Kültür Bitkilerinde Apomiksi Genlerinin Klonlanması

Year 2017, Volume: 10 Issue: 1, 38 - 67, 28.06.2017

Kemal Melik Taşkın

Abstract

Kültür bitkilerinin iyileştirilmesi
amacıyla uygulanan birçok ıslah stratejisinde elde edilen ticari hibritler
üstün özelliklerini genetik açılımlardan dolayı sonraki döllerde koruyamazlar.
Apomiksi, ana bitki ile genetik olarak özdeş tohumlar oluşturmasına olanak
sağlayan ve kültür bitkilerinde başarıldığı takdirde ticari hibritlerin klonal
çoğaltımına izin veren bir üreme şeklidir. Eşeyli üreme mayoz geçirmiş
gametlerin oluşumu ve çifte döllenmeyi gerektiren bir süreçtir. Fakat apomiksi
sırasında bu adımlardan birçoğu ya atlanır ya da değiştirilmiştir. Apomiktik
türlerde, erkek ve dişi gametlerde kromozom sayısı yarıya inmez (apomayoz) buna
rağmen embriyo kesesi ve polen oluşumu devam eder. Ayrıca, apomayotik yumurta
hücresi (2n) döllenme olmaksızın kendiliğinden embriyoyu oluşturur
(partenogenez). Bu nedenle, apomiksi tohum aracılığı ile klonal çoğalmaya yol
açar. Buna karşın, henüz apomiksi doğal apomiktik türlerden tarımı yapılan
kültür bitkilerine melezleme yolu ile aktarım başarılamamıştır. Günümüzde bu
konuda araştırmacılar iki farklı alanda çalışmalar yürütmektedir; doğal
apomiktik bitki türlerinde sorumlu genleri belirlemek veya eşeyli üreme
süreçlerini değiştiren düzenlenmeler sayesinde apomiksiyi oluşturmak. Bu
derlemede, apomiksiyi kontrol eden genetik mekanizmalar üzerine bu güne kadar
elde edilmiş sonuçlar tartışılmıştır.

Keywords

Diplospori, Apospori, Sporofitik apomiksi, Klonal tohum eldesi, Apomayoz

Cloning Apomixis Genes in Crops

Abstract

Hybrid plants,
produced by many breeding strategies for improvement of culture plants could
not conserve their hybrid vigor within the next generations. Apomixis is a
reproduction way which creates genetically identical seeds with the maternal
plant and it will enable the clonal reproduction of hybrids when it is achieved
in culture plants. Sexual reproduction is a process involves gametes formed by
meiosis and double fertilization. However, in apomictic process, many of these
steps are either bypassed or modified. In apomict species; chromosome number in
male and female gametes are not reduced (apomeiosis), nevertheless embryo sac
and pollen formation continues. Furthermore, the apomeiotic egg cell (2n)
spontaneously forms the embryo (parthenogenesis). Therefore, apomixis leads to
clonal reproduction by seeds. Although, introduction of apomixis from natural
apomicts to culture plants haven’t been achieved by hybridization methods.
Recently researchers have been working on this subject with two different
strategies. In this review, the recent knowledge about the molecular mechanisms
controlling apomixis are discussed.

Keywords

Diplospory, Apospory, Sporophytic apomixis, Apomeiosis, Clonal seed production

References

• Akiyama Y., Conner J.A., Goel S., Morishige D.T., Mullet J.E., Hanna W.W., Ozias-Akins P., 2004. High-resolution physical mapping in Pennisetum squamulatum reveals extensive chromosomal heteromorphism of the genomic region associated with apomixis. Plant Physiology, 134 (4): 1733-1741.
• Albertini E., Barcaccia G., Porceddu A., Sorbolini S., Falcinelli M., 2001a. Mode of reproduction is detected by Parth1 and Sex1 SCAR markers in a wide range of facultative apomictic Kentucky bluegrass varieties. Molecular Breeding, 7 (4): 293-300.
• Albertini E., Porceddu A., Ferranti F., Reale L., Barcaccia G., Romano B., Falcinelli M., 2001b. Apospory and parthenogenesis may be uncoupled in Poa pratensis: a cytological investigation. Sexual Plant Reproduction, 14 (4): 213-217.
• Alleman M., Doctor J., 2000. Genomic imprinting in plants: observations and evolutionary implications. Plant Molecular Biology, 43 (2-3): 147-161.
• Anton A.M., Connor H.E., 1995. Floral biology and reproduction in Poa (Poeae: Gramineae). Australian Journal of Botany, 43 (6): 577-599.
• Barcaccia G., Mazzucato A., Albertini E., Zethof J., Gerats A., Pezzotti M., Falcinelli M., 1998. Inheritance of parthenogenesis in Poa pratensis L.: auxin test and AFLP linkage analyses support monogenic control. Theoretical and Applied Genetics, 97 (1-2): 74-82.
• Bicknell R.A., Borst N.K., Koltunow A.M., 2000. Monogenic inheritance of apomixis in two Hieracium species with distinct developmental mechanisms. Heredity, 84 (2): 228-237.
• Blakey C.A., Goldman S.L., Dewald C.L., 2001. Apomixis in Tripsacum: Comparative mapping of a multigene phenomenon. Genome, 44 (2): 222-230.
• Bonilla J.R., Quarin C.L., 1997. Diplosporous and aposporous apomixis in a pentaploid race of Paspalum minus. Plant Science, 127 (1): 97-104.
• Boutilier K., Offringa R., Sharma V.K., Kieft H., Ouellet T., Zhang L.M., Hattori J., Liu C.M., van Lammeren A.A.M., Miki B.L.A., Custers J.B.M., Campagne M.M.V., 2002. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell, 14 (8): 1737-1749.
• Böcher T., 1951. Cytological and Embryological Studies in the Amphi-Apomictic Arabis holboellii Complex. Biol. Skrif., 6: 1-58.
• Carman J.G., 1997. Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biological Journal of the Linnean Society, 61 (1): 51-94.
• Catanach A.S., Erasmuson S.K., Podivinsky E., Jordan B.R., 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 (49): 18650-18655.
• Chaudhury A.M., Koltunow A., Payne T., Luo M., Tucker M.R., Dennis E.S., Peacock W.J., 2001. Control of early seed development. Annual Review of Cell and Developmental Biology, 17: 677-699.
• Chaudhury A.M., Ming L., Miller C., Craig S., Dennis E.S., Peacock W.J., 1997. Fertilization-independent seed development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 94 (8): 4223-4228.
• Chen L.Z., Miyazaki C., Kojima A., Saito A., Adachi T., 1999. Isolation and characterization of a gene expressed during early embryo sac development in apomictic guinea grass (Panicum maximum). Journal of Plant Physiology, 154 (1): 55-62.
• Conner J.A., Goel S., Gunawan G., Cordonnier-Pratt M.M., Johnson V.E., Liang C., Wang H., Pratt L.H., Mullet J.E., DeBarry J., Yang L., Bennetzen J.L., Klein P.E., Ozias-Akins P., 2008. Sequence analysis of bacterial artificial chromosome clones from the apospory-specific genomic region of Pennisetum and Cenchrus. Plant Physiology, 147 (3): 1396-1411.
• Conner J.A., Gunawan G., Ozias-Akins P., 2013. Recombination within the apospory specific genomic region leads to the uncoupling of apomixis components in Cenchrus ciliaris. Planta, 238 (1): 51-63.
• Crane C.F., Carman J.G., 1987. Mechanisms of Apomixis in Elymus-Rectisetus from Eastern Australia and New-Zealand. American Journal of Botany, 74 (4): 477-496.
• Drews G.N., Lee D., Christensen G.A., 1998. Genetic analysis of female gametophyte development and function. Plant Cell, 10 (1): 5-17.
• Garcia-Aguilar M., Michaud C., Leblanc O., Grimanelli D., 2010. Inactivation of a DNA Methylation Pathway in Maize Reproductive Organs Results in Apomixis-Like Phenotypes. Plant Cell, 22 (10): 3249-3267.
• Grimanelli D., Garcia M., Kaszas E., Perotti E., Leblanc O., 2003. Heterochronic expression of sexual reproductive programs during apomictic development in tripsacum. Genetics, 165 (3): 1521-1531.
• Grimanelli D., Hernandez M., Perotti E., Savidan Y., 1997. Dosage effects in the endosperm of diplosporous apomictic Tripsacum (Poaceae). Sexual Plant Reproduction, 10 (5): 279-282.
• Grimanelli D., Leblanc O., Espinosa E., Perotti E., De Leon D.G., Savidan Y., 1998a. Mapping diplosporous apomixis in tetraploid Tripsacum: one gene or several genes? Heredity, 80: 33-39.
• Grimanelli D., Leblanc O., Espinosa E., Perotti E., De Leon D.G., Savidan Y., 1998b. Non-Mendelian transmission of apomixis in maize-Tripsacum hybrids caused by a transmission ratio distortion. Heredity, 80: 40-47.
• Grimanelli D., Leblanc O., Perotti E., Grossniklaus U., 2001. Developmental genetics of gametophytic apomixis. Trends in Genetics, 17 (10): 597-604.
• Grossniklaus U., Koltunow A., Campagne M.V., 1998a. A bright future for apomixis. Trends in Plant Science, 3 (11): 415-416.
• Grossniklaus U., Nogler G.A., van Dijk P.J., 2001a. How to avoid sex: The genetic control of gametophytic apomixis. Plant Cell, 13 (7): 1491-1497.
• Grossniklaus U., Spillane C., Page D.R., Kohler C., 2001b. Genomic imprinting and seed development: endosperm formation with and without sex. Current Opinion in Plant Biology, 4 (1): 21-27.
• Grossniklaus U., Vielle-Calzada J.P., Hoeppner M.A., Gagliano W.B., 1998b. Maternal control of embryogenesis by medea, a Polycomb group gene in Arabidopsis. Science, 280 (5362): 446-450.
• Haig D., Westoby M., 1991. Genomic Imprinting in Endosperm - Its Effect on Seed Development in Crosses between Species, and between Different Ploidies of the Same Species, and Its Implications for the Evolution of Apomixis. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 333 (1266): 1-13.
• Hand M.L., Koltunow A.M.G., 2014. The Genetic Control of Apomixis: Asexual Seed Formation. Genetics, 197 (2): 441-450.
• Hecht V., Vielle-Calzada J.P., Hartog M.V., Schmidt E.D.L., Boutilier K., Grossniklaus U., de Vries S.C., 2001. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiology, 127 (3): 803-816.
• Juranic M., Srilunchang K.O., Krohn N.G., Leljak-Levanic D., Sprunck S., Dresselhaus T., 2012. Germline-Specific MATH-BTB Substrate Adaptor MAB1 Regulates Spindle Length and Nuclei Identity in Maize. Plant Cell, 24 (12): 4974-4991.
• Kindiger B., Sokolov V., Dewald C., 1996. A comparison of apomictic reproduction in eastern gamagrass (Tripsacum dactyloides (L) L) and maize-Tripsacum hybrids. Genetica, 97 (1): 103-110.
• Kojima A., Nagato Y., 1992. Diplosporous Embryo-Sac Formation and the Degree of Diplospory in Allium-Tuberosum. Sexual Plant Reproduction, 5 (1): 72-78.
• Koltunow A.M., 1993. Apomixis - Embryo Sacs and Embryos Formed without Meiosis or Fertilization in Ovules. Plant Cell, 5 (10): 1425-1437.
• Koltunow A.M., Bicknell R.A., Chaudhury A.M., 1995. Apomixis - Molecular Strategies for the Generation of Genetically Identical Seeds without Fertilization. Plant Physiology, 108 (4): 1345-1352.
• Koltunow A.M., Grossniklaus U., 2003. Apomixis: A developmental perspective. Annual Review of Plant Biology, 54: 547-574.
• Koltunow A.M., Johnson S.D., Bicknell R.A., 1998. Sexual and apomictic development in Hieracium. Sexual Plant Reproduction, 11 (4): 213-230.
• Koltunow A.M., Johnson S.D., Bicknell R.A., 2000. Apomixis is not developmentally conserved in related, genetically characterized Hieracium plants of varying ploidy. Sexual Plant Reproduction, 12 (5): 253-266.
• Koltunow A.M.G., Johnson S.D., Rodrigues J.C.M., Okada T., Hu Y.K., Tsuchiya T., Wilson S., Fletcher P., Ito K., Suzuki G., Mukai Y., Fehrer J., Bicknell R.A., 2011. Sexual reproduction is the default mode in apomictic Hieracium subgenus Pilosella, in which two dominant loci function to enable apomixis. Plant Journal, 66 (5): 890-902.
• Kotani Y., Henderson S.T., Suzuki G., Johnson S.D., Okada T., Siddons H., Mukai Y., Koltunow A.M.G., 2014. The LOSS OF APOMEIOSIS (LOA) locus in Hieracium praealtum can function independently of the associated large-scale repetitive chromosomal structure. New Phytologist, 201 (3): 973-981.
• Leblanc O., Armstead I., Pessino S., Ortiz J.P., Evans C., doValle C., Hayward M.D., 1997. Non-radioactive mRNA fingerprinting to visualise gene expression in mature ovaries of Brachiaria hybrids derived from B-brizantha, an apomictic tropical forage. Plant Science, 126 (1): 49-58.
• Leblanc O., Grimanelli D., Gonzalezdeleon D., Savidan Y., 1995a. Detection of the Apomictic Mode of Reproduction in Maize-Tripsacum Hybrids Using Maize Rflp Markers. Theoretical and Applied Genetics, 90 (7-8): 1198-1203.
• Leblanc O., Grimanelli D., IslamFaridi N., Berthaud J., Savidan Y., 1996. Reproductive behavior in maize-Tripsacum polyhaploid plants: Implications for the transfer of apomixis into maize. Journal of Heredity, 87 (2): 108-111.
• Leblanc O., Peel M.D., Carman J.G., Savidan Y., 1995b. Megasporogenesis and Megagametogenesis in Several Tripsacum Species (Poaceae). American Journal of Botany, 82 (1): 57-63.
• Lutts S., Ndikumana J., Louant B.P., 1994. Male and Female Sporogenesis and Gametogenesis in Apomictic Brachiaria-Brizantha, Brachiaria-Decumbens and F1 Hybrids with Sexual Colchicine Induced Tetraploid Brachiaria-Ruziziensis. Euphytica, 78 (1-2): 19-25.
• Ma G.H., Huang X.L., Zhao N.X., Xu Q.S., 2004. Apospory in Paspalum thunbergii. Australian Journal of Botany, 52 (1): 81-86.
• Marimuthu M.P.A., Jolivet S., Ravi M., Pereira L., Davda J.N., Cromer L., Wang L.L., Nogue F., Chan S.W.L., Siddiqi I., Mercier R., 2011. Synthetic Clonal Reproduction Through Seeds. Science, 331 (6019): 876-876.
• Marshall D.R., Brown A.H.D., 1981. The Evolution of Apomixis. Heredity, 47 (Aug): 1-15.
• Martinez E.J., Hopp H.E., Stein J., Ortiz J.P.A., Quarin C.L., 2003. Genetic characterization of apospory in tetraploid Paspalum notatum based on the identification of linked molecular markers. Molecular Breeding, 12 (4): 319-327.
• Martinez E.J., Urbani M.H., Quarin C.L., Ortiz J.P.A., 2001. Inheritance of apospory in babliagrass, Paspalum notatum. Hereditas, 135 (1): 19-25.
• Martonfi P., Brutovska R., Cellarova E., Repcak M., 1996. Apomixis and hybridity in Hypericum perforatum. Folia Geobotanica & Phytotaxonomica, 31 (3): 389-396.
• Matzk F., Hammer K., Schubert I., 2003. Coevolution of apomixis and genome size within the genus Hypericum. Sexual Plant Reproduction, 16 (2): 51-58.
• Matzk F., Meister A., Brutovska R., Schubert I., 2001. Reconstruction of reproductive diversity in Hypericum perforatum L. opens novel strategies to manage apomixis. Plant Journal, 26 (3): 275-282.
• Matzk F., Meister A., Schubert I., 2000. An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant Journal, 21 (1): 97-108.
• Mieulet D., Jolivet S., Rivard M., Cromer L., Vernet A., Mayonove P., Pereira L., Droc G., Courtois B., Guiderdoni E., Mercier R., 2016. Turning rice meiosis into mitosis. Cell Res.
• Mogie M., 1988. A Model for the Evolution and Control of Generative Apomixis. Biological Journal of the Linnean Society, 35 (2): 127-153.
• Morgan R., Ozias-Akins P., Hanna W.W., 1998. Seed set in an apomictic BC3 pearl millet. International Journal of Plant Sciences, 159 (1): 89-97.
• Naumova T., Dennijs A.P.M., Willemse M.T.M., 1993. Quantitative-Analysis of Aposporous Parthenogenesis in Poa-Pratensis Genotypes. Acta Botanica Neerlandica, 42 (3): 299-312.
• Naumova T.N., 1997. Apomixis in tropical fodder crops: cytological and functional aspects. Euphytica, 96 (1): 93-99. Naumova T.N., Hayward M.D., Wagenvoort M., 1999. Apomixis and sexuality in diploid and tetraploid accessions of Brachiaria decumbens. Sexual Plant Reproduction, 12 (1): 43-52.
• Naumova T.N., van der Laak J., Osadtchiy J., Matzk F., Kravtchenko A., Bergervoet J., Ramulu K.S., Boutilier K., 2001. Reproductive development in apomictic populations of Arabis holboellii (Brassicaceae). Sexual Plant Reproduction, 14 (4): 195-200.
• Naumova T.N., Willemse M.T.M., 1995. Ultrastructural Characterization of Apospory in Panicum-Maximum. Sexual Plant Reproduction, 8 (4): 197-204.
• Ng J., Hart C.M., Morgan K., Simon J.A., 2000. A Drosophila ESC-E(Z) protein complex is distinct from other polycomb group complexes and contains covalently modified ESC. Molecular and Cellular Biology, 20 (9): 3069-3078.
• Nogler G.A., 1995. Genetics of Apomixis in Ranunculus-Auricomus .6. Epilogue. Botanica Helvetica, 105 (1): 111-115.
• Noyes R.D., 2005. Inheritance of apomeiosis (diplospory) in fleabanes (Erigeron, Asteraceae). Heredity, 94 (2): 193-198.
• Noyes R.D., Allison J.R., 2005. Cytology, ovule development, and pollen quality in sexual Erigeron strigosus (Asteraceae). International Journal of Plant Sciences, 166 (1): 49-59.
• Noyes R.D., Rieseberg L.H., 2000. Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics, 155 (1): 379-390.
• Oettler G., Burger H., Melchinger A.E., 2003. Heterosis and combining ability for grain yield and other agronomic traits in winter triticale. Plant Breeding, 122 (4): 318-321.
• Ogawa D., Johnson S.D., Henderson S.T., Koltunow A.M.G., 2013. Genetic separation of autonomous endosperm formation (AutE) from the two other components of apomixis in Hieracium. Plant Reprod, 26 (2): 113-123.
• Ohad N., Margossian L., Hsu Y.C., Williams C., Repetti P., Fischer R.L., 1996. A mutation that allows endosperm development without fertilization. Proceedings of the National Academy of Sciences of the United States of America, 93 (11): 5319-5324.
• Okada T., Hu Y.K., Tucker M.R., Taylor J.M., Johnson S.D., Spriggs A., Tsuchiya T., Oelkers K., Rodrigues J.C.M., Koltunow A.M.G., 2013. Enlarging Cells Initiating Apomixis in Hieracium praealtum Transition to an Embryo Sac Program prior to Entering Mitosis. Plant Physiology, 163 (1): 216-231.
• Okada T., Ito K., Johnson S.D., Oelkers K., Suzuki G., Houben A., Mukai Y., Koltunow A.M., 2011. Chromosomes Carrying Meiotic Avoidance Loci in Three Apomictic Eudicot Hieracium Subgenus Pilosella Species Share Structural Features with Two Monocot Apomicts. Plant Physiology, 157 (3): 1327-1341.
• Olmedo-Monfil V., Duran-Figueroa N., Arteaga-Vazquez M., Demesa-Arevalo E., Autran D., Grimanelli D., Slotkin R.K., Martienssen R.A., Vielle-Calzada J.P., 2010. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature, 464 (7288): 628-U200.
• Ozias-Akins P., Roche D., Hanna W.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 (9): 5127-5132.
• Peel M.D., Carman J.G., Liu Z.W., Wang R.R.C., 1997. Meiotic anomalies in hybrids between wheat and apomictic Elymus rectisetus (Nees in Lehm) A Love & Conner. Crop Science, 37 (3): 717-723.
• Pessino S.C., Evans C., Ortiz J.P.A., Armstead I., Do Valle C.B., Hayward M.D., 1998. A genetic map of the apospory-region in Brachiaria hybrids: identification of two markers closely associated with the trait. Hereditas, 128 (2): 153-158.
• Pessino S.C., Ortiz J.P.A., Leblanc O., doValle C.B., Evans C., Hayward M.D., 1997. Identification of a maize linkage group related to apomixis in Brachiaria. Theoretical and Applied Genetics, 94 (3-4): 439-444.
• Pfosser M., Amon A., Lelley T., Heberlebors E., 1995. Evaluation of Sensitivity of Flow-Cytometry in Detecting Aneuploidy in Wheat Using Disomic and Ditelosomic Wheat-Rye Addition Lines. Cytometry, 21 (4): 387-393.
• Plitmann U., 2002. Agamospermy is much more common than conceived: A hypothesis. Israel Journal of Plant Sciences, 50: 111-117.
• Pupilli F., Martinez E.J., Busti A., Calderini O., Quarin C.L., Arcioni S., 2004. Comparative mapping reveals partial conservation of synteny at the apomixis locus in Paspalum spp. Molecular Genetics and Genomics, 270 (6): 539-548.
• Ravi M., Chan S.W.L., 2010. Haploid plants produced by centromere-mediated genome elimination. Nature, 464 (7288): 615-U180.
• Ravi M., Marimuthu M.P.A., Siddiqi I., 2008. Gamete formation without meiosis in Arabidopsis. Nature, 451 (7182): 1121-U1110.
• Rieseberg L.H., Noyes R.D., 1998. Genetic map-based studies of reticulate evolution in plants. Trends in Plant Science, 3 (7): 254-259.
• Roche D., Cong P.S., Chen Z.B., Hanna W.W., Gustine D.L., Sherwood R.T., Ozias-Akins P., 1999. An apospory-specific genomic region is conserved between Buffelgrass (Cenchrus ciliaris L.) and Pennisetum squamulatum Fresen. Plant Journal, 19 (2): 203-208.
• Roche D., Conner J.A., Budiman M.A., Frisch D., Wing R., Hanna W.W., Ozias-Akins P., 2002. Construction of BAC libraries from two apomictic grasses to study the microcolinearity of their apospory-specific genomic regions. Theoretical and Applied Genetics, 104 (5): 804-812.
• Roy B.A., 1995. The Breeding Systems of 6 Species of Arabis (Brassicaceae). American Journal of Botany, 82 (7): 869-877.
• Roy B.A., Rieseberg L.H., 1989. Evidence for Apomixis in Arabis. Journal of Heredity, 80 (6): 506-508.
• Schallau A., Arzenton F., Johnston A.J., Hahnel U., Koszegi D., Blattner F.R., Altschmied L., Haberer G., Barcaccia G., Baumlein H., 2010. Identification and genetic analysis of the APOSPORY locus in Hypericum perforatum L. Plant Journal, 62 (5): 773-784.
• Schneitz K., 1999. The molecular and genetic control of ovule development. Current Opinion in Plant Biology, 2 (1): 13-17.
• Schneitz K., Hulskamp M., Kopczak S.D., Pruitt R.E., 1997. Dissection of sexual organ ontogenesis: A genetic analysis of ovule development in Arabidopsis thaliana. Development, 124 (7): 1367-1376.
• Schneitz K., Hulskamp M., Pruitt R.E., 1995. Wild-Type Ovule Development in Arabidopsis-Thaliana - a Light-Microscope Study of Cleared Whole-Mount Tissue. Plant Journal, 7 (5): 731-749.
• Sezer F., Yuzbasioglu G., Ozbilen A., Taskin K.M., 2016. Genome-wide identification and expression analysis of SWI1 genes in Boechera species. Comput Biol Chem, 62: 75-81.
• Sharbel T.F., Mitchell-Olds T., 2001. Recurrent polyploid origins and chloroplast phylogeography in the Arabis holboellii complex (Brassicaceae). Heredity, 87: 59-68.
• Sharbel T.F., Voigt M.-L., Corral J.M., Galla G., Kumlehn J., Klukas C., Schreiber F., Vogel H., Rotter B., 2010a. Apomictic and Sexual Ovules of Boechera Display Heterochronic Global Gene Expression Patterns. Plant Cell: tpc.109.072223.
• Sharbel T.F., Voigt M.L., Corral J.M., Galla G., Kumlehn J., Klukas C., Schreiber F., Vogel H., Rotter B., 2010b. Apomictic and Sexual Ovules of Boechera Display Heterochronic Global Gene Expression Patterns. Plant Cell, 22 (3): 655-671.
• Sherwood R.T., Berg C.C., Young B.A., 1994. Inheritance of Apospory in Buffelgrass. Crop Science, 34 (6): 1490-1494.
• Silveira E.D., Guimaraes L.A., Dusi D.M.D., da Silva F.R., Martins N.F., Costa M.M.D., Alves-Ferreira M., Carneiro V.T.D., 2012. Expressed sequence-tag analysis of ovaries of Brachiaria brizantha reveals genes associated with the early steps of embryo sac differentiation of apomictic plants. Plant Cell Reports, 31 (2): 403-416.
• Sokolov V.A., Kindiger B., Khatypova I.V., 1998. Investigation of apomictic maize-Tripsacum hybrids. Genetika, 34 (4): 492-498.
• Spielman M., Vinkenoog R., Scott R.J., 2003. Genetic mechanisms of apomixis. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 358 (1434): 1095-1103.
• Spillane C., Steimer A., Grossniklaus U., 2001. Apomixis in agriculture: the quest for clonal seeds. Sexual Plant Reproduction, 14 (4): 179-187.
• Tas I.C.Q., Van Dijk P.J., 1999. Crosses between sexual and apomictic dandelions (Taraxacum). I. The inheritance of apomixis. Heredity, 83: 707-714.
• Taskin K.M., Turgut K., Scott R.J., 2004. Apomictic development in Arabis gunnisoniana. Israel Journal of Plant Sciences, 52 (2): 155-160.
• Taskin K.M., Turgut K., Scott R.J., 2009. Apomeiotic pollen mother cell development in the apomictic Boechera species. Biologia Plantarum, 53 (3): 468-474.
• Taşkin K.M., Özbilen A., Sezer F., Hürkan K., Güneş Ş., 2017. Structure and expression of dna methyltransferase genes from apomictic and sexual Boechera species. Comput Biol Chem, 67: 15-21.
• Tucker M.R., Araujo A.C.G., Paech N.A., Hecht V., Schmidt E.D.L., Rossell J.B., de Vries S.C., Koltunow A.M.G., 2003. Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. Plant Cell, 15 (7): 1524-1537.
• van Baarlen P., van Dijk P., Hoekstra R.F., de Jong J.H., 2000. Meiotic recombination in sexual diploid and apomictic triploid dandelions (Taraxacum officinale L.). Genome, 43 (5): 827-835.
• van Dijk P.J., Bakx-Schotman J.M.T., 2004. Formation of unreduced megaspores (diplospory) in apomictic dandelions (Taraxacum officinale, s.l) is controlled by a sex-specific dominant locus. Genetics, 166 (1): 483-492.
• Van Dijk P.J., Tas I.C.Q., Falque M., Bakx-Schotman T., 1999. Crosses between sexual and apomictic dandelions (Taraxacum). II. The breakdown of apomixis. Heredity, 83: 715-721.
• VielleCalzada J.P., Nuccio M.L., Budiman M.A., Thomas T.L., Burson B.L., Hussey M.A., Wing R.A., 1996. Comparative gene expression in sexual and apomictic ovaries of Pennisetum ciliare (L) Link. Plant Molecular Biology, 32 (6): 1085-1092.
• Vinkenoog R., Bushell C., Spielman M., Adams S., Dickinson H.G., Scott R.J., 2003. Genomic imprinting and endosperm development in flowering plants. Molecular Biotechnology, 25 (2): 149-184.
• Vinkenoog R., Scott R.J., 2001. Autonomous endosperm development in flowering plants: how to overcome the imprinting problem? Sexual Plant Reproduction, 14 (4): 189-194.
• Vinkenoog R., Spielman M., Adams S., Fischer R.L., Dickinson H.G., Scott R.J., 2000. Hypomethylation promotes autonomous endosperm development and rescues postfertilization lethality in fie mutants. Plant Cell, 12 (11): 2271-2282.
• Young B.A., Sherwood R.T., Bashaw E.C., 1979. Cleared-Pistil and Thick-Sectioning Techniques for Detecting Aposporous Apomixis in Grasses. Canadian Journal of Botany-RevueCanadienne De Botanique, 57 (15): 1668-1672.