M-L, Hsu C-M, Chang L-C, Wang C-S, Su T-H, Huang Y-JJ, Jiang L, Jauh G-Y (2004) Gene expression profiles of cold-stored and fresh pollen to investigate pollen germination and growth. Plant Cell Physiol 45:1519–1528
Wang C-S, Huang J-C, Hu J-H (1999) Characterization of two subclasses of PR-10 transcripts in lily anthers and induction of their genes through separate signal transduction pathways. Plant Mol Biol 40:807–814
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
Wang C-S, Walling LL, Eckard KJ, Lord EM (1992) Patterns of protein accumulation in developing anthers of Lilium longiflorum correlate with histological events. Am J Bot 79:118–127
Wang C-S, Wu T-D, Chung C-KW, Lord EM (1996) Two classes of pollen-specific, heat-stable proteins in Lilium longiflorum. Physiol Plant 97:643–650
Willing RP, Bashe D, Mascarenhas JP (1988) An analysis of the quantity and diversity of messenger RNAs from pollen and shoot of Zea mays. Theor Appl Genet 75:751–753
Willing RP, Mascarenhas JP (1984) Analysis of the complexity and diversity of mRNAs from pollen and shoots of Tradescantia. Plant Physiol 75:865–868
Xu H, Weterings K, Vriezen W, Feron R, Xue Y, Derksen J, Mariani C (2002) Isolation and characterization of male-germ-cell transcripts in Nicotiana tabacum. Sex Plant Reprod 14:339–346
Acknowledgments
This work was supported by National Science Council grant NSC 95-2311-B005-006-MY3 to Co-Shine Wang.
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Hsu, YF., Wang, CS. & Raja, R. Gene expression pattern at desiccation in the anther of Lilium longiflorum . Planta 226, 311–322 (2007). https://doi.org/10.1007/s00425-007-0483-5
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DOI: https://doi.org/10.1007/s00425-007-0483-5