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

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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.

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References

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Armstrong SJ, Franklin FCH, Jones GH (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207–4217

    CAS  PubMed  Google Scholar 

  • Asker SE, Jerling L (1992) Apomixis in plants. CRC Press, London

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Barrell PJ, Grossniklaus U (2005) Confocal microscopy of whole ovules for analysis of reproductive development: the elongate1 mutant affects meiosis II. Plant J 43:309–320

    CAS  PubMed  Google Scholar 

  • 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 117:581–594

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16:S228–S245. doi:10.1105/tpc.017921

    PubMed Central  CAS  PubMed  Google Scholar 

  • Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA (2010) Heterosis. Plant Cell 22:2105–2112. doi:10.1105/tpc.110.076133

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 129:1–22

    Google Scholar 

  • Brownfield L, Köhler C (2011) Unreduced gamete formation in plants: mechanisms and prospects. J Exp Bot 62:1659–1668. doi:10.1093/jxb/erq371

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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 12:1718–1727

    CAS  PubMed  Google Scholar 

  • 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 353–375

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chan SWL (2010) Chromosome engineering: power tools for plant genetics. Trends Biotechnol 28:605–610. doi:10.1016/j.tibtech.2010.09.002

    CAS  PubMed  Google Scholar 

  • Chang M-T, Coe EH (2009) Doubled haploids. In: Kriz AL, Larkins BA (eds) Molecular genetic approaches to maize improvement. Springer, Berlin, pp 127–142

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 118:4621–4632

    CAS  PubMed  Google Scholar 

  • Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482. doi:10.1038/nrg3503

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 11:78

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Coe EH Jr (1959) A line of maize with high haploid frequency. Am Nat 93:381–382

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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 7:267

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R (2009) Turning meiosis into mitosis. PLoS Biol 7:e1000124

    PubMed Central  PubMed  Google Scholar 

  • 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:e1000989

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • Finch RA, Bennett MD (1979) Action of triploid inducer (tri) on meiosis in barley (Hordeum vulgare L.). Heredity 43:87–93

    Google Scholar 

  • Geiger HH (2009) Doubled haploids. In: Bennetzen JL, Hake S (eds) Handbook of maize. Springer, New York, pp 641–657

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 11:810–816

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Grandont L, Jenczewski E, Lloyd A (2013) Meiosis and its deviations in polyploid plants. Cytogenet Genome Res 140:171–184

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 80:40–47

    PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Guitton A-E, Berger F (2005) Loss of function of MULTICOPY SUPPRESSOR OF IRA 1 produces nonviable parthenogenetic embryos in arabidopsis. Curr Biol 15:750–754

    CAS  PubMed  Google Scholar 

  • Gustafsson Å (1947) Apomixis in higher plants. II. The causal aspect of apomixis. Lunds Univ Arsskr NF Adv 2:43–71

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 15:948–954

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hand ML, Koltunow AMG (2014) The genetic control of apomixis: asexual seed formation. Genetics 197:441–450. doi:10.1534/genetics.114.163105

    CAS  PubMed  Google Scholar 

  • Havekes FWJ, de Jong JH, Heyting C, Ramanna MS (1994) Synapsis and chiasma formation in four meiotic mutants of tomato (Lycopersicon esculentum). Chromosome Res 2:315–325

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kelliher T, Walbot V (2012) Hypoxia triggers meiotic fate acquisition in maize. Science 337:345–348. doi:10.1126/science.1220080

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Koltunow AM, Grossniklaus U (2003) Apomixis: a developmental perspective. Annu Rev Plant Biol 54:547–574. doi:10.1146/annurev.arplant.54.110901.160842

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 14:239–243

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 93:1195–1205

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 127:1157–1166

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Matzk F (1996) The ‘Salmon System’ of wheat; a suitable model for apomixis research. Hereditas 125:299–304

    Google Scholar 

  • Mayer U, Jurgens G (1998) Pattern formation in plant embryogenesis: a reassessment. Semin Cell Dev Biol 9:187–193

    CAS  PubMed  Google Scholar 

  • Mercier R, Grelon M (2008) Meiosis in plants: ten years of gene discovery. Cytogenet Genome Res 120:281–290

    CAS  PubMed  Google Scholar 

  • 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 15:1859–1871

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 130:3309–3318

    CAS  PubMed  Google Scholar 

  • Nel PM (1975) Crossing over and diploid egg formation in the elongate mutant of maize. Genetics 79:435–450

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nogler G (1984) Gametophytic apomixis. In: Johri B (ed) Embryology of angiosperms. Springer, New York, pp 475–518

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Noyes RD, Rieseberg LH (2000) Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics 155:379–390

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Pawlowski WP, Sheehan MJ, Ronceret A (2007) In the beginning: the initiation of meiosis. BioEssays 29:511–514

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peloquin SJ, Boiteux LS, Carputo D (1999) Meiotic mutants in potato: valuable variants. Genetics 153:1493–1499

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Prasanna BM, Chaikam V, Mahuku G (2012) Doubled haploid technology in maize breeding: theory and practice. CYMMIT Press, Texcoco

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ravi M, Chan SWL (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464:615–618. doi:10.1038/nature08842

    CAS  PubMed  Google Scholar 

  • Ravi M, Marimuthu MPA, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451:1121–1124. doi:10.1038/nature06557

    CAS  PubMed  Google Scholar 

  • Rhoades MM, Dempsey E (1966) Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics 54:505–522

    PubMed Central  CAS  PubMed  Google Scholar 

  • Riley R, Chapman V (1958) Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182:713–715

    Google Scholar 

  • Ronceret A, Pawlowski WP (2010) Chromosome dynamics in meiotic prophase I in plants. Cytogenet Genome Res 129:173–183

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Satina S, Blakeslee AF (1935) Cytological effects of a gene in Datura which causes dyad formation in sporogenesis. Bot Gaz 96:521–532

    Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 109:215–220

    CAS  PubMed  Google Scholar 

  • Spillane C, Curtis MD, Grossniklaus U (2004) Apomixis technology development—Virgin births in farmers’ fields? Nat Biotechnol 22:687–691

    CAS  PubMed  Google Scholar 

  • Sprague GF (1929) Hetero-fertilization in maize. Science 69:526–527. doi:10.1126/science.69.1794.526-a

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 3:231–249

    PubMed Central  PubMed  Google Scholar 

  • Tyrnov V (1997) Producing of parthenogenetic forms of maize. Maize Genet Coop Newsl 71:73

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

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.

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  1. Group of Reproductive Development and Apomixis, UGA Laboratorio Nacional de Genómica para la Biodiversidad, CINVESTAV Irapuato, Km 9.6 Libramiento Norte Carretera Irapuato-León, CP 36821, Irapuato, Guanajuato, Mexico

    Arnaud Ronceret & Jean-Philippe Vielle-Calzada

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  1. Arnaud Ronceret
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  2. Jean-Philippe Vielle-Calzada
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Correspondence to Jean-Philippe Vielle-Calzada.

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Communicated by Silvia Coimbra and Lucia Colombo.

A contribution to the special issue ‘From Gametes to Seeds’.

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Ronceret, A., Vielle-Calzada, JP. Meiosis, unreduced gametes, and parthenogenesis: implications for engineering clonal seed formation in crops. Plant Reprod 28, 91–102 (2015). https://doi.org/10.1007/s00497-015-0262-6

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