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The peri-germ cell membrane: poorly characterized but key interface for plant reproduction

Nature Plants volume 10, pages 1607–1609 (2024)Cite this article

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Over the past 50 years, only a few studies have examined the peri-germ cell membrane. Nonetheless, it has been assigned multiple names. For example, the peri-germ cell membrane was identified in 1969 (ref. 1) as the ‘generative cell envelope’. Subsequent ultrastructural work in the 1980s led to new names, including ‘internal plasma membrane of the vegetative cell’, ‘inner plasma membrane of the pollen grain’ and ‘inner vegetative cell plasma membrane’2,3,4,5,6. Another study referred to it as the ‘pollen tube inner plasma membrane’ when considering the pollen tube7. When the Arabidopsis small GTPase RHO OF PLANTS 9 (AtROP9) was identified as the first protein reported to locate to this membrane, the authors named it the ‘invaginated pollen tube plasma membrane’8. More recently, when the maize NOT-LIKE-DAD protein (NLD; also known as MATRILINEAL (MTL) or PHOSPHOLIPASE-A1 (ZmPLA1)) was found to localize exclusively to the peri-germ cell membrane, the authors named it the ‘pollen endo-plasma membrane’9.

This diverse nomenclature causes confusion and calls for the implementation of a consensus on terminology. For example, the term ‘generative cell envelope’ is too restrictive, as the peri-germ cell membrane also encloses the two sperm cells. Similarly, the use of ‘pollen tube’ in the nomenclature is not appropriate because this membrane is also present before pollen germination. Furthermore, using ‘plasma membrane’ could lead to confusion with the classical plasma membrane (PM) of the generative cell, sperm cells or vegetative cell. Additionally, the term plasma membrane is misleading, given that the peri-germ cell membrane may differ in protein and lipid composition from the classical PM.

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Fig. 1: Peri-germ cell membrane labelling differs from canonical PM makers.

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Acknowledgements

We thank H. Ikeda and H. Kakizaki for technical support; Y. Mizuta for Arabidopsis seeds containing the pLAT52:tdTomato-LTI6b transgene (YMv075); and D. Kurihara for DKv278. We acknowledge the PLATIM imaging facility of the SFR Biosciences (Université Claude Bernard Lyon 1, CNRS UAR3444, Inserm US8, ENS de Lyon). This work was supported by JSPS KAKENHI (JP20H05778 and JP20H05781 to D.M.; JP23K14214 and JP24KJ0184 to N.S.); the Nagahisa Science Foundation (G2023-01 to N.S.); the French National Research Agency (ANR) (ANR-19-CE20-0012 to T.W.); the Région Auvergne-Rhône-Alpes (grant ‘HD-INNOV’ from the ‘pack ambition recherche’ to T.W.); and the DIVEDIT project of the Sélection Végétale Avancée research program, and benefited from government funding managed by the National Research Agency under the France 2030 program, reference ANR-22-PSV-003 to T.W.; A.R.M.C. is currently supported by a PhD fellowship from the Association Nationale de la Recherche Technique (ANRT) (Grant Cifre no. 2023/1284).

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Author notes

  1. These authors contributed equally: Naoya Sugi, Andrea R. M. Calhau.

Authors and Affiliations

  1. Kihara Institute for Biological Research, Yokohama City University, Yokohama, Japan

    Naoya Sugi & Daisuke Maruyama

  2. Laboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Lyon, France

    Andrea R. M. Calhau, Nathanaël M. A. Jacquier, Marina Millan-Blanquez, Daniel Bouyer, Gwyneth Ingram, Yvon Jaillais & Thomas Widiez

  3. Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB NOVA), Oeiras, Portugal

    Jörg D. Becker

  4. Environmental Horticulture Department, University of Florida, Gainesville, FL, USA

    Kevin Begcy

  5. Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Vienna, Austria

    Frédéric Berger

  6. Institute de Biologie Moléculaire des Plantes (IBMP), CNRS, Université de Strasbourg, Strasbourg, France

    Cécile Bousquet-Antonelli

  7. Department of Life Sciences, University of Siena, Siena, Italy

    Giampiero Cai

  8. Department of Biochemistry and Molecular Biology, Molecular Cell Biology and Plant Biology Programs, University of Massachusetts, Amherst, MA, USA

    Alice Y. Cheung

  9. LAQV Requimte, Faculdade de Ciências da Universidade do Porto, Departamento de Biologia, Universidade do Porto, Porto, Portugal

    Sílvia Coimbra

  10. Technical University of Munich, School of Life Sciences, Plant Systems Biology, Freising, Germany

    Philipp Denninger

  11. Department of Cell Biology and Plant Biochemistry, University of Regensburg, Regensburg, Germany

    Thomas Dresselhaus & Stefanie Sprunck

  12. Department of Cell Biology & Molecular Genetics, University of Maryland, College Park, MD, USA

    José A. Feijó

  13. Oregon State University, Department of Botany and Plant Pathology, Corvallis, OR, USA

    John E. Fowler

  14. Horticell, Ghent University, Gent, Belgium

    Danny Geelen

  15. Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland

    Ueli Grossniklaus

  16. Zurich-Basel Plant Science Center, University of Zurich, Zurich, Switzerland

    Ueli Grossniklaus

  17. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan

    Tetsuya Higashiyama

  18. Institute of Experimental Botany, Czech Academy of Sciences, Prague, Czech Republic

    David Honys

  19. Division of Plant Science, Graduate School of Horticulture, Chiba University, Matsudo, Japan

    Tomoko Igawa

  20. Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, RI, USA

    Mark A. Johnson

  21. Institute for Chemical Research, Kyoto University, Kyoto, Japan

    Mariko Kato

  22. Division of Crop Plant Genetics, Department of Crop Science, Georg-August-University Goettingen, Goettingen, Germany

    Miki Kawachi & Stefan Scholten

  23. Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA

    Tomokazu Kawashima

  24. Department of Life Science and Environmental Biochemistry, Life and Industry Convergence Research Institute, Pusan National University, Miryang, Republic of Korea

    Yu-Jin Kim

  25. Key Laboratory of Seed Innovation, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    Hong-Ju Li

  26. Laboratoire de Biogenèse Membranaire, LBM CNRS-Univ. Bordeaux, UMR 5200, Villenave d’Ornon, France

    Sébastien Mongrand

  27. Research Organization of Science and Technology, Ritsumeikan University, Shiga, Japan

    Kazuki Motomura

  28. Division of Biological Sciences, Graduate School of Science, Kyoto University, Kyoto, Japan

    Shiori Nagahara

  29. Department of Biology, Technion – Israel Institute of Technology, Haifa, Israel

    Kohdai P. Nakajima

  30. Department of Plant Biology, University of Georgia, Athens, GA, USA

    Brad Nelms

  31. State Key Laboratory for Protein and Plant Gene Research, Peking-Tsinghua Center for Life Sciences, New Cornerstone Science Laboratory, College of Life Sciences, Peking University, Beijing, China

    Li-Jia Qu

  32. Department of Developmental Biology, Institute for Plant Sciences and Microbiology, University of Hamburg, Hamburg, Germany

    Arp Schnittger

  33. State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China

    Meng-Xiang Sun

  34. Department of Genetics and Genome Biology, University of Leicester, Leicester, UK

    David Twell

  35. Laboratory of Biochemistry, Wageningen University, Wageningen, the Netherlands

    Dolf Weijers

  36. State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    Wei-Cai Yang

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  1. Naoya Sugi
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Contributions

T.W. and D.M. took the lead on the renaming project and wrote the manuscript with the help of M.M.-B. N.S. performed the analysis of Arabidopsis pollen tubes and prepared figure panels. A.R.M.C. and N.M.A.J. observed pollen tubes in maize. All authors participated in the discussion regarding the term peri-germ cell membrane, contributed to the critical reading of the manuscript and approved the manuscript submission.

Corresponding authors

Correspondence to Daisuke Maruyama or Thomas Widiez.

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Sugi, N., Calhau, A.R.M., Jacquier, N.M.A. et al. The peri-germ cell membrane: poorly characterized but key interface for plant reproduction. Nat. Plants 10, 1607–1609 (2024). https://doi.org/10.1038/s41477-024-01818-5

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