Skip to main content
Log in

Behavior of filamentous temperature-sensitive Z2 (FtsZ2) in the male gametophyte during sexual reproduction processes of flowering plants

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Filamentous temperature-sensitive Z (FtsZ) is a critical division protein in bacteria that functions in forming a Z-ring structure to constrict the cell. Since the establishment of the plastid by endosymbiosis of a cyanobacterium into a eukaryotic cell, division via Z-ring formation has been conserved in the plastids of flowering plants. The FtsZ gene was transferred from the cyanobacterial ancestor of plastids to the eukaryotic nuclear genome during evolution, and flowering plants evolved two FtsZ homologs, FtsZ1 and FtsZ2, which are involved in chloroplast division through distinct molecular functions. Regarding the behaviors of FtsZ in nonphotosynthetic cells, the plastid localization of FtsZ1 proteins in the cytoplasm of microspores and pollen vegetative cells but not in generative cells or sperm cells has been reported. On the other hand, the significant accumulation of FtsZ2 transcripts in generative cells has been reported. However, the synthesis of FtsZ2 in the male gamete has not been investigated. Additionally, FtsZ2 behavior has not been analyzed in pollen, a nonphotosynthetic male tissue. Here, we report FtsZ2 protein behaviors in the male gamete by analyzing the localization patterns of GFP-fused protein at various pollen developmental stages and in gametes during the fertilization process. Our results showed that FtsZ2 localization coincided with that of plastids. FtsZ2 protein in male gametes was almost absent, despite the presence of the transcripts. Moreover, transmission of paternal FtsZ2 transcripts to the zygote and endosperm was not observed.

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

  • Bird J, Porter EK, Dickinson HG (1983) Events in the cytoplasm during male meiosis in Lilium. J Cell Sci 59:27–42

    CAS  PubMed  Google Scholar 

  • Borges F, Gomes G, Gardner R, Merono N, McCormick S, Feijó JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 138:2124–2133

    Google Scholar 

  • Borges F, Gardner R, Lopes T, Calarco JP, Boavida LC, Slotkin RK, Martienssen RA, Becker JD (2012) FACS-based purification of Arabidopsis microspores, sperm cells and vegetative nuclei. Plant Methods 8:44

    Article  CAS  Google Scholar 

  • Fujiwara MT, Hashimoto H, Kazama Y, Hirano T, Yoshioka Y, Aoki S, Sato N, Itoh RD, Abe T (2010) Dynamic morphologies of pollen plastids visualised by vegetative-specific FtsZ1-GFP in Arabidopsis thaliana. Protoplasma 242:19–33

    Article  Google Scholar 

  • Fujiwara MT, Yoshioka Y, Hirano T, Kazama Y, Abe T, Hayashi K, Itoh RD (2012) Visualization of plastid movement in the pollen tube of Arabidopsis thaliana. Plant Signal Behav 7:34–37

    Article  CAS  Google Scholar 

  • Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17:1032–1037

    Article  CAS  Google Scholar 

  • Kuang A, Musgrave ME (1996) Dynamics of vegetative cytoplasm during generative cell formation and pollen maturation in Arabidopsis thaliana. Protoplasma 194:81–90

    Article  CAS  Google Scholar 

  • McAndrew RS, Froehlich JE, Vitha S, Stokes KD, Osteryoung KW (2001) Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol 127:1656–1666

    Article  CAS  Google Scholar 

  • Mita T, Kanbe T, Tanaka K, T K (1986) A ring structure around the dividing plane of the Cyanidium caladarium choloroplast. Protoplasma 130:211–213

  • Miyagishima SY (2011) Mechanism of plastid division: from a bacterium to an organelle. Plant Physiol 155:1533–1544

    Article  CAS  Google Scholar 

  • Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15:655–665

    Article  CAS  Google Scholar 

  • Miyagishima SY, Nozaki H, Nishida K, Nishida K, Matsuzaki M, Kuroiwa T (2004) Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 25:291–303

    Article  Google Scholar 

  • Miyamura S, Kuroiwa T, Nagata T (1987) Disappearance of plastid and mitochondrial nucleoids during the formation of generative cells of higher plants revealed by fluorescence microscopy. Protoplasma 141:149–159

    Article  Google Scholar 

  • Mori T, Tanaka I (2000) Isolation of the ftsZ gene from plastid-deficient generative cells of Lilium longiflorum. Protoplasma 214:57–64

    Article  CAS  Google Scholar 

  • Mori T, Takahara S, Kuroiwa H, Kuroiwa T (2001) Visualization of FtsZ rings in plastids of the microspore in Lilium Longiflorum. Cytologia 66:113–115

    Article  Google Scholar 

  • Moriyama T, Toyoshima M, Saito M, Wada H, Sato N (2018) Revisiting the algal “chloroplast lipid droplet”: the absence of an entity that is unlikely to exist. Plant Physiol 176:1519–1530

    Article  CAS  Google Scholar 

  • Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209:53–65

    Article  CAS  Google Scholar 

  • Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kumura T (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104:34–41

    Article  CAS  Google Scholar 

  • Nakamura S, Miki-Hiroshige H (1985) Fine-structural study on the formation of the generative cell wall and intine-3 layer in a growing pollen grain of Lilium longiflorum. Am J Bot 72:365–375

    Article  Google Scholar 

  • Nakanishi H, Suzuki K, Kabeya Y, Miyagishima SY (2009) Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol 19:151–156

    Article  CAS  Google Scholar 

  • Narusaka M, Shiraishi T, Iwabuchi M, Narusaka Y (2010) The floral inoculating protocol: a simplified Arabidopsis thaliana transformation method modified from floral dipping. Plant Biotech 27:349–351

    Article  Google Scholar 

  • Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10:1991–2004

    Article  CAS  Google Scholar 

  • Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185:7–21

    Article  Google Scholar 

  • Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799

    CAS  PubMed  Google Scholar 

  • Sakamoto W, Miyagishima SY, Jarvis P (2008) Chloroplast biogenesis: control of plastid development, protein import, division and inheritance. Arabidopsis Book 6:e0110

    Article  Google Scholar 

  • Schmitz AJ, Glynn JM, Olson BJ, Stokes KD, Osteryoung KW (2009) Arabidopsis FtsZ2-1 and FtsZ2-2 are functionally redundant, but FtsZ-based plastid division is not essential for chloroplast partitioning or plant growth and development. Mol Plant 2:1211–1222

    Article  CAS  Google Scholar 

  • Sodmergen ST, Kawano S, Nakamura S, Tano S, Kuroiwa T (1992) Behavior of organelle nuclei (nucleoids) in generative and vegetative cells during maturation of pollen in Lilium longiflorum and Pelargonium zonale. Protoplasma 168:73–82

    Article  Google Scholar 

  • Suzuki T, Ide N, Tanaka I (1997) Immunocytochemical visualization of the centromeres during male and female meiosis in Lilium longiflorum. Chromosoma 106:435–445

    Article  CAS  Google Scholar 

  • Tanaka I, Taguch T, Ito M (1979) Studies on microspore development in Liliaceaous plants. I. The duration of the cell cycle and developmental aspects in lily microspores. Bot Mag Tokyo 92:291–298

    Article  Google Scholar 

  • Tanaka I, Kitazume C, Ito M (1987) The isolation and culture of lily pollen protoplast. Plant Sci 50:205–211

    Article  CAS  Google Scholar 

  • Tang LY, Nagata N, Matsushima R, Chen Y, Yoshioka Y, Sakamoto W (2009) Visualization of plastids in pollen grains: involvement of FtsZ1 in pollen plastid division. Plant Cell Physiol 50:904–908

    Article  CAS  Google Scholar 

  • TerBush AD, Osteryoung KW (2012) Distinct functions of chloroplast FtsZ1 and FtsZ2 in Z-ring structure and remodeling. J Cell Biol 199:623–637

    Article  CAS  Google Scholar 

  • Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933

    Article  CAS  Google Scholar 

  • Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T (2003) Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol 44:1192–1201

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Miyagishima for providing the AtFtsZ2-1_GFP vector.

Funding

This work was supported by JSPS KAKENHI (Grant Numbers JP17H05832 (to T. I.), JP19H04852 (to T. I.)) and the Strategic Priority Research Promotion Program on Phytochemical Plant Molecular Sciences, Chiba University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomoko Igawa.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Tsuneyoshi Kuroiwa

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ohashi, Y., Mori, T. & Igawa, T. Behavior of filamentous temperature-sensitive Z2 (FtsZ2) in the male gametophyte during sexual reproduction processes of flowering plants. Protoplasma 257, 1201–1210 (2020). https://doi.org/10.1007/s00709-020-01503-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-020-01503-2

Keywords

Navigation