Skip to main content
SpringerLink
Log in

Inducing triploids and tetraploids with high temperatures in Populus sect. Tacamahaca

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

This study is the first to report that triploids and tetraploids have been successfully produced through embryo sac and zygotic embryo chromosome doubling with high temperatures in P. simonii Carr. and its hybrid.

Abstract

A new synthetic polyploid induced by hybridization with unreduced gametes and heterozygotic embryo chromosome doubling can effectively combine polyploidy and heterosis, which can provide two major breeding advantages. In Populus, successfully creating and cultivating new polyploid varieties have economic and ecological production value. This was the first successful study in which embryo sac and zygotic embryo chromosome doubling was induced using high temperatures to produce triploids and tetraploids in Populus simonii Carr. and its hybrid, P. simonii × P. nigra var. Italica, of Populus sect. Tacamahaca. The relationship between flower bud morphological characteristics (time after pollination) and female meiotic stage (embryo sac and zygotic embryo development) was established to guide the induction treatment period. In the resulting progeny, 37 triploids and 12 tetraploids were obtained and identified using flow cytometry. The optimal temperatures for embryo sac and zygotic embryo chromosome doubling were 38 and 41 °C, respectively. Cytogenetic analysis revealed that 66–72 h after pollination (HAP), a period characterized by a high proportion of one-nucleate and two-nucleate embryo sacs, was the optimal period for embryo sac chromosome doubling. For zygotic embryo chromosome doubling, 168 HAP was the optimal induction period, as there was a high proportion of two-cell and four-cell proembryos. The results indicate that inducing embryo sac and zygotic embryo chromosome doubling is an ideal method for producing polyploids. The methods for inducing polyploids and for evaluating ploidy and offspring with different ploidies and heterozygosity in this study will be useful for genetic research and Populus breeding programmes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aversano R, Capomaccio S, Carputo D, Veronesi F, Rosellini D (2012) Variation of DNA methylation and phenotypic traits following unilateral sexual polyploidization in Medicago. Euphytica 186(3):731–739. doi:10.1007/s10681-011-0571-2

    Article  CAS  Google Scholar 

  • Bastiaanssen HJM, Van Den Berg PMMM, Lindhout P, Jacobsen E, Ramanna MS (1998) Postmeiotic restitution in 2n-egg formation of diploid potato. Heredity 81(1):20–27. doi:10.1046/j.1365-2540.1998.00370.x

    Article  CAS  Google Scholar 

  • Bradshaw HD Jr, Stettler RF (1993) Molecular genetics of growth and development in Populus. I. Triploidy in hybrid poplars. Theor Appl Genet 86(2–3):301–307

    PubMed  Google Scholar 

  • Bradshaw HD Jr, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as model forest tree. J Plant Growth Regul 19(3):306–313

    Article  CAS  Google Scholar 

  • Cai X, Kang XY (2011) In vitro tetraploid induction from leaf explants of Populus pseudo-simonii Kitag. Plant Cell Rep 30(9):1771–1778. doi:10.1007/s00299-011-1085-z

    Article  CAS  PubMed  Google Scholar 

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58(1):377–406. doi:10.1146/annurev.arplant.58.032806.103835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhooghe E, Laere KV, Eeckhaut T, Leus L, Huylenbroeck JV (2011) Mitotic chromosome doubling of plant tissues in vitro. Plant Cell Tissue Organ Culture 104(3):359–373. doi:10.1007/s11240-010-9786-5

    Article  Google Scholar 

  • Doležel J, Binarová P, Lucretti S (1989) Analysis of nuclear DNA content in plant cells by flow cytometry. Biol Plant 31(2):113–120. doi:10.1007/BF02907241

    Article  Google Scholar 

  • Dong CB, Suo YJ, Wang J, Kang XY (2014) Analysis of transmission of heterozygosity by 2n gametes in Populus (Salicaceae). Tree Genet Genomes 11(1):1–7. doi:10.1007/s11295-014-0799-9

    CAS  Google Scholar 

  • Ewald D, Ulrich K, Naujoks G, Schröder M-B (2009) Induction of tetraploid poplar and black locust plants using colchicine: chloroplast number as an early marker for selecting polyploids in vitro. Plant Cell Tissue Organ Culture 99(3):353–357. doi:10.1007/s11240-009-9601-3

    Article  Google Scholar 

  • Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal pollinated plants. Am Nat 133(3):323–344

    Article  Google Scholar 

  • Harder M, Verhagen S, Winton L, Einspahr D (1976) Tetraploid aspen production using unreduced pollen from triploid males. For Sci 22(3):329–330

    Google Scholar 

  • Ichiro T (1993) Development of male gametes in flowering plants. J Plant Res 106(1):55–63. doi:10.1007/BF02344373

    Article  Google Scholar 

  • Kadota M, Niimi Y (2002) In vitro induction of tetraploid plants from a diploid Japanese pear cultivar (Pyrus pyrifolia N. cv. Hosui). Plant Cell Rep 21(3):282–286. doi:10.1007/s00299-002-0509-1

    Article  CAS  Google Scholar 

  • Kang XY (1996) Chromosome count and shape of poplar. J Gansu Agric Univ 31(1):67–70

    Google Scholar 

  • Kang XY, Zhu ZT (1997) A study on the 2n pollen vitality and germinant characteristics of white poplars. Acta Bot Yunnanica 19(4):402–406

    Google Scholar 

  • Kang XY, Zhu ZT, Lin HB (1999) Study on the effective treating period for pollen chromosome doubling of Populus tomentosa × P. bolleana. Sci Silvae Sin 35(4):21–24

  • Kang XY, Zhu ZT, Zhang ZY (2000) Breeding of triploids by the reciprocal crossing of Populus alba × P. glandulosa and P. tomentosa × P. bolleana. J Beijing For Univ 22(6):8–11

  • Kang XY, Zhang PD, Gao P, Zhao F (2004) Discovery of a new way of poplar triploids induced with colchicine after pollination. J Beijing For Univ 26(1):1–4

    Google Scholar 

  • Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122(1):1–25

    Article  Google Scholar 

  • Li GP, Huang QC (2006) Ontogeny of pollen and pollination in Keteleeria fortunei. Sci Silvae Sin 42(5):42–47

    Google Scholar 

  • Li WD, Fan RW, Mai XL (1982) On the embryological observations of the seed development of Populus simonii Carr. Sci Silvae Sin 18(2):113–119

    Google Scholar 

  • Li YH, Kang XY, Wang SD, Zhang ZH, Chen HW (2008) Triploid induction in Populus alba × P. glandulosa by chromosome doubling of female gametes. Silvae Genet 57(1):37–40

    Google Scholar 

  • Li A, Hu BQ, Xue ZY, Chen L, Wang WX, Song WQ, Chen CB, Wang CG (2011) DNA methylation in genomes of several annual herbaceous and woody perennial plants of varying ploidy as detected by MSAP. Plant Mol Biol Rep 29(4):784–793. doi:10.1007/s11105-010-0280-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao T, Cheng SP, Zhu XH, Min Y, Kang XY (2016) Effects of triploid status on growth, photosynthesis, and leaf area in Populus. Trees 30(4):1–11. doi:10.1007/s00468-016-1352-2

    Article  Google Scholar 

  • Lu M, Zhang PD, Kang XY (2013) Induction of 2n female gametes in Populus adenopoda Maxim by high temperature exposure during female gametophyte development. Breed Sci 63(1):96–103. doi:10.1270/jsbbs.63.96

    Article  PubMed  PubMed Central  Google Scholar 

  • Magnard JL, Yang M, Chen YCS, 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(3):1157–1166. doi:10.1104/pp.010473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattila RE (1961) On the production of the tetraploid hybrid aspen by colchicine treatment. Hereditas 47(3–4):631–640

    Google Scholar 

  • Matzke MA, Scheid OM, Matzke AJM (1999) Rapid structural and epigenetic changes in polyploid and aneuploid genomes. BioEssays 21(9):761–767

    Article  CAS  PubMed  Google Scholar 

  • Mireille R, Najat J, Charlette S, Russell S, Dumas C (1991) Male gametophyte development and formation of the male germ unit in Populus deltoides following compatible pollination. Protoplasma 162(2):140–150. doi:10.1007/BF02562557

    Google Scholar 

  • Mireille R, Najat J, Charlette S, Russell S, Dumas C (1992) Interspecific incompatibility in Populus: inhibition of tube growth and behaviour of the male germ unit in P. deltoides × P. alba cross. Protoplasma 168(3):107–110. doi:10.1007/BF01666256

    Google Scholar 

  • Mofidabadi AJ, Modir-Rahmati AR, Tavesoli A (1998) Application of ovary and ovule culture in Populus alba L. × P. euphratica OLIV. hybridization. Silvae Genet 47(5):332–334

    Google Scholar 

  • Müntzing A (1936) The chromosomes of a giant Populus tremula. Hereditas 21(2–3):383–393

    Google Scholar 

  • Nilsson-Ehle H (1936) Note regarding the gigas from of Populus tremula found in nature. Hereditas 21:372–382

    Google Scholar 

  • Nomura K, Nakajima J, Ohta H, Kagawa H, Tanaka H, Unuma T, Yamauchi K, Arai K (2004) Induction of triploidy by heat shock in the Japanese eel Anguilla japonica. Fish Sci 70(2):247–255. doi:10.1111/j.1444-2906.2003.00798.x

    Article  CAS  Google Scholar 

  • Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19(3):141–147. doi:10.1016/S0168-9525(03)00015-5

    Article  CAS  PubMed  Google Scholar 

  • Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131(3):452–462. doi:10.1016/j.cell.2007.10.022

    Article  CAS  PubMed  Google Scholar 

  • Pires JC, Zhao JW, Schranz ME, Leon EJ, Quijada PA, Lukens LN, Osborn TC (2004) Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol J Linn Soc 82(4):675–688. doi:10.1111/j.1095-8312.2004.00350.x

    Article  Google Scholar 

  • Randolph LF (1932) Some effects of high temperature on polyploidy and other variations in maize. Proc Natl Acad Sci USA 18(3):222–229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301(5637):1211–1216. doi:10.1126/science.1086949

    Article  CAS  PubMed  Google Scholar 

  • Risso-Pascotto C, Pagliarini MS, Do Valle CB, Jank L (2004) Asynchronous meiosis in an interspecific hybrid of Brachiaria ruziziensis and B. brizantha. Plant Cell Rep 23(5):304–310. doi:10.1007/s00299-004-0802-2

  • Robinson JP (2006) DNA content measurement for DNA ploidy and cell cycle analysis. In: Darzynkiewicz Z, Juan G (eds) Current protocols in cytometry. Wiley, New York, pp 1–24

    Google Scholar 

  • Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14(4):1163–1175. doi:10.1111/j.1365-294X.2005.02488.x

    Article  CAS  PubMed  Google Scholar 

  • Shaked H, Kashkush K, Ozakan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13(8):1749–1759. doi:10.1105/TPC.010083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song K, Lu P, Tang K, Osborn TC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploidy evolution. Proc Natl Acad Sci USA 92(17):7719–7723. doi:10.1073/pnas.92.17.7719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stebbins GL (1985) Polyploidy, hybridization and invasion of new habitats. Ann Mo Bot Gard 72(4):824–832. doi:10.2307/2399224

    Article  Google Scholar 

  • Tavoletti S (1994) Cytological mechanisms of 2n egg formation in a diploid genotype of Medicago sativa subsp. falcate. Euphytica 75(1–2):1–8. doi:10.1007/BF00024525

    Article  Google Scholar 

  • Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homeologous recombination in four mapping populations of Brassica napus L. Genetics 169(2):967–979. doi:10.1534/genetics.104.033209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Kang XY, Li DL, Jing YC, Zhang ZH (2006) Meiosis and chromosome behavior of pollen mother cell in Populus simonii Carr. × P. nigra L. ‘Tongliao’. Acta Bot Boreali Occident Sin 26(11):2231–2238

  • Wang J, Kang XY, Li DL (2008) Chromocenter number and relationship between it and ploidy level in Populus. Acta Bot Boreali Occident Sin 28(10):1968–1971

    Google Scholar 

  • Wang J, Kang XY, Li DL, Chen HW, Zhang PD (2010) Induction of diploid eggs with colchicine during embryo sac development in Populus. Silvae Genet 59(1):40–48

    Google Scholar 

  • Wang J, Kang XY, Li DL (2012) High temperature-induced triploid production during embryo sac development in Populus. Silvae Genet 61(3):85–93

    Google Scholar 

  • Wang J, Shi L, Song SY, Tian J, Kang XY (2013) Tetraploid production through zygotic chromosome doubling in Populus. Silva Fenn 47(2):1–12

    Article  Google Scholar 

  • Wei ZZ, Du QZ, Zhang JF, Li BB, Zhang DQ (2013) Genetic diversity and population structure in Chinese indigenous poplar (Populus simonii) populations using microsatellite markers. Plant Mol Biol Rep 31(3):620–632. doi:10.1007/s11105-012-0527-2

    Article  CAS  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42(l):225–249. doi:10.1007/978-94-011-4221-2_12

  • Winton LL (1968) Fertilization in forced quaking aspen and cottonwood. Silvae Genet 17(1):20–21

    Google Scholar 

  • Winton LL, Einspahr DW (1970) Tetraploid aspen production using unreduced triploid pollen. For Sci 16(2):180–182

    Google Scholar 

  • Wyatt R (1982) Inflorescence architecture: how flower number, arrangement, and phenology affect pollination and fruit set. Am J Bot 69(4):585–594

    Article  Google Scholar 

  • Xi XJ, Li D, Xu WT, Guo LQ, Zhang JF, Li BL (2012) 2n egg formation in Populus × euramericana (Dode) Guinier. Tree Genet Genomes 8(6):1237–1245. doi:10.1007/s11295-012-0510-y

    Article  Google Scholar 

  • Xi XJ, Guo LQ, Xu WT, Zhang JF, Li BL (2014) Megasporogenesis, megagametogenesis and induction of 2n eggs with colchicine in section Aigeiros. Scand J For Res 29(6):527–536. doi:10.1080/02827581.935472

    Article  Google Scholar 

  • Xu JR, Li YY (2014) Experiments design in forestry. China Agricultural Press, Beijing

    Google Scholar 

  • Yang H, Guo X (2006) Polyploid induction by heat shock-induced meiosis and mitosis inhibition in the dwarf surfclam, Mulinia lateralis Say. Aquaculture 252(2):171–182. doi:10.1016/j.aquaculture.2005.07.017

    Article  Google Scholar 

  • Yu JL, Wang HJ, Hou JM, Zhang J, Qiao GJ, Jin ZH (2008) Investigation of flexural strength and porosity of porous Si3N4 ceramics through orthogonal experimental design. J Ceram Process Res 9(6):624–629

    Google Scholar 

  • Zhang ZY, Yu XS (2000) Advances in reproduction biology of poplars. J Beijing For Univ 22(6):69–74

    Google Scholar 

  • Zhang S, Qi L, Chen C, Li X, Song W, Chen R, Han S (2004) A report of triploid Populus of the section Aigeiros. Silvae Genet 53(2):69–75

    Google Scholar 

  • Zhang JF, Wei ZZ, Li D, Li BL (2009) Using SSR markers to study the mechanism of 2n pollen formation in Populus × euramericana (Dode) Guinier and P. × popularis. Ann For Sci 66(5):53–62. doi:10.1051/forest/2009032

  • Zhu ZT (2006) Genetic improvement of Populus tomentosa. China Forestry Press, Beijing

    Google Scholar 

  • Zhu ZT, Lin HB, Kang XY (1995) Studies on allotriploid breeding of Populus tomentosa B301 clones. Sci Silvae Sin 31(6):499–505

    Google Scholar 

  • Zhu ZT, Kang XY, Zhang ZY (1998) Studies on selection of natural triploid of Populus tomentosa. Sci Silvae Sin 34(4):22–31

    Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (Nos. 31370658, J1103516 and 31301803), the Beijing Academy of Agriculture and Forestry Sciences for Youth (QNJJ201403), the Program for Changjiang Scholars and Innovative Research Team in University (IRT13047), the “948” Project of China (2014-4-59) and the Key Project of the Chinese Ministry of Education (No. 109022).

Author information

Author notes

    Authors and Affiliations

    1. National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of State Forestry Administration, College of Biological Science and Biotechnology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

      Liqin Guo, Wenting Xu, Yan Zhang & Jinfeng Zhang

    2. State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation, State Forestry Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, 100091, People’s Republic of China

      Liqin Guo

    3. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China), Ministry of Agriculture, Key Laboratory of Urban Agriculture (North), Ministry of Agriculture, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, People’s Republic of China

      Zunzheng Wei

    Authors
    1. Liqin Guo
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Wenting Xu
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Yan Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Jinfeng Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Zunzheng Wei
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Jinfeng Zhang or Zunzheng Wei.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no competing interests.

    Additional information

    Communicated by D.-B. Zhang.

    L. Guo and W. Xu contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 17441 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Guo, L., Xu, W., Zhang, Y. et al. Inducing triploids and tetraploids with high temperatures in Populus sect. Tacamahaca . Plant Cell Rep 36, 313–326 (2017). https://doi.org/10.1007/s00299-016-2081-0

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00299-016-2081-0

    Keywords

    Search

    Navigation