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Engineering of plant chromosomes

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Abstract

Engineered minimal chromosomes with sufficient mitotic and meiotic stability have an enormous potential as vectors for stacking multiple genes required for complex traits in plant biotechnology. Proof of principle for essential steps in chromosome engineering such as truncation of chromosomes by T-DNA-mediated telomere seeding and de novo formation of centromeres by cenH3 fusion protein tethering has been recently obtained. In order to generate robust protocols for application in plant biotechnology, these steps need to be combined and supplemented with additional methods such as site-specific recombination for the directed transfer of multiple genes of interest on the minichromosomes. At the same time, the development of these methods allows new insight into basic aspects of plant chromosome functions such as how centromeres assure proper distribution of chromosomes to daughter cells or how telomeres serve to cap the chromosome ends to prevent shortening of ends over DNA replication cycles and chromosome end fusion.

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Abbreviations

BFB:

Breakage-fusion-bridge

cenH3:

Centromeric histone H3-variant

Cre:

Phage P1 recombinase

CRISPR:

Clustered regularly interspaced short palindromic repeats

DSB:

Double-strand break

GFP:

Green fluorescence protein

LacI:

Lac inhibitor protein

lacO :

Lac operator sequence

loxP :

Locus of crossing-over on phage P1

PARC:

Plant artificial ring chromosome

References

  • Acevedo-Garcia J, Collins NC, Ahmadinejad N, Ma L, Houben A, Bednarek P, Benjdia M, Freialdenhoven A, Altmuller J, Nurnberg P, Reinhardt R, Schulze-Lefert P, Panstruga R (2013) Fine mapping and chromosome walking towards the Ror1 locus in barley (Hordeum vulgare L.). Theor Appl Genet 126:2969–2982

    Article  CAS  PubMed  Google Scholar 

  • Albert H, Dale EC, Lee E, Ow DW (1995) Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7:649–659

    Article  CAS  PubMed  Google Scholar 

  • Ananiev EV, Wu CC, Chamberlin MA, Svitashev S, Schwartz C, Gordon-Kamm W, Tingey S (2009) Artificial chromosome formation in maize (Zea mays L.). Chromosoma 118:157–177

    Article  CAS  PubMed  Google Scholar 

  • Barnhart MC, Kuich PHJL, Stellfox ME, Ward JA, Bassett EA, Black BE, Foltz DR (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194:229–243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Birchler JA (2014) Engineered minichromosomes in plants. Curr Opin Plant Biol 19:76–80

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA, Han F (2013) Meiotic behavior of small chromosomes in maize. Front Plant Sci 4:505

    Article  PubMed Central  PubMed  Google Scholar 

  • Birchler JA, Krishnaswamy L, Gaeta RT, Masonbrink RE, Zhao CZ (2010) Engineered minichromosomes in plants. Crit Rev Plant Sci 29:135–147

    Article  CAS  Google Scholar 

  • Burrack LS, Berman J (2012) Neocentromeres and epigenetically inherited features of centromeres. Chromosom Res 20:607–619

    Article  CAS  Google Scholar 

  • Carlson SR, Rudgers GW, Zieler H, Mach JM, Luo S, Grunden E, Krol C, Copenhaver GP, Preuss D (2007) Meiotic transmission of an in vitro-assembled autonomous maize minichromosome. PLoS Genet 3:1965–1974

    Article  CAS  PubMed  Google Scholar 

  • Chan SW (2010) Chromosome engineering: power tools for plant genetics. Trends Biotechnol 28:605–610

    Article  CAS  PubMed  Google Scholar 

  • Chilton MD, Que Q (2003) Targeted integration of T-DNA into the tobacco genome at double-stranded breaks: new insights on the mechanism of T-DNA integration. Plant Physiol 133:956–965

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Conant GC, Birchler JA, Pires JC (2014) Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Curr Opin Plant Biol 19:91–98

    Article  CAS  PubMed  Google Scholar 

  • Endo TR (2007) The gametocidal chromosome as a tool for chromosome manipulation in wheat. Chromosom Res 15:67–75

    Article  CAS  Google Scholar 

  • Farr C, Fantes J, Goodfellow P, Cooke H (1991) Functional reintroduction of human telomeres into mammalian cells. Proc Natl Acad Sci U S A 88:7006–7010

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gaeta RT, Masonbrink RE, Krishnaswamy L, Zhao C, Birchler JA (2012) Synthetic chromosome platforms in plants. Annu Rev Plant Biol 63:307–330

    Article  CAS  PubMed  Google Scholar 

  • Gaeta RT, Masonbrink RE, Zhao C, Sanyal A, Krishnaswamy L, Birchler JA (2013) In vivo modification of a maize engineered minichromosome. Chromosoma 122:221–232

    Article  CAS  PubMed  Google Scholar 

  • Han F, Lamb JC, Birchler JA (2006) High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc Natl Acad Sci U S A 103:3238–3243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Han FP, Gao Z, Yu WC, Birchler JA (2007) Minichromosome analysis of chromosome pairing, disjunction, and sister chromatid cohesion in maize. Plant Cell 19:3853–3863

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Houben A, Schlegel R (1991) Chromosomentransfer bei Pflanzen. Wiss Fortschr 41:358–360

    CAS  Google Scholar 

  • Houben A, Schubert I (2007) Engineered plant minichromosomes: a resurrection of B chromosomes? Plant Cell 19:2323–2327

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Houben A, Dawe RK, Jiang JM, Schubert I (2008) Engineered plant minichromosomes: a bottom-up success? Plant Cell 20:8–10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN (2014) Evolution and biology of supernumerary B chromosomes. Cell Mol Life Sci 71:467–478

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575

    Article  CAS  PubMed  Google Scholar 

  • Jovtchev G, Watanabe K, Pecinka A, Rosin FM, Mette MF, Lam E, Schubert I (2008) Size and number of tandem repeat arrays can determine somatic homologous pairing of transgene loci mediated by epigenetic modifications in Arabidopsis thaliana nuclei. Chromosoma 117:267–276

    Article  PubMed  Google Scholar 

  • Jovtchev G, Borisova BE, Kuhlmann M, Fuchs J, Watanabe K, Schubert I, Mette MF (2011) Pairing of lacO tandem repeats in Arabidopsis thaliana nuclei requires the presence of hypermethylated, large arrays at two chromosomal positions, but does not depend on H3-lysine-9-dimethylation. Chromosoma 120:609–619

    Article  CAS  PubMed  Google Scholar 

  • Kapusi E, Ma L, Teo CH, Hensel G, Himmelbach A, Schubert I, Mette MF, Kumlehn J, Houben A (2012) Telomere-mediated truncation of barley chromosomes. Chromosoma 121:181–190

    Article  CAS  PubMed  Google Scholar 

  • Lermontova I, Schubert V, Fuchs J, Klatte S, Macas J, Schubert I (2006) Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18:2443–2451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Louwerse JD, van Lier MCM, van der Steen DM, de Vlaam CMT, Hooykaas PJJ, Vergunst AC (2007) Stable recombinase-mediated cassette exchange in Arabidopsis using Agrobacterium tumefaciens. Plant Physiol 145:1282–1293

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lukaszewski AJ (1997) Construction of midget chromosomes in wheat. Genome 40:566–569

    Article  CAS  PubMed  Google Scholar 

  • Matzke AJM, Huettel B, van der Winden J, Matzke M (2005) Use of two-color fluorescence-tagged transgenes to study interphase chromosomes in living plants. Plant Physiol 139:1586–1596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mendiburo MJ, Padeken J, Fulop S, Schepers A, Heun P (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334:686–690

    Article  CAS  PubMed  Google Scholar 

  • Murata M (2014) Minichromosomes and artificial chromosomes in Arabidopsis. Chromosome Res : Int J Mol Supramol Evol Aspects Chromosome Biol 22:167–178

    Article  CAS  Google Scholar 

  • Murata M, Shibata F, Hironaka A, Kashihara K, Fujimoto S, Yokota E, Nagaki K (2013) Generation of an artificial ring chromosome in Arabidopsis by Cre/LoxP-mediated recombination. Plant J 74:363–371

    Article  CAS  PubMed  Google Scholar 

  • Naqvi S, Farre G, Sanahuja G, Capell T, Zhu C, Christou P (2010) When more is better: multigene engineering in plants. Trends Plant Sci 15:48–56

    Article  CAS  PubMed  Google Scholar 

  • Nelson AD, Lamb JC, Kobrossly PS, Shippen DE (2011) Parameters affecting telomere-mediated chromosomal truncation in Arabidopsis. Plant Cell 23:2263–2272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ohzeki J-I, Bergmann JH, Kouprina N, Noskov VN, Nakano M, Kimura H, Earnshaw WC, Larionov V, Masumoto H (2012) Breaking the HAC barrier: histone H3K9 acetyl/methyl balance regulates CENP-A assembly. EMBO J 31:2391–2402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ow DW (2007) GM maize from site-specific recombination technology, what next? Curr Opin Biotechnol 18:115–120

    Article  CAS  PubMed  Google Scholar 

  • Phan BH, Jin W, Topp CN, Zhong CX, Jiang J, Dawe RK, Parrott WA (2007) Transformation of rice with long DNA-segments consisting of random genomic DNA or centromere-specific DNA. Transgenic Res 16:341–351

    Article  CAS  PubMed  Google Scholar 

  • Puchta H, Fauser F (2014) Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant J 78:727–741

    Article  CAS  PubMed  Google Scholar 

  • Rosin FM, Watanabe N, Cacas JL, Kato N, Arroyo JM, Fang Y, May B, Vaughn M, Simorowski J, Ramu U, McCombie RW, Spector DL, Martienssen RA, Lam E (2008) Genome-wide transposon tagging reveals location-dependent effects on transcription and chromatin organization in Arabidopsis. Plant J 55:514–525

    Article  CAS  PubMed  Google Scholar 

  • Rubtsova M, Kempe K, Gils A, Ismagul A, Weyen J, Gils M (2008) Expression of active Streptomyces phage phiC31 integrase in transgenic wheat plants. Plant Cell Rep 27:1821–1831

    Article  CAS  PubMed  Google Scholar 

  • Schubert I (2001) Alteration of chromosome numbers by generation of minichromosomes—is there a lower limit of chromosome size for stable segregation? Cytogenet Cell Genet 93:175–181

    Article  CAS  PubMed  Google Scholar 

  • Schubert I, Oud JL (1997) There is an upper limit of chromosome size for normal development of an organism. Cell 88:515–520

    Article  CAS  PubMed  Google Scholar 

  • Stuurman J, de Vroomen MJ, Nijkamp HJ, van Haaren MJ (1996) Single-site manipulation of tomato chromosomes in vitro and in vivo using Cre-lox site-specific recombination. Plant Mol Biol 32:901–913

    Article  CAS  PubMed  Google Scholar 

  • Teo CH, Ma L, Kapusi E, Hensel G, Kumlehn J, Schubert I, Houben A, Mette MF (2011) Induction of telomere-mediated chromosomal truncation and stability of truncated chromosomes in Arabidopsis thaliana. Plant J 68:28–39

    Article  CAS  PubMed  Google Scholar 

  • Teo CH, Lermontova I, Houben A, Mette MF, Schubert I (2013) De novo generation of plant centromeres at tandem repeats. Chromosoma 122:233–241

    Article  CAS  PubMed  Google Scholar 

  • Vega JM, Yu WC, Han FP, Kato A, Peters EM, Zhang ZJ, Birchler JA (2008) Agrobacterium-mediated transformation of maize (Zea mays) with Cre-lox site specific recombination cassettes in BIBAC vectors. Plant Mol Biol 66:587–598

    Article  CAS  PubMed  Google Scholar 

  • Vergunst AC, Jansen LET, Hooykaas PJJ (1998) Site-specific integration of Agrobacterium T-DNA in Arabidopsis thaliana mediated by Cre recombinase. Nucleic Acids Res 26:2729–2734

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Watanabe K, Pecinka A, Meister A, Schubert I, Lam E (2005) DNA hypomethylation reduces homologous pairing of inserted tandem repeat arrays in somatic nuclei of Arabidopsis thaliana. Plant J 44:531–540

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Cheng Z, Yu W (2012) Construction of rice mini-chromosomes by telomere-mediated chromosomal truncation. Plant J 70:1070–1079

    Article  CAS  PubMed  Google Scholar 

  • Yu WC, Lamb JC, Han FP, Birchler JA (2006) Telomere-mediated chromosomal truncation in maize. Proc Natl Acad Sci U S A 103:17331–17336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu WC, Han FP, Birchler JA (2007a) Engineered minichromosomes in plants. Curr Opin Biotechnol 18:425–431

    Article  CAS  PubMed  Google Scholar 

  • Yu WC, Han FP, Gao Z, Vega JM, Birchler JA (2007b) Construction and behavior of engineered minichromosomes in maize. Proc Natl Acad Sci U S A 104:8924–8929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang W, Lee HR, Koo DH, 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang H, Phan BH, Wang K, Artelt BJ, Jiang J, Parrott WA, Dawe RK (2012) Stable integration of an engineered megabase repeat array into the maize genome. Plant J 70:357–365

    Article  PubMed  Google Scholar 

  • Zhang J, Zhang B, Su H, Birchler JA, Han F (2014) Molecular mechanisms of homologous chromosome pairing and segregation in plants. J Genet Genomics = Yi Chuan Xue Bao 41:117–123

    Article  Google Scholar 

  • Zhao X, Xu XW, Xie HX, Chen SJ, Jin WW (2013) Fertilization and uniparental chromosome elimination during crosses with maize haploid inducers. Plant Physiol 163:721–731

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by DFG (German Research Council) grant HO 1779/22-1.

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Correspondence to Michael Florian Mette.

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Responsible Editors: Natalay Kouprina and Vladimir Larionov

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Mette, M.F., Houben, A. Engineering of plant chromosomes. Chromosome Res 23, 69–76 (2015). https://doi.org/10.1007/s10577-014-9449-1

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