Abstract
Apomixis is an asexual reproduction process in which clonal seeds are formed without meiosis and fertilization. Because of its potential in permanently preserving hybrid vigor, apomixis has attracted a great deal of interests from plant biologists and the seed industry. However, despite of decades of effort, introgression of apomixis traits from wild relatives into major crops has remained unsuccessful. Therefore, synthetic apomixis has been proposed as an alternative to fix hybrid vigor. In this article, I present the development of the MiMe (Mitosis instead of Meiosis), which turns meiosis into mitosis and leads to the production of clonal gametes. Apomixis-like clonal seeds are generated when MiMe plants are crossed to special genome elimination lines, which contain an altered centromere-specific histone 3 (CENH3). Furthermore, induction of haploid plants from egg cells can be achieved by either egg cell-specific expression of BABY BOOM1 (BBM1), or disruption of MATRILINEAL (MTL) using CRISPR/Cas9 gene-editing technology. Synthetic apomixis is established and clonal seeds are produced by simultaneous engineering MiMe with altering BBM1 expression or MTL disruption. Finally, I discuss how to further improve the apomixis strategy and its applications in crop breeding.
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References
Barcaccia G, Albertini E (2013) Apomixis in plant reproduction: a novel perspective on an old dilemma. Plant Reprod 26:159–179
Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA (2010) Heterosis. Plant Cell 22:2105–2112
Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL et al (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749
Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, Rocques N, Marquez-Lema A, Bhatt AM, Horlow C et al (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118:4621–4632
Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471
Conner JA, Mookkan M, Huo H, Chae K, Ozias-Akins P (2015) A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant. Proc Natl Acad Sci USA 112:11205–11210
Conner JA, Podio M, Ozias-Akins P (2017) Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes. Plant Reprod 30:41–52
Crismani W, Girard C, Froger N, Pradillo M, Santos JL, Chelysheva L, Copenhaver GP, Horlow C, Mercier R (2012) FANCM limits meiotic crossovers. Science 336:1588–1590
Dapp M, Reinders J, Bédiée A, Balsera C, Bucher E, Theiler G, Granier C, Paszkowski J (2015) Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids. Nat Plants 1:15092
De Muyt A, Vezon D, Gendrot G, Gallois JL, Stevens R, Grelon M (2007) AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. EMBO J 26:4126–4137
d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R (2009) Turning meiosis into mitosis. PLoS Biol 7:e1000124
d’Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C, Sun Y, To JP, 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
Gilles LM, Khaled A, Laffaire JB, Chaignon S, Gendrot G, Laplaige J, Berges H, Beydon G, Bayle V, Barret P et al (2017) Loss of pollen-specific phospholipase NOT LIKE DAD triggers gynogenesis in maize. EMBO J 36:707–717
Girard C, Chelysheva L, Choinard S, Froger N, Macaisne N, Lehmemdi A, Mazel J, Crismani W, Mercier R (2015) AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM antagonize meiotic crossovers by distinct mechanisms. PLoS Genet 11:e1005369
Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600
Grossniklaus U, Koltunow A, Lookeren Campagne VMM (1998) A bright future for apomixis. Trends Plant Sci 3:415–416
Grossniklaus U, Nogler GA, van Dijk PJ (2001) How to avoid sex: the genetic control of gametophytic apomixis. Plant Cell 13:1491–1497
Gualtieri G, Conner JA, Morishige DT, Moore LD, Mullet JE, Ozias-Akins P (2006) A segment of the apospory-specific genomic region is highly microsyntenic not only between the apomicts Pennisetum squamulatum and buffelgrass, but also with a rice chromosome 11 centromeric-proximal genomic region. Plant Physiol 140:963–971
Hand ML, Koltunow AM (2014) The genetic control of apomixis: asexual seed formation. Genetics 197:441–450
Ji J, Tang D, Shen Y, Xue Z, Wang H, Shi W, Zhang C, Du G, Li Y, Cheng Z (2016) P31comet, a member of the synaptonemal complex, participates in meiotic DSB formation in rice. Proc Natl Acad Sci USA 113:10577–10582
Kelliher T, Starr D, Richbourg L, Chintamanani S, Delzer B, Nuccio ML, Green J, Chen Z, McCuiston J, Wang W et al (2017) MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature 542:105–109
Kelliher T, Starr D, Su X, Tang G, Chen Z, Carter J, Wittich PE, Dong S, Green J, Burch E et al (2019) One-step genome editing of elite crop germplasm during haploid induction. Nat Biotechnol 37:287–292
Khanday I, Skinner D, Yang B, Mercier R, Sundaresan V (2019) A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565:91–95
Li X, Meng D, Chen S, Luo H, Zhang Q, Jin W, Yan J (2017) Single nucleus sequencing reveals spermatid chromosome fragmentation as a possible cause of maize haploid induction. Nat Commun 8:991
Liu C, Li X, Meng D, Zhong Y, Chen C, Dong X, Xu X, Chen B, Li W, Li L et al (2017) A 4-bp insertion at ZmPLA1 encoding a putative phospholipase A generates haploid induction in maize. Mol Plant 10:520–522
Marimuthu MP, Jolivet S, Ravi M, Pereira L, Davda JN, Cromer L, Wang L, Nogue F, Chan SW, Siddiqi I et al (2011) Synthetic clonal reproduction through seeds. Science (New York, NY) 331:876
Miao C, Tang D, Zhang H, Wang M, Li Y, Tang S, Yu H, Gu M, Cheng Z (2013) Central region component1, a novel synaptonemal complex component, is essential for meiotic recombination initiation in rice. Plant Cell 25:2998–3009
Mieulet D, Jolivet S, Rivard M, Cromer L, Vernet A, Mayonove P, Pereira L, Droc G, Courtois B, Guiderdoni E et al (2016) Turning rice meiosis into mitosis. Cell Res 26:1242–1254
Ozias-Akins P, Roche D, Hanna WW (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. Proc Natl Acad Sci USA 95:5127–5132
Ravi M, Chan SW (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464:615–618
Sailer C, Schmid B, Grossniklaus U (2016) Apomixis allows the transgenerational fixation of phenotypes in hybrid plants. Curr Biol CB 26:331–337
Schnable PS, Springer NM (2013) Progress toward understanding heterosis in crop plants. Annu Rev Plant Biol 64:71–88
Shao T, Tang D, Wang K, Wang M, Che L, Qin B, Yu H, Li M, Gu M, Cheng Z (2011) OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol 156:1386–1396
Spillane C, Curtis MD, Grossniklaus U (2004) Apomixis technology development—virgin births in farmers’ fields? Nat Biotechnol 22:687–691
Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, Wada T, Maxwell A, Roberts K, Sugimoto-Shirasu K (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48:206–216
Tang Y, Yin ZN, Zeng YJ, Zhang QX, Chen LQ, He Y, Lu PL, Ye D, Zhang XQ (2017) MTOPVIB interacts with AtPRD1 and plays important roles in formation of meiotic DNA double-strand breaks in Arabidopsis. Sci Rep 7:10007
van Dijk P, van Damme J (2000) Apomixis technology and the paradox of sex. Trends Plant Sci 5:81–84
Vielle Calzada JP, Crane CF, Stelly DM (1996) Apomixis—the asexual revolution. Science (New York, NY) 274:1322–1323
Wang X, Xu Y, Zhang S, Cao L, Huang Y, Cheng J, Wu G, Tian S, Chen C, Liu Y et al (2017) Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction. Nat Genet 49:765–772
Wang B, Zhu L, Zhao B, Zhao Y, Xie Y, Zheng Z, Li Y, Sun J, Wang H (2019a) Development of a haploid-inducer mediated genome editing (IMGE) system for accelerating maize breeding. Mol Plant 12:597–602
Wang C, Liu Q, Shen Y, Hua Y, Wang J, Lin J, Wu M, Sun T, Cheng Z, Mercier R et al (2019b) Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat Biotechnol 37:283–286
Xue Z, Li Y, Zhang L, Shi W, Zhang C, Feng M, Zhang F, Tang D, Yu H, Gu M et al (2016) OsMTOPVIB Promotes Meiotic DNA Double-Strand Break Formation in Rice. Mol Plant 9:1535–1538
Yu H, Wang M, Tang D, Wang K, Chen F, Gong Z, Gu M, Cheng Z (2010) OsSPO11-1 is essential for both homologous chromosome pairing and crossover formation in rice. Chromosoma 119:625–636
Zhang C, Song Y, Cheng ZH, Wang YX, Zhu J, Ma H, Xu L, Yang ZN (2012) The Arabidopsis thaliana DSB formation (AtDFO) gene is required for meiotic double-strand break formation. Plant J 72:271–281
Acknowledgements
I thank Junjie Wang for preparing the figure. This study was supported by the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences.
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Wang, K. Fixation of hybrid vigor in rice: synthetic apomixis generated by genome editing. aBIOTECH 1, 15–20 (2020). https://doi.org/10.1007/s42994-019-00001-1
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DOI: https://doi.org/10.1007/s42994-019-00001-1