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Cell wall‐mediated maternal control of apical–basal patterning of the kelp Undaria pinnatifida

Eloise Dries, Yannick Meyers, Daniel Liesner, Floriele Gonzaga (UGent) , Jakob Becker, Eliane Zakka (UGent) , Tom Beeckman (UGent) , Susana M. Coelho, Olivier De Clerck (UGent) and Kenny Bogaert (UGent)
(2024) NEW PHYTOLOGIST. 243(5). p.1887-1898
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Abstract
The role of maternal tissue in embryogenesis remains enigmatic in many complex organisms. Here, we investigate the contribution of maternal tissue to apical-basal patterning in the kelp embryo. Focussing on Undaria pinnatifida, we studied the effects of detachment from the maternal tissue using microsurgery, staining of cell wall modifications, morphometric measurements, flow cytometry, genotyping and a modified kelp fertilisation protocol synchronising kelp embryogenesis. Detached embryos are rounder and often show aberrant morphologies. When a part of the oogonial cell wall remains attached to the zygote, the apical-basal patterning is rescued. Furthermore, the absence of contact with maternal tissue increases parthenogenesis, highlighting the critical role of maternal signals in the initial stages of development. These results show a key role for the connection to the maternal oogonial cell wall in apical-basal patterning in kelps. This observation is reminiscent of another brown alga, Fucus, where the cell wall directs the cell fate. Our findings suggest a conserved mechanism across phylogenetically distant oogamous lineages, where localised secretion of sulphated F2 fucans mediates the establishment of the apical-basal polarity. In this model, the maternal oogonial cell wall mediates basal cell fate determination by providing an extrinsic patterning cue to the future kelp embryo.
Keywords
Undaria pinnatifida, apical–basal patterning, cell wall, embryogenesis, kelp, maternal tissue, parthenogenesis, polarity, apical-basal patterning, LAMINARIA-ANGUSTATA PHAEOPHYTA, IMMUNOFLUORESCENCE MICROSCOPY, PARTHENOGENESIS, FERTILIZATION, GAMETOPHYTES, DIVISION, POLARITY, PACIFIC, PARTHENOSPOROPHYTES, ESTABLISHMENT

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Citation

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MLA
Dries, Eloise, et al. “Cell Wall‐mediated Maternal Control of Apical–Basal Patterning of the Kelp Undaria Pinnatifida.” NEW PHYTOLOGIST, vol. 243, no. 5, 2024, pp. 1887–98, doi:10.1111/nph.19953.
APA
Dries, E., Meyers, Y., Liesner, D., Gonzaga, F., Becker, J., Zakka, E., … Bogaert, K. (2024). Cell wall‐mediated maternal control of apical–basal patterning of the kelp Undaria pinnatifida. NEW PHYTOLOGIST, 243(5), 1887–1898. https://doi.org/10.1111/nph.19953
Chicago author-date
Dries, Eloise, Yannick Meyers, Daniel Liesner, Floriele Gonzaga, Jakob Becker, Eliane Zakka, Tom Beeckman, Susana M. Coelho, Olivier De Clerck, and Kenny Bogaert. 2024. “Cell Wall‐mediated Maternal Control of Apical–Basal Patterning of the Kelp Undaria Pinnatifida.” NEW PHYTOLOGIST 243 (5): 1887–98. https://doi.org/10.1111/nph.19953.
Chicago author-date (all authors)
Dries, Eloise, Yannick Meyers, Daniel Liesner, Floriele Gonzaga, Jakob Becker, Eliane Zakka, Tom Beeckman, Susana M. Coelho, Olivier De Clerck, and Kenny Bogaert. 2024. “Cell Wall‐mediated Maternal Control of Apical–Basal Patterning of the Kelp Undaria Pinnatifida.” NEW PHYTOLOGIST 243 (5): 1887–1898. doi:10.1111/nph.19953.
Vancouver
1.
Dries E, Meyers Y, Liesner D, Gonzaga F, Becker J, Zakka E, et al. Cell wall‐mediated maternal control of apical–basal patterning of the kelp Undaria pinnatifida. NEW PHYTOLOGIST. 2024;243(5):1887–98.
IEEE
[1]
E. Dries et al., “Cell wall‐mediated maternal control of apical–basal patterning of the kelp Undaria pinnatifida,” NEW PHYTOLOGIST, vol. 243, no. 5, pp. 1887–1898, 2024.
@article{01J2ZV3B8YJ0MW7CQDJ10KASJ5,
  abstract     = {{The role of maternal tissue in embryogenesis remains enigmatic in many complex organisms. Here, we investigate the contribution of maternal tissue to apical-basal patterning in the kelp embryo. Focussing on Undaria pinnatifida, we studied the effects of detachment from the maternal tissue using microsurgery, staining of cell wall modifications, morphometric measurements, flow cytometry, genotyping and a modified kelp fertilisation protocol synchronising kelp embryogenesis. Detached embryos are rounder and often show aberrant morphologies. When a part of the oogonial cell wall remains attached to the zygote, the apical-basal patterning is rescued. Furthermore, the absence of contact with maternal tissue increases parthenogenesis, highlighting the critical role of maternal signals in the initial stages of development. These results show a key role for the connection to the maternal oogonial cell wall in apical-basal patterning in kelps. This observation is reminiscent of another brown alga, Fucus, where the cell wall directs the cell fate. Our findings suggest a conserved mechanism across phylogenetically distant oogamous lineages, where localised secretion of sulphated F2 fucans mediates the establishment of the apical-basal polarity. In this model, the maternal oogonial cell wall mediates basal cell fate determination by providing an extrinsic patterning cue to the future kelp embryo.}},
  author       = {{Dries, Eloise and Meyers, Yannick and Liesner, Daniel and Gonzaga, Floriele and Becker, Jakob and Zakka, Eliane and Beeckman, Tom and Coelho, Susana M. and De Clerck, Olivier and Bogaert, Kenny}},
  issn         = {{0028-646X}},
  journal      = {{NEW PHYTOLOGIST}},
  keywords     = {{Undaria pinnatifida,apical–basal patterning,cell wall,embryogenesis,kelp,maternal tissue,parthenogenesis,polarity,apical-basal patterning,LAMINARIA-ANGUSTATA PHAEOPHYTA,IMMUNOFLUORESCENCE MICROSCOPY,PARTHENOGENESIS,FERTILIZATION,GAMETOPHYTES,DIVISION,POLARITY,PACIFIC,PARTHENOSPOROPHYTES,ESTABLISHMENT}},
  language     = {{eng}},
  number       = {{5}},
  pages        = {{1887--1898}},
  title        = {{Cell wall‐mediated maternal control of apical–basal patterning of the kelp Undaria pinnatifida}},
  url          = {{http://doi.org/10.1111/nph.19953}},
  volume       = {{243}},
  year         = {{2024}},
}
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