Glycoprotein composition along the pistil of Malus x domestica and the modulation of pollen tube growth
Tóm tắt
The characteristics of pollen tube growth are not constant, but display distinct patterns of growth within the different tissues of the pistil. In the stigma, the growth rate is slow and autotrophic, whereas in the style, it is rapid and heterotrophic. Very little is known about the interactions between these distinct maternal tissues and the traversing pollen tube and the role of this interaction on the observed metabolism. In this work we characterise pollen tube growth in the apple flower and look for differences in glycoprotein epitope localization between two different maternal tissues, the stigma and the style. While immunocytochemically-detected arabinogalactan proteins were present at high levels in the stigma, they were not detected in the transmitting tissue of the style, where extensins were abundant. Whereas extensins remained at high levels in unpollinated pistils, they were no longer present in the style following pollen tube passage. Similarily, while abundant in unpollinated styles, insoluble polysaccharides such as β-glucans, were depleted in pollinated pistils. The switch from autotropic to heterotrophic pollen tube growth correlates spatially with a change of glycoprotein epitopes between the stigma and the style. The depletion of extensins and polysaccharides following pollen tube passage in the style suggest a possible contribution to the acceleration of heterotrophic pollen tube growth, which would imply an active contribution of female tissues on prezygotic male–female crosstalk.
Tài liệu tham khảo
Heslop-Harrison J: Pollen germination and pollen-tube growth. Int Rev Cytol. 1987, 107: 1-78.
Williams JH: Pollen tube growth rates and the diversification of flowering plant reproductive cycles. Int J Plant Sci. 2012, 173: 649-661. 10.1086/665822.
Williams JH: The evolution of pollen germination timing in flowering plants: Austrobaileya scandens (Austrobaileyaceae). AoB Plants. 2012, http://aobpla.oxfordjournals.org/doi 10.1093/aobpla/pls010
Lewis D: The physiology of incompatibility in plants. I. The effect of temperature. Philos Trans R Soc Lond B Biol Sci. 1942, 131: 13-26.
Hedhly A, Hormaza JI, Herrero M: Global warming and sexual plant reproduction. Trends Plant Sci. 2009, 14: 30-36. 10.1016/j.tplants.2008.11.001.
Hedhly A: Sensitivity of flowering plant gametophytes to temperature fluctuations. Environ Exp Bot. 2011, 74: 9-16.
Chae K, Lord EM: Pollen tube growth and guidance: roles of small, secreted proteins. Ann Bot. 2011, 108: 627-636. 10.1093/aob/mcr015.
Herrero M, Dickinson HG: Pollen tube development in Petunia hybrida following compatible and incompatible intraspecific matings. J Cell Sci. 1981, 47: 365-383.
Herrero M, Arbeloa A: Influence of the pistil on pollen tube kinetics in peach (Prunus persica). Am J Bot. 1989, 76: 1441-1447. 10.2307/2444430.
Herrero M: Changes in the ovary related to pollen tube guidance. Ann Bot. 2000, 85: 79-85.
Sogo A, Tobe H: Intermitent pollen-tube growth in pistils of alders (Alnus). Proc Natl Acad Sci USA. 2005, 102: 8770-8775. 10.1073/pnas.0503081102.
Herrero M: Male and female synchrony and the regulation of mating in flowering plants. Philos Trans R Soc Lond B Biol Sci. 2003, 358: 1019-1024. 10.1098/rstb.2003.1285.
Darwin C: In The different forms of flowers on plants of the same species. 2nd edition. Edited by Murray J. London; 1884.
Labarca C, Loewus F: The nutritional role of pistil exudate in pollen tube wall formation in Lilium longiflorum II. Production and utilization of exudate from stigma and stylar canal. Plant Physiol. 1973, 52: 87-92. 10.1104/pp.52.2.87.
Herrero M, Dickinson HG: Pollen-pistil incompatibility in Petunia hybrida: changes in the pistil following compatible and incompatible intraspecific crosses. J Cell Sci. 1979, 36: 1-18.
Stephenson AG, Travers SE, Mena-Ali JI, Winsor JA: Pollen performance before and during the autotrophic–heterotrophic transition of pollen tube growth. Philos Trans R Soc Lond B Biol Sci. 2003, 358: 1009-1018. 10.1098/rstb.2003.1290.
Chapman LA, Goring DR: Pollen-pistil interactions regulating successful fertilization in the Brassicaceae. J Exp Bot. 2010, 61: 1987-1999. 10.1093/jxb/erq021.
Chae K, Kieslich CA, Morikis D, Kim SC, Lord EM: A gain-of-function mutation of Arabidopsis lipid transfer protein 5 disturbs pollen tube tip growth and fertilization. Plant Cell. 2009, 21: 3902-3914. 10.1105/tpc.109.070854.
Kim ST, Zhang K, Dong J, Lord EM: Exogenous free ubiquitin enhances lily pollen tube adhesion to an in vitro stylar matrix and may facilitate endocytosis of SCA. Plant Physiol. 2006, 142: 1397-1411. 10.1104/pp.106.086801.
Chae K, Gonong BJ, Kim SC, Kieslich CA, Morikis D, Balasubramanian S, Lord EM: A multifaced study of stigma/style cysteine-rich adhesin (SCA)-like Arabidopsis lipid transfer proteins (LTPs) suggests diversified roles for these LTPs in plant growth and reproduction. J Exp Bot. 2010, 61: 4277-4290. 10.1093/jxb/erq228.
Knox RB: Pollen-Pistil interactions. In Encyclopedia of plant physiology.Volume 17. Edited by Linskens HF, Heslop-Harrison J. Berlin: Springer; 1984.
Crawford BCW, Yanofsky MF: The formation and function of the female reproductive tract in flowering plants. Curr Biol. 2008, 18: R972-R978. 10.1016/j.cub.2008.08.010.
Palanivelu R, Brass L, Edlund AF, Preuss D: Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell. 2003, 114: 47-59. 10.1016/S0092-8674(03)00479-3.
Renault H, El Amrani A, Palanivelu R, Updegraff EP, Yu A, Renou JP, Preuss D, Bouchereau A, Deleu C: GABA accumulation causes cell elongation defects and a decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana. Plant Cell Physiol. 2011, 52: 894-908. 10.1093/pcp/pcr041.
Estévez JM, Kieliszewski MJ, Khitrov N, Somerville C: Characterization of synthetic hydroxyproline-rich proteoglycans with arabinogalactan protein and extensin motifs in Arabidopsis. Plant Physiol. 2006, 142: 458-470. 10.1104/pp.106.084244.
Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR: A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol. 2010, 153: 485-513. 10.1104/pp.110.156554.
Seifert GJ, Roberts K: The biology of arabinogalactan proteins. Annu Rev Plant Biol. 2007, 58: 137-161. 10.1146/annurev.arplant.58.032806.103801.
Cheung AY, Wang H, Wu HM: A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell. 1995, 82: 383-393. 10.1016/0092-8674(95)90427-1.
Wu HM, Wang H, Cheung AY: A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell. 1995, 82: 395-403. 10.1016/0092-8674(95)90428-X.
Wu HM, Wong E, Ogdahi J, Cheung AY: A pollen tube growth-promoting arabinogalactan protein from Nicotiana alata is similar to the tobacco TTS protein. Plant J. 2000, 22: 165-176. 10.1046/j.1365-313x.2000.00731.x.
Wu H, de Graaf B, Mariani C, Cheung AY: Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell Mol Life Sci. 2001, 58: 1418-1429. 10.1007/PL00000785.
Lamport DTA: Hydroxyprolyne-O-glycosidic linkage of the plant cell wall glycoprotein extensin. Nature. 1967, 216: 1322-1324. 10.1038/2161322a0.
de Graaf BHJ, Knuiman BA, Derksen J, Mariani C: Characterization and localization of the transmitting tissue-specific PELP III proteins of Nicotiana tabacum. J Exp Bot. 2003, 54: 55-63. 10.1093/jxb/erg002.
de Graaf BHJ, Knuiman BA, van der Weerden GM, Feron R, Derksen J, Mariani C: The PELP III glycoproteins in Solanaceae: stylar expression and transfer into pollen tube walls. Sex Plant Reprod. 2004, 16: 245-252. 10.1007/s00497-003-0196-2.
Eberle C, Anderson NO, Clasen BM, Hegeman AD, Smith AG: PELPIII: the class III pistil-specific extension-like Nicotiana tabacum proteins are essential for interspecific incompatibility. Plant J. 2013, 74: 805-814. 10.1111/tpj.12163.
Herrero M, Hormaza JI: Pistil strategies controlling pollen tube growth. Sex Plant Reprod. 1996, 9: 343-347. 10.1007/BF02441953.
Sánchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C: Pistil factors controlling pollination. Plant Cell. 2004, 16: S98-S106. 10.1105/tpc.017806.
Johnson MA, Lord EM: Extracellular guidance cues and intracellular signaling pathways that direct pollen tube growth. The Pollen Tube, a cellular and molecular perspective (Plant Cell Monographs). Edited by: Malhó R. 2006, Berlin: Springer-Verlag, 223-242.
Eberle CA, Clasen BM, Anderson NO, Smith AG: A novel pollen tube growth assay utilizing a transmitting tract-ablated Nicotiana tabacum style. Sex Plant Reprod. 2012, 25: 27-37. 10.1007/s00497-011-0177-9.
Chebli Y, Kaneda M, Zerzour R, Geitmann A: The cell wall of the Arabidopsis pollen tube-spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol. 2012, 160: 1940-1955. 10.1104/pp.112.199729.
Linskens HF, Esser KL: Über eine spezifische anfärbung der pollenschläuche im griffel und die zahl der kallosepfropfen nach selbstung und fremdung. Naturwissenschaften. 1957, 44: 16-16.
Dardelle F, Lehner A, Ramdani Y, Bardor M, Lerouge P, Driouich A, Mollet JC: Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol. 2010, 153: 1563-1576. 10.1104/pp.110.158881.
Strattford S, Barnes WS, Hohorst DL, Sagert JG, Cotter R, Golubiewski A, Showalter AM, McCormick S, Bedinger P: A leucine-rich repeat region is conserved in pollen extensin-like (Pex) proteins in monocots and dicots. Plant Mol Biol. 2001, 46: 43-56. 10.1023/A:1010659425399.
Geitmann A, Steer M: The architecture and properties of the pollen tube cell wall. The Pollen Tube, a cellular and molecular perspective (Plant Cell Monographs). Edited by: Malhó R. 2006, Berlin: Springer-Verlag, 177-200.
Losada JM, Herrero M: Arabinogalactan-protein secretion is associated with the acquisition of stigmatic receptivity in the apple flower. Ann Bot. 2012, 110: 573-584. 10.1093/aob/mcs116.
Cresti M, Ciampolini F, Sansavini S: Ultrastructure and histochemical features of pistil of Malus communis: the stylar transmitting tissue. Sci Hortic. 1980, 12: 327-337. 10.1016/0304-4238(80)90047-3.
Li T, Long S, Li M, Bai S, Zhang W: Determination S-Genotypes and identification of five novel S-Rnase alleles in wild Malus species. Plant Mol Biol. 2012, 30: 453-461.
Herth W, Schnepf E: The fluorochrome, calcofluor white, binds oriented to structural polysaccharide fibrils. Protoplasma. 1980, 105: 129-133. 10.1007/BF01279855.
Meikle PJ, Bonig I, Hoogenraad NJ, Clarke AE, Stone BA: The location of (1–3)-β-glucans in the walls of pollen tubes of Nicotiana alata using a (1–3)-β-glucan-specific monoclonal antibody. Planta. 1991, 185: 1-8.
González MV, Coque M, Herrero M: Pollen pistil interaction in kiwifruit. (Actinidia deliciosa; Actinidiaceae). Am J Bot. 1996, 83: 148-154. 10.2307/2445931.
Martínez-Pallé E, Herrero M: Pollen tube pathway in chalazogamous Pistacia vera L. Int J Plant Sci. 1998, 159: 566-574. 10.1086/297574.
Lora J, Hormaza JI, Herrero M: Stigmatic receptivity in a dichogamous early-divergent angiosperm species, Annona cherimola (Annonaceae): Influence of temperature and humidity. Am J Bot. 2011, 98: 265-274. 10.3732/ajb.1000185.
Distefano G, Gentile A, Herrero M: Pollen-pistil interactions and early fruiting in parthenocarpic citrus. Ann Bot. 2011, 108: 499-509. 10.1093/aob/mcr187.
Parre E, Geitmann A: More than a leak sealant – the physical properties of callose in pollen tubes. Plant Physiol. 2005, 137: 274-286. 10.1104/pp.104.050773.
Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A: Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta. 1998, 206: 452-460. 10.1007/s004250050421.
Stone BA, Clarke AE: Chemistry and biology of (1–3)-β-glucans. Australia: La trobe University Press; 1992.
Guan Y, Guo J, Yang Z: Signaling in pollen tube growth: crosstalk, feedback, and missing links. Mol Plant. 2013, 6: 1053-1064. 10.1093/mp/sst070.
Williams JH, Friedman WE, Arnold ML: Developmental selection within the angiosperm style: using gamete DNA to visualize interspecific pollen competition. Proc Natl Acad Sci U S A. 1999, 96: 9201-9206. 10.1073/pnas.96.16.9201.
Cruden RW: Pollen grain size, stigma depth, and style length: the relationships revisited. Plant Syst Evol. 2009, 278: 223-238. 10.1007/s00606-008-0142-8.
Hormaza JI, Herrero M: Pollen selection. Theor Appl Genet. 1992, 83: 663-672.
Erbar C: Pollen tube transmitting tissue: place of competition of male gametophytes. Int J Plant Sci. 2003, 164: S265-S277. 10.1086/377061.
Bocheneck GM: Eriksen: First come, first served: delayed fertilization does not enhance pollen competition in a wind-pollinated tree, Fraxinus excelsior L. (Oleaceae). Int J Plant Sci. 2011, 172: 60-69. 10.1086/657298.
Lankinen A, Larsson MC: Conflicting selection pressures on reproductive functions and speciation in plants. Evol Ecol. 2009, 23: 147-157. 10.1007/s10682-007-9227-z.
Bernasconi G, Ashman TL, Birkhead TR, Bishop JDD, Grossniklaus U, Kubli E, Marshall DL, Schmid B, Skogsmyr I, Snook RR, Taylor D, Till-Bottraud I, Ward PI, Zeh DW, Hellriegel B: Evolutionary ecology of the prezygotic stage. Science. 2004, 303: 971-975. 10.1126/science.1092180.
Sage TL, Hristova-Sarkovski K, Koehl V, Lyew J, Pontieri V, Bernhardt P, Weston P, Bagha S, Chiu G: Transmitting tissue architecture in basal-relictual angiosperms: Implications for transmitting tissue origins. Am J Bot. 2009, 96: 183-206. 10.3732/ajb.0800254.
Crossgrove DJ, Li LC, Cho HT, Hoffmann-Benning S, Moore RC, Blecker D: The growing world of expansins. Plant Cell Physiol. 2002, 43: 1436-1444. 10.1093/pcp/pcf180.
Valdivia ER, Stephenson AG, Durachko DM, Crossgrove D: Class B beta-expansins are needed for pollen separation and stigma penetration. Sex Plant Reprod. 2009, 22: 141-152. 10.1007/s00497-009-0099-y.
Tabuchi A, Li LC, Crossgrove DJ: Matrix solubilisation and cell wall weakening by beta-expansin (group-1-allergen) from maize pollen. Plant J. 2011, 68: 546-549. 10.1111/j.1365-313X.2011.04705.x.
Hepler PK, Rounds CM, Winship LJ: Control of cell wall extensibility during pollen tube growth. Mol Plant. 2013, 6: 998-1017. 10.1093/mp/sst103.
Rodrigo J, Herrero M, Hormaza JI: Pistil traits and flower fate in apricot (Prunus armeniaca). Ann Appl Biol. 2009, 154: 365-375. 10.1111/j.1744-7348.2008.00305.x.
Arbeloa A, Herrero M: The significance of the obturator in the control of pollen tube entry into the ovary in peach (Prunus persica). Ann Bot. 1987, 60: 681-685.
Cannon MC, Terneus K, Hall Q, Tan L, Wang Y, Wegenhart BL, Chen L, Lamport DTA, Chen Y, Kieliszewski MJ: Self-assembly of the plant cell wall requires an extensin scaffold. Proc Natl Acad Sci U S A. 2008, 105: 2226-2231. 10.1073/pnas.0711980105.
Lamport DTA, Kieliszewski MJ, Chen Y, Cannon MC: Role of the extensin superfamily in primary cell wall architecture. Plant Physiol. 2011, 156: 11-19. 10.1104/pp.110.169011.
Free JB: Comparison of the importance of insect and wind pollination of apple trees. Nature. 1964, 201: 726-727.
Johansen DA: Plant microtechnique. New York: McGraw-Hill eds; 1940.
Jefferies CJ, Belcher AR: A fluorescent brightener used for pollen tube identification in vivo. Stain Tech. 1974, 49: 199-202.
Currier HB: Callose substance in plant cells. Am J Bot. 1957, 44: 478-488. 10.2307/2438916.
Sabatini DD, Bench K, Barrnett RJ: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzimatic activity by aldehyde fixation. J Cell Biol. 1963, 17: 19-58. 10.1083/jcb.17.1.19.
Feder N, O’Brien TP: Plant microtechnique: some principles and new methods. Am J Bot. 1968, 55: 123-142. 10.2307/2440500.
Fisher DB: Protein staining of ribboned epon sections for light microscopy. Histochemie. 1968, 16: 92-96.
Hughes J, McCully ME: The use of an optical brightener in the study of plant structure. Stain Technol. 1975, 50: 319-329.
Nicholas JR, Gates PJ, Grierson P: The use of fluorescence microscopy to monitor root development in micropropagated explants. J Hortic Sci Biotech. 1987, 61: 417-421.
Solís MT, Pintos T, Prado MJ, Bueno MA, Raska I, Risueño MC, Testillano PS: Early markers of in vitro microspore reprogramming to embryogenesis in olive (Olea europaea L.). Plant Sci. 2008, 174: 597-605. 10.1016/j.plantsci.2008.03.014.
Knox JP, Linstead PJ, Peart J, Cooper C, Roberts K: Developmentally-regulated epitopes of cell surface arabinogalactan-proteins and their relations to root tissue pattern formation. Plant J. 1991, 1: 317-326. 10.1046/j.1365-313X.1991.t01-9-00999.x.
Smallwood M, Beven A, Donovan N, Neill SJ, Peart J, Roberts K, Knox JP: Localization of cell wall proteins in relation to the developmental anatomy of the carrot root apex. Plant J. 1994, 5: 237-246. 10.1046/j.1365-313X.1994.05020237.x.
Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG: Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot. 2007, 58: 4027-4035. 10.1093/jxb/erm259.