Plant Reproduction

, Volume 28, Issue 1, pp 1–15 | Cite as

Arabinogalactan proteins: rising attention from plant biologists

  • Ana Marta Pereira
  • Luís Gustavo Pereira
  • Sílvia CoimbraEmail author
Part of the following topical collections:
  1. From Gametes to Seeds


Key message

AGP update: plant reproduction.

Arabinogalactan proteins (AGPs) are a large family of hydroxyproline-rich proteins, heavily glycosylated, ubiquitous in land plants, including basal angiosperms and also in many algae. They have been shown to serve as important molecules in several steps of the reproductive process in plants. Due to their special characteristics, such as high sugar content and their means of association with the membrane, they are often perceived as likely candidates for many different aspects of the reproductive process such as signalling molecules, cell identity determinants, morphogens, nutrient sources and support for pollen tube growth, among others. Nevertheless, the study of these proteins pose many difficulties when it comes to studying them individually. Most of the work done involved the use of the β-glucosyl Yariv reagent and antibodies that recognize the carbohydrate epitopes only. Recently, new approaches have been used to study AGPs largely based in the remarkable growing volume of microarray data made available. Either using older techniques or the most recent ones, a clearer picture is emerging for the functions and mode of action of these molecules in the plant reproductive processes. Here, we present an overview about the most important studies made in this area, focusing on the latest advances and the possibilities for future studies in the field.


Sporophytic tissues Female gametophyte Male gametophyte Pollen tube growth Double fertilization 



This work was financed by FEDER through the COMPETE programme and by Portuguese National funds through FCT—Fundação para a Ciência e Tecnologia (Project PTDC/AGR-GPL/115358/2009) and from an FCT PhD Grant SFRH/BD/60995/2009 awarded to AMP. This project also benefited from financial support from the COST Action FA0903: ‘Harnessing Plant Reproduction for Crop Improvement’. We want to thank BioMed Central, the original publisher of Figure 2, and the authors (Costa M, Nobre MS, Becker JD, Masiero S, Amorim MI, Pereira LG, Coimbra S (2013). Expression-based and co-localization detection of Arabinogalactan protein 6 and Arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes. BMC Plant Biol 13:7) for sharing this image. We also wish to thank to Oxford University Press for permission on using Figure 1a, published in Pereira AM, Masiero S, Nobre MS, Costa ML, Solís M-T, Testillano PS, Sprunck S, Coimbra S (2014) Differential expression patterns of Arabinogalactan Proteins in Arabidopsis thaliana reproductive tissues. J Exp Bot 65(18):5459–5471. We would like to thank Professor Roberto Salema for all the unconditional support given to our scientific research during the last years.


  1. Acosta-García G, Vielle-Calzada J-P (2004) A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16:2614–2628PubMedCentralPubMedGoogle Scholar
  2. Beale KM, Johnson MA (2013) Speed dating, rejection, and finding the perfect mate: advice from flowering plants. Curr Opin Plant Biol 16(5):590–597PubMedGoogle Scholar
  3. Berger F, Hamamura Y, Ingouff M, Higashiyama T (2008) Double fertilization: caught in the act. Trends Plant Sci 13(8):437–443PubMedGoogle Scholar
  4. Bleckmann A, Alter S, Dresselhaus T (2014) The beginning of a seed: regulatory mechanisms of double fertilization. Front Plant Sci 11(5):452Google Scholar
  5. Bosch M, Sommer-Knudsen J, Derksen J, Mariani C (2001) Class III pistil-specific extensin-like proteins from tobacco have characteristics of Arabinogalactan proteins. Plant Physiol 125(4):2180–2188PubMedCentralPubMedGoogle Scholar
  6. Bove J, Vaillancourt B, Kroeger J, Hepler PK, Wiseman PW, Geitmann A (2008) Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy (STICS) and fluorescence recovery after photobleaching (FRAP). Plant Physiol 147(4):1646–1658PubMedCentralPubMedGoogle Scholar
  7. Castro AJ, Suárez C, Zienkiewicz K, Alché JD, Zienkiewicz A, Rodríguez-García MI (2013) Electrophoretic profiling and immunocytochemical detection of pectins and arabinogalactan proteins in olive pollen during germination and pollen tube growth. Ann Bot 112:503–513PubMedCentralPubMedGoogle Scholar
  8. Chen CG, Mau S-L, Clarke AE (1993) Nucleotide sequence and stylespecific expression of a novel proline-rich protein gene from Nicotiana alata. Plant Mol Biol 21:391–395PubMedGoogle Scholar
  9. Cheung AY, Wang H, Wu HM (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82:383–393PubMedGoogle Scholar
  10. Cheung AY, Wu HM, de Stilio V, Glaven R, Chen C, Wong E, Ogdahl J, Estavillo A (2000) Pollen-Pistil Interactions in Nicotiana tabacum. Ann Bot 85(Supplement A):29–37Google Scholar
  11. Chudzik B, Zarzyka B, Śnieżko R (2005) Immunodetection of arabinogalactan proteins in different types of plant ovules. Acta Biol Crac 47(1):139–146Google Scholar
  12. Clarke A, Gleeson P, Harrison S, Knox RB (1979) Pollen-stigma interactions: identification and characterization of surface components with recognition potential. Proc Natl Acad Sci 76(7):3358–3362PubMedCentralPubMedGoogle Scholar
  13. 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 hypocondriacus. Euphytica 133:171–178Google Scholar
  14. Coimbra S, Pereira LG (2012) Arabinogalactan proteins in Arabidopsis thaliana pollen development. In: Yelda Özden Çiftçi (ed) Transgenic plants—advances and limitations. ISBN: 978-953-51-0181-9, InTech. pp 329–352Google Scholar
  15. Coimbra S, Salema R (1997) Immunolocalization of arabinogalactan proteins in Amaranthus hypocondriacus L. ovules. Protoplasma 199:75–82Google Scholar
  16. Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG (2007) Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot 58:4027–4035PubMedGoogle Scholar
  17. Coimbra S, Jones BJ, Pereira LG (2008) Arabinogalactan proteins (AGPs) related to pollen tube guidance into the embryo sac in Arabidopsis. Plant Signal Behav 3:455–456PubMedCentralPubMedGoogle Scholar
  18. Coimbra S, Costa M, Jones B, Mendes MA, Pereira LG (2009) Pollen grain development is compromised in Arabidopsis agp6 agp11 null mutants. J Exp Bot 60(11):3133–3142PubMedCentralPubMedGoogle Scholar
  19. Coimbra S, Costa ML, Mendes MA, Pereira AM, Pinto J, Pereira LG (2010) Early germination of Arabidopsis pollen in a double null mutant for the arabinogalactan protein genes AGP6 and AGP11. Sex Plant Reprod 23:199–205PubMedGoogle Scholar
  20. Costa M, Nobre MS, Becker JD, Masiero S, Amorim MI, Pereira LG, Coimbra S (2013a) Expression-based and co-localization detection of Arabinogalactan protein 6 and Arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes. BMC Plant Biol 13:7PubMedCentralPubMedGoogle Scholar
  21. Costa M, Pereira AM, Rudall PJ, Coimbra S (2013b) Immunolocalization of arabinogalactan proteins (AGPs) in reproductive structures of an early-divergent angiosperm, Trithuria (Hydatellaceae). Ann Bot 111(2):183–190PubMedCentralPubMedGoogle Scholar
  22. Costa ML, Sobral R, Costa MMR, Amorim MI, Coimbra S (2014) Evaluation of the presence of arabinogalactan proteins and pectins during Quercus suber male gametogenesis. Ann Bot. doi: 10.1093/aob/mcu223 PubMedCentralGoogle Scholar
  23. Crawford BC, Yanofsky MF (2008) The formation and function of the female reproductive tract in flowering plants. Curr Biol 18:R972–R978PubMedGoogle Scholar
  24. Dardelle F, Lehner A, Ramdani Y, Bardor M, Lerouge P, Driouich A, Mollet J-C (2010) Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol 153:1563–1576PubMedCentralPubMedGoogle Scholar
  25. de Graaf BHJ, Knuiman BA, Derksen J, Mariani C (2003) Characterization and localization of the transmitting tissue-specific PELPIII proteins of Nicotiana tabacum. J Exp Bot 54(380):55–63PubMedGoogle Scholar
  26. Demesa-Arévalo E, Vielle-Calzada J-P (2013) The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis. Plant Cell 25(4):1274–1287PubMedCentralPubMedGoogle Scholar
  27. Dresselhaus T, Franklin-Tong N (2013) Male–female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6(4):1018–1036PubMedGoogle Scholar
  28. Drews GN, Yadegari N (2002) Development and function of the angiosperm female gametophyte. Annu Rev Genet 36:99–124PubMedGoogle Scholar
  29. Du H, Simpson RJ, Moritz RL, Clarke AE, Bacic A (1994) Isolation of the protein backbone of an arabinogalactan-protein from the styles of Nicotiana alata and characterization of a corresponding cDNA. Plant Cell 6(11):1643–1653PubMedCentralPubMedGoogle Scholar
  30. Du H, Simpson RJ, Clarke AE, Bacic A (1996) Molecular characterization of a stigma-specific gene encoding an arabinogalactan-protein (AGP) from Nicotiana alata. Plant J 9(3):313–323PubMedGoogle Scholar
  31. Eberle CA, Anderson NO, Clasen BM, Hegeman AD, Smith AG (2013) PELPIII: the class III pistil-specific extensin-like Nicotiana tabacum proteins are essential for interspecific incompatibility. Plant J 74:805–814PubMedGoogle Scholar
  32. El-Tantawy A-A, Solís M-T, Costa ML, Coimbra S, Risueño MC, Testillano PS (2013) Arabinogalactan protein profiles and distribution patterns during microspore embryogenesis and pollen development in Brassica napus. Plant Reprod 26:23–243Google Scholar
  33. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660PubMedGoogle Scholar
  34. FAO (2014) Food and nutrition in numbers 2014. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  35. Faure JE, Rotman N, Fortune P, Dumas C (2002) Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30:481–488PubMedGoogle Scholar
  36. Fragkostefanakis S, Dandachi F, Kalaitzis P (2012) Expression of arabinogalactan proteins during tomato fruit ripening and in response to mechanical wounding, hypoxia and anoxia. Plant Physiol Biochem 52:112–118PubMedGoogle Scholar
  37. Gane AM, Clarke AE, Bacic A (1995) Localisation and expression of arabinogalactan-proteins in the ovaries of Nicotiana alata Link and Otto. Sex Plant Reprod 8:278–282Google Scholar
  38. Gao M, Showalter AM (2000) Immunolocalization of LeAGP-1, a modular arabinogalactan-protein, reveals its developmentally regulated expression in tomato. Planta 210:865–874PubMedGoogle Scholar
  39. Gao M, Kieliszewski MJ, Lamport DTA, Showalter AM (1999) Isolation, characterization and immunolocalization of a novel, modular tomato arabinogalactan-protein corresponding to the LeAGP-1 gene. Plant J 18:4–55Google Scholar
  40. Gaspar Y, Johnson KL, McKenna JA, Bacic A, Schultz CJ (2001) The complex structures of arabinogalactan-proteins and the journey towards understanding function. Plant Mol Biol 47:161–176PubMedGoogle Scholar
  41. Gell AC, Bacic A, Clarke AE (1986) Arabinogalactan-proteins of the female sexual tissue of Nicotiana alata: I. Changes during flower development and pollination. Plant Physiol 82(4):885–889PubMedCentralPubMedGoogle Scholar
  42. Gleeson PA, Clarke AE (1980) Arabinogalactans of sexual and somatic tissues of Gladiolus and Lilium. Phytochemistry 19:1777–1782Google Scholar
  43. Goldman MHS, Pezotti M, Seurinck J, Mariani C (1992) Developmental expression of tobacco pistil-specific genes encoding novel extensin-like proteins. Plant Cell 4:104–1051Google Scholar
  44. Hancock CN, Kent L, McClurE BA (2005) The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716–723PubMedGoogle Scholar
  45. Higashiyama T (2014) Discovery of AMOR glycan for pollen tube guidance: microfluidics and synthetic chemistry approaches. 23rd International congress on sexual plant reproduction Porto 2014Google Scholar
  46. Hoggart RM, Clarke AE (1984) Arabinogalactans are common components of Angiosperm styles. Phytochemistry 23:1571–1573Google Scholar
  47. Jauh GY, Lord EM (1996) Localization of pectins and arabinogalactan-proteins in lily (Lilium longittorum L.) pollen tube and style, and their possible roles in pollination. Planta 199:251–261Google Scholar
  48. Johnson MA, Preuss D (2002) Plotting a course: multiple signals guide pollen tubes to their targets. Dev Cell 2:273–281PubMedGoogle Scholar
  49. Johnson KL, Jones BJ, Bacic A, Schultz CJ (2003) The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol 133:1911–1925PubMedCentralPubMedGoogle Scholar
  50. Kitazawa K, Tryfona T, Yoshimi Y, Hayashi Y, Kawauchi S, Antonov L, Tanaka H, Takahashi T, Kaneko S, Dupree P, Tsumuraya Y, Kotake T (2013) β-Galactosyl Yariv reagent binds to the β-1,3-galactan of arabinogalactan proteins. Plant Physiol 161(3):1117–1126PubMedCentralPubMedGoogle Scholar
  51. Lalanne E, Honys D, Johnson A, Borner GHH, Lilley KS, Dupree P, Grossniklaus U, Twell D (2004) SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell 16:229–240PubMedCentralPubMedGoogle Scholar
  52. Lamport DT, Várnai P (2012) Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol 197(1):58–64PubMedGoogle Scholar
  53. Lee CB, Swatek KN, McClure B (2008) Pollen proteins bind to the C-terminal domain of Nicotiana alata pistil Arabinogalactan proteins. J Biol Chem 283:26965–26973PubMedGoogle Scholar
  54. Lee CB, Kim S, McClure B (2009) A pollen protein, NaPCCP, that binds pistil Arabinogalactan proteins also binds phosphatidylinositol 3-phosphate and associates with the pollen tube endomembrane system. Plant Physiol 149:791–802PubMedCentralPubMedGoogle Scholar
  55. 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 11:49–59Google Scholar
  56. Levitin B, Richter D, Markovich I, Zik M (2008) Arabinogalactan proteins 6 and 11 are required for stamen and pollen function in Arabidopsis. Plant J 56:351–363PubMedGoogle Scholar
  57. Li J, Yu M, Geng L-L, Zhao J (2010) The fasciclin-like arabinogalactan protein gene, FLA3, is involved in microspore development of Arabidopsis. Plant J 64:482–497PubMedGoogle Scholar
  58. Lind JL, Bacic A, Clarke AE, Anderson MA (1994) A style-specific hydroxyproline-rich glycoprotein with properties of both extensins and arabinogalactan proteins. Plant J 6:491–502PubMedGoogle Scholar
  59. Lind JL, Bonig I, Clarke AE, Anderson MA (1996) A style-specific 120 kDa glycoprotein enters pollen tubes of Nicotiana alata in vivo. Sex Plant Reprod 9:75–86Google Scholar
  60. Lindner H, Müller LM, Boisson-Dernier A, Grossniklaus U (2012) CrRLK1L receptor-like kinases: not just another brick in the wall. Curr Opin Plant Biol 15(6):659–669PubMedGoogle Scholar
  61. Lord EM (2002) Adhesion and guidance in compatible pollination. J Exp Bot 54(380):47–54Google Scholar
  62. Losada JM, Herrero M (2012) Arabinogalactan-protein secretion is associated with the acquisition of stigmatic receptivity in the apple flower. Ann Bot 110(3):573–584PubMedCentralPubMedGoogle Scholar
  63. Losada JM, Herrero M (2014) Glycoprotein composition along the pistil of Malus x domestica and the modulation of pollen tube growth. BMC Plant Biol 14:1PubMedCentralPubMedGoogle Scholar
  64. Ma H, Sundaresan V (2010) Development of flowering plants gametophytes. Curr Top Dev Biol 91:379–412PubMedGoogle Scholar
  65. Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–9PubMedCentralPubMedGoogle Scholar
  66. Nguema-Ona E, Coimbra S, Vicré-Gibouin M, Mollet J-C, Driouich A (2012) Arabinogalactan proteins in root and pollen-tube cells: distribution and functional aspects. Ann Bot 110(2):383–404PubMedCentralPubMedGoogle Scholar
  67. Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174:195–291PubMedGoogle Scholar
  68. Palanivelu R, Tsukamoto T (2012) Pathfinding in angiosperm reproduction: pollen tube guidance by pistils ensures successful double fertilization. WIREs Dev Biol 1:96–113Google Scholar
  69. Peng Y-B, Zou C, Gong H-Q, Bai S-N, Xu Z-H, Li Y-Q (2005) Immunolocalization of Arabinogalactan proteins and pectins in floral buds of Cucumber (Cucumis sativus L.) during sex determination. J Integr Plant Biol 47(2):194–200Google Scholar
  70. Pennell RI, Roberts K (1990) Sexual development in the pea is presaged by altered expression of Arabinogalactan protein. Nature 344:547–549Google Scholar
  71. Pennell RI, Knox JP, Scofield GN, Selvendran RR, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108:1967–1977PubMedGoogle Scholar
  72. Pennell RI, Janniche L, Kjellbom P, Scofield GN, Peart JM, Roberts K (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3(12):1317–1326PubMedCentralPubMedGoogle Scholar
  73. Pereira LG, Coimbra S, Oliveira H, Monteiro L, Sottomayor M (2006) Expression of Arabinogalactan protein genes in pollen tubes of Arabidopsis thaliana. Planta 223:374–380PubMedGoogle Scholar
  74. Pereira LG, Costa M, Coimbra S (2013) Localization of arabinogalactan protein 6 fused with Sirius ultramarine fluorescent protein in Arabidopsis pollen and pollen tubes. Plant Signal Behav 8(10):e25998. doi: 10.4161/psb.25998 PubMedCentralPubMedGoogle Scholar
  75. Pereira AM, Masiero S, Nobre MS, Costa ML, Solís M-T, Testillano PS, Sprunck S, Coimbra S (2014) Differential expression patterns of Arabinogalactan proteins in Arabidopsis thaliana reproductive tissues. J Exp Bot 65(18):5459–5471PubMedGoogle Scholar
  76. Pina C, Pinto F, Feijó J, Becker J (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756PubMedCentralPubMedGoogle Scholar
  77. Qin Y, Zhao J (1996) Localization of arabinogalactan proteins in egg cells, zygotes, and two-celled proembryos and effects of b-d-glucosyl Yariv reagent on egg cell fertilization and zygote division in Nicotiana tabacum L. J Exp Bot 57(9):2061–2074Google Scholar
  78. Rafińska K, Bednarska E (2011) Localisation pattern of homogalacturonan and Arabinogalactan proteins in developing ovules of the gymnosperm plant Larix decidua Mill. Sex Plant Reprod 24:75–87PubMedGoogle Scholar
  79. Ray S, Park S-S, Ray A (1997) Pollen tube guidance by the female gametophyte. Development 124:2489–2498PubMedGoogle Scholar
  80. Schneitz K, Hülskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7(5):731–749Google Scholar
  81. Schultz CJ, Hauser K, Lind JL, Arkinson AH, Pu ZY, Anderson MA, Clarke AE (1997) Molecular characterization of a cDNA sequence encoding the backbone of a style-specific 120 kDa glycoprotein which has features of both extensins and arabinogalactan proteins. Plant Mol Biol 35:833–845PubMedGoogle Scholar
  82. Schultz C, Gilson P, Oxley D, Youl J, Bacic A (1998) GPI-anchors on Arabinogalactan proteins: implications for signalling in plants. Trends Plant Sci 3(11):1360–1385Google Scholar
  83. Schultz CJ, Johnson KL, Currie G, Bacic A (2000) The classical arabinogalactan protein gene family of Arabidopsis. Plant Cell 12:1751–1767PubMedCentralPubMedGoogle Scholar
  84. Schultz CJ, Rumsewicz MP, Johnson KL, Jones BJ, Gaspar YM, Bacic A (2002) Using genomic resources to guide research directions: the arabinogalactan protein gene family as a test case. Plant Physiol 129:1448–1463PubMedCentralPubMedGoogle Scholar
  85. Sedgley M, Blesing MA, Bonig I, Anderson MA, Clarke AE (1985) Arabinogalactan-proteins are localized extracellularly in the transmitting tissue of Nicotiana alata link and otto, an ornamental tobacco. Micron Microsc Acta 16:247–254Google Scholar
  86. Seifert GJ, Roberts K (2007) The biology of Arabinogalactan proteins. Annu Rev Plant Biol 58:137–161PubMedGoogle Scholar
  87. Shimizu KK, Okada K (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127:4511–4518PubMedGoogle Scholar
  88. Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417PubMedGoogle Scholar
  89. Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol 153:485–513PubMedCentralPubMedGoogle Scholar
  90. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedCentralPubMedGoogle Scholar
  91. Sommer-Knudsen J, Clarke AE, Bacic A (1996) A galactose-rich, cellwall glycoprotein from styles of Nicotiana alata. Plant J 9:71–83PubMedGoogle Scholar
  92. Suárez C, Zienkiewicz A, Castro AJ, Zienkiewicz K, Majewska-Sawka A, Rodríguez-García MI (2013) Cellular localization and levels of pectins and Arabinogalactan proteins in olive (Olea europaea L.) pistil tissues during development: implications for pollen–pistil interaction. Planta 237:305–319PubMedGoogle Scholar
  93. Sun W, Kieliszewski MJ, Showalter AM (2004) Overexpression of tomato LeAGP-1 arabinogalactan-protein promotes lateral branching and hampers reproductive development. Plant J 40:870–881PubMedGoogle Scholar
  94. Tan H, Liang W, Hu J, Zhang D (2012) MTR1 encodes a secretory fasciclin glycoprotein required for male reproductive development in rice. Dev Cell 22(6):1127–1137PubMedGoogle Scholar
  95. Tucker MR, Koltunow AMJ (2014) Traffic monitors at the cell periphery: the role of cell walls during early female reproductive cell differentiation in plants. Curr Opin Plant Biol 17:137–145PubMedGoogle Scholar
  96. Tucker MR, Okada T, Hu Y, Scholefield A, Taylor JM, Koltunow AMJ (2012) Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139:1399–1404PubMedGoogle Scholar
  97. Twomey MC, Brooks JK, Corey JM, Singh-Cundy A (2013) Characterization of PhPRP1, a histidine domain arabinogalactan protein from Petunia hybrida pistils. J Plant Physiol 170:1384–1388PubMedGoogle Scholar
  98. van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, Van Kammen A, de Vries SC (2001) N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol 125:1880–1890PubMedCentralPubMedGoogle Scholar
  99. Webb MC, Williams EG (1988) The pollen tube pathway in the pistil of Lycopersicon peruvianum. Ann Bot 61:415–423Google Scholar
  100. 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(3):395–403PubMedGoogle Scholar
  101. Wu H, Wong E, Ogdahl J, Cheung AY (2000) A pollen tube growth-promoting arabinogalactan protein from Nicotiana alata is similar to the tobacco TTS protein. Plant J 22:165–176PubMedGoogle Scholar
  102. Yang J, Sardar HS, McGovern KR, Zhang Y, Showalter AM (2007) A lysine-rich arabinogalactan protein in Arabidopsis is essential for plant growth and development, including cell division and expansion. Plant J 49:629–640PubMedGoogle Scholar
  103. Yariv J, Lis H, Katchalski E (1967) Precipitation of arabic acid and some seed polysaccharides by glycosylphenylazo dyes. Biochem J 105(1):1C–2CPubMedCentralPubMedGoogle Scholar
  104. Yates EA, Valdor J-F, Haslam SM et al (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiol 6:131–139Google Scholar
  105. Zhao Y, Yan A, Feijó JA, Furutani M, Takenawa T, Hwang I, Fu Y, Yang Z (2010) Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco. Plant Cell 22(12):4031–4044PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ana Marta Pereira
    • 1
    • 2
  • Luís Gustavo Pereira
    • 1
    • 2
  • Sílvia Coimbra
    • 1
    • 2
    Email author
  1. 1.Departamento de Biologia, Faculdade de CiênciasUniversidade do PortoPortoPortugal
  2. 2.Biosystems and Integrative Sciences Institute (BioISI)PortoPortugal

Personalised recommendations