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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
EVOLUTIONARY REVIEW

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

Matthew R. Tucker A and Anna M. G. Koltunow A B
+ Author Affiliations
- Author Affiliations

A CSIRO Plant Industry, PO Box 350, Glen Osmond, SA 5064, Australia.

B Corresponding author. Email: anna.koltunow@csiro.au

This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.

Functional Plant Biology 36(6) 490-504 https://doi.org/10.1071/FP09078
Submitted: 7 April 2009  Accepted: 21 April 2009   Published: 1 June 2009

Abstract

Reproduction in the flowering plants (angiosperms) is a dynamic process that relies upon the formation of inflorescences, flowers and eventually seed. Most angiosperms reproduce sexually by generating gametes via meiosis that fuse during fertilisation to initiate embryo and seed development, thereby perpetuating the processes of adaptation and evolution. Despite this, sex is not a ubiquitous reproductive strategy. Some angiosperms have evolved an alternate form of reproduction termed apomixis, which avoids meiosis during gamete formation and leads to the production of embryos without paternal contribution. Therefore, apomixis results in the production of clonal progeny through seed. The molecular nature and evolutionary origin of apomixis remain unclear, but recent studies suggest that apomixis evolved from the same molecular framework supporting sex. In this review, we consider physical and molecular relationships between the two pathways, with a particular focus on the initial stages of female reproduction where apomixis deviates from the sexual pathway. We also consider theories that explain the origin of apomictic processes from sexual progenitors. Detailed characterisation of the relationship between sex and apomixis in an evolutionary and developmental sense is an important step towards understanding how apomixis might be successfully integrated into agriculturally important, but currently sexual crops.

Additional keywords: apomixis, evolution, Hieracium, ovule, reproduction.


Acknowledgements

We apologise to the many investigators who could not be cited in this review due to space restrictions. We especially thank John Bennett, Steve Swain, Susan Johnson and other members of the Koltunow laboratory for helpful comments and discussions. Research in the Koltunow laboratory is supported by a Department of Education, Science and Training (DEST) Australia–India grant.


References


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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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. open url image1

Araujo A, Nobrega J, Pozzobon M, Carneiro V (2005) Evidence of sexuality in induced tetraploids of Brachiaria brizantha (Poaceae). Euphytica 144, 39–50.
Crossref | GoogleScholarGoogle Scholar | open url image1

Asker SE , Jerling L (1992) ‘Apomixis in plants.’ (CRC Press: Boca Raton)

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
CAS | PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bicknell RA (1997) Isolation of a diploid, apomictic plant of Hieracium aurantiacum. Sexual Plant Reproduction 10, 168–172.
Crossref | GoogleScholarGoogle Scholar | open url image1

Blachford A, Doebeli M (2009) On luck and sex. Evolution 63, 40–47.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. The EMBO Journal 17, 170–180.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bouman F (1984) The ovule. In ‘Embryology of angiosperms’. (Ed. BM Johri) pp. 123–157. (Springer-Verlag: Berlin Heidelberg)

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bray RA (1978) Evidence for facultative apomixis in Cenchrus ciliaris. Euphytica 27, 801–804.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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)

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)

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Chapman D, Shivji M, Louis E, Sommer J, Fletcher H, Prodohl P (2007) Virgin birth in a hammerhead shark. Biology Letters 3, 425–427.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology 58, 377–406.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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, 11 436–11 441.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Colombo L, Battaglia R, Kater MM (2008) Arabidopsis ovule development and its evolutionary conservation. Trends in Plant Science 13, 444–450.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Crepet W, Niklas K (2009) Darwin’s second “Abominable mystery”: why are there so many angiosperm species? American Journal of Botany 96, 366–381.
Crossref | GoogleScholarGoogle Scholar | open url image1

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)

Darwin C (1903) ‘More letters of Charles Darwin, a record of his work in hitherto unpublished letters.’ (John Murray: London, UK)

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Deyhle F, Sarkar AK, Tucker EJ, Laux T (2007) WUSCHEL regulates cell differentiation during anther development. Developmental Biology 302, 154–159.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Diévart A, Clark SE (2004) LRR-containing receptors regulating plant development and defense. Development 131, 251–261.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Engelstädter J (2008) Constraints on the evolution of asexual reproduction. BioEssays 30, 1138–1150.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ernst A (1918) ‘Die Bastardierung als Ursache der Apogamie im Pflanzenre.’ (Fischer: Jena, Germany)

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Grimanelli D, Leblanc O, Perotti E, Grossniklaus U (2001) Developmental genetics of gametophytic apomixis. Trends in Genetics 17, 597–604.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Grossniklaus U, Schneitz K (1998) The molecular and genetic basis of ovule and megagametophyte development. Seminars in Cell & Developmental Biology 9, 227–238.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Groß-Hardt R, Lenhard M, Laux T (2002) WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes & Development 16, 1129–1138.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Köhler C, Grossniklaus U (2005) Seed development and genomic imprinting in plants. Progress in Molecular and Subcellular Biology 38, 237–262.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Koltunow AM, Bicknell RA, Chaudhury AM (1995a) Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiology 108, 1345–1352.
CAS | PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Koltunow AM, Johnson SD, Bicknell RA (1998) Sexual and apomictic development in Hieracium. Sexual Plant Reproduction 11, 213–230.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lakshmanan KK , Ambegaokar KK (1984) Polyembryony. In ‘Embryology of angiosperms’. (Ed. BM Johri) pp. 445–474. (Springer-Verlag: Berlin)

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.
CAS | PubMed |
open url image1

Levy A, Erlanger M, Rosenthal M, Epel B (2007) A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. The Plant Journal 49, 669–682.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, 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.
CAS | PubMed |
open url image1

Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annual Review of Plant Biology 56, 393–434.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Mercier R, Grelon M (2008) Meiosis in plants: ten years of gene discovery. Cytogenetic and Genome Research 120, 281–290.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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)

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Naumova TN (1993) ‘Apomixis in angiosperms. Nucellar and integumentary embryony.’ (CRC Press: Boca Raton)

Nogler G (1984) Gametophytic apomixis. In ‘Embryology of angiosperms’. (Ed. BM Johri) pp. 475–518. (Springer-Verlag: Berlin Heidelberg)

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Noyes RD (2000) Diplospory and parthenogenesis in sexual × agamospermous (apomictic) Erigeron (Asteraceae) hybrids. International Journal of Plant Sciences 161, 1–12.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Noyes RD (2005) Inheritance of apomeiosis (diplospory) in fleabanes (Erigeron, Asteraceae). Heredity 94, 193–198.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Otto S (2003) The advantages of segregation and the evolution of sex. Genetics 164, 1099–1118.
PubMed |
open url image1

Ozias-Akins P, van Dijk PJ (2007) Mendelian genetics of apomixis in plants. Annual Review of Genetics 41, 509–537.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ozias-Akins P, Roche D, Hanna W (1998) Tight clustering and hemizygosity 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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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)

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Quarin CL, Hanna WW (1980) Effect of three ploidy levels on meiosis and mode of reproduction in Paspalum hexastachyum. Crop Science 20, 69–75. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Radford J, Vesk M, Overall R (1998) Callose deposition at plasmodesmata. Protoplasma 201, 30–37.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Ravi M, Marimuthu MP, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451, 1121–1124.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Reiser L, Fischer RL (1993) The ovule and the embryo sac. The Plant Cell 5, 1291–1301.
Crossref | PubMed |
open url image1

Rieseberg LH, Willis JH (2007) Plant speciation. Science 317, 910–914.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rinne PL, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. The Plant Journal 26, 249–264.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rodkiewicz B (1970) Callose in cell walls during megasporogensis in angiosperms. Planta 93, 39–47.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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, 11 664–11 669.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. The Plant Cell 16(Suppl), S46–S60.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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. ,
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
CAS | PubMed |
open url image1

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.
CAS | PubMed |
open url image1

Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Science STKE 113, RE22. open url image1

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.
CAS | PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Skinner DJ, Hill TA, Gasser CS (2004) Regulation of ovule development. The Plant Cell 16(Suppl), S32–S45.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Stone BA , Clarke AE (1992) ‘Chemistry & biology of (1,3)-b-glucans.’ (La Trobe University Press: Bundoora, Vic.)

Taylor J, Jacobson D, Fisher M (1999) The evolution of asexual fungi: reproduction, speciation and classification. Annual Review of Phytopathology 37, 197–246.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Theissen G, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Annals of Botany 100, 603–619.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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)

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vaucheret H (2008) Plant ARGONAUTES. Trends in Plant Science 13, 350–358.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Webb MC, Gunning BES (1990) Embryo sac development in Arabidopsis thaliana. I. Megasporogenesis, including the microtubular cytoskeleton. Sexual Plant Reproduction 3, 244–256.
Crossref |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Webb MC, Gunning BES (1994) Embryo sac development in Arabidopsis thaliana II: The cytoskeleton during megagametogenesis. Sexual Plant Reproduction 7, 153–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Willemse MTM, De Boer-De Jeu MJ (1981) Megasporogenesis and early megagametogenesis. Acta Societatis Botanicorum Poloniae 50, 111–120. open url image1

Willemse MTM , van Went JL (1984) The female gametophyte. In ‘Embryology of angiosperms’. (Ed. BM Johri) pp. 159–191. (Springer-Verlag: Berlin Heidelberg)

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.
CAS | Crossref | PubMed |
open url image1

Wu H, Cheung A (2000) Programmed cell death in plant reproduction. Plant Molecular Biology 44, 267–281.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
CAS |
open url image1

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)

Yang W, Sundaresan V (2000) Genetics of gametophyte biogenesis in Arabidopsis. Current Opinion in Plant Biology 3, 53–57.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1