Arabinogalactan proteins as interactors along the crosstalk between the pollen tube and the female tissues

Frontiers in Plant Science

Volumn 7, Issue DECEMBER2016, 2016, Pages

  Pereira, Ana M ^a,b   Lopes, Ana L ^a,b   Coimbra, Sílvia ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b Biosystems and Integrative Sciences Institute (BioISI)   (Portugal)

Author keywords

Arabinogalactan proteins; Double fertilization; Plant reproduction; Pollen tube guidance; Signaling

Indexed keywords

EID: 85007367561     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01895     Document Type: Article

References (151)

1. Acosta-García, G., and Vielle-Calzada, J.-P. (2004). A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16, 2614–2628. doi: 10.1105/tpc.104. 024588
2. Alandete-Saez, M., Ron, M., and McCormick, S. (2008). GEX3, expressed in the male gametophyte and in the egg cell of Arabidopsis thaliana, is essential for micropylar pollen tube guidance and plays a role during early embryogenesis. Mol. Plant. 1, 586–598. doi: 10.1093/mp/ssn015
3. Amien, S., Kliwer, I., Marton, M. L., Debener, T., Geiger, D., Becker, D., et al. (2010). Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS Biol. 8:e1000388. doi: 10.1371/journal.pbio.1000388
4. 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. J. Biol. Chem. 288, 10132–10143. doi: 10.1074/jbc.M112.432609
5. Basu, D., Tian, L., Wang, W., Bobbs, S., Herock, H., Travers, A., et al. (2015a). A small multigene hydroxyproline-O-galactosyltransferase family functions in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. BMC Plant Biol. 15:295. doi: 10.1186/s12870-015-0670-7
6. Basu, D., Wang, W., Ma, S., DeBrosse, T., Poirier, E., Emch, K., et al. (2015b). Two hydroxyproline galactosyltransferases, GALT5 and GALT2, function in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. PLoS ONE 10:e0125624. doi: 10.1371/journal.pone.0125624
7. Beale, K. M., and Johnson, M. A. (2013). Speed dating, rejection, and finding the perfect mate: advice from flowering plants. Curr. Opin. Plant Biol. 16, 590–597. doi: 10.1016/j.pbi.2013.08.005
8. Bircheneder, S., and Dresselhaus, T. (2016). Why cellular communication during plant reproduction is particularly mediated by CRP signalling. J. Exp. Bot. 67, 4849–4861. doi: 10.1093/jxb/erw271
9. Bleckmann, A., Alter, S., and Dresselhaus, T. (2014). The beginning of a seed: regulatory mechanisms of double fertilization. Front. Plant Sci. 11:452. doi: 10.3389/fpls.2014.00452
10. Boavida, L. C., Borges, F., Becker, J. D., and Feijó, J. A. (2011). Whole genome analysis of gene expression reveals coordinated activation of signaling and metabolic pathways during pollen-pistil interactions in Arabidopsis. Plant Physiol. 155, 2066–2080. doi: 10.1104/pp.110.169813
11. Boisson-Dernier, A., Frietsch, S., Kim, T.-H., Dizon, M. B., and Schroeder, J. I. (2008). The peroxin loss-of-function mutation abstinence by mutual consent disrupts male-female gametophyte recognition. Curr. Biol. 18, 63–68. doi: 10.1016/j.cub.2007.11.067
12. Boisson-Dernier, A., Lituiev, D. S., Nestorova, A., Franck, C. M., Thirugnanarajah, S., and Grossniklaus, U. (2013). ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol. 11:e1001719. doi: 10.1371/journal.pbio. 1001719
13. Boisson-Dernier, A., Roy, S., Kritsas, K., Grobei, M. A., Jaciubek, M., Schroeder, J. I., et al. (2009). Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136, 3279–3288. doi: 10.1242/dev.040071
14. Borg, M., and Twell, D. (2010). Life after meiosis: patterning the angiosperm male gametophyte. Biochem. Soc. Trans. 38, 577–582. doi: 10.1042/ BST0380577
15. Borner, G. H. H., Lilley, K. S., Stevens, T. J., and Dupree, P. (2003). Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol. 132, 568–577.
16. Capron, A., Gourgues, M., Neiva, L. S., Faure, J. E., Berger, F., Pagnussat, G., et al. (2008). Maternal control of male- gamete delivery in Arabidopsis involves a putative GPI-anchored protein encoded by the LORELEI gene. Plant Cell 20, 3038–3049. doi: 10.1105/tpc.108.061713
17. Chapman, L. A., and Goring, D. R. (2010). Pollen-pistil interactions regulating successful fertilization in the Brassicaceae. J. Exp. Bot. 61, 1987–1999. doi: 10.1093/jxb/erq021
18. Chapman, L. A., and Goring, D. R. (2011). Misregulation of phosphoinositides in Arabidopsis thaliana decreases pollen hydration and maternal fertility. Sex. Plant Reprod. 24, 319–326. doi: 10.1007/s00497-011-0172-1
19. Chen, Y.-H., Li, H.-J., Shi, D.-Q., Yuan, L., Liu, J., Sreenivasan, R., et al. (2007). The central cell plays a critical role in pollen tube guidance in Arabidopsis. Plant Cell 19, 3563–3577. doi: 10.1105/tpc.107.053967
20. Cheung, A. Y., Wang, H., and Wu, H. M. (1995). A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82, 383–393. doi: 10.1016/0092-8674(95)90427-1
21. Cheung, A. Y., Wu, H. M., de Stilio, V., Glaven, R., Chen, C., Wong, E., et al. (2000). Pollen-pistil interactions in Nicotiana tabacum. Ann. Bot. 85(Suppl. A), 29–37. doi: 10.1006/anbo.1999.1016
22. Coimbra, S., Almeida, J., Junqueira, V., Costa, M. L., and Pereira, L. G. (2007). Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J. Exp. Bot. 58, 4027–4035. doi: 10.1093/jxb/erm259
23. Coimbra, S., and 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. doi: 10.1023/A:1025564920478
24. Coimbra, S., and Salema, R. (1997). Immunolocalization of arabinogalactan proteins in Amaranthus hypochondriacus L. ovules. Protoplasma 199, 75–82. doi: 10.1007/BF02539808
25. Costa, M., Pereira, A. M., Rudall, P. J., and Coimbra, S. (2013). Immunolocalization of arabinogalactan proteins (AGPs) in reproductive structures of an early-divergent angiosperm, Trithuria (Hydatellaceae). Ann. Bot. 111, 183–190. doi: 10.1093/aob/mcs256
26. Crawford, B., Ditta, G., and Yanofsky, M. (2007). The ntransmitting tract gene is required for transmitting- tract development in carpels of Arabidopsis thaliana. Curr. Biol. 17, 1101–1108. doi: 10.1016/j.cub.2007.05.079
27. Crawford, B. C., and Yanofsky, M. F. (2008). The formation and function of the female reproductive tract in flowering plants. Curr. Biol. 18, R972–R978. doi: 10.1016/j.cub.2008.08.010
28. Dardelle, F., Lehner, A., Ramdani, Y., Bardor, M., Lerouge, P., Driouich, A., et al. (2010). Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol. 153, 1563–1576. doi: 10.1104/pp.110.158881
29. de Graaf, B. H. J., Knuiman, B. A., Derksen, J., and Mariani, C. (2003). Characterization and localization of the transmittingtissue-specific PELPIII proteins of Nicotiana tabacum. J. Exp. Bot. 54, 55–63. doi: 10.1093/jxb/erg002
30. Demesa-Arévalo, E., and Vielle-Calzada, J.-P. (2013). The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis. Plant Cell. 25, 1274–1287. doi: 10.1105/tpc.112.106237
31. Denninger, P., Bleckmann, A., Lausser, A., Vogler, F., Ott, T., Ehrhardt, D., et al. (2014). Male-female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Commun. 5:4645. doi: 10.1038/ncomms5645
32. Dong, J., Kim, S. T., and Lord, E. M. (2005). Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol. 138, 778–789. doi: 10.1104/pp.105.063388
33. Doucet, J., Lee, H. K., and Goring, D. R. (2016). Pollen acceptance or rejection: a tale of two pathways. Trends Plant Sci. 21, 1058–1067. doi: 10.1016/j.tplants.2016.09.004
34. Dresselhaus, T., and Coimbra, S. (2016). Plant reproduction: AMOR enables males to respond to female signals. Curr. Biol. 26, R321–R323. doi: 10.1016/j.cub.2016.03.019
35. Dresselhaus, T., and Franklin-Tong, N. (2013). Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol. Plant. 6, 1018–1036. doi: 10.1093/mp/sst061
36. Dresselhaus, T., Sprunck, S., and Wessel, G. M. (2016). Fertilization mechanisms in flowering plants. Curr. Biol. 26, R125–R139. doi: 10.1016/j.cub.2015.12.032
37. Drews, G. N., Lee, D., and Christensen, C. A. (1998). Genetic analysis of the female gametophyte development and function. Plant Cell 10, 5–17. doi: 10.1105/tpc.10.1.5
38. 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 317, 656–660. doi: 10.1126/science.1143562
39. Faure, J. E., Rotman, N., Fortune, P., and Dumas, C. (2002). Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J. 30, 481–488. doi: 10.1046/j.1365-313X.2002.01305.x
40. Gleeson, P. A., and Clarke, A. E. (1980). Arabinogalactans of sexual and somatic tissues of Gladiolus and Lilium. Phytochemistry 19, 1777–1782. doi: 10.1016/ S0031-9422(00)83812-1
41. Gremski, K., Ditta, G., and Yanofsky, M. F. (2007). The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 134, 3593–3601. doi: 10.1242/dev.011510
42. Guan, Y., Lu, J., Xu, J., McClure, B., and Zhang, S. (2014). Two mitogen-activated protein kinases, MPK3 and MPK6, are required for funicular guidance of pollen tubes in Arabidopsis. Plant Physiol. 165, 528–533. doi: 10.1104/pp.113.231274
43. Hamamura, Y., Saito, C., Awai, C., Kurihara, D., Miyawaki, A., Nakagawa, T., et al. (2011). Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr. Biol. 21, 497–502. doi: 10.1016/j.cub.2011.02.013
44. Hao, L., Liu, J., Zhong, S., Gu, H., and Qu, L. J. (2016). AtVPS41-mediated endocytic pathway is essential for pollen tube-stigma interaction in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 113, 6307–6312. doi: 10.1073/pnas.1602757113
45. He, B., Xi, F., Zhang, X., Zhang, J., and Guo, W. (2007). Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J. 26, 4053–4065. doi: 10.1038/sj.emboj.7601834
46. Higashiyama, T., and Hamamura, Y. (2008). Gametophytic pollen tube guidance. Sex. Plant Reprod. 21, 17–26. doi: 10.1007/s00497-007-0064-6
47. Higashiyama, T., Kuroiwa, H., Kawano, S., and Kuroiwa, T. (1998). Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri. Plant Cell 10, 2019–2032. doi: 10.2307/3870781
48. Higashiyama, T., and Takeuchi, H. (2015). The mechanism and key molecules involved in pollen tube guidance. Annu. Rev. Plant Biol. 66, 393–413. doi: 10.1146/annurev-arplant-043014-115635
49. Higashiyama, T., Yabe, S., Sasaki, N., and Nishimura, Y. (2001). Pollen tube attraction by the synergid cell. Science 293, 1480–1483. doi: 10.1126/science.1062429
50. Hiscock, S. J., and Allen, A. M. (2008). Diverse cell signalling pathways regulate pollen-stigma interactions: the search for consensus. New Phytol. 179, 286–317. doi: 10.1111/j.1469-8137.2008.02457.x
51. Hoggart, R. M., and Clarke, A. E. (1984). Arabinogalactans are common components of Angiosperm styles. Phytochemistry 23, 1571–1573. doi: 10.1016/ S0031-9422(00)83441-X
52. 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. Curr. Biol. 26, 1–8. doi: 10.1016/j.cub.2016.06.053
53. Huang, B.-Q., and Russell, S. D. (1992). Female germ unit: organization, isolation, and function. Int. Rev. Cytol. 140, 233–292. doi: 10.1016/S0074-7696(08) 61099-2
54. Huck, N., Moore, J. M., Federer, M., and Grossniklaus, U. (2003). The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130, 2149–2159. doi: 10.1242/dev.00458
55. Hulskamp, M., Schneitz, K., and Pruitt, R. E. (1995). Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7, 57–64. doi: 10.1105/tpc.7.1.57
56. 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. doi: 10.1242/dev.081208
57. Iwano, M., Shiba, H., Miwa, T., Che, F. S., Takayama, S., Nagai, T., et al. (2004). Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol. 136, 3562–3571. doi: 10.1104/pp.104.046961
58. Jauh, G. Y., and Lord, E. M. (1996). Localization of pectins and arabinogalactan-proteins in lily (Lilium longittorum L.) pollen tube and style, and their possible roles in pollination. Planta 199, 251–261. doi: 10.1007/BF00196566
59. Johnson, M. A., and Preuss, D. (2002). Plotting a course: multiple signals guide pollen tubes to their targets. Dev. Cell 2, 273–281. doi: 10.1016/S1534-5807(02) 00130-2
60. Kasahara, R. D., Portereiko, M. F., Sandaklie-Nikolova, L., Rabiger, D. S., and Drews, G. N. (2005). MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17, 2981–2992. doi: 10.1105/tpc.105.034603
61. Kessler, S. A., Shimosato-Asano, H., Keinath, N. F., Wuest, S. E., Ingram, G., Panstruga, R., et al. (2010). Conserved molecular components for pollen tube reception and fungal invasion. Science 330, 968–971. doi: 10.1126/science.1195211
62. Kim, S., Mollet, J.-C., Dong, J., Zhang, K., Park, S.-Y., and Lord, E. M. (2003). Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc. Natl. Acad. Sci. U.S.A. 100, 16125–16130. doi: 10.1073/pnas.2533800100
63. 2+ flux capacitor. Ann. Bot. 114, 1069–1085. doi: 10.1093/aob/mcu161
64. Lamport, D. T., and Várnai, P. (2012). Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol. 197, 58–64. doi: 10.1111/nph.12005
65. Lennon, K. A., Roy, S., Hepler, P. K., and Lord, E. M. (1998). The structure of the transmitting tissue of Arabidopsis thaliana (L.) and the path of pollen tube growth. Sex. Plant Reprod. 11, 49–59. doi: 10.1007/s004970050120
66. Leshem, Y., Johnson, C., and Sundaresan, V. (2013). Pollen tube entry into the synergid cell of Arabidopsis is observed at a site distinct from the filiform apparatus. Plant Reprod. 26, 93–99. doi: 10.1007/s00497-013-0211-1
67. Li, C., Yeh, F. L., Cheung, A. Y., Duan, Q., Kita, D., Liu, M. C., et al. (2015). Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. Elife 4:e06587. doi: 10.7554/eLife.06587
68. Li, L., and Sheen, J. (2016). Dynamic and diverse sugar signaling. Curr. Opin. Plant Biol. 33, 116–125. doi: 10.1016/j.pbi.2016.06.018
69. Liang, Y., Tan, Z.-M., Zhu, L., Niu, Q.-K., Zhou, J.-J., Li, M., et al. (2013). MYB97, MYB101 and MYB120 function as male factors that control pollen tube- synergid interaction in Arabidopsis thaliana fertilization. PLoS Genet. 9:e1003933. doi: 10.1371/journal.pgen.1003933
70. Lindner, H., Muller, L. M., Boisson-Dernier, A., and Grossniklaus, U. (2012a). CrRLK1L receptor- like kinases: not just another brick in the wall. Curr. Opin. Plant Biol. 15, 659–669. doi: 10.1016/j.pbi.2012.07.003
71. Lindner, H., Raissig, M. T., Sailer, C., Shimosato-Asano, H., Bruggmann, R., and Grossniklaus, U. (2012b). SNP-Ratio Mapping (SRM): identifying lethal alleles and mutations in complex genetic backgrounds by next-generation sequencing. Genetics 191, 1381–1386. doi: 10.1534/genetics.112.141341
72. Liu, J., Zhong, S., Guo, X., Hao, L., Wei, X., Huang, Q., et al. (2013). Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis. Curr. Biol. 23, 993–998. doi: 10.1016/j.cub.2013.04. 043
73. Liu, J., Zuo, X., Yue, P., and Guo, W. (2007). Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol. Biol. Cell 18, 4483–4492. doi: 10.1091/mbc.E07-05-0461
74. 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. doi: 10.1105/tpc.15.00703
75. Lord, E. M., and Russell, S. D. (2002). The mechanisms of pollination and fertilization in plants. Annu. Rev. Cell Dev. Biol. 18, 81–105. doi: 10.1146/annurev.cellbio.18.012502.083438
76. Lopes, A. L., Costa, M. L., Sobral, R., Costa, M. M., Amorim, M. I., and Coimbra, S. (2016). Arabinogalactan proteins and pectin distribution during female gametogenesis in Quercus suber L. Ann. Bot. 117, 949–961. doi: 10.1093/aob/mcw019
77. Losada, J. M., and Herrero, M. (2012). Arabinogalactan-protein secretion is associated with the acquisition of stigmatic receptivity in the apple flower. Ann. Bot. 110, 573–584. doi: 10.1093/aob/mcs116
78. Losada, J. M., and Herrero, M. (2014). Glycoprotein composition along the pistil of Malus x domestica and the modulation of pollen tube growth. BMC Plant Biol. 14:1. doi: 10.1186/1471-2229-14-1
79. Lu, Y., Chanroj, S., Zulkifli, L., Johnson, M. A., Uozumi, N., Cheung, A., et al. (2011). Pollen tubes lacking a pair of K+ transporters fail to target ovules in Arabidopsis. Plant Cell 23, 81–93. doi: 10.1105/tpc.110.080499
80. Márton, M. L., Cordts, S., Broadhvest, J., and Dresselhaus, T. (2005). Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 307, 573–576. doi: 10.1126/science.1104954
81. Márton, M. L., Fastner, A., Uebler, S., and Dresselhaus, T. (2012). Overcoming hybridization barriers by the secretion of the maize pollen tube attractant ZmEA1 from Arabidopsis ovules. Curr. Biol. 22, 1194–1198. doi: 10.1016/j.cub.2012.04.061
82. Maruyama, D., Hamamura, Y., Takeuchi, H., Susaki, D., Nishimaki, M., Kurihara, D., et al. (2013). Independent control by each female gamete prevents the attraction of multiple pollen tubes. Dev. Cell 25, 317–323. doi: 10.1016/j.devcel.2013.03.013
83. 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. doi: 10.1016/j.cell.2015.03.018
84. Mashiguchi, K., Asami, T., and Suzuki, Y. (2009). Genome-wide identification, structure and expression studies, and mutant collection of 22 early nodulin-like protein genes in Arabidopsis. Biosci. Biotechnol. Biochem. 73, 2452–2459. doi: 10.1271/bbb.90407
85. Matias-Hernandez, L., Battaglia, R., Galbiati, F., Rubes, M., Eichenberger, C., Grossniklaus, U., et al. (2010). VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell 22, 1702–1715. doi: 10.1105/tpc.109.068627
86. Mayfield, J. A., Fiebig, A., Johnstone, S. E., and Preuss, D. (2001). Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292, 2482–2485. doi: 10.1126/science.1060972
87. Mayfield, J. A., and Preuss, D. (2000). Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat. Cell Biol. 2, 128–130. doi: 10.1038/35000084
88. McCormick, S. (2004). Control of male gametophyte development. Plant Cell 16, S142–S153. doi: 10.1105/tpc.016659
89. Mendes, M. A., Guerra, R. F., Castelnovo, B., Silva-Velazquez, Y., Morandini, P., Manrique, S., et al. (2016). Live and let die: a REM complex promotes fertilization through synergid cell death in Arabidopsis. Development 143, 2780–2790. doi: 10.1242/dev.134916
90. Michard, E., Lima, P. T., Borges, F., Silva, A. C., Portes, M. T., Carvalho, J. E., et al. (2011). Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-Serine. Science 332, 434–437. doi: 10.1126/science.1201101
91. Miyazaki, S., Murata, T., Sakurai-Ozato, N., Kubo, M., Demura, T., Fukuda, H., et al. (2009). ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr. Biol. 19, 1327–1331. doi: 10.1016/j.cub.2009.06.064
92. 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. Curr. Biol. 26, 1091–1097. doi: 10.1016/j.cub.2016.02.040
93. Mollet, J. C., Park, S. Y., Nothnagel, E. A., and Lord, E. M. (2000). A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12, 1737–1750. doi: 10.1105/tpc.12.9.1737
94. Mori, T., Igawa, T., Tamiya, G., Miyagishima, S.-Y., and Berger, F. (2014). Gamete attachment requires GEX2 for successful fertilization in Arabidopsis. Curr. Biol. 24, 170–175. doi: 10.1016/j.cub.2013.11.030
95. Mori, T., Kuroiwa, H., Higashiyama, T., and Kuroiwa, T. (2005). GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat. Cell Biol. 8, 64–71. doi: 10.1038/ncb1345
96. Mosher, S., and Kemmerling, B. (2013). PSKR1 and PSY1R-mediated regulation of plant defense responses. Plant Signal. Behav. 8:e24119. doi: 10.4161/psb.24119
97. Motomura, K., Berger, F., Kawashima, T., Kinoshita, T., Higashiyama, T., and Maruyama, D. (2016). Fertilization-independent cell-fusion between the synergid and central cell in the polycomb mutant. Cell Struct. Funct. 41, 121–125. doi: 10.1247/csf.16010
98. Ngo, Q. A., Vogler, H., Lituiev, D. S., Nestorova, A., and Grossniklaus, U. (2014). A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev. Cell 29, 491–500. doi: 10.1016/j.devcel.2014. 04.008
99. 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. Front. Plant Sci. 5:499. doi: 10.3389/fpls.2014.00499
100. Ogawa-Ohnishi, M., and Matsubayashi, Y. (2015). Identification of three potent hydroxyproline Ogalactosyltransferases in Arabidopsis. Plant J. 81, 736–746. doi: 10.1111/tpj.12764
101. Okuda, S., Tsutsui, H., Shiina, K., Sprunck, S., Takeuchi, H., Yui, R., et al. (2009). Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458, 357–361. doi: 10.1038/nature07882
102. Palanivelu, R., Brass, L., Edlund, A. F., and Preuss, D. (2003). Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 47–59. doi: 10.1016/S0092-8674(03)00479-3
103. Palanivelu, R., and Preuss, D. (2006). Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol. 6:7. doi: 10.1186/1471-2229-6-7
104. Palanivelu, R., and Tsukamoto, T. (2012). Pathfinding in angiosperm reproduction: pollen tube guidance by pistils ensures successful double fertilization. Wiley Interdiscip. Rev. Dev. Biol. 1, 96–113. doi: 10.1002/wdev.6
105. Park, S. Y., Jauh, G. Y., Mollet, J. C., Eckard, K. J., Nothnagel, E. A., Walling, L. L., et al. (2000). A lipid transfer-like protein is necessary for lily pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12, 151–164. doi: 10.1105/tpc.12.1.151
106. Peng, Y.-B., Zou, C., Gong, H.-Q., Bai, S.-N., Xu, Z.-H., and 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, 194–200. doi: 10.1111/j.1744-7909.2005.00023.x
107. Pennell, R. I., Janniche, L., Kjellbom, P., Scofield, G. N., Peart, J. M., and Roberts, K. (1991). Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3, 1317–1326. doi: 10.1105/tpc.3.12.1317
108. Pennell, R. I., Knox, J. P., Scofield, G. N., Selvendran, R. R., and 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, 1967–1977. doi: 10.1083/jcb.108.5.1967
109. Pennell, R. I., and Roberts, K. (1990). Sexual development in the pea is presaged by altered expression of Arabinogalactan protein. Nature 344, 547–549. doi: 10.1038/344547a0
110. Pereira, A. M., Lopes, A. L., and Coimbra, S. (2016a). JAGGER, an AGP essential for persistent synergid degeneration and polytubey block in Arabidopsis. Plant Signal. Behav. 11:e1209616. doi: 10.1080/15592324.2016.1209616
111. Pereira, A. M., Masiero, S., Nobre, M. S., Costa, M. L., Soliìs, M.-T., Testillano, P. S., et al. (2014). Differential expression patterns of Arabinogalactan Proteins in Arabidopsis thaliana reproductive tissues. J. Exp. Bot. 65, 5459–5471. doi: 10.1093/jxb/eru300
112. Pereira, A. M., Nobre, M. S., Pinto, S. C., Lopes, A. L., Costa, M. L., Masiero, S., et al. (2016b). “Love is strong, and you’re so sweet”: JAGGER is essential for persistent synergid degeneration and polytubey block in Arabidopsis thaliana. Mol. Plant. 9, 601–614. doi: 10.1016/j.molp.2016.01.002
113. Pereira, L. G., Coimbra, S., Oliveira, H., Monteiro, L., and Sottomayor, M. (2006). Expression of arabinogalactan protein genes in pollen tubes of Arabidopsis thaliana. Planta 223, 374–380. doi: 10.1007/s00425-005-0137-4
114. Pereira, A. M., Pereira, L. G., and Coimbra, S. (2015). Arabinogalactan proteins: rising attention from plant biologists. Plant Reprod. 28, 1–15. doi: 10.1007/s00497-015-0254-6
115. Punwani, J. A., and Drews, G. N. (2008). Development and function of the synergid cell. Sex. Plant Reprod. 21, 7–15. doi: 10.1007/s00497-007-0059-3
116. Qin, Y., Leydon, A. R., Manziello, A., Pandey, R., Mount, D., Denic, S., et al. (2009). Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet. 5:e1000621. doi: 10.1371/journal.pgen.1000621
117. Qu, L. J., Li, L., Lan, Z., and Dresselhaus, T. (2015). Peptide signalling during the pollen tube journey and double fertilization. J. Exp. Bot. 66, 5139–5150. doi: 10.1093/jxb/erv275
118. Raghavan, V. (2003). Some reflections on double fertilization, from its discovery to the present. New Phytol. 159, 565–583. doi: 10.1046/j.1469-8137.2003.00846.x
119. Rotman, N., Rozier, F., Boavida, L., Dumas, C., Berger, F., and Faure, J. E. (2003). Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr. Biol. 13, 432–436. doi: 10.1016/S0960-9822(03)00093-9
120. Samuel, M. A., Chong, Y. T., Haasen, K. E., Aldea-Brydges, M. G., Stone, S. L., and Goring, D. R. (2009). Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21, 2655–2671. doi: 10.1105/tpc.109.069740
121. Sandaklie-Nikolova, L., Palanivelu, R., King, E. J., Copenhaver, G. P., and Drews, G. N. (2007). Synergid cell death in Arabidopsis is triggered following direct interaction with the pollen tube. Plant Physiol. 144, 1753–1762. doi: 10.1104/pp.107.098236
122. Schneitz, K., Hülskamp, M., and Pruitt, R. E. (1995). Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J. 7, 731–749. doi: 10.1046/j.1365-313X.1995.07050731.x
123. Schultz, C. J., Rumsewicz, M. P., Johnson, K. L., Jones, B. J., Gaspar, Y. M., and Bacic, A. (2002). Using genomic resources to guide research directions: the arabinogalactan protein gene family as a test case. Plant Physiol. 129, 1448–1463. doi: 10.1104/pp.003459
124. Sedbrook, J. C., Carroll, K. L., Hung, K. F., Masson, P. H., and Somerville, C. R. (2002). The Arabidopsis SKU5 gene encodes an extracellular glycosyl phosphatidylinositolanchored glycoprotein involved in directional root growth. Plant Cell 14, 1635–1648. doi: 10.1105/tpc.002360
125. Sedgley, M., Blesing, M. A., Bonig, I., Anderson, M. A., and Clarke, A. E. (1985). Arabinogalactan- proteins are localized extracellularly in the transmitting tissue of Nicotiana alata link and otto, an ornamental tobacco. Micron Microsc. Acta 16, 247–254. doi: 10.1016/0739-6260(85)90049-8
126. Seifert, G. J., and Roberts, K. (2007). The biology of arabinogalactan proteins. Annu. Rev. Plant Biol. 58, 137–161. doi: 10.1146/annurev.arplant.58.032806.103801
127. Shimizu, K. K., Ito, T., Ishiguro, S., and Okada, K. (2008). MAA3 (MAGATAMA3) helicase gene is required for female gametophyte development and pollen tube guidance in Arabidopsis thaliana. Plant Cell Physiol. 49, 1478–1483. doi: 10.1093/pcp/pcn130
128. Shimizu, K. K., and Okada, K. (2000). Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127, 4511–4518.
129. Showalter, A. M., Keppler, B., Lichtenberg, J., Gu, D., and Welch, L. R. (2010). A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol. 153, 485–513. doi: 10.1104/pp.110.156554
130. Sprunck, S., Rademacher, S., Vogler, F., Gheyselinck, J., Grossniklaus, U., and Dresselhaus, T. (2012). Egg cell-secreted EC1 triggers sperm cell activation during double fertilization. Science 338, 1093–1097. doi: 10.1126/science.1223944
131. Stührwohldt, N., Dahlkea, R. I., Kutschmara, A., Pengb, X., Sunb, M.-X., and Sautera, M. (2015). Phytosulfokine peptide signaling controls pollen tube growth and funicular pollen tube guidance in Arabidopsis thaliana. Physiol. Plant. 153, 643–653. doi: 10.1111/ppl.12270
132. Suárez, C., Zienkiewicz, A., Castro, A. J., Zienkiewicz, K., Majewska-Sawka, A., and Rodriìguez-Garciìa, M. I. (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, 305–319. doi: 10.1007/s00425-012-1774-z
133. 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. doi: 10.1105/tpc.112.107334
134. Takeuchi, H., and Higashiyama, T. (2012). A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol. 10:e1001449. doi: 10.1371/journal.pbio.1001449
135. Takeuchi, H., and Higashiyama, T. (2016). Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531, 245–248. doi: 10.1038/nature17413
136. Tsukamoto, T., Qin, Y., Huang, Y., Dunatunga, D., and Palanivelu, R. (2010). A role for LORELEI, a putative glycosylphosphatidylinositol-anchored protein, in Arabidopsis thaliana double fertilization and early seed development. Plant J. 62, 571–588. doi: 10.1111/j.1365-313X.2010.04177.x
137. Tucker, M. R., and Koltunow, A. M. J. (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, 137–145. doi: 10.1016/j.pbi.2013.11.015
138. Tucker, M. R., Okada, T., Hu, Y., Scholefield, A., Taylor, J. M., and Koltunow, A. M. J. (2012). Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139, 1399–1404. doi: 10.1242/dev.075390
139. Tung, C.-W., Dwyer, K. G., Nasrallah, M. E., and Nasrallah, J. B. (2005). Genome-wide identification of genes expressed in Arabidopsis pistils specifically along the path of pollen tube growth. Plant Physiol. 138, 977–989. doi: 10.1104/pp.105.060558
140. Völz, R., Heydlauff, J., Ripper, D., von Lyncker, L., and Gross-Hardt, R. (2013). Ethylene signaling is required for synergid degeneration and the establishment of a pollen tube block. Dev Cell. 25, 310–316. doi: 10.1016/j.devcel.2013.04.001
141. von Besser, K., Frank, A. C., Johnson, M. A., and Preuss, D. (2006). Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133, 4761–4769. doi: 10.1242/dev.02683
142. Wang, T., Liang, L., Xue, Y., Jia, P. F., Chen, W., Zhang, M. X., et al. (2016). A receptor heteromer mediates the male perception of female attractants in plants. Nature 531, 241–244. doi: 10.1038/nature16975
143. Webb, M. C., and Williams, E. G. (1988). The pollen tube pathway in the pistil of Lycopersicon peruvianum. Ann. Bot. 61, 415–423.
144. Wolters-Arts, M., Lush, W. M., and Mariani, C. (1998). Lipids are required for directional pollen- tube growth. Nature 392, 818–821. doi: 10.1038/33929
145. Woriedh, M., Merkl, R., and Dresselhaus, T. (2015). Maize EMBRYO SAC family peptides interact differentially with pollen tubes and fungal cells. J. Exp. Bot. 66, 5205–5216. doi: 10.1093/jxb/erv268
146. Wu, H., de Graaf, B., Mariani, C., and Cheung, A. Y. (2001). Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell Mol. Life Sci. 58, 1418–1429. doi: 10.1007/PL00000785
147. Wu, H., Wong, E., Ogdahl, J., and Cheung, A. Y. (2000). A pollen tube growth-promoting arabinogalactan protein from Nicotiana alata is similar to the tobacco transmitting tractS protein. Plant J. 22, 165–176. doi: 10.1046/j.1365-313x.2000.00731.x
148. Wu, H. M., Wang, H., and Cheung, A. Y. (1995). A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82, 395–403. doi: 10.1016/0092-8674(95) 90428-X
149. Yadegari, R., and Drews, G. N. (2004). Female gametophyte development. Plant Cell 16, S133–S141. doi: 10.1105/tpc.018192
150. Yang, J., Sardar, H. S., McGovern, K. R., Zhang, Y., and Showalter, A. M. (2007). A lysine-rich arabinogalactan protein in Arabidopsis is essential for plant growth and development, including cell division and expansion. Plant J. 49, 629–640. doi: 10.1111/j.1365-313X.2006.02985.x
151. Zinkl, G. M., Zwiebel, B. I., Grier, D. G., and Preuss, D. (1999). Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development 126, 5431–5440.