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Journal of Plant Research

, Volume 128, Issue 3, pp 407–421 | Cite as

Phytochrome-mediated regulation of cell division and growth during regeneration and sporeling development in the liverwort Marchantia polymorpha

  • Ryuichi NishihamaEmail author
  • Kimitsune Ishizaki
  • Masashi Hosaka
  • Yoriko Matsuda
  • Akane Kubota
  • Takayuki Kohchi
JPR Symposium Reprogramming of plant cells as adaptive strategies

Abstract

Light regulates various aspects of development throughout the life cycle of sessile land plants. Photoreceptors, such as the red (R) and far-red (FR) light receptors phytochromes, play pivotal roles in modulating developmental programs. Reflecting high developmental plasticity, plants can regenerate tissues, organs, and whole bodies from varieties of cells. Among land plants, bryophytes exhibit extraordinary competency of regeneration under hormone-free conditions. As an environmental factor, light plays critical roles in regeneration of bryophytes. However, how light regulates regeneration remains unknown. Here we show that using the liverwort Marchantia polymorpha, which contains a single phytochrome gene, the phytochrome regulates re-entry into the cell cycle and cell shape in newly regenerating tissues. Our morphological and cytological observations revealed that S-phase entry of G1-arrested epidermal cells around the midrib on the ventral surface of thallus explants was greatly retarded in the dark or under phytochrome-inactive R/FR cycle irradiation conditions, where, nevertheless, small, laterally narrow regenerants were eventually formed. Thus, consistent with earlier descriptions published over a century ago, light is not essential for, but exerts profound effects on regeneration in M. polymorpha. Ventral cells in regenerants grown under R/FR cycle conditions were longer and narrower than those under R cycle. Expression of a constitutively active mutant of M. polymorpha phytochrome allowed regeneration of well grown, widely expanded thalli even in the dark when sugar was supplied, further demonstrating that the phytochrome signal promotes cell proliferation, which is rate-limited by sucrose availability. Similar effects of R and FR irradiation on cell division and elongation were observed in sporelings as well. Thus, besides activation of photosynthesis, major roles of R in regeneration of M. polymorpha are to facilitate proliferation of rounder cells through the phytochrome by mechanisms that are likely to operate in the sporeling.

Keywords

Cell division cycle Cell shape Dedifferentiation Phytochrome Regeneration Sugar signaling 

Notes

Acknowledgments

We thank John Bowman for information on classical literature and helpful discussion, Tom Dierschke for translating German literature, Sachihiro Matsunaga for the EdU technique, and Keisuke Inoue for experimental supports and discussion. This work was supported by KAKENHI Grant-in-Aids for Scientific Research on Innovative Area (Nos. 23120516 and 25113009 to T.K.), for Young Scientists (B) (No. 22770035 to K.I.), and for Scientific Research (C) (No. 24570048 to R. N.) from the Japan Society for the Promotion of Science.

Supplementary material

10265_2015_724_MOESM1_ESM.pdf (1.7 mb)
Fig. S1 Apical-basal polarity in regeneration. a Schematic illustration of excision. A thallus of M. polymorpha (thin green line) was excised with a scalpel along the red broken lines. Thick green line midrib. b, c Micrographs of explants. Both apical and basal explants (b) were incubated for 5 days on sugar-free medium (c). Arrows regenerants. Bars 2 mm. Fig. S2 Schematic illustrations of excision. Pink-shaded fragments were used for the experiments shown in Figs. 2, S3, S5 (a) and Figs. 4–6, S7 (b). The excision pattern in a was used for SEM analyses to make sure that only one midrib is included in an explant. Fig. S3 SEM observation of the ventral side of a thallus and explant. a, b Ventral view of a 12-day-old thallus. Magnified view of the boxed region in a is shown in b. The dotted line marks a typical excision position. pr pegged rhizoid, sc scale, sr smooth rhizoid. c Ventral view of an explant 72 h after excision. Bars 500 µm (a, c), 100 µm (b). Fig. S4 Light irradiation patterns for R and R/FR cycle conditions used in this study. Fig. S5 SEM observation of initial stages in regeneration under various light conditions. Explants were grown for 96 h in the dark (a, d) or under R (b, e) or R/FR cycle (c, f) in the absence (ac) or presence (df) of 1 % sucrose. Ventral-side views are presented. Apical side of each explant is shown upside. Bars 100 µm. Fig. S6 An amino-acid sequence alignment of GAF domains. The alignment of GAF domains in PHY from M. polymorpha and PHYB from Arabidopsis was constructed using the MUSCLE program [Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797] implemented in the Geneious software (version 6.1.8; Biomatters; http://www.geneious.com/) with default parameters. The conserved tyrosine residue that was substituted to histidine is marked by triangle. Black shade identical residues. Fig. S7 Comparison of morphology of regenerants grown under R or R/FR cycle. Explants of 10-day-old thalli were incubated on sugar-free media under R (a, b) or R/FR cycle (c, d) for 2 weeks. a, c Dorsal, side, and ventral views of regenerants. b, d Transverse sections of agar-embedded regenerants dissected approximately along the broken lines in a and c. Red arrow air chamber. Bars 200 µm (a, c), 100 µm (b, d).(PDF 1729 kb)
10265_2015_724_MOESM2_ESM.mpg (5.9 mb)
Supplemental Movie 1 Complete series of time-lapse observation of regeneration for 5 days from a thallus explant of M. polymorpha. A basal fragment obtained from a 14-day-old thallus of Tak-1 was placed on solid medium containing 1 % sucrose and incubated under continuous white light. Photographs were taken with 1-h intervals.(MPG 6 044 kb)

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Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  • Ryuichi Nishihama
    • 1
    Email author
  • Kimitsune Ishizaki
    • 1
    • 2
  • Masashi Hosaka
    • 1
  • Yoriko Matsuda
    • 1
  • Akane Kubota
    • 1
    • 3
  • Takayuki Kohchi
    • 1
  1. 1.Graduate School of BiostudiesKyoto UniversityKyotoJapan
  2. 2.Graduate School of ScienceKobe UniversityKobeJapan
  3. 3.Department of BiologyUniversity of WashingtonSeattleUSA

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