Skip to main content
Log in

Meiotic chromosome behavior of the male-fertile allotriploid lily cultivar ‘Cocossa’

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

Abstract

Key message

Cytological observations of microsporogenesis in the allotriploid lily cultivar ‘Cocossa’ showed that viable pollen production could be attributed mainly to disoriented spindles, abnormal cytokinesis, and cytomixis during male meiosis.

Abstract

To identify the reasons why the allotriploid lily cultivar ‘Cocossa’ can produce aneuploid and euploid functional male gametes and can be used as the paternal parent in lily introgression breeding, we performed a detailed investigation of microsporogenesis using the conventional cytological methods. The allotriploid not only produced single pollen grains with variable sizes but also produced adherent pollen grains. Pollen viability was estimated at 50.1% based on staining and 30.8% based on germination. Based on the chromosomal analysis of BC2 plants derived from Oriental cultivars (♀) crossed with the OOT cultivar ‘Cocossa’ (♂), it was concluded that the objective allotriploid contributed haploid (x), diploid (2x), and aneuploid chromosome complements. Common meiotic abnormalities were observed, indicating the high genetic imbalance of this allotriploid. In addition to normally oriented metaphase II spindles (linear and perpendicular), abnormal spindles, such as parallel, tripolar, fused, and multiple spindles, accounted for 6.21, 6.41, 14.27, and 1.17%, respectively. Tripolar and fused spindles resulted in the production of triads and dyads, which contributed to unreduced pollen production. Some microsporocytes exhibited complete or partial absence of cytokinesis, which led to relatively high frequencies of monads, dyads, and triads. Furthermore, the phenomenon of cytomixis during microsporogenesis occurred mainly in the first meiotic prophase and early development of pollen grains, which we assume is a possible cause of unreduced gamete generation. Our study offers a new resource for lily introgression 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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Barba-Gonzalez R, Van Silfhout AA, Visser RGF, Ramanna MS, Van Tuyl JM (2006) Progenies of allotriploids of Oriental × Asiatic lilies (Lilium) examined by GISH analysis. Euphytica 151:243–250

    Article  Google Scholar 

  • Bosco SFD, Tusa N, Conicella C (1999) Microsporogenesis in a Citrus interspecific tetraploid somatic hybrid and its fusion parents. Heredity 83:373–377

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Brown RC, Lemmon BE (1991) Pollen development in orchids 1. Cytoskeleton and the control of division plane in irregular patterns of cytokinesis. Protoplasma 163:9–18

    Article  Google Scholar 

  • Brownfield L, Yi J, Jiang H, Minina EA, Twell D, Köhler C (2015) Organelles maintain spindle position in plant meiosis. Nat Commun 6:6492

    Article  CAS  PubMed  Google Scholar 

  • Chung MY, Chung JD, Ramanna M, Van Tuyl JM, Lim KB (2013) Production of polyploids and unreduced gametes in Lilium auratum × L. henryi hybrid. Int J Biol Sci 9:693–701

    Article  PubMed  PubMed Central  Google Scholar 

  • Dewitte A, Van Laere K, Van Huylenbroeck J (2012) Use of 2n-gametes in plant breeding. In: Abdurakhmonov IY (ed) Plant breeding, InTech Open Access Publisher, Croatia, pp 59–86. doi:10.5772/29827

  • Du YP, Wei C, Wang ZX, Li S, He HB, Jia GX (2014) Lilium spp. pollen in China (Liliaceae): taxonomic and phylogenetic implications and pollen evolution related to environmental conditions. PLoS One 9:1–19

    CAS  Google Scholar 

  • Falistocco E, Tosti N, Falcinelli M (1995) Cytomixis in pollen mother cells of diploid Dactylis, one of the origins of 2n gametes. J Hered 86:448–453

    Article  Google Scholar 

  • Fang L, Yang B, Zhang WN, Xin HY, Gao TT, Shi JS, Guo J, Xi ML (2014) The ploidy level investigation and FISH analysis of the progenies from allotriploid Lilium as male. Mol Plant Breed 12:138–143

    CAS  Google Scholar 

  • Ghaffari SM (2006) Occurrence of diploid and polyploid microspores in Sorghum bicolor (Poaceae) is the result of cytomixis. Afr J Biotechnol 5:1450–1453

    Google Scholar 

  • Hulskamp M, Parekh NS, Grini P, Schneitz K, Zimmermann I, Lolle SJ, Pruitt RE (1997) The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Dev Biol 187:114–124

    Article  CAS  PubMed  Google Scholar 

  • Khan N, Zhou SJ, Ramanna MS, Aren P, Herrera J, Visser RGF, Van Tuyl JM (2009) Potential for analytic breeding in allopolyploids: an illustration from Longiflorum × Asiatic hybrid lilies (Lilium). Euphytica 166:399–409

    Article  Google Scholar 

  • Lim KB, Ramanna MS, Jacobsen E, Van Tuyl JM (2003) Evaluation of BC2 progenies derived from 3x–2x and 3x–4x crosses of Lilium hybrids: a GISH analysis. Theor Appl Genet 106:568–574

    Article  PubMed  Google Scholar 

  • Lora J, Testillano PS, Risueño MC, Hormaza JI, Herrero M (2009) Pollen development in Annona cherimola Mill. (Annonaceae). Implications for the evolution of aggregated pollen. BMC Plant Biol 9:129

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo JR, Ramanna MS, Arens P, Niu LX, Van Tuyl JM (2012) GISH analyses of backcross progenies of two Lilium species hybrids and their relevance to breeding. J Hortic Sci Biotechnol 87:654–660

    Article  Google Scholar 

  • Luo JR, Van Tuyl JM, Arens P, Niu LX (2013) Cytogenetic studies on meiotic chromosome behaviors in sterile Oriental × Trumpet lily. Genet Mol Res 12:6673–6684

    Article  CAS  PubMed  Google Scholar 

  • Mursalimov SR, Deineko EV (2015) How cytomixis can form unreduced gametes in tobacco. Plant Syst Evol 301:1293–1297

    Article  CAS  Google Scholar 

  • Mursalimov SR, Sidorchuk YV, Deineko EV (2013) New insights into cytomixis: specific cellular features and prevalence in higher plants. Planta 238:415–423

    Article  CAS  PubMed  Google Scholar 

  • Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264:1458–1460

    Article  CAS  PubMed  Google Scholar 

  • Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement—a review. Euphytica 133:3–18

    Article  Google Scholar 

  • Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639

    Article  Google Scholar 

  • Rani S, Chahota RK, Sharma TR (2016) Cytomixis and Associated Meiotic Abnormalities during Male Meiosis in Angelica glauca Edgew. (Apiaceae) from North-Western Himalayas. Cytologia 81:161–168

    Article  Google Scholar 

  • Rhee SY, Osborne E, Poindexter PD, Somerville CR (2003) Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol 133:1170–1180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Risso-Pascotto C, Pagliarini MS, Valle CBD (2005) Multiple spindles and cellularization during microsporogenesis in an artificially induced tetraploid accession of Brachiaria ruziziensis (Gramineae). Plant Cell Rep 23:522–527

    Article  CAS  PubMed  Google Scholar 

  • Sidorchuk YV, Novikovskaya AA, Deineko EV (2016) Cytomixis in the cereal (Gramineae) microsporogenesis. Protoplasma 253:291–298

    Article  CAS  PubMed  Google Scholar 

  • Singhal VK, Kumar P (2008) Impact of cytomixis on meiosis, pollen viability and pollen size in wild populations of Himalayan poppy (Meconopsis aculeata Royle). J Biosci 33:371–380

    Article  CAS  PubMed  Google Scholar 

  • Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG (1997) TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124:2645–2657

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tilquin JP, De Brouwer K, Horvat F (1984) Unusual cytological patterns in microsporogenesis in a cultivar of Fuchsia: 1. Multiple spindle. Theor Appl Genet 67:413–417

    Article  CAS  PubMed  Google Scholar 

  • Tondini F, Tavoletti S, Mariani A, Veronesi F (1993) A statistical approach to estimate the frequency of n, 2n and 4n pollen grains in diploid alfalfa. Euphytica 69:109–114

    Article  Google Scholar 

  • Van Tuyl JM, Van Dijken A, Chi HS, Lim KB, Villemoes S, Van Kronenburg BCE (2000) Breakthroughs in interspecific hybridization of lily. Acta Hortic 508:83–90

    Article  Google Scholar 

  • Volkova OA, Remizowa MV, Sokoloff DD, Severova EE (2016) A developmental study of pollen dyads and notes on floral development in Scheuchzeria (Alismatales: Scheuchzeriaceae). Bot J Linn Soc 182:791–810

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wang J, You HL, Tian J, Wang YF, Liu MH, Duan WL (2015) Abnormal meiotic chromosome behavior and gametic variation induced by intersectional hybridization in Populus L. Tree Genet Genomes 11:61

    Article  Google Scholar 

  • Xi ML, Van Tuyl JM, Arens P (2015) GISH analyzed progenies generated from allotriploid lilies as female parent. Sci Hortic 183:130–135

    Article  CAS  Google Scholar 

  • Younis A, Hwang YJ, Lim KB (2014) Classical vs. modern genetic and breeding approaches for lily (Lilium) crop improvement: a review. Flower Res J 22:39–47

    Article  Google Scholar 

  • Zhang ZH, Kang XY (2010) Cytological characteristics of numerically unreduced pollen production in Populus tomentosa Carr. Euphytica 173:151–159

    Article  Google Scholar 

  • Zhang XX, Ren G, Li K, Zhou GX, Zhou SJ (2012) Genomic variation of new cultivars selected from distant hybridization in Lilium. Plant Breed 131:227–230

    Article  CAS  Google Scholar 

  • Zheng GC, Yang QL, Zheng YR (1987) The Relationship between cytomixis, chromosome mutation and karyotype evolution in lily. Caryologia 40:243–259

    Article  Google Scholar 

  • Zhou SJ, Yuan GL, Xu P, Gong HX (2014) Study on lily introgression breeding using allotriploids as maternal parents in interploid hybridizations. Breed Sci 64:97–102

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants from the National Forestry Public Welfare Industry Research Project (201204609) and the National Natural Science Foundation of China (31470106).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guixia Jia.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by Xian Sheng Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, X., Cao, Q., Zhou, P. et al. Meiotic chromosome behavior of the male-fertile allotriploid lily cultivar ‘Cocossa’. Plant Cell Rep 36, 1641–1653 (2017). https://doi.org/10.1007/s00299-017-2180-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-017-2180-6

Keywords

Navigation