Skip to main content
Log in

The different origins of artificially-induced unreduced female gametes and their effect on transmitted parental heterozygosity in Populus

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

The induction of unreduced gametes via chromosome doubling is an effective way to produce triploids. During this process, the transmitted parental heterozygosity varies by different origins of unreduced gametes. In this study, a total of 110 allotriploid individuals from two cross combinations who shared only one male parent were obtained by chromosome doubling of megaspore via high temperature treatment in Populus tomentosa. Twenty-six SSR loci, at which the allelic configurations of the female parents ‘MC1’ and ‘MC2’ were heterozygous and different from male parent ‘YX1’, were screened. Among them, five pairs of pericentromeric SSR primers were selected to identify the origins of unreduced female gametes. Our results showed that 30 individuals from 110 allotriploids derived from the first division restitution (FDR), and 80 allotriploids from the second division restitution (SDR) in these two cross combinations. The transmitted parental heterozygosity of unreduced female gametes via FDR were 0.824 and 0.769 in two cross combinations, respectively, which was significantly higher than that of SDR (0.395 and 0.396, respectively). The FDR type unreduced gametes with higher heterozygosity transmitted from parents may be more desirable in triploid breeding. However, no significant difference in transmitted parental heterozygosity was found between the two FDR groups and two SDR groups. Correct elucidation of the origins of unreduced gametes may be conducive to their effective utilization for further sexual hybridization in triploid poplar breeding.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arrigo N, Barker MS (2012) Rarely successful polyploids and their legacy in plant genomes. Curr Opin Plant Biol 15(2):140–146

    Article  CAS  PubMed  Google Scholar 

  • Bakulin VJG (1966) Triploid clone of aspen in the Novosibirsk region forests. Genetika 11:58–68

    Google Scholar 

  • Barone A, Gebhardt C, Frusciante L (1995) Heterozygosity in 2n gametes of potato evaluated by RFLP markers. Theor Appl Genet 91(1):98–104

    Article  CAS  PubMed  Google Scholar 

  • Bauer E, Falque M, Walter H, Bauland C, Camisan C, Campo L, Meyer N, Ranc N, Rincent R, Schipprack W, Altmann T, Flament P, Melchinger AE, Menz M, Moreno-González J, Ouzunova M, Revilla P, Charcosset A, Martin OC, Schön C-C (2013) Intraspecific variation of recombination rate in maize. Genome Biol 14(9):R103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA (2010) Heterosis. Plant Cell 22(7):2105–2112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cervera MT, Storme V, Soto A, Ivens B, Van Montagu M, Rajora OP, Boerjan W (2005) Intraspecific and interspecific genetic and phylogenetic relationships in the genus Populus based on AFLP markers. Theor Appl Genet 111(7):1440–1456

    Article  CAS  PubMed  Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6(11):836–846

    Article  CAS  PubMed  Google Scholar 

  • Cromie GA, Smith GR (2007) Branching out: meiotic recombination and its regulation. Trends Cell Biol 17(9):448–455

    Article  CAS  PubMed  Google Scholar 

  • De Storme N, Geelen D (2013) Sexual polyploidization in plants—cytological mechanisms and molecular regulation. New Phytol 198(3):670–684

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong CB, Suo YJ, Kang XY (2014a) Assessment of the genetic composition of triploid hybrid Populus using SSR markers with low recombination frequencies. Can J For Res 44(7):692–699

    Article  Google Scholar 

  • Dong CB, Mao JF, Suo YJ, Shi L, Wang J, Zhang PD, Kang XY (2014b) A strategy for characterization of persistent heteroduplex DNA in higher plants. Plant J 80(2):282–291

    Article  CAS  PubMed  Google Scholar 

  • Dong CB, Suo YJ, Wang J, Kang XY (2015) Analysis of transmission of heterozygosity by 2n gametes in Populus (Salicaceae). Tree Genet Genomes 11(1):1–7

    Article  Google Scholar 

  • Einspahr DW (1984) Production and utilization of triploid hybrid aspen. Iowa State J Res 58(4):401

    Google Scholar 

  • Fort A, Ryder P, Mckeown PC, Wijnen CL, Aarts MGM, Sulpice R, Spillane C (2016) Disaggregating polyploidy, parental genome dosage and hybridity contributions to heterosis in Arabidopsis thaliana. New Phytol 209(2):590–599

    Article  CAS  PubMed  Google Scholar 

  • Geng XN, Ren YY, Han ZQ, Du K, Kang XY (2018) Production of hybrid triploids via inducing chromosome doubling of megaspore with high temperature treatment in Leuce poplar. J Beijing For Univ 29(11):22–25

    Google Scholar 

  • Han ZQ, Geng XN, Du K, Xu CP, Yao PQ, Bai FY, Kang XY (2018) Analysis of genetic composition and transmitted parental heterozygosity of natural 2n gametes in Populus tomentosa based on SSR markers. Planta 247(6):1407–1421

    Article  CAS  PubMed  Google Scholar 

  • Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11(12):2467–2474

    Article  PubMed  Google Scholar 

  • Hermsen JGT (1984) Mechanisms and genetic implications of 2n gamete formation. Iowa State J Res 58:421–434

    Google Scholar 

  • Hulce D, Li X, Snyderleiby T, Johathan Liu CS (2011) GeneMarker® genotyping software: tools to increase the statistical power of DNA fragment analysis. J Biomol Tech JBT 22(Suppl):S35

    Google Scholar 

  • Hutten RC, Schippers MG, Hermsen JG, Ramanna MS (1994) Comparative performance of FDR and SDR progenies from reciprocal 4x–2x crosses in potato. Theor Appl Genet 89(5):545–550

    Article  CAS  PubMed  Google Scholar 

  • Kang XY (2002) Cytogenetics and triploid breeding of Populus tomentosa. China Environmental Science Press, Beijing, p 2002

    Google Scholar 

  • Kang XY (2016) Polyploid induction techniques and breeding strategies in poplar. In: Mason AS (ed) Polyploidy and hybridization for crop improvement. CRC Press, Boca Raton, pp 76–96

    Google Scholar 

  • Lambing C, Franklin FC, Wang CR (2017) Understanding and manipulating meiotic recombination in plants. Plant Physiol 173(3):1530–1542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320(5875):481–483

    Article  CAS  PubMed  Google Scholar 

  • Lexer C, Heinze B, Steinkellner H, Kampfer S, Ziegenhagen B, Glössl JJT, Genetics A (2000) Microsatellite analysis of maternal half-sib families of Quercus robur, pedunculate oak: II. Inference of the seed parents from the offspring. Theor Appl Genet 99(1–2):858–865

    Article  Google Scholar 

  • Li YH, Kang XY (2007) Triploid induction in white poplar by chromosome doubling of megaspore. J Beijing For Univ 29(5):22–25

    Google Scholar 

  • Li X, Li L, Yan J (2015) Dissecting meiotic recombination based on tetrad analysis by single-microspore sequencing in maize. Nat Commun 6:6648

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Wang Y, Wang P, Yang J, Kang X (2016) Induction of unreduced megaspores in Eucommia ulmoides by high temperature treatment during megasporogenesis. Euphytica 212(3):515–524

    Article  Google Scholar 

  • Li D, Tian J, Xue Y, Chen H, Wang J (2019) Triploid production via heat-induced diploidisation of megaspores in Populus pseudo-simonii. Euphytica 215:10

    Article  Google Scholar 

  • Liao T, Cheng S, Zhu X, Min Y, Kang X (2016) Effects of triploid status on growth, photosynthesis, and leaf area in Populus. Trees 30(4):1137–1147

    Article  CAS  Google Scholar 

  • Liesebach H, Ulrich K, Ewald D (2015) FDR and SDR processes in meiosis and diploid gamete formation in poplars (Populus L.) detected by centromere-associated microsatellite markers. Tree Genet Genomes 11(1):1–10

    Article  Google Scholar 

  • Lu M, Zhang P, Kang X (2013) Induction of 2n female gametes in Populus adenopoda Maxim by high temperature exposure during female gametophyte development. Breed Sci 63(1):96–103

    Article  PubMed  PubMed Central  Google Scholar 

  • Mason AS, Pires JC (2015) Unreduced gametes: meiotic mishap or evolutionary mechanism? Trends Genet 31(1):5–10

    Article  CAS  PubMed  Google Scholar 

  • Modliszewski JL, Wang H, Albright AR, Lewis SM, Bennett AR, Huang J, Ma H, Wang Y, Copenhaver GP (2018) Elevated temperature increases meiotic crossover frequency via the interfering (Type I) pathway in Arabidopsis thaliana. PLoS Genet 14(5):e1007384

    Article  PubMed  PubMed Central  CAS  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 form of Populous tremula found in nature. Hereditas 21(1/2):372–382

    Google Scholar 

  • Nilsson-Ehle H, Tidn SP (1938) Production of forest trees with increased chromosome number and increased timber yield. Svensk Papp Tidn 2:5

    Google Scholar 

  • Peloquin SJ, Boiteux LS, Simon PW, Jansky SH (2008) A chromosome-specific estimate of transmission of heterozygosity by 2n gametes in potato. J Hered 99(2):177–181

    Article  CAS  PubMed  Google Scholar 

  • Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement—a review. Euphytica 133(1):3–8

    Article  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18(2):233–234

    Article  CAS  PubMed  Google Scholar 

  • Si W, Yuan Y, Huang J, Zhang XH, Zhang YC, Zhang YD, Tian DC, Wang CL, Yang YH, Yang SH (2015) Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants. New Phytol 206(4):1491–1502

    Article  CAS  PubMed  Google Scholar 

  • Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proc Nat Acad Sci USA 97(13):7051–7057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian MD, Li YJ, Zhang PD, Wang J, Hao JY (2018) Pollen chromosome doubling induced by high temperature exposure to produce hybrid triploids in Populus canescens. Sci Silvae Sin 54(3):39–47

    Google Scholar 

  • Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH (2012) Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genom 13(1):1–19

    Article  CAS  Google Scholar 

  • Vorsa N, Rowland LJ (1997) Estimation of 2n megagametophyte heterozygosity in a diploid Blueberry (Vaccinium darrowi Camp) clone using RAPDs. J Hered 88(5):423–426

    Article  CAS  Google Scholar 

  • Wang J, Li DL, Kang XY (2011) Induction of unreduced megaspores with high temperature during megasporogenesis in Populus. Ann For Sci 69(1):59–67

    Article  Google Scholar 

  • Wang J, Li DL, Shang FN, Kang XY (2017) High temperature-induced production of unreduced pollen and its cytological effects in Populus. Sci Rep 7(1):5281

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang YX, Copenhaver GP (2018) Meiotic recombination: mixing it up in plants. Annu Rev Plant Biol 69:577–609

    Article  CAS  PubMed  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

    Article  Google Scholar 

  • Xie KD, Wang XP, Biswas MK, Liang WJ, Xu Q, Grosser JW, Guo WW (2014) 2n megagametophyte formed via SDR contributes to tetraploidization in polyembryonic 'Nadorcott' tangor crossed by citrus allotetraploids. Plant Cell Rep 33(10):1641–1650

    Article  CAS  PubMed  Google Scholar 

  • Yao CL, Pu JW (1998) Timber characteristics and pulp properties of the triploid of Populus tomentosa. J Beijing For Univ 20(5):18–21

    Google Scholar 

  • Yao CL, Wu DX, Lin HB, Wang R, Wang JH (1992) Studies on timber characterization and paper properties of the hybrid clones of Populus tomentosa. J Beijing For Univ 14(S3):72–77

    Google Scholar 

  • Yao PQ, Li GH, Long QY, He LG, Kang XY (2016) Male parent identification of triploid rubber trees (Hevea brasiliensis) and the mechanism of 2n gametes formation. Forests 7(12):301

    Article  Google Scholar 

  • Yao PQ, Li GH, Long QY, He LG, Kang XY (2017) Microsporogenesis and induction of unreduced pollen with high temperatures in rubber tree clone RRIM 600. Forests 8(5):152

    Article  Google Scholar 

  • Yin TM, Zhang XY, Gunter LE, Li SX, Wullschleger SD, Huang MR, Tuskan GA (2009) Microsatellite primer resource for Populus developed from the mapped sequence scaffolds of the Nisqually-1 genome. New Phytol 181(2):498–503

    Article  CAS  PubMed  Google Scholar 

  • Zhang JF, Wei ZZ, Li D, Li B (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):506

    Article  CAS  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 triploids of Populus tomentosa. Sci Silvae Sin 34(4):22–31

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank Professor Jun Wang and Professor Pingdong Zhang, College of Biological Sciences and Technology, Beijing Forestry University for precious suggestion before the submission. And the authors would like to thank the staff of Guanxian nursery in Shandong Province, China for providing the experimental field. We are also grateful to the anonymous reviewers and editors for their constructive comments. This research was financially supported by the National Natural Science Foundation of China (No. 31470667).

Author information

Authors and Affiliations

Authors

Contributions

XG and XK conceived and designed the study. XG and ZH conducted experiments. XG, QH and KD analyzed the data. XK supervised experiments. XG, JY and XK wrote and edited manuscripts. All authors read and approved the manuscript.

Corresponding author

Correspondence to Xiangyang Kang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 12 kb)

Supplementary file2 (XLSX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Geng, X., Han, Z., Yang, J. et al. The different origins of artificially-induced unreduced female gametes and their effect on transmitted parental heterozygosity in Populus. Euphytica 215, 181 (2019). https://doi.org/10.1007/s10681-019-2501-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-019-2501-7

Keywords

Navigation