The ability to generate haploids and subsequently induce chromosome doubling significantly accelerates the crop breeding process. Haploids have been induced through the generation of plants from haploid tissues (in situ gynogenesis and androgenesis) and through the selective loss of a parental chromosome set via inter- or intraspecific hybridization. Here, we focus on the mechanisms responsible for this selective chromosome elimination. CENH3, a variant of the centromere-specific histone H3, has been exploited to create an efficient method of haploid induction, and we discuss this approach in some detail. Parallels have been drawn with chromosome-specific elimination, which occurs as a normal part of differentiation and sex determination in many plant and animal systems.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Akbari OS, Antoshechkin I, Hay BA, Ferree PM. 1.  2013. Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio. G3 3:1597–605 [Google Scholar]
  2. Barret P, Brinkmann M, Beckert M. 2.  2008. A major locus expressed in the male gametophyte with incomplete penetrance is responsible for in situ gynogenesis in maize. Theor. Appl. Genet. 117:581–94 [Google Scholar]
  3. Batzenschlager M, Lermontova I, Schubert V, Fuchs J, Berr A. 3.  et al. 2015. Arabidopsis MZT1 homologs GIP1 and GIP2 are essential for centromere architecture. PNAS 112:8656–60 [Google Scholar]
  4. Bennett MD, Finch RA, Barclay IR. 4.  1976. The time rate and mechanism of chromosome elimination in Hordeum hybrids. Chromosoma 54:175–200 [Google Scholar]
  5. Boyer HW. 5.  1971. DNA restriction and modification mechanisms in bacteria. Annu. Rev. Microbiol. 25:153–76 [Google Scholar]
  6. Carchilan M, Delgado M, Ribeiro T, Costa-Nunes P, Caperta A. 6.  et al. 2007. Transcriptionally active heterochromatin in rye B chromosomes. Plant Cell 19:1738–49 [Google Scholar]
  7. Chang M, Coe E. 7.  2009. Doubled haploids. Molecular Genetics Approaches to Maize Improvement AL Kriz, BA Larkins 127–42 Biotechnol. Agric. For 63 Berlin: Springer [Google Scholar]
  8. Chmatal L, Gabriel SI, Mitsainas GP, Martinez-Vargas J, Ventura J. 8.  et al. 2014. Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr. Biol. 24:2295–300 [Google Scholar]
  9. Coe EH. 9.  1959. A line of maize with high haploid frequency. Am. Nat. 93:381–82 [Google Scholar]
  10. Crouse HV. 10.  1979. X heterochromatin subdivision and cytogenetic analysis of Sciara coprophila (Diptera, Sciaridae) II. The controlling element. Chromosoma 74:219–39 [Google Scholar]
  11. Davies DR. 11.  1956. Cytogenetic studies in wild and cultivated species of Hordeum PhD Thesis, Univ. Wales, Cardiff, UK
  12. Davies DR. 12.  1974. Chromosome elimination in inter-specific hybrids. Heredity 32:267–70 [Google Scholar]
  13. de Saint Phalle B, Sullivan W. 13.  1996. Incomplete sister chromatid separation is the mechanism of programmed chromosome elimination during early Sciara coprophila embryogenesis. Development 122:3775–84 [Google Scholar]
  14. Dong X, Xu X, Miao J, Li L, Zhang D. 14.  et al. 2013. Fine mapping of qhir1 influencing in vivo haploid induction in maize. Theor. Appl. Genet. 126:1713–20 [Google Scholar]
  15. Dunwell JM. 15.  2010. Haploids in flowering plants: origins and exploitation. Plant Biotechnol. J. 8:377–424 [Google Scholar]
  16. Dwivedi SL, Britt AB, Tripathi L, Sharma S, Upadhyaya HD, Ortiz R. 16.  2015. Haploids: constraints and opportunities in plant breeding. Biotechnol. Adv. 33:812–29 [Google Scholar]
  17. Escriba MC, Goday C. 17.  2013. Histone H3 phosphorylation and elimination of paternal X chromosomes at early cleavages in sciarid flies. J. Cell Sci. 126:3214–22 [Google Scholar]
  18. Evans MMS. 18.  2007. The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell 19:46–62 [Google Scholar]
  19. Finch RA. 19.  1983. Tissue-specific elimination of alternative whole parental genomes in one barley hybrid. Chromosoma 88:386–93 [Google Scholar]
  20. Finch RA, Bennett MD. 20.  1982. The mechanism of somatic chromosome elimination in Hordeum. Kew Chromosome Conference II PE Brandham, MD Bennett 146–53 London: Allen & Unwin
  21. Forster BP, Heberle-Bors E, Kasha KJ, Touraev A. 21.  2007. The resurgence of haploids in higher plants. Trends Plant Sci. 12:368–75 [Google Scholar]
  22. Fulcher N, Teubenbacher A, Kerdaffrec E, Farlow A, Nordborg M, Riha K. 22.  2015. Genetic architecture of natural variation of telomere length in Arabidopsis thaliana. Genetics 199:625–35 [Google Scholar]
  23. Gaeta RT, Masonbrink RE, Krishnaswamy L, Zhao CZ, Birchler JA. 23.  2012. Synthetic chromosome platforms in plants. Annu. Rev. Plant Biol. 63:307–30 [Google Scholar]
  24. Geiger H. 24.  2009. Doubled haploids. Handbook of Maize Genetics and Genomics JL Bennetzen, S Hake 641–57 Berlin: Springer [Google Scholar]
  25. Gernand D, Rutten T, Pickering R, Houben A. 25.  2006. Elimination of chromosomes in Hordeum vulgare×H. bulbosum crosses at mitosis and interphase involves micronucleus formation and progressive heterochromatinization. Cytogenet. Genome Res. 114:169–74 [Google Scholar]
  26. Gernand D, Rutten T, Varshney A, Rubtsova M, Prodanovic S. 26.  et al. 2005. Uniparental chromosome elimination at mitosis and interphase in wheat and pearl millet crosses involves micronucleus formation, progressive heterochromatinization, and DNA fragmentation. Plant Cell 17:2431–38 [Google Scholar]
  27. Goday C, Pigozzi MI. 27.  2010. Heterochromatin and histone modifications in the germline-restricted chromosome of the zebra finch undergoing elimination during spermatogenesis. Chromosoma 119:325–36 [Google Scholar]
  28. Goday C, Ruiz MF. 28.  2002. Differential acetylation of histones H3 and H4 in paternal and maternal germline chromosomes during development of sciarid flies. J. Cell Sci. 115:4765–75 [Google Scholar]
  29. Gupta SB. 29.  1969. Duration of mitotic cycle and regulation of DNA replication in Nicotiana plumbaginifolia and a hybrid derivative of N. tabacum showing chromosome instability. Can. J. Genet. Cytol. 11:133–42 [Google Scholar]
  30. Hagberg A, Hagberg G. 30.  1980. High-frequency of spontaneous haploids in the progeny of an induced mutation in barley. Hereditas 93:341–43 [Google Scholar]
  31. Hagberg A, Hagberg G. 31.  1987. Production of spontaneously doubled haploids in barley using a breeding system with marker genes and the hap-gene. Biol. Zentralblatt 106:53–58 [Google Scholar]
  32. Hayman DL, Martin PG. 32.  1965. Supernumerary chromosomes in the marsupial Schoinobates volans (Ker). Aust. J. Biol. Sci. 18:1081–82 [Google Scholar]
  33. Ho KM, Kasha KJ. 33.  1975. Genetic control of chromosome elimination during haploid formation in barley. Genetics 81:263–75 [Google Scholar]
  34. Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN. 34.  2014. Evolution and biology of supernumerary B chromosomes. Cell. Mol. Life Sci. 71:467–78 [Google Scholar]
  35. Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC. 35.  et al. 2000. Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. PNAS 97:1148–53 [Google Scholar]
  36. Humphreys MW. 36.  1978. Chromosome instability in Hordeum vulgare×H. bulbosum hybrids. Chromosoma 65:301–7 [Google Scholar]
  37. Imai HT. 37.  1974. B-chromosomes in the myrmicine ant, Leptothorax spinosior. Chromosoma 45:431–44 [Google Scholar]
  38. Ingouff M, Rademacher S, Holec S, Soljic L, Xin N. 38.  et al. 2010. Zygotic resetting of the histone 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20:2137–43 [Google Scholar]
  39. Ishii T, Sunamura N, Matsumoto A, Eltayeb AE, Tsujimoto H. 39.  2015. Preferential recruitment of the maternal centromere-specific histone H3 (CENH3) in oat (Avena sativa L.)×pearl millet (Pennisetum glaucum L.) hybrid embryos. Chromosome Res. 23:709–18 [Google Scholar]
  40. Ishii T, Ueda T, Tanaka H, Tsujimoto H. 40.  2010. Chromosome elimination by wide hybridization between Triticeae or oat plant and pearl millet: pearl millet chromosome dynamics in hybrid embryo cells. Chromosome Res. 18:821–31 [Google Scholar]
  41. Jin WW, Melo JR, Nagaki K, Talbert PB, Henikoff S. 41.  et al. 2004. Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell 16:571–81 [Google Scholar]
  42. Jones RN, Rees H. 42.  1982. B Chromosomes London: Academic
  43. Karimi-Ashtiyani R, Ishii I, Niessen M, Stein N, Heckmann S. 43.  et al. 2015. Point mutation impairs centromeric CENH3 loading and induces haploid plants. PNAS 112:11211–16 [Google Scholar]
  44. Kasha KJ, Kao KN. 44.  1970. High frequency haploid production in barley (Hordeum vulgare L.). Nature 225:874–76Provided a pioneering description of uniparental chromosome elimination and haploidization in wide crosses. [Google Scholar]
  45. Kermicle JL. 45.  1969. Androgenesis conditioned by a mutation in maize. Science 166:1422–24 [Google Scholar]
  46. Kindiger B, Hamann S. 46.  1993. Generation of haploids in maize—a modification of the indeterminate gametophyte (Ig) system. Crop Sci. 33:342–44 [Google Scholar]
  47. Kloc M, Zagrodzinska B. 47.  2001. Chromatin elimination—an oddity or a common mechanism in differentiation and development?. Differentiation 68:84–91 [Google Scholar]
  48. Kumar SV, Wigge PA. 48.  2010. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–47 [Google Scholar]
  49. Kumlehn J. 49.  2014. Haploid technology. Biotechnological Approaches to Barley Improvement J Kumlehn, N Stein 379–92 Biotechnol. Agric. For. Vol. 69 Berlin: Springer [Google Scholar]
  50. Kuppu S, Tan EH, Nguyen H, Rodgers A, Comai L. 50.  et al. 2015. Point mutations in centromeric histone induce post-zygotic incompatibility and uniparental inheritance. PLOS Genet 11:e1005494 [Google Scholar]
  51. Lange W. 51.  1969. Cytogenetisch en embryologisch onderzoek aan kruisingen tussen Hordeum vulgare en H. bulbosum [Cytogenetical and embryological research on crosses between Hordeum vulgare and H. bulbosum]. Versl. Landbouwk. Onderz. 719. Wageningen, Neth: Cent. Landbouwpubl. Landbouwdoc [Google Scholar]
  52. Lange W. 52.  1971. Crosses between Hordeum vulgare L. and H. bulbosum L. II. Elimination of chromosomes in hybrid tissue. Euphytica 20:181–94 [Google Scholar]
  53. Lange W, Jochemsen G. 53.  1976. Karyotypes, nucleoli, and amphiplasty in hybrids between Hordeum vulgare L. and Hordeum bulbosum L. Genetica 46:217–33 [Google Scholar]
  54. Laurie DA, Bennett MD. 54.  1989. The timing of chromosome elimination in hexaploid wheat×maize crosses. Genome 32:953–61 [Google Scholar]
  55. Lermontova I, Kuhlmann M, Friedel S, Rutten T, Heckmann S. 55.  et al. 2013. Arabidopsis KINETOCHORE NULL2 is an upstream component for centromeric histone H3 variant cenH3 deposition at centromeres. Plant Cell 25:3389–404 [Google Scholar]
  56. Liu ST, Rattner JB, Jablonski SA, Yen TJ. 56.  2006. Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J. Cell Biol. 175:41–53 [Google Scholar]
  57. Maheshwari S, Tan EH, West A, Franklin FC, Comai L, Chan SW. 57.  2015. Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLOS Genet. 11:e1004970Demonstrated the effect of naturally occurring CENH3 differences on zygotic chromosome segregation. [Google Scholar]
  58. Majer C, Hochholdinger F. 58.  2011. Defining the boundaries: structure and function of LOB domain proteins. Trends Plant Sci. 16:47–52 [Google Scholar]
  59. Marimuthu MPA, Jolivet S, Ravi M, Pereira L, Davda JN. 59.  et al. 2011. Synthetic clonal reproduction through seeds. Science 331:876 [Google Scholar]
  60. Melchinger AE, Schipprack W, Wurschum T, Chen SJ, Technow F. 60.  2013. Rapid and accurate identification of in vivo-induced haploid seeds based on oil content in maize. Sci. Rep. 32129
  61. Mette MF, Houben A. 61.  2015. Engineering of plant chromosomes. Chromosome Res. 23:69–76 [Google Scholar]
  62. Metz CW. 62.  1926. Genetic evidence of a selective segregation of chromosomes in Sciara (Diptera). PNAS 12:690–92 [Google Scholar]
  63. Mochida K, Tsujimoto H, Sasakuma T. 63.  2004. Confocal analysis of chromosome behavior in wheat×maize zygotes. Genome 47:199–205Provided evidence that tubulin-centromere interactions are impaired in the first mitotic division of a wide-cross zygote. [Google Scholar]
  64. Mogensen HL. 64.  1982. Double fertilization in barley and the cytological explanation for haploid embryo formation, embryoless caryopses, and ovule abortion. Carlsberg Res. Commun. 47:313–54 [Google Scholar]
  65. Nanda DK, Chase SS. 65.  1966. An embryo marker for detecting monoploids of maize (Zea mays L). Crop Sci. 6:213–15 [Google Scholar]
  66. Perpelescu M, Fukagawa T. 66.  2011. The ABCs of CENPs. Chromosoma 120:425–46 [Google Scholar]
  67. Pickering RA. 67.  1985. Partial control of chromosome elimination by temperature in immature embryos of Hordeum vulgare L. × H. bulbosum. Euphytica 14:869–74 [Google Scholar]
  68. Pigozzi MI, Solari AJ. 68.  1998. Germ cell restriction and regular transmission of an accessory chromosome that mimics a sex body in the zebra finch, Taeniopygia guttata. Chromosome Res. 6:105–13 [Google Scholar]
  69. Portemer V, Renne C, Guillebaux A, Mercier R. 69.  2015. Large genetic screens for gynogenesis and androgenesis haploid inducers in Arabidopsis thaliana failed to identify mutants. Front. Plant Sci. 6:147 [Google Scholar]
  70. Prigge V, Melchinger AE. 70.  2012. Production of haploids and doubled haploids in maize. Methods Mol. Biol. 877:161–72 [Google Scholar]
  71. Prigge V, Xu X, Li L, Babu R, Chen S. 71.  et al. 2012. New insights into the genetics of in vivo induction of maternal haploids, the backbone of doubled haploid technology in maize. Genetics 190:781–93 [Google Scholar]
  72. Puchta H, Fauser F. 72.  2014. Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant J. 78:727–41 [Google Scholar]
  73. Ravi M, Chan SW. 73.  2010. Haploid plants produced by centromere-mediated genome elimination. Nature 464:615–18Provided the first demonstration of the manipulation of CENH3 to induce haploidization in plants. [Google Scholar]
  74. Ravi M, Marimuthu MPA, Tan EH, Maheshwari S, Henry IM. 74.  et al. 2014. A haploid genetics toolbox for Arabidopsis thaliana. Nat. Commun. 5:5334 [Google Scholar]
  75. Raychaudhuri N, Dubruille R, Orsi GA, Bagheri HC, Loppin B, Lehner CF. 75.  2012. Transgenerational propagation and quantitative maintenance of paternal centromeres depends on Cid/Cenp-A presence in Drosophila sperm. PLOS Biol. 10:e1001434 [Google Scholar]
  76. Reed KM, Werren JH. 76.  1995. Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. Mol. Reprod. Dev. 40:408–18 [Google Scholar]
  77. Riddle NC, Birchler JA. 77.  2003. Effects of reunited diverged regulatory hierarchies in allopolyploids and species hybrids. Trends Genet. 19:597–600 [Google Scholar]
  78. Sanchez L, Perondini ALP. 78.  1999. Sex determination in sciarid flies: a model for the control of differential X-chromosome elimination. J. Theor. Biol. 197:247–59 [Google Scholar]
  79. Sanei M, Pickering R, Kumke K, Nasuda S, Houben A. 79.  2011. Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. PNAS 108:E498–505Implicated uniparental centromere inactivation as the cause of haploidization in unstable interspecific hybrids. [Google Scholar]
  80. Sarkar KR, Coe EH. 80.  1966. A genetic analysis of origin of maternal haploids in maize. Genetics 54:453–64 [Google Scholar]
  81. Sato H, Shibata F, Murata M. 81.  2005. Characterization of a Mis12 homologue in Arabidopsis thaliana. Chromosome Res. 13:827–34 [Google Scholar]
  82. Schoenmakers S, Wassenaar E, Laven JS, Grootegoed JA, Baarends WM. 82.  2010. Meiotic silencing and fragmentation of the male germline restricted chromosome in zebra finch. Chromosoma 119:311–24 [Google Scholar]
  83. Schwarzacher Robinson T, Finch RA, Smith JB, Bennett MD. 83.  1987. Genotypic control of centromere positions of parental genomes in Hordeum × Secale hybrid metaphases. J. Cell Sci. 87:291–304 [Google Scholar]
  84. Seymour DK, Filiault DL, Henry IM, Monson-Miller J, Ravi M. 84.  et al. 2012. Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. PNAS 109:4227–32 [Google Scholar]
  85. Shuai L, Zhou Q. 85.  2014. Haploid embryonic stem cells serve as a new tool for mammalian genetic study. Stem Cell Res. Ther. 5:20 [Google Scholar]
  86. Subrahmanyam NC, Kasha KJ. 86.  1973. Selective chromosomal elimination during haploid formation in barley following interspecific hybridization. Chromosoma 42:111–25 [Google Scholar]
  87. Swim MM, Kaeding KE, Ferree PM. 87.  2012. Impact of a selfish B chromosome on chromatin dynamics and nuclear organization in Nasonia. J. Cell Sci. 125:5241–49 [Google Scholar]
  88. Symko S. 88.  1969. Haploid barley from crosses of Hordeum bulbosum (2x) × Hordeum vulgare (2x). Can. J. Genet. Cytol. 11:602–8 [Google Scholar]
  89. Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S. 89.  2002. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–66 [Google Scholar]
  90. Tan EH, Henry IM, Ravi M, Bradnam KR, Mandakova T. 90.  et al. 2015. Catastrophic chromosomal restructuring during genome elimination in plants. eLife 4:e06516 [Google Scholar]
  91. Utani K, Okamoto A, Shimizu N. 91.  2011. Generation of micronuclei during interphase by coupling between cytoplasmic membrane blebbing and nuclear budding. PLOS ONE 6:e27233 [Google Scholar]
  92. Wang J, Davis RE. 92.  2014. Programmed DNA elimination in multicellular organisms. Curr. Opin. Genet. Dev. 27:26–34 [Google Scholar]
  93. Wang Z, Yin H, Lv L, Feng Y, Chen S. 93.  et al. 2014. Unrepaired DNA damage facilitates elimination of uniparental chromosomes in interspecific hybrid cells. Cell Cycle 13:1345–56 [Google Scholar]
  94. Wedzony M, Röber DK, Geiger HH. 94.  2002. Chromosome elimination observed in selfed progenies of maize inducer line RWS. XVIIth International Congress on Sex Plant Reproduction173 Lublin, Pol: Maria Curie–Sklodowska Univ. Press [Google Scholar]
  95. Wijnker E, Deurhof L, van de Belt J, de Snoo CB, Blankestijn H. 95.  et al. 2014. Hybrid recreation by reverse breeding in Arabidopsis thaliana. Nat. Protoc. 9:761–72 [Google Scholar]
  96. Wijnker E, van Dun K, de Snoo CB, Lelivelt CL, Keurentjes JJ. 96.  et al. 2012. Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nat. Genet. 44:467–70 [Google Scholar]
  97. Xu XW, Li L, Dong X, Jin WW, Melchinger AE, Chen SJ. 97.  2013. Gametophytic and zygotic selection leads to segregation distortion through in vivo induction of a maternal haploid in maize. J. Exp. Bot. 64:1083–96 [Google Scholar]
  98. Yu W, Lamb JC, Han F, Birchler JA. 98.  2006. Telomere-mediated chromosomal truncation in maize. PNAS 103:17331–36Provided the first description of telomere-mediated chromosomal truncation in plants. [Google Scholar]
  99. Zhang ZL, Qiu FZ, Liu YZ, Ma KJ, Li ZY, Xu SZ. 99.  2008. Chromosome elimination and in vivo haploid production induced by Stock 6-derived inducer line in maize (Zea mays L.). Plant Cell Rep. 27:1851–60 [Google Scholar]
  100. Zhao X, Xu X, Xie H, Chen S, Jin W. 100.  2013. Fertilization and uniparental chromosome elimination during crosses with maize haploid inducers. Plant Physiol. 163:721–31 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error