Sexual and asexual (apomictic) seed development in flowering plants: Molecular, morphological and evolutionary relationships

Functional Plant Biology

Volumn 36, Issue 6, 2009, Pages 490-504

  Tucker, Matthew R ^a   Koltunow, Anna M G ^a  

^a CSIRO   (Australia)

Author keywords

Apomixis; Evolution; Hieracium; Ovule; Reproduction.

Indexed keywords

APOMIXIS; EVOLUTION; HIERACIUM; OVULE; REPRODUCTION.;

SEED;

ANGIOSPERM; CLONAL GROWTH; CROP PLANT; EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; GAMETE; MORPHOLOGY; REPRODUCTIVE STRATEGY; SEED PRODUCTION;

HIERACIUM; MAGNOLIOPHYTA;

EID: 67650067596     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP09078     Document Type: Review

References (132)

1. Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proceedings of the National Academy of Sciences of the United States of America 100, 4649-4654. doi: 10.1073/pnas.0630618100
2. Akiyama Y, Hanna W, Ozias-Akins P (2005) High-resolution physical mapping reveals that the apospory-specific genomic region (ASGR) in Cenchrus ciliaris is located on a heterochromatic and hemizygous region of a single chromosome. Theoretical and Applied Genetics 111, 1042-1051. doi: 10.1007/s00122-005-0020-5
3. Albertini E, Marconi G, Reale L, Barcaccia G, Porceddu A, Ferranti F, Falcinelli M (2005) SERK and APOSTART. Candidate genes for apomixis in Poa pratensis. Plant Physiology 138, 2185-2199. doi: 10.1104/pp.105. 062059
4. Araujo ACG, Mukhambetzhanov S, Pozzobon MT, Santana EF, Carneiro VTC (2000) Female gametophyte development in apomictic and sexual Brachiaria brizantha (Poaceae). Revue de Cytologie et Biologie vegetales-Le Botaniste 23, 13-26.
5. Araujo A, Nobrega J, Pozzobon M, Carneiro V (2005) Evidence of sexuality in induced tetraploids of Brachiaria brizantha (Poaceae). Euphytica 144, 39-50. doi: 10.1007/s10681-005-2842-2
6. Asker SE, Jerling L (1992) 'Apomixis in plants.' (CRC Press: Boca Raton)
7. Bajon C, Horlow C, Motamayor J, Sauvanet A, Robert D (1999) Megasporogenesis in Arabidopsis thaliana L.: an ultrastructural study. Sexual Plant Reproduction 12, 99-109. doi: 10.1007/s004970050178
8. Balasubramanian S, Schneitz K (2000) NOZZLE regulates proximal-distal pattern formation, cell proliferation and early sporogenesis during ovule development in Arabidopsis thaliana. Development 127, 4227-4238.
9. Barrell P, Grossniklaus U (2005) Confocal microscopy of whole ovules for analysis of reproductive development: the elongate1 mutant affects meiosis. II. The Plant Journal 43, 309-320. doi: 10.1111/j.1365-313X.2005. 02456.x
10. Bicknell RA (1997) Isolation of a diploid, apomictic plant of Hieracium aurantiacum. Sexual Plant Reproduction 10, 168-172. doi: 10.1007/s004970050084
11. Blachford A, Doebeli M (2009) On luck and sex. Evolution 63, 40-47. doi: 10.1111/j.1558-5646.2008.00523.x
12. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C (1998) AGO1 definesa novel locus of Arabidopsis controlling leaf development . The EMBO Journal 17, 170-180. doi: 10.1093/emboj/17.1.170
13. Bouman F (1984) The ovule. In 'Embryology of angiosperms'. (Ed. BM Johri) pp. 123-157. (Springer-Verlag: Berlin Heidelberg)
14. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617-619. doi: 10.1126/science.289.5479.617
15. Bray RA (1978) Evidence for facultative apomixis in Cenchrus ciliaris. Euphytica 27, 801-804. doi: 10.1007/BF00023716
16. Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Current Biology 12, 1718-1727. doi: 10.1016/S0960-9822(02)01151-X
17. Canzoniero LM, Babcock DJ, Gottron FJ, Grabb MC, Manzerra P, Snider BJ, Choi DW (2004) Raising intracellular calcium attenuates neuronal apoptosis triggered by staurosporine or oxygen-glucose deprivation in the presence of glutamate receptor blockade. Neurobiology of Disease 15, 520-528. doi: 10.1016/j.nbd.2003.10.013
18. Carman JG (1997) Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biological Journal of the Linnean Society. Linnean Society of London 61, 51-94. doi: 10.1111/j.1095-8312.1997.tb01778.x
19. Carman JG (2001) The gene effect: genome collisions and apomixis. In 'The flowering of apomixis: from mechanisms to genetic engineering'. (Eds Y Savidan, JG Carman, T Dresselhaus) pp. 95-110. (CIMMYT, IRS, Eur. Comm. DG VI: Mexico)
20. Carman J (2007) Do duplicate genes cause apomixis? In Apomixis: evolution, mechanisms and perspectives'. (Eds E Hörandl, U Grossniklaus, PJ van Dijk, TF Sharbel) pp. 63-92. (A.R.G. Gantner Verlag: Rugell, Liechtenstein)
21. Catanach AS, Erasmuson SK, Podivinsky E, Jordan BR, Bicknell R (2006) Deletion mapping of genetic regions associated with apomixis in Hieracium. Proceedings of the National Academy of Sciences of the United States of America 103, 18 650-18 655. doi: 10.1073/pnas.0605588103
22. Chapman D, Shivji M, Louis E, Sommer J, Fletcher H, Prodohl P (2007) Virgin birth in a hammerhead shark. Biology Letters 3, 425-427. doi: 10.1098/rsbl.2007.0189
23. Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, Peacock WJ (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 94, 4223-4228. doi: 10.1073/pnas.94.8.4223
24. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology 58, 377-406. doi: 10.1146/annurev.arplant.58.032806.103835
25. Chen J, Ding J, Ouyang Y, Du H, Yang J, et al. (2008) A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proceedings of the National Academy of Sciences of the United States of America 105, 11436-11441. doi: 10.1073/pnas.0804761105
26. Citterio S, Albertini E, Varotto S, Feltrin E, Soattin M, Marconi G, Sgorbati S, Lucchin M, Barcaccia G (2005) Alfalfa Mob 1-like genes are expressed in reproductive organs during meiosis and gametogenesis. Plant Molecular Biology 58, 789-807. doi: 10.1007/s11103-005-8104-9
27. Colombo L, Battaglia R, Kater MM (2008) Arabidopsis ovule development and its evolutionary conservation. Trends in Plant Science 13, 444-450. doi: 10.1016/j.tplants.2008.04.011
28. Crepet W, Niklas K (2009) Darwin's second "Abominable mystery": why are there so many angiosperm species? American Journal of Botany 96, 366-381. doi: 10.3732/ajb.0800126
29. Curtis MD, Grossniklaus U (2007) Amphimixis and apomixis: two sides of the same coin? In Apomixis: evolution, mechanisms and perspectives'. (Eds E Hörandl, U Grossniklaus, PJ van Dijk, TF Sharbel) pp. 37-62. (A.R.G Gantner Verlag: Rugell, Liechtenstein)
30. Darwin C (1903) 'More letters of Charles Darwin, a record of his work in hitherto unpublished letters.' (John Murray: London, UK)
31. Delmotte F, Leterme N, Bonhomme J, Rispe C, Simon J (2001) Multiple routes to asexuality in an aphid species. Proceedings of the Royal Society of London. Series B. Biological Sciences 268, 2291-2299. doi: 10.1098/rspb.2001.1778
32. Deyhle F, Sarkar AK, Tucker EJ, Laux T (2007) WUSCHEL regulates cell differentiation during anther development. Developmental Biology 302, 154-159. doi: 10.1016/j.ydbio.2006.09.013
33. Diévart A, Clark SE (2004) LRR-containing receptors regulating plant development and defense. Development 131, 251-261. doi: 10.1242/dev.00998
34. Donofrio NM, Delaney TP (2001) Abnormal callose response phenotype and hypersusceptibility to Peronospoara parasitica in defence-compromised Arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. Molecular Plant-Microbe Interactions 14, 439-450. doi: 10.1094/MPMI.2001.14.4.439
35. Engelstädter J (2008) Constraints on the evolution of asexual reproduction. BioEssays 30, 1138-1150. doi: 10.1002/bies.20833
36. Ernst A (1918) 'Die Bastardierung als Ursache der Apogamie imPflanzenre.' (Fischer: Jena, Germany)
37. García-Heredia J, Hervas M, De la Rosa M, Navarro J (2008) Acetylsalicylic acid induces programmed cell death in Arabidopsis cell cultures. Planta 228, 89-97. doi: 10.1007/s00425-008-0721-5
38. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. The Journal of Cell Biology 119, 493-501. doi: 10.1083/jcb.119.3.493
39. Ge X, Dietrich C, Matsuno M, Li G, Berg H, Xia Y (2005) An Arabidopsis aspartic protease functions as an anti-cell-death component in reproduction and embryogenesis. EMBO Reports 6, 282-288. doi: 10.1038/sj.embor.7400357
40. Grimanelli D, Leblanc O, Espinosa E, Perotti E, De Leon DG, Savidan Y (1998) Mapping diplosporous apomixis in tetraploid Tripsacum: one gene or several genes? Heredity 80, 33-39. doi: 10.1046/j.1365-2540.1998. 00263.x
41. Grimanelli D, Leblanc O, Perotti E, Grossniklaus U (2001) Developmental genetics of gametophytic apomixis. Trends in Genetics 17, 597-604. doi: 10.1016/S0168-9525(01)02454-4
42. Grossniklaus U, Schneitz K (1998) The molecular and genetic basis of ovule and megagametophyte development. Seminars in Cell & Developmental Biology 9, 227-238. doi: 10.1006/scdb.1997.0214
43. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280, 446-450. doi: 10.1126/science. 280.5362.446
44. Grossniklaus U, Spillane C, Page DR, Kohler C (2001) Genomic imprinting and seed development: endosperm formation with and without sex. Current Opinion in Plant Biology 4, 21-27. doi: 10.1016/S1369-5266 (00)00130-8
45. Groß-Hardt R, Lenhard M, Laux T (2002) WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes & Development 16, 1129-1138. doi: 10.1101/|gad.225202
46. Gu YQ, Coleman-Derr D, Kong X, Anderson OD (2004) Rapid genome evolution revealed by comparative sequence analysis of orthologous regions from four Triticeae genomes. Plant Physiology 135, 459-470. doi: 10.1104/pp.103.038083
47. Guitton A, Berger F (2005) Loss of function of MULTICOPY SUPPRESSOR OF IRA 1 produces nonviable parthenogenetic embryos in Arabidopsis. Current Biology 15, 750-754. doi: 10.1016/j.cub.2005.02.066
48. Hirabayashi S, Nakagawa K, Sumita K, Hidaka S, Kawai T, Ikeda M, Kawata A, Ohno K, Hata Y (2008) Threonine 74 of MOB1 is a putative key phosphorylation site by MST2 to form the scaffold to activate nuclear Dbf2-related kinase 1. Oncogene 27, 4281-4292. doi: 10.1038/onc.2008.66
49. Hird D, Worrall D, Hodge R, Smartt S, Paul W, Scott R (1993) The anther-specific protein encoded by the Brassica napus and Arabidopsis thaliana A6-gene displays similarity to beta-1,3-glucanases. The Plant Journal 4, 1023-1033. doi: 10.1046/j.1365-313X.1993.04061023.x
50. Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant & Cell Physiology 46, 23-47. doi: 10.1093/pcp/pci501
51. Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proceedings of the National Academy of Sciences of the United States of America 105, 2220-2225. doi: 10.1073/pnas.0708795105
52. Köhler C, Grossniklaus U (2005) Seed development and genomic imprinting in plants. Progress in Molecular and Subcellular Biology 38, 237-262. doi: 10.1007/3-540-27310-7-10
53. Koltunow AM, Tucker MR (2008) Functional embryo sac formation in Arabidopsis without meiosis - one step towards asexual seed formation (apomixis) in crops? Journal of Biosciences 33, 309-311. doi: 10.1007/s12038-008-0049-0
54. Koltunow AM, Bicknell RA, Chaudhury AM (1995a) Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiology 108, 1345-1352.
55. Koltunow AM, Soltys K, Nito N, Mcclure S (1995b) Anther, ovule seed, and nucellar embryo development in Citrus sinensis cv. Valencia. Canadian Journal of Botany 73, 1567-1582. doi: 10.1139/b95-170
56. Koltunow AM, Johnson SD, Bicknell RA (1998) Sexual and apomictic development in Hieracium. Sexual Plant Reproduction 11, 213-230. doi: 10.1007/s004970050144
57. Koltunow AM, Johnson SD, Bicknell RA (2000) Apomixis is not developmentally conserved in related, genetically characterized Hieracium plants of varying ploidy. Sexual Plant Reproduction 12, 253-266. doi: 10.1007/s004970050193
58. Lakshmanan KK, Ambegaokar KK (1984) Polyembryony. In 'Embryology of angiosperms'. (Ed. BM Johri) pp. 445-474. (Springer-Verlag: Berlin)
59. Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87-96.
60. Levy A, Erlanger M, Rosenthal M, Epel B (2007) A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. The Plant Journal 49, 669-682. doi: 10.1111/j.1365-313X.2006.02986.x
61. Li LC, Qin GJ, Tsuge T, Hou XH, Ding MY, et al. (2008) SPOROCYTELESS modulates YUCCA expression to regulate the development of lateral organs in Arabidopsis. New Phytologist 179, 751-764. doi: 10.1111/j.1469-8137.2008.02514.x
62. Lynn K,Fernandez A, AidaM, Sedbrook J, TasakaM, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126, 469-481.
63. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annual Review of Plant Biology 56, 393-434. doi: 10.1146/annurev.arplant.55.031903.141717
64. Matzk F, Prodanovic S, Baumlein H, Schubert I (2005) The inheritance of apomixis in Poa pratensis confirms a five locus model with differences in gene expressivity and penetrance. The Plant Cell 17, 13-24. doi: 10.1105/tpc.104.027359
65. Mercier R, Grelon M (2008) Meiosis in plants: ten years of gene discovery. Cytogenetic and Genome Research 120, 281-290. doi: 10.1159/000121077
66. Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, Lefevre F, Pelletier G, Horlow C (2001) SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes & Development 15, 1859-1871. doi: 10.1101/gad.203201
67. Mogie M, Britton NF, Stewart-Cox JA (2007) Asexuality, polyploidy and the male function. In 'Apomixis: evolution, mechanisms and perspectives'. (Eds E Hörandl, U Grossniklaus, PJ van Dijk, TF Sharbel) pp. 63-92. (A.R.G. Gantner Verlag: Rugell, Liechtenstein)
68. Moussian B, Schoof H, Haecker A, Jurgens G, Laux T (1998) Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. The EMBO Journal 17, 1799-1809. doi: 10.1093/emboj/17.6.1799
69. Naumova TN (1993) Apomixis in angiosperms. Nucellar and integumentary embryony.' (CRC Press: Boca Raton)
70. Nogler G (1984) Gametophytic apomixis. In 'Embryology of angiosperms'. (Ed. BM Johri) pp. 475-518. (Springer-Verlag: Berlin Heidelberg)
71. Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. The Plant Cell 15, 1728-1739. doi: 10.1105/tpc.012401
72. Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (2007) A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. The Plant Cell 19, 2583-2594. doi: 10.1105/tpc.107.053199
73. Noyes RD (2000) Diplospory and parthenogenesis in sexual × agamospermous (apomictic) Erigeron (Asteraceae) hybrids. International Journal of Plant Sciences 161, 1-12. doi: 10.1086/314238
74. Noyes RD (2005) Inheritance of apomeiosis (diplospory) in fleabanes (Erigeron, Asteraceae). Heredity 94, 193-198. doi: 10.1038/sj.hdy.6800597
75. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294. doi: 10.1126/science.1150083
76. Ohad N, Margossian L, Hsu Y, Williams C, Repetti P, Fischer RL (1996) A mutation that allows endosperm development without fertilization. Proceedings of the National Academy of Sciences of the United States of America 93, 5319-5324. doi: 10.1073/pnas.93.11.5319
77. Okada T, Catanach A, Johnson S, Bicknell R, Koltunow A (2007) An Hieracium mutant, loss of apomeiosis 1 (loa1) is defective in the initiation of apomixis. Sexual Plant Reproduction 20, 199-211. doi: 10.1007/s00497-007-0057-5
78. Otto S (2003) The advantages of segregation and the evolution of sex. Genetics 164, 1099-1118.
79. Ozias-Akins P, van Dijk PJ (2007) Mendelian genetics of apomixis in plants. Annual Review of Genetics 41, 509-537. doi: 10.1146/annurev.genet.40.110405.090511
80. Ozias-Akins P, Roche D, Hanna W (1998) Tight clustering andhemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum genetic control of apospory by a divergent locus that may have no allelic form in sexual genotypes. Proceedings of the National Academy of Sciences of the United States of America 95, 5127-5132. doi: 10.1073/pnas.95.9.5127
81. Peacock WJ, Luo M, Craig S, Dennis E, Chaudhury A (1995) A mutagenesis programme for apomixis genes in Arabidopsis. In 'Induced mutations and molecular techniques for crop improvement'. pp. 117-125. (FAO/IAEA: Vienna, Austria)
82. Pessino S, Evans C, Ortiz J, Armstead I, Do Valle C, Hayward M (1998) A genetic map of the apospory-region in Brachiaria hybrids: identification of two markers closely associated with the trait. Hereditas 128, 153-158. doi: 10.1111/j.1601-5223.1998.00153.x
83. Qiu Y, Liu R, Xie C, Russell S, Tian H (2008) Calcium changes during megasporogenesis and megaspore degeneration in lettuce (Lactuca sativa L.). Sexual Plant Reproduction 21, 197-204. doi: 10.1007/s00497-008-0079-7
84. Quarin CL, Hanna WW (1980) Effect of three ploidy levels on meiosis and mode of reproduction in Paspalum hexastachyum. Crop Science 20, 69-75.
85. Quarin CL, Espinoza F, Martinez EJ, Pessino SC, Bovo OA (2001) A rise of ploidy level induces the expression of apomixis in Paspalum notatum. Sexual Plant Reproduction 13, 243-249. doi: 10.1007/s004970100070
86. Radford J, Vesk M, Overall R (1998) Callose deposition at plasmodesmata. Protoplasma 201, 30-37. doi: 10.1007/BF01280708
87. Ravi M, Marimuthu MP, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451, 1121-1124. doi: 10.1038/nature06557
88. Reiser L, Fischer RL (1993) The ovule and the embryo sac. The Plant Cell 5, 1291-1301.
89. Rieseberg LH, Willis JH (2007) Plant speciation. Science 317, 910-914. doi: 10.1126/science.1137729
90. RinnePL, Kaikuranta PM, van derSchootC(2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. The Plant Journal 26, 249-264. doi: 10.1046/j.1365-313X. 2001.01022.x
91. Roche D, Cong PS, Chen ZB, Hanna WW, Gustine DL, Sherwood RT, Ozias-Akins P (1999) An apospory-specific genomic region is conserved between Buffelgrass (Cenchrus ciliaris L.) and Pennisetum squamulatum Fresen. The Plant Journal 19, 203-208. doi: 10.1046/j.1365-313X.1999.00514.x
92. Rodkiewicz B (1970) Callose in cell walls during megasporogensis in angiosperms. Planta 93, 39-47. doi: 10.1007/BF00387650
93. Rodrigues JC, Tucker MR, Johnson SD, Hrmova M, Koltunow AM (2008) Sexual and apomictic seed formation in Hieracium requires the plant polycomb-group gene FERTILIZATION INDEPENDENT ENDOSPERM. The Plant Cell 20, 2372-2386. doi: 10.1105/tpc.108.059287
94. Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 96, 11664-11 669. doi: 10.1073/pnas.96.20.11664
95. Schneitz K, Hulskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana - a light-microscope study of cleared whole-mount tissue. The Plant Journal 7, 731-749. doi: 10.1046/j.1365-313X. 1995.07050731.x
96. Schoof H, Lenhard M, Haecker A, Mayer KFX, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635-644. doi: 10.1016/S0092-8674(00)80700-X
97. Schranz M, Dobes C, Koch M, Mitchell-Olds T (2005) Sexual reproduction, hybridization, apomixis, and polyploidization in the genus Boechera (Brassicaceae). American Journal of Botany 92, 1797-1810. doi: 10.3732/ajb.92.11.1797
98. Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133, 251-261. doi: 10.1242/dev.02194
99. Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. The Plant Cell 16(Suppl), S46-S60. doi: 10.1105/tpc.017012
100. Sharbel TF, Voigt ML, Corral JM, Thiel T, Varshney A, Kumlehn J, Vogel H, Rotter B (2009) Molecular signatures of apomictic and sexual ovules in the Boechera holboellii complex. The Plant Journal, in press. doi: 10.1111/j.1365-313X.2009.03826.x
101. Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya IN (1996) The mac1 gene: controlling the commitment to the meiotic pathway in maize. Genetics 142, 1009-1020.
102. Sheridan WF, Golubeva EA, Abrhamova LI, Golubovskaya IN (1999) The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153, 933-941.
103. Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Science STKE 113, RE22.
104. Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V (2000) The DYAD gene is required for progression through female meiosis in Arabidopsis. Development 127, 197-200.
105. Sieber P, Gheyselinck J, Gross-Hardt R, Laux T, Grossniklaus U, Schneitz K (2004) Pattern formation during early ovule development in Arabidopsis thaliana. Developmental Biology 273, 321-334. doi: 10.1016/j.ydbio.2004.05.037
106. Skinner DJ, Hill TA, Gasser CS (2004) Regulation of ovule development. The Plant Cell 16(Suppl), S32-S45. doi: 10.1105/tpc.015933
107. Stone BA, Clarke AE (1992) 'Chemistry & biology of (1,3)-b-glucans.' (La Trobe University Press: Bundoora, Vic.)
108. Taylor J, Jacobson D, Fisher M (1999) The evolution of asexual fungi: reproduction, speciation and classification. Annual Review of Phytopathology 37, 197-246. doi: 10.1146/annurev.phyto.37.1.197
109. Theissen G, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Annals of Botany 100, 603-619. doi: 10.1093/aob/mcm143
110. Tucker M, Paech N, Willemse M, Koltunow A (2001) Dynamics of callose deposition and beta-1,3-glucanase expression during reproductive events in sexual and apomictic Hieracium. Planta 212, 487-498. doi: 10.1007/s004250000445
111. Tucker M, Araujo A, Paech N, Hecht V, Schmidt E, Rossell J, de Vries S, Koltunow A (2003) Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. The Plant Cell 15, 1524-1537. doi: 10.1105/tpc.011742
112. Tucker M, Hinze A, Tucker E, Takada S, Jurgens G, Laux T (2008) Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo. Development 135, 2839-2843. doi: 10.1242/dev.023648
113. van Dijk PJ (2007) Potential and realized costs of sex in dandelions, Taraxacum officinale s.l. In 'Apomixis: evolution, mechanisms and perspectives'. (Eds E Hörandl, U Grossniklaus, PJ van Dijk, TF Sharbel) pp. 63-92. (A.R.G. Gantner Verlag: Rugell, Liechtenstein)
114. van Dijk PJ, Tas ICQ, Falque M, Bakx-Schotman T (1999) Crosses between sexual and apomictic dandelions (Taraxacum). II. The breakdown of apomixis. Heredity 83, 715-721. doi: 10.1038/sj.hdy.6886200
115. Vaucheret H (2008) Plant ARGONAUTES. Trends in Plant Science 13, 350-358. doi: 10.1016/j.tplants.2008.04.007
116. Vijverberg K, Van der Hulst R, Lindhout P, Van Dijk P (2004) A genetic linkage map of the diplosporous chromosomal region in Taraxacum officinale (common dandelion; Asteraceae). Theoretical and Applied Genetics 108, 725-732. doi: 10.1007/s00122-003-1474-y
117. Webb MC, Gunning BES (1990) Embryo sac development in Arabidopsis thaliana. I. Megasporogenesis, including the microtubular cytoskeleton. Sexual Plant Reproduction 3, 244-256.
118. Webb MC, Gunning BES (1991) The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184, 187-195. doi: 10.1007/BF01102418
119. Webb MC, Gunning BES (1994) Embryo sac development in Arabidopsis thaliana II: The cytoskeleton during megagametogenesis. Sexual Plant Reproduction 7, 153-163. doi: 10.1007/BF00228488
120. Whitton J, Sears C, Baack E, Otto S (2008) The dynamic nature of apomixis in the angiosperms. International Journal of Plant Sciences 169, 169-182. doi: 10.1086/523369
121. Willemse MTM, De Boer-De Jeu MJ (1981) Megasporogenesis and early megagametogenesis. Acta Societatis Botanicorum Poloniae 50, 111-120.
122. Willemse MTM, van Went JL (1984) The female gametophyte. In 'Embryology of angiosperms'. (Ed. BM Johri) pp. 159-191. (Springer-Verlag: Berlin Heidelberg)
123. Worrall D, Hird DL, Hodge R, Wyatt P, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. The Plant Cell 4, 759-771.
124. Wu H, Cheung A (2000) Programmed cell death in plant reproduction. Plant Molecular Biology 44, 267-281. doi: 10.1023/A:1026536324081
125. Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211-4218. doi: 10.1242/dev.02602
126. Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. The EMBO Journal 23, 980-988. doi: 10.1038/sj.emboj.7600086
127. Yamaguchi Y, Yamamoto Y, Matsumoto H (1999) Cell death process initiated by a combination of aluminium and iron in suspension-cultured tobacco cells (Nicotiana tabacum): apoptosis-like cell death mediated by calcium and proteinase. Soil Science and Plant Nutrition 45, 647-657.
128. Yang W (2006) Female gametophyte development. In 'Handbook of seed science and technology'. (Ed. A Basra) pp. 27-62. (Food Products Press, The Harworth Press, Inc.: New York)
129. Yang W, Sundaresan V (2000) Genetics of gametophyte biogenesis in Arabidopsis. Current Opinion in Plant Biology 3, 53-57. doi: 10.1016/S1369-5266(99)00037-0
130. Yang WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes & Development 13, 2108-2117. doi: 10.1101/gad.13.16.2108
131. Zhao DZ, Wang GF, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes & Development 16, 2021-2031. doi: 10.1101/gad.997902
132. Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Herve P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. The Plant Journal 54, 375-387. doi: 10.1111/j.1365-313X.2008.03426.x