A brief note on genes that trigger components of apomixis

  • Vladimir BrukhinEmail author
  • Ramamurthy Baskar


Apomixis or asexual reproduction through seeds occurs in about 400 species of flowering plants producing genetically uniform progeny. During apomixis, meiosis is bypassed and embryos develop by parthenogenesis. However, the endosperm could form either autonomously without fertilization or sexually, depending on the plant species. Most probably, a heterochronic expression of sexually expressed genes is one of the reason that causes apomixis. A better understanding of the genetic components regulating apomixis is important for developmental and evolutionary studies and also for engineering apomixis traits into crop plants that may realize a possibility to propagate hybrid vigor in a range of subsequent generations.


Apomixis-associated genes asexual reproduction heterosis sexual reproduction 



This work was supported by Grants 15-54-45001 from RFBR (to VB) and DST, New Delhi. The study was carried out within the framework of the state Assignment No. AAAA-A18-118051590112-8 to BIN RAS.


  1. Albertini E, Marconi G, Barcaccia G, Raggi L and Falcinelli M 2004 Isolation of candidate genes for apomixis in Poa pratensis L. Plant Mol. Biol. 56 879–894CrossRefGoogle Scholar
  2. Albertini E, Marconi G, Reale L, Barcaccia G, Porceddu A, Ferranti F and Falcinelli M 2005 SERK and APOSTART: candidate genes for apomixis in Poa pratensis. Plant Physiol. 138 2185–2199Google Scholar
  3. Bhatt AM, Lister C, Page T, Fransz P, Findlay K, Jones GH, Dickinson HG and Dean C 1999 The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J. 19 463–472CrossRefGoogle Scholar
  4. Bicknell RA and Koltunow AM 2004 Understanding apomixis: recent advances and remaining conundrums. Plant Cell 6 S228–S245CrossRefGoogle Scholar
  5. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB and van Lookeren Campagne MM 2002 Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell. 14 1737–1749CrossRefGoogle Scholar
  6. Brukhin V 2017 Molecular and genetic regulation of apomixis. Russ. J. Genet. 53 943–964CrossRefGoogle Scholar
  7. Brukhin V, Curtis MD and Grossniklaus U 2005 The angiosperm female gametophyte: no longer forgotten generation. Curr. Sci. 89 1844–1852Google Scholar
  8. Brukhin V, Jaciubek M, Bolaños Carpio A, Kuzmina V and Grossniklaus U 2011 Female gametophytic mutants of Arabidopsis thaliana identified in a gene trap insertional mutagenesis screen. Int. J. Dev. Biol. 55 73–84CrossRefGoogle Scholar
  9. Carman JG 2007 Do duplicate genes cause apomixis? In: Apomixis: evolution, mechanisms and perspectives (eds) E Hörandl, U Grossniklaus, P van Dijk, T Sharbel (Lichtenstein: ARG Gantner Verlag KG) pp 169–194Google Scholar
  10. Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES and Peacock WJ 1997 Fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94 4223–4228CrossRefGoogle Scholar
  11. Corral JM, Vogel H, Aliyu OM, Hensel G, Thiel T, Kumlehn J and Sharbel TF 2013 A conserved apomixis-specific polymorphism is correlated with exclusive exonuclease expression in premeiotic ovules of apomictic Boechera species. Plant Physiol. 163 1660–1672CrossRefGoogle Scholar
  12. Cromer L, Heyman J, Touati S, Harashima H, Araou E, Girard C, Horlow C, Wassmann K, Schnittger A, De Veylder L and 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 e1002865CrossRefGoogle Scholar
  13. D’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, et al. 2009 Turning meiosis into mitosis. PLoS Biol. 7 e1000124CrossRefGoogle Scholar
  14. Day RC, Grossniklaus U and Macknight RC 2005 Be more specific! Laser-assisted microdissection of plant cells. Trends Plant Sci. 10 397–406CrossRefGoogle Scholar
  15. Florez Rueda AM, Grossniklaus U and Schmidt A 2016 Laser-assisted microdissection (LAM) as a tool for transcriptional profiling of individual cell types. J. Vis. Exp. 111 1–10Google Scholar
  16. Gaj MD, Zhang S, Harada JJ and Lemaux PG 2005 Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222 977–988CrossRefGoogle Scholar
  17. Grossniklaus U 2001 From sexuality to apomixis: molecular and genetic approaches; In: The flowering of apomixis: from mechanisms to genetic engineering (eds) Y Savidan, JG Carman, T Dresselhaus (Mexico, D.F.: CIMMYT, IRD, European Commission DG VI) pp 168–211Google Scholar
  18. Grossniklaus U, Vielie-Calzada J-P, Hoeppner M and Gogiiono W 1998 Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280 446–450CrossRefGoogle Scholar
  19. Grossniklaus U, Moore JM, Brukhin V, Gheyselinck J, Baskar R, Vielle-Calzada J-P, Baroux C, Page DR and Spillane C 2003 Engineering of apomixis in crop plants: what can we learn from sexual model systems; In: Plant biotechnology 2002 & beyond (ed) IK Vasil (Dordrecht: Kluwer Academic Publishers) pp 309–314Google Scholar
  20. Guitton AE and Berger F 2005 Loss of function of multicopy suppressor of IRA1 produces nonviable parthenogenetic embryos in Arabidopsis. Curr. Biol. 15 750–754CrossRefGoogle Scholar
  21. Jefferson RA 1994 Apomixis: a social revolution for agriculture? Biotechnol. Dev. Monit. 19 14–16Google Scholar
  22. Johnston AJ, Meier P, Gheyselinck J, Wuest SE, Federer M, Schlagenhauf E, Becker JD and Grossniklaus U 2007 Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biol. 8 204CrossRefGoogle Scholar
  23. Kerk NM, Ceserani T, Tausta SL, Sussex IM and Nelson TM 2003 Laser capture microdissection of cells from plant tissues. Plant Physiol. 132 27–35CrossRefGoogle Scholar
  24. Kliver S, Rayko M, Komissarov A, Bakin E, Zhernakova D, Prasad K, Rushworth C, Baskar R, Smetanin D1, Schmutz J, Rokhsar DS, Mitchell-Olds T, Grossniklaus U and Brukhin V 2018 Assembly of the Boechera retrofracta genome and evolutionary analysis of apomixis-associated genes. Genes (Basel). 9 pii: E185CrossRefGoogle Scholar
  25. Koltunow AM and Grossniklaus U 2003 Apomixis: a developmental perspective. Annu. Rev. Plant Biol. 54 547–574CrossRefGoogle Scholar
  26. Laux T, Mayer KF, Berger J and Jurgens GG 1996 The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122 87–96Google Scholar
  27. Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ and Chaudhury AM 1999 Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96 296–301CrossRefGoogle Scholar
  28. Meagher RB, Kandasamy MK, Deal RB and McKinney EC 2007 Actin-related proteins in chromatin-level control of the cell cycle and developmental transitions. Trends Cell Biol. 2007 325–332CrossRefGoogle Scholar
  29. Meister G 2013 Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 14 447–459CrossRefGoogle Scholar
  30. Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, Lefèvre F, Pelletier G and 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 1859–1871CrossRefGoogle Scholar
  31. Naumova TN, van der Laak J, Osadtchiy J, Matzk F, Kravtchenko A, Bergervoet J, Ramulu KS and Boutilier K 2001 Reproductive development in apomictic populations of Arabis holboellii (Brassicaceae). Sex Plant Reprod. 14 195–200CrossRefGoogle Scholar
  32. Naumova TN 1993 Apomixis in angiosperms: nucellar and integumentary embryony (Boca Raton, FL: CRC Press)Google Scholar
  33. Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB and Fischer RL 1999 Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11 407–416CrossRefGoogle Scholar
  34. Olmedo-Monfil V, Durán-FIgueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA and Vielle-Calzada JP 2010 Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464 628–632CrossRefGoogle Scholar
  35. Peragine A, Yoshikawa M, Wu G, Albrecht HL and Poethig RS 2004 SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 18 2368–2379CrossRefGoogle Scholar
  36. Rabiger DS, Taylor JM, Spriggs A, Hand ML, Henderson ST, Johnson SD, Oelkers K, Hrmova M, Saito K, Suzuki G, Mukai Y, Carroll BJ and Koltunow AMG 2016 Generation of an integrated Hieracium genomic and transcriptomic resource enables exploration of small RNA pathways during apomixis initiation. BMC Biol. 14 86Google Scholar
  37. Ravi M, Marimuthu MPA and Siddiqi I 2008 Gamete formation without meiosis in Arabidopsis. Nature 451 1121–1124CrossRefGoogle Scholar
  38. Rodriguez-Leal D and Vielle-Calzada J-P 2012 Regulation of apomixis: learning from sexual experience. Curr. Opin. Plant Biol. 15 549–555CrossRefGoogle Scholar
  39. Savidan Y 2000 Apomixis: genetics and breeding. In: Plant Breeding Reviews (ed) J. Janick (New York: Wiley), pp 13–86CrossRefGoogle Scholar
  40. Schmidt MW, Schmidt A, Klostermeier UC, Barann M, Rosenstiel P and Grossniklaus U 2012 A powerful method for transcriptional profiling of specific cell types in eukaryotes: laser-assisted microdissection and RNA sequencing. PLoS One 7 e29685CrossRefGoogle Scholar
  41. Schmidt A, Wöhrmann HJ, Raissig MT, Arand J, Gheyselinck J, Gagliardini V, Heichinger C, Walter J, Grossniklaus U 2013 The polycomb group protein MEDEA and the DNA methyltransferase MET1 interact to repress autonomous endosperm development in Arabidopsis. Plant J. 73 776–787CrossRefGoogle Scholar
  42. Schoft VK, Chumak N, Choi Y, Hannon M, Garcia-Aguilar M, Machlicova A, Slusarz L, Mosiolek M, Park JS, Park GT, Fischer RL and Tamaru H 2011 Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc. Natl. Acad. Sci. USA 108 8042–8047CrossRefGoogle Scholar
  43. Siddiqi I, Ganesh G, Grossniklaus U and Subbiah V 2000 The dyad gene is required for progression through female meiosis in Arabidopsis. Development 127 197–207Google Scholar
  44. Singh M, Goel S, Meeley RB, Dantec C, Parri-nello H, et al. 2011 Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23 443–458CrossRefGoogle Scholar
  45. Sprink T and Hartung F 2014 The splicing fate of plant SPO11 genes. Front Plant Sci. 5 214Google Scholar
  46. Toennissen G 2001 The flowering of apomixis: from mechanisms to genetic engineering. European Commission DG 6 1–7Google Scholar
  47. Wang F and Perry SE 2013 Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 161 1251–1264CrossRefGoogle Scholar
  48. Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenführer J, von Mering C and Grossniklaus U 2010 Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol. 20 506–512CrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2019

Authors and Affiliations

  1. 1.Dobzhansky Center for Genome BioinformaticsSt. Petersburg State UniversitySaint PetersburgRussia
  2. 2.Department of Plant EmbryologyKomarov Botanical Institute RASSaint PetersburgRussia
  3. 3.Department of Biotechnology, Bhupat and Jyoti Mehta School of BiosciencesIndian Institute of Technology, MadrasChennaiIndia

Personalised recommendations