Type II arabinogalactans initiated by hydroxyproline-O-galactosyltransferases play important roles in pollen-pistil interactions.
Arabidopsis
arabinogalactan proteins
galactosyltransferases
ovule development
plant reproduction
pollen-pistil interactions
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
10
08
2022
accepted:
01
02
2023
medline:
11
4
2023
pubmed:
14
2
2023
entrez:
13
2
2023
Statut:
ppublish
Résumé
Arabinogalactan-proteins (AGPs) are hydroxyproline-rich glycoproteins containing a high sugar content and are widely distributed in the plant kingdom. AGPs have long been suggested to play important roles in sexual plant reproduction. The synthesis of their complex carbohydrates is initiated by a family of hydroxyproline galactosyltransferase (Hyp-GALT) enzymes which add the first galactose to Hyp residues in the protein backbone. Eight Hyp-GALT enzymes have been identified so far, and in the present work a mutant affecting five of these enzymes (galt2galt5galt7galt8galt9) was analyzed regarding the reproductive process. The galt25789 mutant presented a low seed set, and reciprocal crosses indicated a significant female gametophytic contribution to this mutant phenotype. Mutant ovules revealed abnormal callose accumulation inside the embryo sac and integument defects at the micropylar region culminating in defects in pollen tube reception. In addition, immunolocalization and biochemical analyses allowed the detection of a reduction in the amount of glucuronic acid in mutant ovary AGPs. Dramatically low amounts of high-molecular-weight Hyp-O-glycosides obtained following size exclusion chromatography of base-hydrolyzed mutant AGPs compared to the wild type indicated the presence of underglycosylated AGPs in the galt25789 mutant, while the monosaccharide composition of these Hyp-O-glycosides displayed no significant changes compared to the wild-type Hyp-O-glycosides. The present work demonstrates the functional importance of the carbohydrate moieties of AGPs in ovule development and pollen-pistil interactions.
Substances chimiques
arabinogalactan
SL4SX1O487
Hydroxyproline
RMB44WO89X
Galactosyltransferases
EC 2.4.1.-
Plant Proteins
0
Mucoproteins
0
Glycosides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
371-389Informations de copyright
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
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, 2614-2628.
Ajayi, O.O., Held, M.A. & Showalter, A.M. (2021) Three β-glucuronosyltransferase genes involved in arabinogalactan biosynthesis function in arabidopsis growth and development. Plants, 10, 1172.
Aloisi, I., Cai, G., Faleri, C., Navazio, L., Serafini-Fracassini, D. & del Duca, S. (2017) Spermine regulates pollen tube growth by modulating Ca2+-dependent Actin organization and cell wall structure. Frontiers in Plant Science, 8, 1701.
Basu, D., Liang, Y., Liu, X., Himmeldirk, K., Faik, A., Kieliszewski, M. et al. (2013) Functional identification of a hydroxyproline-O-galactosyltransferase specific for arabinogalactan protein biosynthesis in arabidopsis. Journal of Biological Chemistry, 288, 10132-10143.
Basu, D., Tian, L., Wang, W., Bobbs, S., Herock, H., Travers, A. et al. (2015) A small multigene hydroxyproline-O-galactosyltransferase family functions in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. BMC Plant Biology, 15, 295.
Basu, D., Wang, W., Ma, S., DeBrosse, T., Poirier, E., Emch, K. et al. (2015) Two hydroxyproline galactosyltransferases, GALT5 and GALT2, function in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. PLoS One, 10, e0125624.
Beihammer, G., Maresch, D., Altmann, F. & Strasser, R. (2020) Glycosylphosphatidylinositol-anchor synthesis in plants: a glycobiology perspective. Frontiers in Plant Science, 11, 611188.
Borner, G.H.H., Lilley, K.S., Stevens, T.J. & Dupree, P. (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiology, 132, 568-577.
Brambilla, V., Battaglia, R., Colombo, M., Masiero, S., Bencivenga, S., Kater, M.M. et al. (2007) Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell, 19, 2544-2556.
Chaudhary, A., Gao, J. & Schneitz, K. (2018) The genetic control of ovule development. In Reference Module in Life Sciences (pp. 1-10). https://doi.org/10.1016/B978-0-12-809633-8.20737-1
Chávez Montes, R.A., Ranocha, P., Martinez, Y., Minic, Z., Jouanin, L., Marquis, M. et al. (2008) Cell Wall modifications in Arabidopsis plants with altered α-L-Arabinofuranosidase activity. Plant Physiology, 147, 63-77.
Coimbra, S., Almeida, J., Junqueira, V., Costa, M.L. & Pereira, L.G. (2007) Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. Journal of Experimental Botany, 58, 4027-4035.
Coimbra, S., Costa, M., Jones, B., Mendes, M.A. & Pereira, L.G. (2009) Pollen grain development is compromised in Arabidopsis agp6 agp11 null mutants. Journal of Experimental Botany, 60, 3133-3142.
Costa, M., Nobre, M.S., Becker, J.D., Masiero, S., Amorim, M.I., Pereira, L.G. et al. (2013) Expression-based and co-localization detection of arabinogalactan protein 6 and arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes. BMC Plant Biology, 13, 7.
Demesa-Arévalo, E. & Vielle-Calzada, J.P. (2013) The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis. Plant Cell, 25, 1274-1287.
Denninger, P., Bleckmann, A., Lausser, A., Vogler, F., Ott, T., Ehrhardt, D.W. et al. (2014) Male-female communication triggers calcium signatures during fertilization in Arabidopsis. Nature Communications, 5, 4645.
Dresselhaus, T., Sprunck, S. & Wessel, G.M. (2016) Fertilization mechanisms in flowering plants. Current Biology, 26, R125-R139.
Duan, Q., Liu, M.C.J., Kita, D., Jordan, S.S., Yeh, F.L.J., Yvon, R. et al. (2020) FERONIA controls pectin- and nitric oxide-mediated male-female interaction. Nature, 579, 561-566.
Duchow, S., Dahlke, R.I., Geske, T., Blaschek, W. & Classen, B. (2016) Arabinogalactan-proteins stimulate somatic embryogenesis and plant propagation of Pelargonium sidoides. Carbohydrate Polymers, 152, 149-155.
Ellis, M., Egelund, J., Schultz, C.J. & Bacic, A. (2010) Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiology, 153, 403-419.
Escobar-Restrepo, J.M., Huck, N., Kessler, S., Gagliardini, V., Gheyselinck, J., Yang, W.C. et al. (2007) The Feronia receptor-like kinase mediates male-female interactions during pollen tube reception. Science, 1979, 317-660.
Eudes, A., Mouille, G., Thevenin, J., Goyallon, A., Minic, Z. & Jouanin, L. (2008) Purification, cloning and functional characterization of an endogenous beta-glucuronidase in Arabidopsis thaliana. Plant & Cell Physiology, 49, 1331-1341.
Fincher, G.B., Stone, B.A. & Clarke, A.E. (1983) Arabinogalactan-proteins: structure, biosynthesis, and function. Annual Review of Plant Physiology, 34(1), 47-70.
Galindo-Trigo, S., Blanco-Touriñán, N., DeFalco, T.A., Wells, E.S., Gray, J.E., Zipfel, C. et al. (2020) Cr RLK 1L receptor-like kinases HERK 1 and ANJEA are female determinants of pollen tube reception. EMBO Reports, 21, e48466.
Ge, L.L., Tian, H.Q. & Russell, S.D. (2007) Calcium function and distribution during fertilization in angiosperms. American Journal of Botany, 94, 1046-1060.
Hamamura, Y., Nishimaki, M., Takeuchi, H., Geitmann, A., Kurihara, D. & Higashiyama, T. (2014) Live imaging of calcium spikes during double fertilization in Arabidopsis. Nature Communications, 5(1).
Higashiyama, T. & Takeuchi, H. (2015) The mechanism and key molecules involved in pollen tube guidance. Annual Review of Plant Biology, 66, 393-413.
Hijazi, M., Velasquez, S.M., Jamet, E., Estevez, J.M. & Albenne, C. (2014) An update on post-translational modifications of hydroxyproline-rich glycoproteins: toward a model highlighting their contribution to plant cell wall architecture. Frontiers in Plant Science, 5, 395.
Hou, Y., Guo, X., Cyprys, P., Zhang, Y., Bleckmann, A., Cai, L. et al. (2016) Maternal ENODLs are required for pollen tube reception in Arabidopsis. Current Biology, 26, 2343-2350.
Huck, N., Moore, J.M., Federer, M. & Grossniklaus, U. (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube receptor. Development, 130, 2149-2159.
Imaizumi, C., Tomatsu, H., Kitazawa, K., Yoshimi, Y., Shibano, S., Kikuchi, K. et al. (2017) Heterologous expression and characterization of an Arabidopsis β-l-arabinopyranosidase and α-d-galactosidases acting on β-l-arabinopyranosyl residues. Journal of Experimental Botany, 68, 4651-4661.
Iwano, M., Entani, T., Shiba, H., Takayama, S. & Isogai, A. (2004) Calcium crystals in the anther of petunia: the existence and biological significance in the pollination process. Plant & Cell Physiology, 45, 40-47.
Iwano, M., Ngo, Q.A., Entani, T., Shiba, H., Nagai, T., Miyawaki, A. et al. (2012) Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells. Development, 139, 4202-4209.
Jiao, J., Mizukami, A.G., Sankaranarayanan, S., Yamguchi, J., Itami, K. & Higashiyama, T. (2016) Structure-activity relation of AMOR sugar molecule that activates pollen-tubes for ovular guidance. Plant Physiology, 173(1), 354-363.
Kaur, D., Held, M.A., Smith, M.R. & Showalter, A.M. (2021) Functional characterization of hydroxyproline-O-galactosyltransferases for Arabidopsis arabinogalactan-protein synthesis. BMC Plant Biology, 21, 590.
Kaur, D., Moreira, D., Coimbra, S. & Showalter, A.M. (2022) Hydroxyproline-O-galactosyltransferases synthesizing type II arabinogalactans are essential for male gametophytic development in Arabidopsis. Frontiers in Plant Science, 13, 935413.
Kim, M.-J., Jeon, B.W., Oh, E., Seo, P.J. & Kim, J. (2021) Peptide signaling during plant reproduction. Trends in Plant Science, 26, 822-835.
Kitazawa, K., Tryfona, T., Yoshimi, Y., Hayashi, Y., Kawauchi, S., Antonov, L. et al. (2013) β-Galactosyl Yariv reagent binds to the β-1,3-Galactan of arabinogalactan proteins. Plant Physiology, 161, 1117-1126.
Knox, J.P., Linstead, P.J., Cooper, J.P.C. & Roberts, K. (1991) Developmentally regulated epitopes of cell surface arabinogalactan proteins and their relation to root tissue pattern formation. The Plant Journal, 1, 317-326.
Kotake, T., Yamanashi, Y., Imaizumi, C. & Tsumuraya, Y. (2016) Metabolism of l-arabinose in plants. Journal of Plant Research, 129, 781-792.
Lamport, D.T.A. & Miller, D.H. (1971) Hydroxyproline arabinosides in the plant kingdom. Plant Physiology, 48(4), 454-456.
Lamport, D.T.A., Tan, L., Held, M.A. & Kieliszewski, M.J. (2018) Pollen tube growth and guidance: Occam's razor sharpened on a molecular arabinogalactan glycoprotein Rosetta stone. New Phytologist, 217, 491-500.
Lamport, D.T.A., Tan, L. & Kieliszewski, M.J. (2021) A molecular pinball machine of the plasma membrane regulates plant growth-a new paradigm. Cell, 10, 1935.
Levitin, B., Richter, D., Markovich, I. & Zik, M. (2008) Arabinogalactan proteins 6 and 11 are required for stamen and pollen function in Arabidopsis. The Plant Journal, 56, 351-363 Available at: https://pubmed.ncbi.nlm.nih.gov/18644001/ [Accessed January 7, 2022]
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 Journal, 64, 482-497.
Li, L. & Sheen, J. (2016) Dynamic and diverse sugar signaling. Current Opinion in Plant Biology, 33, 116-125.
Liu, X., Adhikari, P.B. & Kasahara, R.D. (2019) Pollen tube contents from failed fertilization contribute to seed coat initiation in Arabidopsis. F1000Res, 8, 348. Available at: https://pubmed.ncbi.nlm.nih.gov/31031972/ [Accessed July 21, 2022]
Liu, X., Castro, C., Wang, Y., Noble, J., Ponvert, N., Bundy, M. et al. (2016) The role of LORELEI in pollen tube reception at the interface of the synergid cell and pollen tube requires the modified eight-cysteine motif and the receptor-like kinase FERONIA. Plant Cell, 28, 1035-1052.
Lopes, A.L., Moreira, D., Ferreira, M.J., Pereira, A.M. & Coimbra, S. (2019) Insights into secrets along the pollen tube pathway in need to be discovered. Journal of Experimental Botany, 70, 2979-2992.
Lopez-Hernandez, F., Tryfona, T., Rizza, A., Yu, X.L., Harris, M.O.B., Webb, A.A.R. et al. (2020) Calcium binding by arabinogalactan polysaccharides is important for normal plant development. Plant Cell, 32, 3346-3369.
Lora, J., Laux, T. & Hormaza, J.I. (2019) The role of the integuments in pollen tube guidance in flowering plants. New Phytologist, 221, 1074-1089.
Ma, X., Wu, Y. & Zhang, G. (2021) Formation pattern and regulatory mechanisms of pollen wall in Arabidopsis. Journal of Plant Physiology, 260, 153388.
Maruyama, D., Völz, R., Takeuchi, H., Mori, T., Igawa, T., Kurihara, D. et al. (2015) Rapid elimination of the persistent Synergid through a cell fusion mechanism. Cell, 161, 907-918.
Mizukami, A.G., Inatsugi, R., Jiao, J., Kotake, T., Kuwata, K., Ootani, K. et al. (2016) The AMOR arabinogalactan sugar chain induces pollen-tube competency to respond to ovular guidance. Current Biology, 26, 1091-1097.
Moreira, D., Lopes, A.L., Silva, J., Ferreira, M.J., Pinto, S.C., Mendes, S. et al. (2022) New insights on the expression patterns of specific arabinogalactan proteins in reproductive tissues of Arabidopsis thaliana. Frontiers in Plant Science, 13, 1083098.
Newbigin, E., Bacic, A. & Read, S. (2009) Callose and its role in pollen and embryo sac development in flowering plants. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides, 465-498.
Nguema-Ona, E., Vicré-Gibouin, M., Gotté, M., Plancot, B., Lerouge, P., Bardor, M. et al. (2014) Cell wall O-glycoproteins and N-glycoproteins: aspects of biosynthesis and function. Frontiers in Plant Science, 5, 499.
Nibbering, P., Petersen, B.L., Motawia, M.S., Jørgensen, B., Ulvskov, P. & Niittylä, T. (2020) Golgi-localized exo-β1,3-galactosidases involved in cell expansion and root growth in Arabidopsis. Journal of Biological Chemistry, 295, 10581-10592.
Nothnagel, E.A. (1997) Proteoglycans and related components in plant cells. International Review of Cytology, 195-291.
Ogawa-Ohnishi, M. & Matsubayashi, Y. (2015) Identification of three potent hydroxyproline O-galactosyltransferases in Arabidopsis. Plant Journal, 81, 736-746.
Pennell, R.I., Janniche, L., Kjellbom, P., Scofield, G.N., Peart, J.M. & Roberts, K. (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. The Plant Cell, 3, 1317-1326.
Pereira, A.M., Masiero, S., Nobre, M.S., Costa, M.L., Solís, M.T., Testillano, P.S. et al. (2014) Differential expression patterns of arabinogalactan proteins in Arabidopsis thaliana reproductive tissues. Journal of Experimental Botany, 65, 5459-5471.
Pereira, A.M., Moreira, D., Coimbra, S. & Masiero, S. (2021) Paving the way for fertilization: the role of the transmitting tract. International Journal of Molecular Sciences, 22, 2603.
Pereira, A.M., Pereira, L.G. & Coimbra, S. (2015) Arabinogalactan proteins: rising attention from plant biologists. Plant Reproduction, 28, 1-15.
Pereira, A.M., Lopes, A.L. & Coimbra, S. (2016) Arabinogalactan proteins as interactors along the crosstalk between the pollen tube and the female tissues. Frontiers in Plant Science, 7, 1895.
Pereira, A.M., Nobre, M.S., Pinto, S.C., Lopes, A.L., Costa, M.L., Masiero, S. et al. (2016) “Love is strong, and You're so sweet”: JAGGER is essential for persistent Synergid degeneration and Polytubey block in Arabidopsis thaliana. Molecular Plant, 9, e1209616.
Přerovská, T., Pavlů, A., Hancharyk, D., Rodionova, A., Vavříková, A. & Spiwok, V. (2021) Structural basis of the function of Yariv reagent-an important tool to study arabinogalactan proteins. Frontiers in Molecular Biosciences, 8, 682858.
Ray, S., Park, S.S. & Ray, A. (1997) Pollen tube guidance by the female gametophyte. Development, 124, 2489-2498.
Rivas-Sendra, A., Calabuig-Serna, A. & Seguí-Simarro, J.M. (2017) Dynamics of calcium during In vitro microspore embryogenesis and In vivo microspore development in Brassica napus and Solanum melongena. Frontiers in Plant Science, 8, 1177.
Robichaux, K.J. & Wallace, I.S. (2021) Signaling at physical barriers during pollen-pistil interactions. International Journal of Molecular Sciences, 22, 12230.
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675.
Schultz, C.J., Rumsewicz, M.P., Johnson, K.L., Jones, B.J., Gaspar, Y.M. & Bacic, A. (2002) Using genomic resources to guide research directions. The arabinogalactan protein gene family as a test case. Plant Physiology, 129, 1448-1463.
Shimizu, K.K. & Okada, K. (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development, 127, 4511-4518.
Showalter, A.M. (2001) Arabinogalactan-proteins: structure, expression and function. Cellular and Molecular Life Sciences, 58(10), 1399-1417.
Showalter, A.M. & Basu, D. (2016) Extensin and arabinogalactan-protein biosynthesis: glycosyltransferases, research challenges, and biosensors. Frontiers in Plant Science, 7, 814.
Showalter, A.M., Keppler, B., Lichtenberg, J., Gu, D. & Welch, L.R. (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiology, 153(2), 485-513.
Silva, J., Ferraz, R., Dupree, P., Showalter, A.M. & Coimbra, S. (2020) Three decades of advances in arabinogalactan-protein biosynthesis. Frontiers in Plant Science, 11, 610377.
Smallwood, M., Yates, E.A., Willats, W.G.T., Martin, H. & Knox, J.P. (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta, 198, 452-459.
Smyth, D.R., Bowman, J.L. & Meyerowitz, E.M. (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767.
Steinhorst, L. & Kudla, J. (2013) Calcium and reactive oxygen species rule the waves of signaling. Plant Physiology, 163, 471-485.
Takeuchi, H. & Higashiyama, T. (2016) Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature, 531, 245-248.
Tan, H., Liang, W., Hu, J. & Zhang, D. (2012) MTR1 encodes a secretory Fasciclin glycoprotein required for male reproductive development in Rice. Developmental Cell, 22, 1127-1137.
Tan, L., Eberhard, S., Pattathil, S., Warder, C., Glushka, J., Yuan, C. et al. (2013) An arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell, 25, 270-287.
Tsumuraya, Y., Ogura, K., Hashimoto, Y., Mukoyama, H. & Yamamoto, S. (1988) Arabinogalactan-proteins from primary and mature roots of radish (Raphanus sativus L.). Plant Physiology, 86(1), 155-160.
Tucker, M.R. & Koltunow, A.M.G. (2014) Traffic monitors at the cell periphery: the role of cell walls during early female reproductive cell differentiation in plants. Current Opinion in Plant Biology, 17, 137-145.
Tucker, M.R., Okada, T., Hu, Y., Scholefield, A., Taylor, J.M. & Koltunow, A.M.G. (2012) Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in arabidopsis. Development, 139, 1399-1404.
Vishnyakova, M.A. (1991) Callose as an indicator of sterile ovules. Phytomorphology, 41, 245-252.
Winnicki, K. (2020) The winner takes it all: auxin-the Main player during plant embryogenesis. Cell, 9, 606.
Zhang, Y., Held, M.A., Kaur, D. & Showalter, A.M. (2021) CRISPR-Cas9 multiplex genome editing of the hydroxyproline-O-galactosyltransferase gene family alters arabinogalactan-protein glycosylation and function in Arabidopsis. BMC Plant Biology, 21, 16.
Zheng, R., Su, S., Xiao, H. & Tian, H. (2019) Calcium: a critical factor in pollen germination and tube elongation. International Journal of Molecular Sciences, 20, 420.
Zhou, H.C., Jin, L., Li, J. & Wang, X.J. (2016) Altered callose deposition during embryo sac formation of multi-pistil mutant (mp1) in Medicago sativa. Genetics and Molecular Research, 15, gmr.15027968.
Zhou, K. (2019) Glycosylphosphatidylinositol-anchored proteins in Arabidopsis and one of their common roles in signaling transduction. Frontiers in Plant Science, 10, 1022.
Zhou, L.z. & Dresselhaus, T. (2019) Friend or foe: signaling mechanisms during double fertilization in flowering seed plants. Current Topics in Developmental Biology, 131, 453-496.