Skip to main content
SpringerLink
Log in

Syncyte formation in the microsporangium of Chrysanthemum (Asteraceae): a pathway to infraspecific polyploidy

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Polyploidy, which is thought to have played an important role in plant evolution and speciation, is prevalent in Chrysanthemum (x = 9). In fact, polyploid series are known in C. zawadskii (2x, 4x, 6x, 8x, and 10x) and C. indicum (2x, 4x, and 6x), but the mechanism by which polyploidization occurs is unknown. Here we show that in diploid individuals of both C. zawadskii and C. indicum, the fusion between two adjacent pollen mother cells (PMCs) occurs at a frequency of 1.1–1.3% early in the first meiotic division. While possessing the chromosomes of both PMCs, the fused cell or syncyte undertakes subsequent meiotic division processes as a single large PMC, producing four 2n pollen grains that are able to germinate. Despite their low frequency, syncyte formation may have played a major role in the production of infraspecific polyploids in Chrysanthemum.

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

Similar content being viewed by others

References

  • Bahl JR, Tyagi BR (1988) Cytomixis in pollen mother cells of Papaver dubium L. Cytologia 53:771–775

    Google Scholar 

  • Bino RJ, van Tuyl JM, de Vries JN (1990) Flow cytometric determination of relative nuclear DNA contents in bicellulate and tricellulate pollen. Ann Bot 65:3–8

    CAS  Google Scholar 

  • Boldrini KR, Pagliarini MS, do Valle CB (2006) Cell fusion and cytomixis during microsporogenesis in Brachiaria humidicola (Poaceae). S Afr J Bot 72:478–481

    Article  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 

  • Brochmann C, Borgen L, Stabbetorp OE (2000) Multiple diploid hybrid speciation of the Canary island endemic Argyranthemum sundingii (Asteraceae). Pl Syst Evol 220:77–92

    Article  Google Scholar 

  • Caetano-Pereira CM, Pagliarini MS, Brasil EM (1999) Cell fusion and chromatin degeneration in an inbreed line of maize. Genet Mol Biol 22:69–72

    Article  Google Scholar 

  • Cammareri M, Errico A, Sebastiano A, Conicella C (2004) Genetic relationships among Aster species by multivariate analysis and AFLP markers. Hereditas 140:193–200

    Article  PubMed  CAS  Google Scholar 

  • Cook LM, Soltis PS, Brunsfeld SJ, Soltis DE (1998) Multiple independent formations of Tragopogon tetraploids (Asteraceae): evidence from RAPD markers. Mol Ecol 7:1293–1302

    Article  Google Scholar 

  • Denda T, Yokota M (2004) Cytogeography of Ixeris nakazonei (Asteraceae, Lactuceae) in the Ryukyu archipelago of Japan and Taiwan. J Plant Res 117:3–11

    Article  PubMed  Google Scholar 

  • DeWet JMJ (1980) Origins of polyploids. In: Lewis H (ed) Polyploidy. Plenum, New York, pp 3–15

    Google Scholar 

  • Du B, Lin Q, Zhu C, Ke S (1989) Karyotype studies of two species of Dendranthema. J Wuhan Bot Res 7:293–296

    Google Scholar 

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

    Google Scholar 

  • Galbany-Casals M, Romo AM (2008) Polyploidy and new chromosome counts in Helichrysum (Asteraceae, Gnaphalieae). Bot J Linn Soc 158:511–521

    Article  Google Scholar 

  • Gates RR (1911) Pollen formation in Oenothera gigas. Ann Bot 25:909–940

    Google Scholar 

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

    Google Scholar 

  • Grant V (1981) Plant speciation, 2nd edn. Columbia University Press, New York

    Google Scholar 

  • Harlan JR, DeWet JMJ (1975) On Ö. Winge and a prayer: the origin of polyloidy. Bot Rev 41:361–690

    Article  Google Scholar 

  • Ito M, Yahara T, King RM, Watanabe K, Oshita S, Yokoyama J, Crawford DJ (2000) Molecular phylogeny of Eupatrieae (Asteraceae) estimated from cpDNA RFLP and its implication for the polyploid origin hypothesis of the tribe. J Plant Res 113:91–96

    Article  CAS  Google Scholar 

  • Kim JS, Pak J-H, Seo B-B, Tobe H (2003) Karyotypes of metaphase chromosomes in diploid populations of Dendranthema zawadskii and related species (Asteraceae) from Korea: diversity and evolutionary implications. J Plant Res 116:47–55

    PubMed  Google Scholar 

  • Kim JS, Pak J-H, Tobe H (2004) Chromosome number of Dendranthema coreana (Asteraceae). Acta Phytotax Geobot 55:63–64

    Google Scholar 

  • Kim JS, Oginuma K, Tobe H (2008) Analysis of meiotic chromosome behaviour in diploid individuals of Chrysanthemum zawadskii and related species (Asteraceae): evidence for chromosome rearrangements. Cytologia 73:425–435

    Article  Google Scholar 

  • Kimoto Y, Tobe H (2003) Embryology of Siparunaceae (Laurales): characteristics and character evolution. J Plant Res 116:281–294

    Article  PubMed  Google Scholar 

  • Lee YN, Oh YG (1976) Taxonomical study on yellow-flowered wild Chrysanthemum in Korea. Korean J Bot 15:143–154

    Google Scholar 

  • Levan A (1941) Syncyte formation in the pollen mother cells of haploid Phleum pratense. Hereditas 27:243–253

    Article  Google Scholar 

  • Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, New York

    Google Scholar 

  • Li W-P (2005) The cytogeography of Aster ageratoides var. laticorymbus (Asteraceae), a polyploid complex endemic to China. Bot Bull Acad Sin (Taipei) 46:355–361

    Google Scholar 

  • Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–423

    Article  PubMed  CAS  Google Scholar 

  • Mavrodiev EV, Nawchoo I, Soltis PS, Soltis DE (2008) Molecular data reveal that the tetraploid Tragopogon kashmirianus (Asteraceae: Lactuceae) is distinct from the North American T. mirus. Bot J Linn Soc 158:391–398

    Article  Google Scholar 

  • Mendes-Bonato AB, Risso-Pasctto C, Pagliarini MS (2003) Normal microspore production after cell fusion in Brachiaria jubata (Gramineae). Genet Mol Biol 26:517–520

    Article  Google Scholar 

  • Nakata M, Kumagai A (1999) Octoploid cytotype of Dendranthema zawadskii (Asteraceae) found in Iwate prefecture and its implications in evolutional history. Bull Bot Gard Toyama 4:1–25

    Google Scholar 

  • Nakata M, Tanaka R, Taniguchi K, Shimotomai N (1987) Species of wild Chrysanthemum in Japan: cytological and cytogenetical views on its entity. Acta Phytotax Geobot 38:241–259

    Google Scholar 

  • Nakata M, Hong D-Y, Qiu J-Z, Uchiyama H, Tanaka R, Chen S-C (1991) Cytogenetic studies on wild Chrysanthemum sensu lato in China. I. karyotype of Dendranthema vestitum. J Jpn Bot 66:199–204

    Google Scholar 

  • Oberprieler Ch, Vogt R, Watson LE (2007) Tribe Anthemideae. In: Kadereit JW, Jeffrey C (eds) The families and genera of vascular plants. VIII. Flowering plants. Eudicots: Asterales. Springer, Berlin, pp 342–374

    Google Scholar 

  • Padmaja V (1988) Studies on manifold abnormalities at meiosis in Petunia 2n = 14. Cytologia 53:199–204

    Google Scholar 

  • Sarbhoy RK (1980) Spontaneous occurrence of cytomixis and syndiploidy in Cyamopsis tetragonoloba (L.) Taub. Cytologia 45:375–379

    Google Scholar 

  • Shivanna KR, Rangaswamy NS (1992) Pollen biology––a laboratory manual. Springer, Berlin

    Google Scholar 

  • Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E (2004) Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biol J Linn Soc 82:485–501

    Article  Google Scholar 

  • Stuessy TF, Weiss-Schneeweiss H, Keil DJ (2004) Diploid and polyploid cytotype distribution in Melampodium cinereum and M. leucanthum (Asteraceae, Heliantheae). Am J Bot 91:889–898

    Article  Google Scholar 

  • Tanaka R (1959a) On the speciation and karyotype in diploid and tetraploid species of Chrysanthemum. II. Karyotype in Chrysanthemum makinoi (2n = 18). J Sci Hiroshima Univ Ser B Div 2(9):17–30

    Google Scholar 

  • Tanaka R (1959b) On the speciation and karyotype in diploid and tetraploid species of Chrysanthemum. IV. Karyotype in Chrysanthemum wakasaense (2n = 36). J Sci Hiroshima Univ Ser B Div 2(9):41–57

    Google Scholar 

  • Taniguchi K (1987) Cytogenetical studies on the speciation of tetraploid Chrysanthemum indicum L. with special reference to C-bands. J Sci Hiroshima Univ Ser. B Div 2(21):105–157

    Google Scholar 

  • Tyagi BR (2003) Cytomixis in pollen mother cells of spearmint. Cytologia 68:67–73

    Article  Google Scholar 

  • Veilleux RE (1985) Diploid and polyploidy gametes in crop plants: mechanisms of formation and utilization in plant breeding. Plant Breed Rev 3:253–288

    Google Scholar 

  • Watanabe K (1981a) Studies on the control of diploid-like meiosis in polyploidy taxa of Chrysanthemum. I. Hexaploid Ch.japonense Nakai. Cytologia 46:459–498

    Google Scholar 

  • Watanabe K (1981b) Studies on the control of diploid-like meiosis in polyploidy taxa of Chrysanthemum. II. Octoploid Ch. ornatum Hemsley. Cytologia 46:499–513

    Google Scholar 

  • Watanabe K (1981c) Studies on the control of diploid-like meiosis in polyploidy taxa of Chrysanthemum. III. Decaploid Ch. crassum Kitamura. Cytologia 46:515–530

    Google Scholar 

  • Watanabe K (1983) Studies on the control of diploid-like meiosis in polyploid taxa of Chrysanthemum. Theor Appl Genet 66:9–14

    Article  Google Scholar 

  • Yang W, Glover BJ, Rao G-Y, Yang J (2006) Molecular evidence for multiple polyploidization and lineage recombination in the Chrysanthemum indicum polyploid complex (Asteraceae). New Phytol 171:875–886

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This study was supported in part by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (No. 18370036).

Author information

Authors and Affiliations

  1. Division of Life Science, School of Life Science and Biotechnology, Korea University, Seoul, 136-701, Korea

    Jung Sung Kim

  2. Department of Environmental Science, Faculty of Human Life and Environmental Science, Kochi Women’s University, Kochi, 780-8515, Japan

    Kazuo Oginuma

  3. Department of Botany, Graduate School of Science, Kyoto University, Kyoto, 606-8502, Japan

    Hiroshi Tobe

Authors
  1. Jung Sung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuo Oginuma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroshi Tobe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroshi Tobe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, J.S., Oginuma, K. & Tobe, H. Syncyte formation in the microsporangium of Chrysanthemum (Asteraceae): a pathway to infraspecific polyploidy. J Plant Res 122, 439–444 (2009). https://doi.org/10.1007/s10265-009-0232-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-009-0232-x

Keywords

Search

Navigation