Plant Reproduction

, Volume 28, Issue 2, pp 91–102 | Cite as

Meiosis, unreduced gametes, and parthenogenesis: implications for engineering clonal seed formation in crops

  • Arnaud Ronceret
  • Jean-Philippe Vielle-CalzadaEmail author
Part of the following topical collections:
  1. From Gametes to Seeds


Key message

Meiosis and unreduced gametes.

Sexual flowering plants produce meiotically derived cells that give rise to the male and female haploid gametophytic phase. In the ovule, usually a single precursor (the megaspore mother cell) undergoes meiosis to form four haploid megaspores; however, numerous mutants result in the formation of unreduced gametes, sometimes showing female specificity, a phenomenon reminiscent of the initiation of gametophytic apomixis. Here, we review the developmental events that occur during female meiosis and megasporogenesis at the light of current possibilities to engineer unreduced gamete formation. We also provide an overview of the current understanding of mechanisms leading to parthenogenesis and discuss some of the conceptual implications for attempting the induction of clonal seed production in cultivated plants.


Meiosis Fertilization Apomixis Sexuality Seed Maize 



We thank Zac Cande and Inna Golubovskaya for their dedication and generosity on sharing their meiotic mutant collection of maize. Research in our laboratory is sponsored by Consejo Nacional de Ciencia y Tecnologia (CONACyT), Consejo de Ciencia y Tecnología del Estado de Guanajuato (CONCyTEG) and the DuPont Pioneer regional initiatives to benefit local subsistence farmers.

Supplementary material

497_2015_262_MOESM1_ESM.xlsx (27 kb)
Supplementary material 1 (XLSX 26 kb)


  1. 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 Physiol 138:2185–2199. doi: 10.1104/pp.105.062059 PubMedCentralPubMedGoogle Scholar
  2. Anderson LK, Lohmiller LD, Tang X, Hammond DB, Javernick L, Shearer L, Basu-Roy S, Martin OC, Falque M (2014) Combined fluorescent and electron microscopic imaging unveils the specific properties of two classes of meiotic crossovers. Proc Natl Acad Sci USA 111:13415–13420. doi: 10.1073/pnas.1406846111 PubMedCentralPubMedGoogle Scholar
  3. Armstrong SJ, Franklin FCH, Jones GH (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207–4217PubMedGoogle Scholar
  4. Asker SE, Jerling L (1992) Apomixis in plants. CRC Press, LondonGoogle Scholar
  5. Barakate A, Higgins JD, Vivera S, Stephens J, Perry RM, Ramsay L, Colas I, Oakey H, Waugh R, Franklin FCH, Armstrong SJ, Halpin C (2014) The synaptonemal complex protein ZYP1 is required for imposition of meiotic crossovers in barley. Plant Cell 26:729–740. doi: 10.1105/tpc.113.121269 PubMedCentralPubMedGoogle Scholar
  6. Barcaccia G, Albertini E (2013) Apomixis in plant reproduction: a novel perspective on an old dilemma. Plant Reprod 26:159–179. doi: 10.1007/s00497-013-0222-y PubMedCentralPubMedGoogle Scholar
  7. Barcaccia G, Varotto S, Meneghetti S, Albertini E, Porceddu A, Parrini P, Lucchin M (2001) Analysis of gene expression during flowering in apomeiotic mutants of Medicago spp.: cloning of ESTs and candidate genes for 2n eggs. Sex Plant Reprod 14:233–238. doi: 10.1007/s00497-001-0108-2 PubMedGoogle Scholar
  8. Barrell PJ, Grossniklaus U (2005) Confocal microscopy of whole ovules for analysis of reproductive development: the elongate1 mutant affects meiosis II. Plant J 43:309–320PubMedGoogle Scholar
  9. Barret P, Brinkmann M, Beckert M (2008) A major locus expressed in the male gametophyte with incomplete penetrance is responsible for in situ gynogenesis in maize. Theor Appl Genet 117:581–594PubMedGoogle Scholar
  10. Berger F, Twell D (2011) Germline specification and function in plants. Annu Rev Plant Biol 62:461–484. doi: 10.1146/annurev-arplant-042110-103824 PubMedGoogle Scholar
  11. Bhullar R, Nagarajan R, Bennypaul H, Sidhu GK, Sidhu G, Rustgi S, von Wettstein D, Gill KS (2014) Silencing of a metaphase I-specific gene results in a phenotype similar to that of the Pairing homeologous 1 (Ph1) gene mutations. Proc Natl Acad Sci USA 111:14187–14192. doi: 10.1073/pnas.1416241111 PubMedCentralPubMedGoogle Scholar
  12. Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16:S228–S245. doi: 10.1105/tpc.017921 PubMedCentralPubMedGoogle Scholar
  13. Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA (2010) Heterosis. Plant Cell 22:2105–2112. doi: 10.1105/tpc.110.076133 PubMedCentralPubMedGoogle Scholar
  14. Boateng KA, Yang X, Dong F, Owen HA, Makaroff CA (2008) SWI1 is required for meiotic chromosome remodeling events. Mol Plant 1:620–633. doi: 10.1093/mp/ssn030 PubMedGoogle Scholar
  15. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu C-M, van Lammeren AAM, Miki BLA, Custers JBM, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749. doi: 10.1105/tpc.001941 PubMedCentralPubMedGoogle Scholar
  16. Bretagnolle F, Thompson JD (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol 129:1–22Google Scholar
  17. Brownfield L, Köhler C (2011) Unreduced gamete formation in plants: mechanisms and prospects. J Exp Bot 62:1659–1668. doi: 10.1093/jxb/erq371 PubMedGoogle Scholar
  18. Bulankova P, Riehs-Kearnan N, Nowack MK, Schnittger A, Riha K (2010) Meiotic progression in arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I-specific cyclin TAM. Plant Cell 22:3791–3803. doi: 10.1105/tpc.110.078378 PubMedCentralPubMedGoogle Scholar
  19. Byun MY, Kim WT (2014) Suppression of OsRAD51D results in defects in reproductive development in rice (Oryza sativa L.). Plant J 79:256–269. doi: 10.1111/tpj.12558 PubMedGoogle Scholar
  20. Cabral G, Marques A, Schubert V, Pedrosa-Harand A, Schlögelhofer P (2014) Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes. Nat Commun. doi: 10.1038/ncomms6070 PubMedCentralPubMedGoogle Scholar
  21. Cai X, Xu S, Zhu X (2010) Mechanism of haploidy-dependent unreductional meiotic cell division in polyploid wheat. Chromosoma 119:275–285. doi: 10.1007/s00412-010-0256-y PubMedGoogle Scholar
  22. 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. Curr Biol 12:1718–1727PubMedGoogle Scholar
  23. Cande WZ, Golubovskaya I, Wang CJR, Harper L (2009) Meiotic genes and meiosis in maize. In: Bennetzen JL, Hake S (eds) Handbook of maize. Springer, New York, pp 353–375Google Scholar
  24. Catanach AS, Erasmuson SK, Podivinsky E, Jordan BR, Bicknell R (2006) Deletion mapping of genetic regions associated with apomixis in Hieracium. Proc Natl Acad Sci USA 103:18650–18655. doi: 10.1073/pnas.0605588103 PubMedCentralPubMedGoogle Scholar
  25. Chan SWL (2010) Chromosome engineering: power tools for plant genetics. Trends Biotechnol 28:605–610. doi: 10.1016/j.tibtech.2010.09.002 PubMedGoogle Scholar
  26. Chang M-T, Coe EH (2009) Doubled haploids. In: Kriz AL, Larkins BA (eds) Molecular genetic approaches to maize improvement. Springer, Berlin, pp 127–142Google Scholar
  27. Chang F, Wang Y, Wang S, Ma H (2011) Molecular control of microsporogenesis in Arabidopsis. Curr Opin Plant Biol 14:66–73. doi: 10.1016/j.pbi.2010.11.001 PubMedGoogle Scholar
  28. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, Rocques N, Marquez-Lema A, Bhatt AM, Horlow C, Mercier R, Mezard C, Grelon M (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118:4621–4632PubMedGoogle Scholar
  29. Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482. doi: 10.1038/nrg3503 PubMedGoogle Scholar
  30. Cifuentes M, Eber F, Lucas M-O, Lode M, Chèvre A-M, Jenczewski E (2010a) Repeated polyploidy drove different levels of crossover suppression between homoeologous chromosomes in Brassica napus allohaploids. Plant Cell 22:2265–2276. doi: 10.1105/tpc.109.072991 PubMedCentralPubMedGoogle Scholar
  31. Cifuentes M, Grandont L, Moore G, Chèvre AM, Jenczewski E (2010b) Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytol 186:29–36. doi: 10.1111/j.1469-8137.2009.03084.x PubMedGoogle Scholar
  32. Cigliano R, Sanseverino W, Cremona G, Consiglio F, Conicella C (2011) Evolution of Parallel Spindles Like genes in plants and highlight of unique domain architecture. BMC Evol Biol 11:78PubMedCentralPubMedGoogle Scholar
  33. Citterio S, Albertini E, Varotto S, Feltrin E, Soattin M, Marconi G, Sgorbati S, Lucchin M, Barcaccia G (2005) Alfalfa Mob1-like genes are expressed in reproductive organs during meiosis and gametogenesis. Plant Mol Biol 58:789–807. doi: 10.1007/s11103-005-8104-9 PubMedGoogle Scholar
  34. Coe EH Jr (1959) A line of maize with high haploid frequency. Am Nat 93:381–382Google Scholar
  35. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361. doi: 10.1105/tpc.105.036731 PubMedCentralPubMedGoogle Scholar
  36. Comai L (2014) Genome elimination: translating basic research into a future tool for plant breeding. PLoS Biol 12:e1001876. doi: 10.1371/journal.pbio.1001876 PubMedCentralPubMedGoogle Scholar
  37. Crismani W, Baumann U, Sutton T, Shirley N, Webster T, Spangenberg G, Langridge P, Able J (2006) Microarray expression analysis of meiosis and microsporogenesis in hexaploid bread wheat. BMC Genom 7:267Google Scholar
  38. Cromer L, Heyman J, Touati S, Harashima H, Araou E, Girard C, Horlow C, Wassmann K, Schnittger A, De Veylder L, Mercier R (2012) OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLoS Genet 8:e1002865. doi: 10.1371/journal.pgen.1002865 PubMedCentralPubMedGoogle Scholar
  39. De Storme N, Geelen D (2011) The Arabidopsis mutant jason produces unreduced first division restitution male gametes through a parallel/fused spindle mechanism in meiosis II. Plant Physiol 155:1403–1415. doi: 10.1104/pp.110.170415 PubMedCentralPubMedGoogle Scholar
  40. De Storme N, Geelen D (2013) Sexual polyploidization in plants—cytological mechanisms and molecular regulation. New Phytol 198:670–684. doi: 10.1111/nph.12184 PubMedCentralPubMedGoogle Scholar
  41. De Storme N, Copenhaver GP, Geelen D (2012) Production of diploid male gametes in arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol 160:1808–1826. doi: 10.1104/pp.112.208611 PubMedCentralPubMedGoogle Scholar
  42. De Storme N, De Schrijver J, Van Criekinge W, Wewer V, Dörmann P, Geelen D (2013) GLUCAN SYNTHASE-LIKE8 and STEROL METHYLTRANSFERASE2 are required for ploidy consistency of the sexual reproduction system in Arabidopsis. Plant Cell 25:387–403. doi: 10.1105/tpc.112.106278 PubMedCentralPubMedGoogle Scholar
  43. Deng Z-Y, Wang T (2007) OsDMC1 is required for homologous pairing in Oryza sativa. Plant Mol Biol 65:31–42. doi: 10.1007/s11103-007-9195-2 PubMedGoogle Scholar
  44. d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Simon M, Jenczewski E, Mercier R (2008) Mutations in AtPS1 (Arabidopsis thaliana Parallel Spindle 1) lead to the production of diploid pollen grains. PLoS Genet 4:e1000274. doi: 10.1371/journal.pgen.1000274 PubMedCentralPubMedGoogle Scholar
  45. d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R (2009) Turning meiosis into mitosis. PLoS Biol 7:e1000124PubMedCentralPubMedGoogle Scholar
  46. d’Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C, Sun Y, To JPC, Berchowitz LE, Copenhaver GP, Mercier R (2010) The CYCLIN-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet 6:e1000989PubMedCentralPubMedGoogle Scholar
  47. Dong Q, Han F (2012) Phosphorylation of histone H2A is associated with centromere function and maintenance in meiosis. Plant J 71:800–809. doi: 10.1111/j.1365-313X.2012.05029.x PubMedGoogle Scholar
  48. Dong X, Xu X, Miao J, Li L, Zhang D, Mi X, Liu C, Tian X, Melchinger AE, Chen S (2013) Fine mapping of qhir1 influencing in vivo haploid induction in maize. Theor Appl Genet 126:1713–1720. doi: 10.1007/s00122-013-2086-9 PubMedGoogle Scholar
  49. Erilova A, Brownfield L, Exner V, Rosa M, Twell D, Scheid OM, Hennig L, Köhler C (2009) Imprinting of the polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLoS Genet 5:e1000663. doi: 10.1371/journal.pgen.1000663 PubMedCentralPubMedGoogle Scholar
  50. Finch RA, Bennett MD (1979) Action of triploid inducer (tri) on meiosis in barley (Hordeum vulgare L.). Heredity 43:87–93Google Scholar
  51. Geiger HH (2009) Doubled haploids. In: Bennetzen JL, Hake S (eds) Handbook of maize. Springer, New York, pp 641–657Google Scholar
  52. Gent JI, Dong Y, Jiang J, Dawe RK (2012) Strong epigenetic similarity between maize centromeric and pericentromeric regions at the level of small RNAs, DNA methylation and H3 chromatin modifications. Nucleic Acids Res 40:1550–1560. doi: 10.1093/nar/gkr862 PubMedCentralPubMedGoogle Scholar
  53. Golubovskaya IN, Mashnenkov AS (1975) Genetic control of meiosis. I. Meiotic mutation in corn (Zea mays L.) afd, causing the elimination of the first meiotic division. Genetika 11:810–816Google Scholar
  54. Golubovskaya IN, Hamant O, Timofejeva L, Wang C-JR, Braun D, Meeley R, Cande WZ (2006) Alleles of afd1 dissect REC8 functions during meiotic prophase I. J Cell Sci 119:3306–3315. doi: 10.1242/jcs.03054 PubMedGoogle Scholar
  55. Grandont L, Jenczewski E, Lloyd A (2013) Meiosis and its deviations in polyploid plants. Cytogenet Genome Res 140:171–184PubMedGoogle Scholar
  56. Grandont L, Cuñado N, Coriton O, Huteau V, Eber F, Chèvre AM, Grelon M, Chelysheva L, Jenczewski E (2014) Homoeologous Chromosome sorting and progression of meiotic recombination in Brassica napus: ploidy does matter! Plant Cell 26:1448–1463. doi: 10.1105/tpc.114.122788 PubMedCentralPubMedGoogle Scholar
  57. Greer E, Martín AC, Pendle A, Colas I, Jones AME, Moore G, Shaw P (2012) The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell 24:152–162. doi: 10.1105/tpc.111.094771 PubMedCentralPubMedGoogle Scholar
  58. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600PubMedCentralPubMedGoogle Scholar
  59. Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, Reader S, Colas I, Moore G (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439:749–752. doi: 10.1038/nature04434 PubMedGoogle Scholar
  60. Grimanelli D, Leblanc O, Espinosa E, Perotti E, Gonzalez De Leon D, Savidan Y (1998) Non-Mendelian transmission of apomixis in maize-Tripsacum hybrids caused by a transmission ratio distortion. Heredity 80:40–47PubMedGoogle Scholar
  61. Grossniklaus U, Nogler GA, van Dijk PJ (2001) How to avoid sex: the genetic control of gametophytic apomixis. Plant Cell 13:1491–1498. doi: 10.1105/tpc.13.7.1491 PubMedCentralPubMedGoogle Scholar
  62. Groszmann M, Greaves IK, Fujimoto R, James Peacock W, Dennis ES (2013) The role of epigenetics in hybrid vigour. Trends Genet 29:684–690. doi: 10.1016/j.tig.2013.07.004 PubMedGoogle Scholar
  63. Guitton A-E, Berger F (2005) Loss of function of MULTICOPY SUPPRESSOR OF IRA 1 produces nonviable parthenogenetic embryos in arabidopsis. Curr Biol 15:750–754PubMedGoogle Scholar
  64. Gustafsson Å (1947) Apomixis in higher plants. II. The causal aspect of apomixis. Lunds Univ Arsskr NF Adv 2:43–71Google Scholar
  65. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668. doi: 10.1242/dev.00963 PubMedGoogle Scholar
  66. Hagberg A, Hagberg G (1980) High frequency of spontaneous haploids in the progeny of an induced mutation in barley. Hereditas 93:341–343. doi: 10.1111/j.1601-5223.1980.tb01375.x Google Scholar
  67. Hamant O, Golubovskaya I, Meeley R, Fiume E, Timofejeva L, Schleiffer A, Nasmyth K, Cande WZ (2005) A REC8-dependent plant Shugoshin is required for maintenance of centromeric cohesion during meiosis and has no mitotic functions. Curr Biol 15:948–954PubMedGoogle Scholar
  68. Hamant O, Ma H, Cande WZ (2006) Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57:267–302. doi: 10.1146/annurev.arplant.57.032905.105255 PubMedGoogle Scholar
  69. Hand ML, Koltunow AMG (2014) The genetic control of apomixis: asexual seed formation. Genetics 197:441–450. doi: 10.1534/genetics.114.163105 PubMedGoogle Scholar
  70. Havekes FWJ, de Jong JH, Heyting C, Ramanna MS (1994) Synapsis and chiasma formation in four meiotic mutants of tomato (Lycopersicon esculentum). Chromosome Res 2:315–325PubMedGoogle Scholar
  71. Hecht V, Vielle-Calzada J-P, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816. doi: 10.1104/pp.010324 PubMedCentralPubMedGoogle Scholar
  72. Heckmann S, Jankowska M, Schubert V, Kumke K, Ma W, Houben A (2014) Alternative meiotic chromatid segregation in the holocentric plant Luzula elegans. Nat Commun. doi: 10.1038/ncomms5979 Google Scholar
  73. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500. doi: 10.1101/gad.354705 PubMedCentralPubMedGoogle Scholar
  74. Higgins JD, Osman K, Jones GH, Franklin FCH (2014) Factors underlying restricted crossover localization in barley meiosis. Annu Rev Genet 48:29–47. doi: 10.1146/annurev-genet-120213-092509 PubMedGoogle Scholar
  75. Hu X, Cheng X, Jiang H, Zhu S, Cheng B, Xiang Y (2010) Genome-wide analysis of cyclins in maize (Zea mays). Genet Mol Res 9:1490–1503. doi: 10.4238/vol9-3gmr861 PubMedGoogle Scholar
  76. Iwata E, Ikeda S, Matsunaga S, Kurata M, Yoshioka Y, Criqui M-C, Genschik P, Ito M (2011) GIGAS CELL1, a novel negative regulator of the anaphase-promoting complex/cyclosome, is required for proper mitotic progression and cell fate determination in Arabidopsis. Plant Cell 23:4382–4393. doi: 10.1105/tpc.111.092049 PubMedCentralPubMedGoogle Scholar
  77. Jin W, Lamb J, Zhang W, Kolano B, Birchler J, Jiang J (2008) Histone modifications associated with both A and B chromosomes of maize. Chromosome Res 16:1203–1214. doi: 10.1007/s10577-008-1269-8 PubMedGoogle Scholar
  78. Kelliher T, Walbot V (2012) Hypoxia triggers meiotic fate acquisition in maize. Science 337:345–348. doi: 10.1126/science.1220080 PubMedCentralPubMedGoogle Scholar
  79. Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153. doi: 10.1105/tpc.8.2.137 PubMedCentralPubMedGoogle Scholar
  80. Koltunow AM, Grossniklaus U (2003) Apomixis: a developmental perspective. Annu Rev Plant Biol 54:547–574. doi: 10.1146/annurev.arplant.54.110901.160842 PubMedGoogle Scholar
  81. Koltunow AMG, Johnson SD, Rodrigues JCM, Okada T, Hu Y, Tsuchiya T, Wilson S, Fletcher P, Ito K, Suzuki G, Mukai Y, Fehrer J, Bicknell RA (2011) Sexual reproduction is the default mode in apomictic Hieracium subgenus Pilosella, in which two dominant loci function to enable apomixis. Plant J 66:890–902. doi: 10.1111/j.1365-313X.2011.04556.x PubMedGoogle Scholar
  82. Kumlehn J, Kirik V, Czihal A, Altschmied L, Matzk F, Lörz H, Bäumlein H (2001) Parthenogenetic egg cells of wheat: cellular and molecular studies. Sex Plant Reprod 14:239–243PubMedGoogle Scholar
  83. Lashermes P, Beckert M (1988) Genetic control of maternal haploidy in maize (Zea mays L.) and selection of haploid inducing lines. Theor Appl Genet 76:405–410. doi: 10.1007/BF00265341 PubMedGoogle Scholar
  84. Lau S, Slane D, Herud O, Kong J, Jürgens G (2012) Early embryogenesis in flowering plants: setting up the basic body pattern. Annu Rev Plant Biol 63:483–506. doi: 10.1146/annurev-arplant-042811-105507 PubMedGoogle Scholar
  85. Leflon M, Grandont L, Eber F, Huteau V, Coriton O, Chelysheva L, Jenczewski E, Chèvre A-M (2010) Crossovers get a boost in brassica allotriploid and allotetraploid hybrids. Plant Cell 22:2253–2264. doi: 10.1105/tpc.110.075986 PubMedCentralPubMedGoogle Scholar
  86. Lermontova I, Koroleva O, Rutten T, Fuchs J, Schubert V, Moraes I, Koszegi D, Schubert I (2011) Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J 68:40–50. doi: 10.1111/j.1365-313X.2011.04664.x PubMedGoogle Scholar
  87. Li J, Wen T-J, Schnable PS (2008) Role of RAD51 in the repair of MuDR-induced double-strand breaks in maize (Zea mays L.). Genetics 178:57–66. doi: 10.1534/genetics.107.080374 PubMedCentralPubMedGoogle Scholar
  88. Li L, Xu X, Jin W, Chen S (2009) Morphological and molecular evidences for DNA introgression in haploid induction via a high oil inducer CAUHOI in maize. Planta 230:367–376. doi: 10.1007/s00425-009-0943-1 PubMedGoogle Scholar
  89. Lotan T, M-a Ohto, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205PubMedGoogle Scholar
  90. Luo Q, Li Y, Shen Y, Cheng Z (2014) Ten years of gene discovery for meiotic event control in rice. J Genet Genomics 41:125–137. doi: 10.1016/j.jgg.2014.02.002 PubMedGoogle Scholar
  91. Lutes AA, Neaves WB, Baumann DP, Wiegraebe W, Baumann P (2010) Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature 464:283–286. doi: 10.1038/nature08818 PubMedCentralPubMedGoogle Scholar
  92. Magnard J-L, Yang M, Chen Y-CS, Leary M, McCormick S (2001) The arabidopsis gene Tardy Asynchronous Meiosis is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiol 127:1157–1166PubMedCentralPubMedGoogle Scholar
  93. Marimuthu MPA, Jolivet S, Ravi M, Pereira L, Davda JN, Cromer L, Wang L, Nogué F, Chan SWL, Siddiqi I, Mercier R (2011) Synthetic clonal reproduction through seeds. Science 331:876. doi: 10.1126/science.1199682 PubMedGoogle Scholar
  94. Matzk F (1996) The ‘Salmon System’ of wheat; a suitable model for apomixis research. Hereditas 125:299–304Google Scholar
  95. Mayer U, Jurgens G (1998) Pattern formation in plant embryogenesis: a reassessment. Semin Cell Dev Biol 9:187–193PubMedGoogle Scholar
  96. Mercier R, Grelon M (2008) Meiosis in plants: ten years of gene discovery. Cytogenet Genome Res 120:281–290PubMedGoogle Scholar
  97. 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 Dev 15:1859–1871PubMedCentralPubMedGoogle Scholar
  98. Mercier R, Armstrong SJ, Horlow C, Jackson NP, Makaroff CA, Vezon D, Pelletier G, Jones GH, Franklin FCH (2003) The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130:3309–3318PubMedGoogle Scholar
  99. Nel PM (1975) Crossing over and diploid egg formation in the elongate mutant of maize. Genetics 79:435–450PubMedCentralPubMedGoogle Scholar
  100. Nogler G (1984) Gametophytic apomixis. In: Johri B (ed) Embryology of angiosperms. Springer, New York, pp 475–518Google Scholar
  101. Nonomura K-I, 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. Plant Cell 15:1728–1739. doi: 10.1105/tpc.012401 PubMedCentralPubMedGoogle Scholar
  102. Noyes RD, Rieseberg LH (2000) Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics 155:379–390PubMedCentralPubMedGoogle Scholar
  103. Ochogavía A, Seijo J, González A, Podio M, Duarte Silveira E, Machado Lacerda A, de Campos Tavares, Carneiro V, Ortiz J, Pessino S (2011) Characterization of retrotransposon sequences expressed in inflorescences of apomictic and sexual Paspalum notatum plants. Sex Plant Reprod 24:231–246. doi: 10.1007/s00497-011-0165-0 PubMedGoogle Scholar
  104. Ozias-Akins P, van Dijk PJ (2007) Mendelian genetics of apomixis in plants. Annu Rev Genet 41:509. doi: 10.1146/annurev.genet.40.110405.090511 PubMedGoogle Scholar
  105. Palmer RG, Sandhu D, Curran K, Bhattacharyya MK (2008) Molecular mapping of 36 soybean male-sterile, female-sterile mutants. Theor Appl Genet 117:711–719. doi: 10.1007/s00122-008-0812-5 PubMedGoogle Scholar
  106. Pawlowski WP, Golubovskaya IN, Timofejeva L, Meeley RB, Sheridan WF, Cande WZ (2004) Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science 303:89–92. doi: 10.1126/science.1091110 PubMedGoogle Scholar
  107. Pawlowski WP, Sheehan MJ, Ronceret A (2007) In the beginning: the initiation of meiosis. BioEssays 29:511–514PubMedGoogle Scholar
  108. Pawlowski WP, Wang C-JR, Golubovskaya IN, Szymaniak JM, Shi L, Hamant O, Zhu T, Harper L, Sheridan WF, Cande WZ (2009) Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc Natl Acad Sci USA 106:3603–3608. doi: 10.1073/pnas.0810115106 PubMedCentralPubMedGoogle Scholar
  109. Peloquin SJ, Boiteux LS, Carputo D (1999) Meiotic mutants in potato: valuable variants. Genetics 153:1493–1499PubMedCentralPubMedGoogle Scholar
  110. Phillips D, Mikhailova EI, Timofejeva L, Mitchell JL, Osina O, Sosnikhina SP, Jones RN, Jenkins G (2008) Dissecting meiosis of rye using translational proteomics. Ann Bot 101:873–880. doi: 10.1093/aob/mcm202 PubMedCentralPubMedGoogle Scholar
  111. Podio M, Felitti S, Siena L, Delgado L, Mancini M, Seijo J, González A, Pessino S, Ortiz J (2014) Characterization and expression analysis of SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes in sexual and apomictic Paspalum notatum. Plant Mol Biol 84:479–495. doi: 10.1007/s11103-013-0146-9 PubMedGoogle Scholar
  112. Prasanna BM, Chaikam V, Mahuku G (2012) Doubled haploid technology in maize breeding: theory and practice. CYMMIT Press, TexcocoGoogle Scholar
  113. Prigge V, Xu X, Li L, Babu R, Chen S, Atlin GN, Melchinger AE (2012) New insights into the genetics of in vivo induction of maternal haploids, the backbone of doubled haploid technology in maize. Genetics 190:781–793. doi: 10.1534/genetics.111.133066 PubMedCentralPubMedGoogle Scholar
  114. Ravi M, Chan SWL (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464:615–618. doi: 10.1038/nature08842 PubMedGoogle Scholar
  115. Ravi M, Marimuthu MPA, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451:1121–1124. doi: 10.1038/nature06557 PubMedGoogle Scholar
  116. Rhoades MM, Dempsey E (1966) Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics 54:505–522PubMedCentralPubMedGoogle Scholar
  117. Riley R, Chapman V (1958) Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182:713–715Google Scholar
  118. Ronceret A, Pawlowski WP (2010) Chromosome dynamics in meiotic prophase I in plants. Cytogenet Genome Res 129:173–183PubMedGoogle Scholar
  119. Ronceret A, Doutriaux M-P, Golubovskaya IN, Pawlowski WP (2009) PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. Proc Natl Acad Sci USA 106:20121–20126. doi: 10.1073/pnas.0906273106 PubMedCentralPubMedGoogle Scholar
  120. Šamanić I, Simunić J, Riha K, Puizina J (2013) Evidence for distinct functions of MRE11 in Arabidopsis meiosis. PLoS ONE 8:e78760. doi: 10.1371/journal.pone.0078760 PubMedCentralPubMedGoogle Scholar
  121. Sanchez-Moran E, Armstrong SJ (2014) Meiotic chromosome synapsis and recombination in Arabidopsis thaliana: new ways of integrating cytological and molecular approaches. Chromosome Res 22:179–190. doi: 10.1007/s10577-014-9426-8 PubMedGoogle Scholar
  122. Sanei M, Pickering R, Kumke K, Nasuda S, Houben A (2011) Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci USA 108:E498–E505. doi: 10.1073/pnas.1103190108 PubMedCentralPubMedGoogle Scholar
  123. Satina S, Blakeslee AF (1935) Cytological effects of a gene in Datura which causes dyad formation in sporogenesis. Bot Gaz 96:521–532Google Scholar
  124. Serra H, Da Ines O, Degroote F, Gallego ME, White CI (2013) Roles of XRCC2, RAD51B and RAD51D in RAD51-independent SSA recombination. PLoS Genet 9:e1003971. doi: 10.1371/journal.pgen.1003971 PubMedCentralPubMedGoogle Scholar
  125. Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya IN (1996) The mac1 gene: controlling the commitment to the meiotic pathway in maize. Genetics 142:1009–1020PubMedCentralPubMedGoogle Scholar
  126. 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 153:933–941PubMedCentralPubMedGoogle Scholar
  127. Sidhu GK, Rustgi S, Shafqat MN, von Wettstein D, Gill KS (2008) Fine structure mapping of a gene-rich region of wheat carrying Ph1, a suppressor of crossing over between homoeologous chromosomes. Proc Natl Acad Sci USA 105:5815–5820. doi: 10.1073/pnas.0800931105 PubMedCentralPubMedGoogle Scholar
  128. Sosnikhina SP, Mikhailova EI, Tikholiz OA, Priyatkina SN, Smirnov VG, Dadashev SY, Kolomiets OL, Bogdanov YF (2005) Meiotic mutations in rye Secale cereale L. Cytogenet Genome Res 109:215–220PubMedGoogle Scholar
  129. Spillane C, Curtis MD, Grossniklaus U (2004) Apomixis technology development—Virgin births in farmers’ fields? Nat Biotechnol 22:687–691PubMedGoogle Scholar
  130. Sprague GF (1929) Hetero-fertilization in maize. Science 69:526–527. doi: 10.1126/science.69.1794.526-a PubMedGoogle Scholar
  131. Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh T-F, Fischer RL, Goldberg RB, Harada JJ (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci USA 105:3151–3156. doi: 10.1073/pnas.0712364105 PubMedCentralPubMedGoogle Scholar
  132. Timofejeva L, Skibbe DS, Lee S, Golubovskaya I, Wang R, Harper L, Walbot V, Cande WZ (2013) Cytological characterization and allelism testing of anther developmental mutants identified in a screen of maize male sterile lines. G3 3:231–249PubMedCentralPubMedGoogle Scholar
  133. Tyrnov V (1997) Producing of parthenogenetic forms of maize. Maize Genet Coop Newsl 71:73Google Scholar
  134. Uanschou C, Ronceret A, Von Harder M, De Muyt A, Vezon D, Pereira L, Chelysheva L, Kobayashi W, Kurumizaka H, Schlögelhofer P, Grelon M (2013) Sufficient amounts of functional HOP2/MND1 complex promote interhomolog DNA repair but are dispensable for intersister DNA repair during meiosis in arabidopsis. Plant Cell 25:4924–4940. doi: 10.1105/tpc.113.118521 PubMedCentralPubMedGoogle Scholar
  135. Veronesi F, Mariani A, Bingham ET (1986) Unreduced gametes in diploid Medicago and their importance in alfalfa breeding. Theor Appl Genet 72:37–41. doi: 10.1007/BF00261451 PubMedGoogle Scholar
  136. Vielle-Calzada J-P, Crane CF, Stelly DM (1996) Apomixis—the asexual revolution. Science 274:1322–1323. doi: 10.1126/science.274.5291.1322 Google Scholar
  137. Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K (2011) The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 21:1277–1281. doi: 10.1016/j.cub.2011.07.001 PubMedGoogle Scholar
  138. Wang M, Wang K, Tang D, Wei C, Li M, Shen Y, Chi Z, Gu M, Cheng Z (2010) The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22:417–430. doi: 10.1105/tpc.109.070789 PubMedCentralPubMedGoogle Scholar
  139. Wang M, Tang D, Wang K, Shen Y, Qin B, Miao C, Li M, Cheng Z (2011) OsSGO1 maintains synaptonemal complex stabilization in addition to protecting centromeric cohesion during rice meiosis. Plant J 67:583–594. doi: 10.1111/j.1365-313X.2011.04615.x PubMedGoogle Scholar
  140. Wang C-JR, Nan G-L, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN, Harper L, Egger R, Walbot V, Cande WZ (2012) Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139:2594–2603. doi: 10.1242/dev.077891 PubMedGoogle Scholar
  141. Wang Y, Xiao R, Wang H, Cheng Z, Li W, Zhu G, Wang Y, Ma H (2014) The Arabidopsis RAD51 paralogs RAD51B, RAD51D and XRCC2 play partially redundant roles in somatic DNA repair and gene regulation. New Phytol 201:292–304. doi: 10.1111/nph.12498 PubMedGoogle Scholar
  142. Wu C-C, Diggle PK, Friedman WE (2013) Kin recognition within a seed and the effect of genetic relatedness of an endosperm to its compatriot embryo on maize seed development. Proc Natl Acad Sci 110:2217–2222. doi: 10.1073/pnas.1220885110 PubMedCentralPubMedGoogle Scholar
  143. Xu X, Li L, Dong X, Jin W, Melchinger AE, Chen S (2013a) Gametophytic and zygotic selection leads to segregation distortion through in vivo induction of a maternal haploid in maize. J Exp Bot 64:1083–1096. doi: 10.1093/jxb/ers393 PubMedCentralPubMedGoogle Scholar
  144. Xu X, Li L, Dong X, Jin W, Melchinger AE, Chen S (2013b) Gametophytic and zygotic selection leads to segregation distortion through in vivo induction of a maternal haploid in maize. J Exp Bot 64:1083–1096. doi: 10.1093/jxb/ers393 PubMedCentralPubMedGoogle Scholar
  145. Yamashita K, Nakazawa Y, Namai K, Amagai M, Tsukazaki H, Wako T, Kojima A (2012) Modes of inheritance of two apomixis components, diplospory and parthenogenesis, in Chinese chive (Allium ramosum) revealed by analysis of the segregating population generated by back-crossing between amphimictic and apomictic diploids. Breed Sci 62:160–169. doi: 10.1270/jsbbs.62.160 PubMedCentralPubMedGoogle Scholar
  146. Yang S-L, Xie L-F, Mao H-Z, Puah CS, Yang W-C, Jiang L, Sundaresan V, Ye D (2003) TAPETUM DETERMINANT1 is required for cell specialization in the arabidopsis anther. Plant Cell 15:2792–2804. doi: 10.1105/tpc.016618 PubMedCentralPubMedGoogle Scholar
  147. Yang W-C, Shi D-Q, Chen Y-H (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108. doi: 10.1146/annurev-arplant-042809-112203 PubMedGoogle Scholar
  148. Yant L, Hollister JD, Wright KM, Arnold BJ, Higgins JD, Franklin FCH, Bomblies K (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr Biol 23:2151–2156. doi: 10.1016/j.cub.2013.08.059 PubMedGoogle Scholar
  149. Zamariola L, Storme N, Tiang CL, Armstrong SJ, Franklin FCH, Geelen D (2013) SGO1 but not SGO2 is required for maintenance of centromere cohesion in Arabidopsis thaliana meiosis. Plant Reprod. doi: 10.1007/s00497-013-0231-x Google Scholar
  150. Zhang X, Li X, Marshall JB, Zhong CX, Dawe RK (2005) Phosphoserines on maize CENTROMERIC HISTONE H3 and histone H3 demarcate the centromere and pericentromere during chromosome segregation. Plant Cell 17:572–583. doi: 10.1105/tpc.104.028522 PubMedCentralPubMedGoogle Scholar
  151. Zhang W, Lee H-R, Koo D-H, Jiang J (2008) Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell 20:25–34. doi: 10.1105/tpc.107.057083 PubMedCentralPubMedGoogle Scholar
  152. Zhao D-Z, Wang G-F, 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 Dev 16:2021–2031. doi: 10.1101/gad.997902 PubMedCentralPubMedGoogle Scholar
  153. 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. Plant J 54:375–387. doi: 10.1111/j.1365-313X.2008.03426.x PubMedCentralPubMedGoogle Scholar
  154. Zhao X, Xu X, Xie H, Chen S, Jin W (2013) Fertilization and uniparental chromosome elimination during crosses with maize haploid inducers. Plant Physiol 163:721–731. doi: 10.1104/pp.113.223982 PubMedCentralPubMedGoogle Scholar
  155. Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, Birchler JA, Jiang J, Dawe RK (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14:2825–2836. doi: 10.1105/tpc.006106 PubMedCentralPubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Group of Reproductive Development and Apomixis, UGA Laboratorio Nacional de Genómica para la BiodiversidadCINVESTAV IrapuatoIrapuatoMexico

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