Skip to main content
SpringerLink
Log in

Abnormal meiotic chromosome behavior and gametic variation induced by intersectional hybridization in Populus L.

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Abnormal meiotic chromosome behavior and pollen variation in two intersectional hybrids between Populus simonii Carr. (section Tacamahaca Spach) and Populus euphratica Oliv. (section Turanga Bge.) were investigated by the squashed technique and indirect immunofluorescence. Both hybrids produced abnormal flower buds characterized by a primary bud with an accessary bud at frequencies of 39.0 and 17.8 %, respectively. Chromosome pairing analysis at late diakinesis showed average configurations 20.31 I + 7.04 II + 1.42 III + 0.04 IV in hybrid “Xhu-DK” and 19.18 I + 7.16 II + 1.45 III + 0.04 IV in hybrid “Xhu-TL”, indicating high divergence between their parent species. Meiotic abnormalities, including precocious chromosome migration, lagging chromosomes, chromosome bridges, and micronuclei, were observed at high frequency, resulting in imbalanced chromosome segregation and chromosome elimination and caused high gamete sterility. Some micronuclei triggered formation of minispindles in Metaphase II, which were responsible for the formation of microcytes. Fused and tripolar spindles in the second meiotic division developed into dyads and triads, respectively, leading to viable first meiotic division restitution (FDR) type unreduced pollen formation. However, Xhu-TL was completely sterile because the high frequency of precocious cytokinesis during the second division prevented unreduced pollen formation though spindle fusion. Xhu-DK produced 29.6 % viable pollen grains. The diameter of viable pollen ranged from 19.6 to 64.9 μm, suggesting that Xhu-DK might be capable of producing unreduced pollen or pollen with a higher ploidy level. The strategy of using the distant hybrids for chromosome introgression and polyploidy breeding in Populus L. was considered.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anton KA, Ward JR, Cruzan MB (2013) Pollinator-mediated selection on floral morphology evidence for transgressive evolution in a derived hybrid lineage. J Evol Biol 26(3):660–673

    Article  CAS  PubMed  Google Scholar 

  • Becerra Lopez-Lavalle LA, Orjeda G (2002) Occurrence and cytological mechanism of 2n pollen formation in a tetraploid accession of Ipomoea batatas (sweet patato). J Hered 93(3):185–192

    Article  PubMed  Google Scholar 

  • Bednara J, Gielwanowska I, Rodkiewicz B (1986) Regular arrangements of mitochondria and plastids during sporogenesis in Equisetum. Protoplasma 130:145–152

    Article  Google Scholar 

  • Bretagnolle F, Thompson JD (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of polyploid plants. New Phytol 129(1):1–22

    Article  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 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Einspahr DW (1984) Production and utilization of triploid hybrid aspen. Iowa State J Res 58(4):401–409

    Google Scholar 

  • FAO (2012) Synthesis of country progress reports. Food and Agriculture Organization of the United Nations: the 24rd session of the International Poplar Commission, Dehradun

  • Farco GE, Dematteis M (2014) Meiotic behavior and pollen fertility in triploid and tetraploid natural populations of Campuloclinium macrocephalum (Eupatorieae, Asteraceae). Plant Syst Evol 300(8):1843–1852

    Article  Google Scholar 

  • Fuzinatto VA, Pagliarini MS, Valle CB (2007) Evidence of programmed cell death during microsporogenesis in an interspecific Brachiaria (Poaceae: Panicoideae: Paniceae) hybrid. Genet Mol Res 6(2):308–315

    CAS  PubMed  Google Scholar 

  • Girke A, Schierholt A, Becker HC (2012) Extending the rapeseed gene pool with resynthesized Brassica napus II: Heterosis. Theor Appl Genet 124(6):1017–1026

    Article  PubMed Central  PubMed  Google Scholar 

  • Halket AC (1932) A note on the occurrence of abnormal flowers of Nasturtium officinale R. Br New Phytol 31(4):284–286

    Article  Google Scholar 

  • He JH, Shahid MQ, Chen ZX, Chen XA, Liu XD, Lu YG (2011) Abnormal PMC microtubule distribution pattern and chromosome behavior resulted in low pollen fertility of an intersubspecific autotetraploid rice hybrid. Plant Syst Evol 291(3–4):257–265

    Article  Google Scholar 

  • Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458

    Article  CAS  PubMed  Google Scholar 

  • Jauhar PP (2007) Meiotic restitution in wheat polyhaploids (amphihaploids): a potent evolutionary force. J Hered 98(2):188–193

    Article  CAS  PubMed  Google Scholar 

  • Kalloo G (1992) Utilization of wild species. In: Kalloo G, Chowdhury JB (eds) Distant hybridization of crop plants. Springer, Berlin Heidelberg, pp 149–167

    Chapter  Google Scholar 

  • Kamstra SA, Ramanna MS, de Jeu MJ, Kuipers AG, Jacobsen E (1999) Homoeologous chromosome pairing in the distant hybrid Alstroemeria aurea × A. inodora and the genome composition of its backcross derivatives determined by fluorescence in situ hybridization with species-specific probes. Heredity 82:69–78

    Article  PubMed  Google Scholar 

  • Kang XY (1996) Secondary chromosomal synapsis and evolution of Populus. J Gansu Agric Univ 31(4):323–326

    Google Scholar 

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

    Google Scholar 

  • Kang XY, Zhu ZT, Zhang ZY (2000) Meiosis and its stages of pollen mother cells in Chinese white poplar. J Beijing For Univ 22(6):5–7

    Google Scholar 

  • Khan MMR, Hasnunnahar M, Isshiki S (2013) Production of amphidiploids of the hybrids between Solanum macrocarpon and eggplant. HortSci 48(4):422–424

    Google Scholar 

  • Kumar S, Imtiaz M, Gupta S, Pratap A (2011) Distant hybridization and alien gene introgression. In: Pratap A, Kumar J (eds) Biology and breeding of food legumes. CABI, Oxfordshire, pp 81–110

    Google Scholar 

  • Liberloo M, Calfapietra C, Lukac M, Godbold D, Luo ZB, Polle A, Hoosbeek MR, Kull O, Marek M, Raines C, Rubino M, Taylor G, Scarascia-Mugnozza G, Ceulemans R (2006) Woody biomass production during the second rotation of a bio-energy Populus plantation increases in a future high CO2 world. Glob Chang Biol 12:1094–1106

    Article  Google Scholar 

  • Liu D, Zhang H, Zhang L, Yuan Z, Hao M, Zheng Y (2014) Distant hybridization: a tool for interspecific manipulation of chromosomes. In: Pratap A, Kumar J (eds) Alien gene transfer in crop plants, vol 1, Innovations, methods and risk assessment. Springer, New York, pp 25–42

    Chapter  Google Scholar 

  • Mashkina OS, Burdaeva LM, Belozerova MM, Vyunova LN (1989) Method of obtaining diploid pollen of woody species. Lesovedenie 1:19–25

    Google Scholar 

  • Moreno PE, Caetano CM, Olaya CA, Agrono TC, Torres EA (2014) Chromosome elimination in intergeneric hybrid of Oryza sativa × Luziola peruviana. Agric Sci 5(13):1344–1350

    Google Scholar 

  • Naghiloo S, Dadpour MR, Gohari G, Endress PK (2013) Comparative study of inflorescence development in Oleaceae. Am J Bot 100(4):647–663

    Article  PubMed  Google Scholar 

  • Ortiz AM, Seijo JG, Fernández A, Lavia GI (2011) Meiotic behavior and pollen viability of tetraploid Arachis glabrata and A. nitida species (Section Rhizomatosae, Leguminosae): implications concerning their polyploid nature and seed set production. Plant Syst Evol 292(1–2):73–83

    Article  Google Scholar 

  • Rae AM, Street NR, Rodríguez-Acosta M (2007) Populus trees. In: Kole C (ed) Genome mapping and molecular breeding in plants, vol 7, Forest trees. Springer, Berlin Heidelberg, pp 1–28

    Google Scholar 

  • Risso-Pascotto C, Pagliarini MS, do Valle CB, Jank L (2004) Asynchronous meiotic rhythm as the cause of selective chromosome elimination in an interspecific Brachiaria hybrid. Plant Cell Rep 22(12):945–950

    Article  CAS  PubMed  Google Scholar 

  • Risso-Pascotto C, Pagliarini MS, do Valle CB (2005) Meiotic behavior in interspecific hybrids between Brachiaria ruziziensis and Brachiaria brizantha (Poaceae). Euphytica 145(1–2):155–159

    Article  Google Scholar 

  • Sannigrahi P, Ragauskas AJ, Tuskan GA (2010) Poplar as a feedstock for biofuels: a review of compositional characteristics. Biofuels Bioprod Bioref 4(2):209–226

    Article  CAS  Google Scholar 

  • Seitz FW (1954) The occurrence of triploids after self-pollination of anomalous androgynous flowers of a grey poplar. Z Forstgenet 3(1):1–6

    Google Scholar 

  • Shamina NV, Gordeeva EI, Kovaleva NM, Seriukova EG, Dorogova NV (2007) Formation and function of phragmoplast during successive cytokinesis stages in higher plant meiosis. Cell Biol Int 31:1–10

    Article  Google Scholar 

  • Silkova OG, Shchapova AI, Shumny VK (2011a) Meiotic restitution in amphihaploids in the tribe Triticeae. Russ J Genet 47(4):383–393

    Article  CAS  Google Scholar 

  • Silkova OG, Shchapova AI, Shumny VK (2011b) Patterns of meiosis in ABDR amphihaploids depend on the specific type of univalent chromosome division. Euphytica 178(3):415–426

    Article  Google Scholar 

  • Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588

    Article  CAS  PubMed  Google Scholar 

  • Sosnowska K, Cegielska-Taras T (2014) Application of in vitro pollination of opened ovaries to obtain Brassica oleracea L. × B. rapa L. hybrids. In Vitro Cell Dev Biol Plant 50(2):257–262

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sterck L, Rombauts S, Jansson S, Sterky F, Rouzé P, Van de Peer Y (2005) EST data suggest that poplar is an ancient polyploid. New Phytol 167(1):165–170

    Article  PubMed  Google Scholar 

  • Tang QY (2010) Studies on hybridization of Tacamahaca and Populus euphratica and their chromosome doubling technique. Dissertation, Beijing Forestry University

  • Tel-Zur N, Abbo S, Mizrahi Y (2005) Cytogenetics of semi-fertile triploid and aneuploid intergeneric vine cacti hybrids. J Hered 96(2):124–131

    Article  CAS  PubMed  Google Scholar 

  • Trojak-Goluch A, Berbeć A (2003) Cytological investigations of the interspecific hybrids of Nicotiana tabacum L. × N. glauca Grah. J Appl Genet 44(1):45–54

    PubMed  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Kang X (2009) Distribution of microtubular cytoskeletons and organelle nucleoids during microsporogenesis in a 2n pollen producer of hybrid Populus. Silvae Genet 58(5/6):220–226

    Google Scholar 

  • Wang J, Kang X, Zhu Q (2010) Variation in pollen formation and its cytological mechanism in an allotriploid white poplar. Tree Genet Genomics 6(2):281–290

    Article  Google Scholar 

  • Wang J, Wu Y, Ren G, Guo Q, Liu J, Lascoux M (2011) Genetic differentiation and delimitation between ecologically diverged Populus euphratica and P. pruinosa. PLoS One 6(10), e26530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ward JR, Cowart ML, Clifford J, Camp M, Cruzan MB (2014) Variation in sex allocation and floral morphology in an expanding distylous plant hybrid complex. Int J Plant Sci 175(5):518–525

    Article  Google Scholar 

  • Xu WY (1988) Poplar. Heilongjiang People’s Publishing House, Harbin

    Google Scholar 

  • Zhang Z, Kang X, Zhang P, Li Y, Wang J (2007) Incidence and molecular markers of 2n pollen in Populus tomentosa Carr. Euphytica 154:145–152

    Article  CAS  Google Scholar 

  • Zhang LQ, Liu DC, Zheng YL, Yan ZH, Dai SF, Li YF, Jiang Q, Ye YQ, Yen Y (2010) Frequent occurrence of unreduced gametes in Triticum turgidum–Aegilops tauschii hybrids. Euphytica 172(2):285–294

    Article  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Beijing Higher Education Young Elite Teacher Project (Grant No. YETP0758), the Program for New Century Excellent Talents in University (Grant No. NCET-13-0672), the Program for Changjiang Scholars and Innovative Research Team in University (Grant No. IRT13047), the Beijing Nova program (Grant No. Z141105001814007), and the Students’ Innovation and Entrepreneurship Training Program of BJFU (Grant No. X201410022032).

Data archiving statement

We have submitted no data to public databases.

Author information

Authors and Affiliations

  1. National Engineering Laboratory in Tree Breeding, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Jun Wang & Hanli You

  2. Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, MOE, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Jun Wang & Hanli You

  3. College of Biological Sciences and Technology, Beijing Forestry University, P.O. Box 118, Beijing, 100083, People’s Republic of China

    Jun Wang

  4. The Academy of Forestry of the Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Ju Tian

  5. Forestry Research Institute of Tongliao City, Tongliao, Inner Mongolia, 028000, People’s Republic of China

    Yongfu Wang

  6. Experimental Center of Desert Forestry, Chinese Academy of Forestry, Dengkou County, Inner Mongolia, 015200, People’s Republic of China

    Minghu Liu & Wula Duan

Authors
  1. Jun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hanli You
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ju Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yongfu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Minghu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wula Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jun Wang.

Additional information

Communicated by A. Brunner

The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, please see:

http://www.textcheck.com/certificate/o1yJHH

This article is part of the Topical Collection on Hybridization

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., You, H., Tian, J. et al. Abnormal meiotic chromosome behavior and gametic variation induced by intersectional hybridization in Populus L.. Tree Genetics & Genomes 11, 61 (2015). https://doi.org/10.1007/s11295-015-0880-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-015-0880-z

Keywords

Search

Navigation