Abstract
We have identified and characterised the temporal and spatial distribution of the homogalacturonan (HG) and arabinogalactan proteins (AGP) epitopes that are recognised by the antibodies JIM5, JIM7, LM2, JIM4, JIM8 and JIM13 during ovule differentiation in Larix decidua Mill. The results obtained clearly show differences in the pattern of localisation of specific HG epitopes between generative and somatic cells of the ovule. Immunocytochemical studies revealed that the presence of low-esterified HG is characteristic only of the wall of megasporocyte and megaspores. In maturing female gametophytes, highly esterified HG was the main form present, and the central vacuole of free nuclear gametophytes was particularly rich in this category of HG. This pool will probably be used in cell wall building during cellularisation. The selective labelling obtained with AGP antibodies indicates that some AGPs can be used as markers for gametophytic and sporophytic cells differentiation. Our results demonstrated that the AGPs recognised by JIM4 may constitute molecules determining changes in ovule cell development programs. Just after the end of meiosis, the signal detected with JIM4 labelling appeared only in functional and degenerating megaspores. This suggests that the antigens bound by JIM4 are involved in the initiation of female gametogenesis in L. decidua. Moreover, the analysis of AGPs distribution showed that differentiation of the nucellus cells occurs in the very young ovule stage before megasporogenesis. Throughout the period of ovule development, the pattern of localisation of the studied AGPs was different both in tapetum cells surrounding the gametophyte and in nucellus cells. Changes in the distribution of AGPs were also observed in the nucellus of the mature ovule, and they could represent an indicator of tissue arrangement to interact with the growing pollen tube. The possible role of AGPs in fertilisation is also discussed.
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References
Acosta-Garcia G, Vielle-Calzada JP (2004) A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16:2614–2628
Aouali N, Laporte P, Clément Ch (2001) Pectin secretion and distribution in the anther during pollen development in Lilium. Planta 213:71–79
Bednarska E, Lenartowska M, Niekraś L (2005) Localization of pectins and Ca2+ ions in unpollinated and pollinated wet (Petunia hybrida Hort.) and dry (Haemanthus albiflos L.) stigma. Folia Histochem Cytobiol 43:259
Caffal KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydrate Res 344:1879–1900
Casero PJ, Casimiro I, Knox JP (1998) Occurrence of cell surface arabinogalactan-protein and extension epitopes in relation to pericycle and vascular tissue development in the root apex of four species. Planta 204:252–259
Cheung AY, Wang H, Wu HM (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82:383–393
Chudzik B, Zarzyka B, Śnieżko R (2005) Immunodetection of arabinogalactan proteins in different types of plant ovules. Acta Biologica Cracoviensia 47:139–146
Clausen MH, Willats WGT, Knox JP (2003) Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydrate Res 338:1797–1800
Coimbra S, Duarte C (2003) Arabinogalactan proteins may facilitate the movement of pollen tubes from the stigma to the ovules in Actinidia deliciosa and Amaranthus hypochondriacus. Euphytica 133:171–178
Coimbra S, Salema R (1997) Immunolocalization of arabinogalactan proteins in Amaranthus hypochondriacus L. ovules. Protoplasma 199:75–82
Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG (2007) Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot 58:4027–4035
Dolan L, Linstead P, Roberts K (1995) An AGP epitope distinguishes a central metaxylem initial from other vascular initials in the Arabidopsis root. Protoplasma 189:149–155
Gedalovich E, Kuijt J (1987) An ultrastructural study of the viscin tissue of Phthirusa pyrifolia (A. B. K.) Eichler (Loranthaceae). Protoplasma 187:145–155
Gibeaut DM, Carpita NC (1991) Tracing cell wall biogenesis in intact cells and plants, selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol 97:551–561
Huang B-Q, Russell SD (1992) Female germ unit: organization, isolation and function. Intl Rev Cytol 140:233–292
Jauh GY, Lord EM (1995) Localization of pectins and arabinogalactan-proteins in lily (Lilium longiflorum L.) pollen tube and style, and their possible roles in pollination. Planta 199:251–261
Knox JP (1997) The use of antibodies to study the architecture and development regulation of plant cell walls. Intl Rev Cytol 171:79–120
Knox JP (2006) Up against the wall: arabinogalactan-protein dynamics at the cell surfaces. New Phytol 169:443–445
Kreuger M, Van Holst GJ (1996) Arabinogalactan proteins and plant differentiation. Plant Mol Biol 30:1077–1086
Lenartowska M, Rodriguez-Garcia MI, Bednarska E (2001) Immunocytochemical localization of esterified and unesterified pectins in unpollinated and pollinated styles of Petunia hybrida. Hort Planta 213:182–191
von Lurzer E (1956) Megasporenmembranen bei einigen Cupressaceen. Grana Palynol 1:70–78
Majewska-Sawka A, Nothnagel A (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–9
McCormick S (2004) Control of male gametophyte development. Plant Cell 16:142–153
Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277
Mollet JC, Park SY, Nothnagel EA, Lord EM (2000) A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12:1737–1749
Osorio S, Castillejo C, Quesada MA, Medina-Escobar N, Brownsey GJ, Suau R, Heredia A, Botella A, Valpuesta V (2008) Partial demethylation of oligogalacturonides by pectin methyl esterase 1 is required for eliciting defence response in wild strawberry (Fragaria vesca). Plant J 54:43–55
Pennell RI, Roberts K (1990) Sexual development in the pea is presaged by altered expression of arabinogalactan protein. Lett Nat 344:547–549
Pennell RI, Janniche L, Kjellbom P, Scofield GN, Peart JM, Roberts K (1991) Developmental regulation of plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3:1317–1326
Qin Y, Zhao J (2006) Localization of arabinogalactan proteins In egg cells, zygotes, and two-celled proembryos and effects of β-D-glucosyl Yariv reagent on egg cell fertilization and zygote division in Nicotiana tabacum L. J Exp Bot 57:2061–2074
Ramawat KG, Merillon JM (2008) Bioactive molecules and medicinal plants. Springer, Berlin
Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967
Runions CJ, Owens JN (1999) Sexual reproduction of interior spruce (Pinaceae). I. Pollen germination to archegonial maturation. Intl J Plant Sci 160:631–640
Samaj J, Samajová O, Peters M, Baluska F, Lichtscheidl I, Knox JP, Volkmann D (2000) Immunolocalization of LM2 arabinogalactan protein epitope associated with endomembranes of plant cells. Protoplasma 212:186–196
Schindler T, Bergfeld R, Schopfer P (1995) Arabinogalactan proteins in maize coleoptiles: developmental relationship to cell death during xylem differentiation but not to extension growth. Plant J 7:25–36
Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161
Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417
Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459
Southworth D, Kwiatkowski S (1996) Arabinogalactan proteins at the cell surface of Brassica sperm and Lilium sperm and generative cells. Sex Plant Reprod 9:262–272
Takeuchi Y, Komamine A (1980) Turnover of cell wall polysaccharides of a Vinca rosea suspension culture. III. Turnover of arabinogalactan. Physiol Plant 50:113–118
Webb MC, Gunning BE (1990) Embryo sac development in Arabidopsis thaliana. Sex Plant Reprod 3:244–256
Willats WGT, Limberg G, Buchholt HC, van Alebeek G-J, Benen J, Christensen TMIE, Visser J, Voragen A, Mikkelsen JD, Knox JP (2000) Analysis of pectic epitopes recognized by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides and enzymatic degradation. Carbohydrate Res 327:309–320
Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27
Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851–860
Wu HM, Wang H, Cheung AY (1995) A pollen-tube growth-stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82:395–403
Wu H, de Graaf B, Mariani C, Cheung AY (2001) Hydroxyproline rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell Mol Life Sci 58:1418–1429
Yates EA, Knox JP (1994) Investigation into the occurrence of plant cell surface epitopes in exudates gums. Carbohydr Polym 24:281–286
Yates EA, Valdor JF, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6:131–139
Acknowledgments
We would like to thank M. Świdziński for technical assistance. This work was supported by European Social Fund and Kujawsko-Pomorski Province Council project “Stypendia dla doktorantów 2008/2009—ZPORR” and Nicolaus Copernicus University Grant [304-B].
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Communicated by Scott Russell.
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Supplementary Figure S1
. A-B Localisation of callose. C-D Controls. (A) The wall of the megasporocyte is devoid of callose. (B) Positive control. Callose is present in cells walls of the ovuliferous scale. (B)C-D Controls for antibodies (C) Negative control showing no labelling in the ovule when first antibody was omitted. (D) Negative immunodepletion control in which JIM13 antibody was preincubated with inhibitor (gum arabic) showing no labelling of the ovule. MMC – megasporocyte, T – tapetum, SC – ovuliferous scale, G – gametophyte, FN – free nucleus, N – nucellus, V-vacuole. Bar 10 μm (TIFF 1019 kb)
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Rafińska, K., Bednarska, E. Localisation pattern of homogalacturonan and arabinogalactan proteins in developing ovules of the gymnosperm plant Larix decidua Mill. Sex Plant Reprod 24, 75–87 (2011). https://doi.org/10.1007/s00497-010-0154-8
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DOI: https://doi.org/10.1007/s00497-010-0154-8