Skip to main content
Log in

Morphological and physiological differences between dehiscent and indehiscent anthers of Chrysanthemum morifolium

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

An Erratum to this article was published on 02 September 2016

Abstract

Spray cut chrysanthemums ornamental value and vase life are rapidly reduced with an increase in the pollen dispersal of the middle tubular bisexual flowers, and excessive pollen grains floating in the air are usually harmful to people. Thus, two cultivars were selected: the dehiscent ‘Qx-097’ and the indehiscent ‘Qx-007’, to investigate the morphological, structural and physiological differences in anthers. (1) Prior to the opening of the tubular flower, the anther was completely dehisced, and the pollen grains of ‘Qx-097’ were then released. ‘Qx-007’ inflorescences showed no pollen dispersal, and this cultivar was therefore not contaminated by its own pollen grains during flowering. (2) The anther cell structure of ‘Qx-007’ was abnormal, such that the entire anther wall exhibited hypertrophy due to the non-selective thickening of the endothecium cell size in different areas. Moreover, cracks did not form in the ‘Qx-007’ anther due to failure of septum degradation and stomium breakage, which resulted in the anther locules being inwardly crushed. Besides, the indehiscent anther accompanies partial pollen abortion due to the impairment of tapetum development, this is not conducive to pollen dispersal. (3) The ‘Qx-007’ anther contained higher water levels compared with ‘Qx-097’, and the dehydration of the ‘Qx-007’ anther was relatively moderate. Furthermore, the ‘Qx-007’ anther exhibited higher Ca2+ and Mg2+ levels compared with ‘Qx-097’ during dehiscing periods. (4) The ‘Qx-007’ anther showed significantly lower jasmonic acid levels and higher indole-3-acetic acid levels compare with the ‘Qx-097’ anther. These results suggest that the endothecium, septum and stomium constituent of the anther structure exhibit developmental abnormalities, which likely serve as the cellular basis of anther indehiscence. In addition, anther dehydration, the enhancement of anther cell toughness due to a high level of ions, and JA (IAA) dysregulation may be the determining physiological factors of anther indehiscence.

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

Similar content being viewed by others

References

  • Anderson NO (2006) Chrysanthemum. Flower breeding and genetics: issues, challenges and opportunities for the 21st century 389–437

  • Beals TP, Goldberg RB (1997) A novel cell ablation strategy blocks tobacco anther dehiscence. Plant Cell 9:1527–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonner LJ, Dickinson H (1989) Anther dehiscence in Lycopersicon esculentum Mill. I. Structural aspects. New Phytol 113(1):97–115

  • Bonner LJ, Dickinson H (1990) Anther dehiscence in Lycopersicon esculentum. New Phytol 115:367–375

    Article  Google Scholar 

  • Bots M, Vergeldt F, Wolters-Arts M, Weterings K, van As H, Mariani C (2005) Aquaporins of the PIP2 class are required for efficient anther dehiscence in tobacco. Plant Physiol 137:1049–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyer JS (2009) Evans review: cell wall biosynthesis and the molecular mechanism of plant enlargement. Funct Plant Biol 36:383–394

    Article  CAS  Google Scholar 

  • Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900

    Article  CAS  PubMed  Google Scholar 

  • Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20:1760–1774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cecchetti V, Altamura MM, Brunetti P, Petrocelli V, Falasca G, Ljung K, Costantino P, Cardarelli M (2013) Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. Plant J 74:411–422

    Article  CAS  PubMed  Google Scholar 

  • Chen L (2005) Research and analysis of the international market of chrysanthemum. Greenhouse Hortic 8:20–22

    Google Scholar 

  • Dai SL (2012) The fascinations of Chinese Chrysanthemum. Chin Landsc Archit 8:026

    Google Scholar 

  • Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46:268–278

    Article  CAS  PubMed  Google Scholar 

  • Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R, Patrick E, Davis J, Sherratt L, Coleman M, Turner JG (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin–ligase complex in Arabidopsis. Plant J 32:457–466

    Article  CAS  PubMed  Google Scholar 

  • Ge YX, Angenent GC, Wittich PE, Peters J, Franken J, Busscher M, Zhang LM, Dahlhaus E, Kater MM, Wullems GJ (2000) NEC1, a novel gene, highly expressed in nectary tissue of Petunia hybrida. Plant J 24:725–734

    Article  CAS  PubMed  Google Scholar 

  • Ge Y, Angenent G, Dahlhaus E, Franken J, Peters J, Wullems G, Creemers-Molenaar J (2001) Partial silencing of the NEC1 gene results in early opening of anthers in Petunia hybrida. Mol Genet Genom 265:414–423

    Article  CAS  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groenewoud G, De Jong N, Burdorf A, De Groot H, Van Wÿk RG (2002) Prevalence of occupational allergy to Chrysanthemum pollen in greenhouses in The Netherlands. Allergy 57:835–840

    Article  CAS  PubMed  Google Scholar 

  • Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin B, Wang L, Wang J, Jiang K-Z, Wang Y, Jiang X-X, Ni C-Y, Wang Y-L, Teng N-J (2011) The effect of experimental warming on leaf functional traits, leaf structure and leaf biochemistry in Arabidopsis thaliana. BMC Plant Biol 11:35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keijzer C (1987) The processes of anther dehiscence and pollen dispersal. New Phytol 105:487–498

    Article  Google Scholar 

  • Lee YW, Choi SY, Lee EK, Sohn JH, Park J-W, Hong C-S (2007) Cross-allergenicity of pollens from the Compositae family: Artemisia vulgaris, Dendranthema grandiflorum, and Taraxacum officinale. Ann Allergy Asthma Immunol 99:526–533

    Article  CAS  PubMed  Google Scholar 

  • Lemaire F, Sintes G, Morel P (1994) Mineral needs of Begonia x elatior during the growing period and the flowering time. Hydroponics Transpl Prod 396:219–226

    Google Scholar 

  • Li H (1993) Chrysanthemums in China. Jiangsu Scientific and Technical Press, Nanjing, pp 5–11

  • Li YF, Fang WM, Chen FD, Chen SM, Shi CL (2009) Effect of different planting date on phenophase and quality of spray cut chrysanthemum produced in summer. J Yangzhou Univ Agric Life Sci Ed 30:80–83

    Google Scholar 

  • Li FT, Chen SM, Chen FD, Teng NJ, Fang WM, Zhang F, Deng YM (2010) Anther wall development, microsporogenesis and microgametogenesis in male fertile and sterile chrysanthemum (Chrysanthemum morifolium Ramat., Asteraceae). Sci Hortic 126:261–267

    Article  CAS  Google Scholar 

  • Liu HB, Li XH, Xiao JH, Wang SP (2012) A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant methods 8:1–12

    Article  CAS  Google Scholar 

  • Luo C, Peng SA, Ma XT (1999) Studies on changes of calcium, calmodulin and the floral substance content during flower bud differentiation in strawberry (Fragaria ananassa Buch.). J Mt Agric Biol 19:266–271

    Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J 50:751–766

    Article  CAS  PubMed  Google Scholar 

  • Rehman S, Yun S (2006) Developmental regulation of K accumulation in pollen, anthers, and papillae: are anther dehiscence, papillae hydration, and pollen swelling leading to pollination and fertilization in barley (Hordeum vulgare L.) regulated by changes in K concentration? J Exp Bot 57:1315–1321

    Article  CAS  PubMed  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire K, Hsu Y-C, Lee PY, Truong MT, Beals T, Goldberg R (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12:1041–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanders PM, Bui AQ, Le BH, Goldberg RB (2005) Differentiation and degeneration of cells that play a major role in tobacco anther dehiscence. Sex Plant Reprod 17:219–241

    Article  Google Scholar 

  • Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16(suppl 1):S46–S60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senatore A, Trobacher CP, Greenwood JS (2009) Ricinosomes predict programmed cell death leading to anther dehiscence in tomato. Plant Physiol 149:775–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun CQ, Huang ZZ, Wang YL, Chen FD, Teng NJ, Fang WM, Liu ZL (2011) Overcoming pre-fertilization barriers in the wide cross between Chrysanthemum grandiflorum (Ramat.) Kitamura and C. nankingense (Nakai) Tzvel. by using special pollination techniques. Euphytica 178:195–202

    Article  Google Scholar 

  • Teng NJ, Wang J, Chen T, Wu XQ, Wang YH, Lin JX (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172:92–103

    Article  CAS  PubMed  Google Scholar 

  • Teng NJ, Wang YL, Sun CQ, Fang WM, Chen FD (2012) Factors influencing fecundity in experimental crosses of water lotus (Nelumbo nucifera Gaertn.) cultivars. BMC Plant Biol 12:82

    Article  PubMed  PubMed Central  Google Scholar 

  • Thévenin J, Pollet B, Letarnec B, Saulnier L, Gissot L, Maia-Grondard A, Lapierre C, Jouanin L (2011) The simultaneous repression of CCR and CAD, two enzymes of the lignin biosynthetic pathway, results in sterility and dwarfism in Arabidopsis thaliana. Mol Plant 4:70–82

    Article  PubMed  Google Scholar 

  • Wang BS, Zhao KF (1995) Comparison of extractive methods of Na and K in wheat leaves. Plant Physiol Comm 31:50–51

  • Wang XG, Fang WM, Chen FD, Teng NJ (2013) Determination of pollen quantity and features of pollen dispersal for 41 spray cut chrysanthemum cultivars. Acta Hortic Sin 40:703–712

    Google Scholar 

  • Wang XG, Wang HB, Chen FD, Jiang JF, Fang WM, Liao Y, Teng NJ (2014) Factors affecting quantity of pollen dispersal of spray cut chrysanthemum (Chrysanthemum morifolium). BMC Plant Biol 14:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson ZA, Song J, Taylor B, Yang C (2011) The final split: the regulation of anther dehiscence. J Exp Bot 62:1633–1649

    Article  CAS  PubMed  Google Scholar 

  • Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Xu Z, Song J, Conner K, Barrena GV, Wilson ZA (2007) Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. Plant Cell 19:534–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuor H, Abu-Abied M, Belausov E, Madmony A, Sadot E, Riov J, Rubin B (2006) Glyphosate-induced anther indehiscence in cotton is partially temperature dependent and involves cytoskeleton and secondary wall modifications and auxin accumulation. Plant Physiol 141:1306–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Z, Zhang Y, Liu X, Zhang X, Liu S, Yu X, Ren Y, Zheng X, Zhou K, Jiang L, Guo X, Gai Y, Wu C, Zhai H, Wang H, Wan J (2013) A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev Cell 27:113–122

    Article  CAS  PubMed  Google Scholar 

  • Zhu QH, Ramm K, Shivakkumar R, Dennis ES, Upadhyaya NM (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiol 135:1514–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China (31471901), the Fundamental Research Funds for the Central Universities (KYZ201308, KYTZ201602), the Natural Science Fund of Jiangsu Province (BK2016449), and the fourth phase of Jiangsu “333” project to Dr. Nianjun Teng.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nianjun Teng.

Ethics declarations

Conflict of interest

All authors declare no competing interests.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s10265-016-0861-9.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fei, J., Tan, S., Zhang, F. et al. Morphological and physiological differences between dehiscent and indehiscent anthers of Chrysanthemum morifolium . J Plant Res 129, 1069–1082 (2016). https://doi.org/10.1007/s10265-016-0854-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-016-0854-8

Keywords

Navigation