Pathfinding in angiosperm reproduction: Pollen tube guidance by pistils ensures successful double fertilization

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 1, 2012, Pages 96-113

  Palanivelu, Ravishankar ^a   Tsukamoto, Tatsuya ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOGALACTAN; CALCIUM;

ANGIOSPERM; ARABIDOPSIS; CELL DEGENERATION; EXTRACELLULAR MATRIX; FEMALE GAMETOPHYTE; FERTILIZATION; GAMETOPHYTE; GENE EXPRESSION; NONHUMAN; OVULE; PISTIL; PISTIL STIGMA; POLLEN GERMINATION; POLLEN TUBE; POLLEN TUBE GROWTH; POLLINATION; REPRODUCTION; REVIEW;

EID: 84862663504     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.6     Document Type: Review

References (123)

1. Weterings K, Russell SD. Experimental analysis of the fertilization process. Plant Cell 2004, 16(suppl): S107-S118.
2. Lord EM, Russell SD. The mechanisms of pollination and fertilization in plants. Annu Rev Cell Dev Biol 2002, 18:81-105.
3. Herrero M, Hormaza JI. Pistil strategies controlling pollen tube growth. Sex Plant Reprod 1996, 9:343-347.
4. Sogo A, Tobe H. Mode of pollen-tube growth in Pistils of Myrica rubra (Myricaceae): a comparison with related families. Ann Bot 2006, 97:71-77.
5. Yadegari R, Drews GN. Female gametophyte development. Plant Cell 2004, 16(suppl):S133-S141.
6. Sundaresan V, Alandete-Saez M. Pattern formation in miniature: the female gametophyte of flowering plants. Development 2010, 137:179-189.
7. Huck N, Moore JM, Federer M, Grossniklaus U. The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 2003, 130:2149-2159.
8. Berger F, Hamamura Y, Ingouff M, Higashiyama T. Double fertilization-caught in the act. Trends Plant Sci 2008, 13:437-443.
9. Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C. Pistil factors controlling pollination. Plant Cell 2004, 16:S98-S106.
10. Higashiyama T, Hamamura Y. Gametophytic pollen tube guidance. Sex Plant Reprod 2008, 21:17-26.
11. Chapman LA, Goring DR. Pollen-pistil interactions regulating successful fertilization in the Brassicaceae. J Exp Bot 2010, 61:1987-1999.
12. Chae K, Lord EM. Pollen tube growth and guidance: roles of small, secreted proteins. Ann Bot 2011, 108: 627-636.
13. Ma H, Sundaresan V. Development of flowering plant gametophytes. Curr Top Dev Biol 2010, 91:379-412.
14. Zinkl GM, Zwiebel BI, Grier DG, Preuss D. Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development 1999, 126:5431-5440.
15. Fiebig A, Kimport R, Preuss D. Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. Proc Natl Acad Sci U S A 2004, 101:3286-3291.
16. Kandasamy MK, Kristen U. Developmental aspects of ultrastructure, histochemistry and receptivity of the stigma of Nicotiana sylvestris. Ann Bot 1987, 60:427-437.
17. Nasrallah JB, Nishio T, Nasrallah ME. The self-incompatibility genes of Brassica: expression and use in genetic ablation of floral tissues. Annu Rev Plant Physiol Plant Mol Biol 1991, 42:393-422.
18. Goldman MH, Goldberg RB, Mariani C. Female sterile tobacco plants are produced by stigma-specific cell ablation. EMBO J 1994, 13:2976-2984.
19. Wolters-Arts M, Lush WM, Mariani C. Lipids are required for directional pollen-tube growth. Nature 1998, 392:818-821.
20. Preuss D, Lemieux B, Yen G, Davis RW. A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev 1993, 7:974-985.
21. 2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 2004, 136:3562-3571.
22. Holdaway-Clarke TL, Hepler PK. Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 2003, 159:539-563.
23. Heslop-Harrison Y, Heslop-Harrison J. Germination of monocolpate angiosperm pollen: evolution of the actin cytoskeleton and wall during hydration, activation and tube emergence. Ann Bot 1992, 69:385-394.
24. Heslop-Harrison J, Heslop-Harrison Y. Germination of monocolpate angiosperm pollen: effects of inhibitory factors and the Ca2+-channel blocker, nifedipine. Ann Bot 1992, 69:395-403.
25. Tsukamoto Y, Matsubara S. Studies on germination of chrysanthemum pollen II. Occurence of a germination-promoting substance. Plant Cell Physiol 1967, 9:237-245.
26. Wengier DL, Mazzella MA, Salem TM, McCormick S, Muschietti JP. STIL, a peculiar molecule from styles, specifically dephosphorylates the pollen receptor kinase LePRK2 and stimulates pollen tube growth in vitro. BMC Plant Biol 2010, 10:33.
27. Mo Y, Nagel C, Taylor LP. Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc Natl Acad Sci U S A 1992, 89:7213-7217.
28. Pollak RE, Hansen K, Astwood JD, Taylor LR. Conditional male fertility in maize. Sex Plant Reprod 1995, 8:231-241.
29. Burbulis IE, Iacobucci M, Shirley BW. A null mutation in the first enzyme of flavonoid biosynthesis does not affect male fertility in Arabidopsis. Plant Cell 1996, 8:1013-1025.
30. Ylstra B, Muskens M, Van Tunen AJ. Flavonols are not essential for fertilization in Arabidopsis thaliana. Plant Mol Biol 1996, 32:1155-1158.
31. Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM. Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci U S A 2003, 100:16125-16130.
32. Dong J, Kim ST, Lord EM. Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 2005, 138:778-789.
33. Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T. Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri. Plant Cell 1998, 10:2019-2032.
34. Palanivelu R, Preuss D. Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 2006, 6:7.
35. Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R. Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 2009, 5:e1000621.
36. Boavida LC, Borges F, Becker D Jr, Feijo J. Whole genome analysis of gene expression reveals coordinated activation of signaling and metabolic pathways during pollen-pistil interactions in Arabidopsis. Plant Physiol 2011, 155:2066-2080.
37. Muschietti J, Eyal Y, McCormick S. Pollen tube localization implies a role in pollen-pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell 1998, 10:319-330.
38. Wengier D, Valsecchi I, Cabanas ML, Tang WH, McCormick S, Muschietti J. The receptor kinases LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract. Proc Natl Acad Sci U S A 2003, 100:6860-6865.
39. Zhang D, Wengier D, Shuai B, Gui CP, Muschietti J, McCormick S, Tang WH. The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth. Plant Physiol 2008, 148:1368-1379.
40. Crawford BC, Ditta G, Yanofsky MF. The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr Biol 2007, 17: 1101-1108.
41. Gremski K, Ditta G, Yanofsky MF. The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 2007, 134:3593-3601.
42. Park SY, Jauh GY, Mollet JC, Eckard KJ, Nothnagel EA, Walling LL, Lord EM. A lipid transfer-like protein is necessary for lily pollen tube adhesion to an in vitro stylar matrix. Plant Cell 2000, 12:151-164.
43. Mollet JC, Park SY, Nothnagel EA, Lord EM. A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 2000, 12:1737-1750.
44. Wu MF, Tian Q, Reed JW. Arabidopsis micro-RNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 2006, 133:4211-4218.
45. Tung CW, Dwyer KG, Nasrallah ME, Nasrallah JB. Genome-wide identification of genes expressed in Arabidopsis pistils specifically along the path of pollen tube growth. Plant Physiol 2005, 138:977-989.
46. Jauh GY, Lord E. Localization of pectins and arabinogalactan-proteins in lily pollen tube and style, and their possible roles in pollination. Planta 1996, 199:251-261.
47. Wu HM, Wong E, Ogdahl 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.
48. Cheung AY, Wang H, Wu HM. A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 1995, 82:383-393.
49. 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.
50. Lind JL, Bacic A, Clarke AE, Anderson MA. A style-specific hydroxyproline-rich glycoprotein with properties of both extensins and arabinogalactan proteins. Plant J 1994, 6:491-502.
51. 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.
52. 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 decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana. Plant Cell Physiol 2011, 52:894-908.
53. 2+ channels in pollen tubes and are regulated by pistil D-serine. Science 2011, 332:434-437.
54. Lennon KA, Roy S, Hepler PK, Lord EM. The structure of the transmitting tissue of Arabidopsis thaliana (L.) and the path of pollen tube growth. Sex Plant Reprod 1998, 11:49-59.
55. Johnson MA, von Besser K, Zhou Q, Smith E, Aux G, Patton D, Levin JZ, Preuss D. Arabidopsis hapless mutations define essential gametophytic functions. Genetics 2004, 168:971-982.
56. Sandaklie-Nikolova L, Palanivelu R, King EJ, Copenhaver GP, Drews GN. Synergid cell death in Arabidopsis is triggered following direct interaction with the pollen tube. Plant Physiol 2007, 144:1753-1762.
57. Tsukamoto T, Qin Y, Huang Y, Dunatunga D, Palanivelu R. A role for LORELEI, a putative glycosylphosphatidylinositol-anchored protein, in Arabidopsis thaliana double fertilization and early seed development. Plant J 2010, 62:571-588.
58. Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure JE. Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 2003, 13:432-436.
59. Shimizu KK, Okada K. Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 2000, 127:4511-4518.
60. Hulskamp M, Schneitz K, Pruitt RE. Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 1995, 7:57-64.
61. Schneitz K, Hulskamp M, Kopczak SD, Pruitt RE. Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development 1997, 124:1367-1376.
62. Hauser BA, Villanueva JM, Gasser CS. Arabidopsis TSO1 regulates directional processes in cells during floral organogenesis. Genetics 1998, 150:411-423.
63. De Martinis D, Mariani C. Silencing gene expression of the ethylene-forming enzyme results in a reversible inhibition of ovule development in transgenic tobacco plants. Plant Cell 1999, 11:1061-1072.
64. Baker SC, Robinson-Beers K, Villanueva JM, Gaiser JC, Gasser CS. Interactions among genes regulating ovule development in Arabidopsis thaliana. Genetics 1997, 145:1109-1124.
65. Srilunchang KO, Krohn NG, Dresselhaus T. DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize. Development 2010, 137:333-345.
66. Lausser A, Kliwer I, Srilunchang KO, Dresselhaus T. Sporophytic control of pollen tube growth and guidance in maize. J Exp Bot 2010, 61:673-682.
67. Ray SM, Park SS, Ray A. Pollen tube guidance by the female gametophyte. Development 1997, 124:2489-2498.
68. Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T. Pollen tube attraction by the synergid cell. Science 2001, 293:1480-1483.
69. Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN. MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 2005, 17:2981-2992.
70. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, et al. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 2009, 458:357-361.
71. Kanaoka MM, Kawano N, Matsubara Y, Susaki D, Okuda S, Sasaki N, Higashiyama T. Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor. Ann Bot 2011, 108:739-747.
72. Marton ML, Cordts S, Broadhvest J, Dresselhaus T. Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 2005, 307:573-576.
73. Dresselhaus T, Lausser A, Márton ML. Using maize as a model to study pollen tube growth and guidance, cross-incompatibility and sperm delivery in grasses. Ann Bot 2011, 108:727-737.
74. Marton ML, Dresselhaus T. Female gametophyte-controlled pollen tube guidance. Biochem Soc Trans 2010, 38:627-630.
75. Punwani JA, Rabiger DS, Drews GN. MYB98 positively regulates a battery of synergid-expressed genes encoding filiform apparatus localized proteins. Plant Cell 2007, 19:2557-2568.
76. Punwani JA, Rabiger DS, Lloyd A, Drews GN. The MYB98 subcircuit of the synergid gene regulatory network includes genes directly and indirectly regulated by MYB98. Plant J 2008, 55:406-414.
77. Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V. Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 2005, 132:603-614.
78. Steffen JG, Kang IH, Macfarlane J, Drews GN. Identification of genes expressed in the Arabidopsis female gametophyte. Plant J 2007, 51:281-292.
79. Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenfuhrer J, von Mering C, Grossniklaus U. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 2010, 20:506-512.
80. Jones-Rhoades MW, Borevitz JO, Preuss D. Genome-wide expression profiling of the Arabidopsis female gametophyte identifies families of small, secreted proteins. PLoS Genet 2007, 3:1848-1861.
81. Chen YH, Li HJ, Shi DQ, Yuan L, Liu J, Sreenivasan R, Baskar R, Grossniklaus U, Yang WC. The central cell plays a critical role in pollen tube guidance in Arabidopsis. Plant Cell 2007, 19:3563-3577.
82. Alandete-Saez M, Ron M, McCormick S. 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 2008, 1:586-598.
83. Faure JE, Rotman N, Fortune P, Dumas C. Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 2002, 30:481-488.
84. Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T. Explosive discharge of pollen tube contents in Torenia fournieri. Plant Physiol 2000, 122:11-13.
85. Boisson-Dernier A, Frietsch S, Kim TH, Dizon MB, Schroeder JI. The peroxin loss-of-function mutation abstinence by mutual consent disrupts male-female gametophyte recognition. Curr Biol 2008, 18:63-68.
86. Matias-Hernandez L, Battaglia R, Galbiati F, Rubes M, Eichenberger C, Grossniklaus U, Kater MM, Colombo L. VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell 2010, 22:1702-1715.
87. Christensen CA, Gorsich SW, Brown RH, Jones LG, Brown J, Shaw JM, Drews GN. Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell 2002, 14:2215-2232.
88. Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF. A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci U S A 2004, 101:9502-9507.
89. Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T. GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 2006, 8:64-71.
90. von Besser K, Frank AC, Johnson MA, Preuss D. Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 2006, 133:4761-4769.
91. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 2007, 317:656-660.
92. Capron A, Gourgues M, Neiva LS, Faure JE, Berger F, Pagnussat G, Krishnan A, Alvarez-Mejia C, Vielle-Calzada JP, Lee YR, et al. Maternal control of male-gamete delivery in Arabidopsis involves a putative GPI-anchored protein encoded by the LORELEI gene. Plant Cell 2008, 20:3038-3049.
93. Rotman N, Gourgues M, Guitton AE, Faure JE, Berger F. A dialogue between the Sirene pathway in synergids and the fertilization independent seed pathway in the central cell controls male gamete release during double fertilization in Arabidopsis. Mol Plant 2008, 1:659-666.
94. Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U. Conserved molecular components for pollen tube reception and fungal invasion. Science 2010, 330:968-971.
95. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci U S A 2005, 102:3135-3140.
96. Panstruga R. Serpentine plant MLO proteins as entry portals for powdery mildew fungi. Biochem Soc Trans 2005, 33:389-392.
97. Kim MC, Panstruga R, Elliott C, Muller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P. Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 2002, 416:447-451.
98. Govers F, Angenent GC. Plant science. Fertility goddesses as Trojan horses. Science 2010, 330:922-923.
99. Russell SD. Fertilization in Plumbago zeylanica: entry and discharge of the pollen tube in the embryo sac. Can J Bot 1982, 60:2219-2230.
100. Amien S, Kliwer I, Márton ML, Debener T, Geiger D, Becker D, Dresselhaus T. Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS Biol 2010, 8:e1000388.
101. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 2009, 136:3279-3288.
102. Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M. ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 2009, 19: 1327-1331.
103. Berger F. Double-fertilization, from myths to reality. Sex Plant Reprod 2008, 21:3-5.
104. Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 2007, 17:1032-1037.
105. Liu Y, Tewari R, Ning J, Blagborough AM, Garbom S, Pei J, Grishin NV, Steele RE, Sinden RE, Snell WJ, et al. The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev 2008, 22:1051-1068.
106. Sprunck S. Let's get physical: gamete interaction in flowering plants. Biochem Soc Trans 2010, 38: 635-640.
107. Berger F. Imaging fertilization in flowering plants, not so abominable after all. J Exp Bot 2011, 62:1651-1658.
108. Grossniklaus U, Schneitz K. The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev Biol 1998, 9:227-238.
109. Spielman M, Scott R. Polyspermy barriers in plants: from preventing to promoting fertilization. Sex Plant Reprod 2008, 21:53-65.
110. Kato A. Heterofertilization exhibited by trifluralin-induced bicellular pollen on diploid and tetraploid maize crosses. Genome 2001, 44:1114-1121.
111. Prado AM, Colaco R, Moreno N, Silva AC, Feijõ JA. Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Mol Plant 2008, 1:703-714.
112. Prado AM, Porterfield DM, Feijo JA. Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 2004, 131:2707-2714.
113. Boavida LC, Shuai B, Yu HJ, Pagnussat G, Sundaresan V, McCormick S. A collection of Ds insertional mutants associated with defects in male gametophyte development and function in Arabidopsis thaliana. Genetics 2009, 181:1369-1385.
114. Drews GN, Lee D, Christensen CA. Genetic analysis of female gametophyte development and function. Plant Cell 1998, 10:5-17.
115. Christensen CA, Subramanian S, Drews GN. Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev Biol 1998, 202:136-151.
116. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301:653-657.
117. Christensen CA, King EJ, Jordan JR, Drews GN. Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex Plant Reprod 1997, 10:49-64.
118. Drews GN, Yadegari R. Development and function of the angiosperm female gametophyte. Annu Rev Genet 2002, 36:99-124.
119. Boavida LC, McCormick S. Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 2007, 52:570-582.
120. Yetisen AK, Jiang L, Cooper JR, Qin Y, Palanivelu R, Zohar Y. A microsystem-based assay for studying pollen tube guidance in plant reproduction. J Micromech Microeng 2011, 21:054018.
121. Yu HJ, Hogan P, Sundaresan V. Analysis of the female gametophyte transcriptome of Arabidopsis by comparative expression profiling. Plant Physiol 2005, 139:1853-1869.
122. Honys D, Twell D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 2004, 5:R85.
123. Pina C, Pinto F, Feijo JA, Becker JD. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 2005, 138:744-756.