Biophysical Reviews

, Volume 10, Issue 6, pp 1683–1693 | Cite as

Cytoskeletal discoveries in the plant lineage using the moss Physcomitrella patens

  • Shu-Zon Wu
  • Moe Yamada
  • Darren R. Mallett
  • Magdalena BezanillaEmail author


Advances in cell biology have been largely driven by pioneering work in model systems, the majority of which are from one major eukaryotic lineage, the opisthokonts. However, with the explosion of genomic information in many lineages, it has become clear that eukaryotes have incredible diversity in many cellular systems, including the cytoskeleton. By identifying model systems in diverse lineages, it may be possible to begin to understand the evolutionary origins of the eukaryotic cytoskeleton. Within the plant lineage, cell biological studies in the model moss, Physcomitrella patens, have over the past decade provided key insights into how the cytoskeleton drives cell and tissue morphology. Here, we review P. patens attributes that make it such a rich resource for cytoskeletal cell biological inquiry and highlight recent key findings with regard to intracellular transport, microtubule-actin interactions, and gene discovery that promises for many years to provide new cytoskeletal players.


Actin Microtubules Myosin Kinesin Organelle transport Tip growth Phragmoplast 



We thank Xiaohang Cheng for careful reading of the manuscript.

Funding information

MY was supported by a Japan Society for the Promotion of Science pre-doctoral fellowship (16J02796). A grant from the National Science Foundation (MCB-1715785) supported S-Z W and MB. DM and MB were supported by funds from Dartmouth College.

Compliance with ethical standards

Conflict of interest

Shu-Zon Wu declares that she has no conflict of interest. Moe Yamada declares that she has no conflict of interest. Darren R. Mallett declares that he has no conflict of interest. Magdalena Bezanilla declares that she has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Ashton NW, Cove DJ, Featherstone DR (1979) The isolation and physiological analysis of mutants of the moss, Physcomitrella patens, which over-produce gametophores. Planta 144:437–442. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Åström H, Sorri O, Raudaskoski M (1995) Role of microtubules in the movement of the vegetative nucleus and generative cell in tobacco pollen tubes. Sex Plant Reprod 8:61–69. CrossRefGoogle Scholar
  3. Bascom CS, Hepler PK, Bezanilla M (2018) Interplay between ions, the cytoskeleton, and cell wall properties during tip growth. Plant Physiol 176:28–40. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bascom CS, Wu S-Z, Nelson K et al (2016) Long-term growth of moss in microfluidic devices enables subcellular studies in development. Plant Physiol 172:28–37. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bashline L, Lei L, Li S, Gu Y (2014) Cell wall, cytoskeleton, and cell expansion in higher plants. Mol Plant 7:586–600. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cai G, Cresti M (2012) Are kinesins required for organelle trafficking in plant cells? Front Plant Sci 3:170. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Collonnier C, Epert A, Mara K et al (2017) CRISPR-Cas9-mediated efficient directed mutagenesis and RAD51-dependent and RAD51-independent gene targeting in the moss Physcomitrella patens. Plant Biotechnol J 15:122–131. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Ding X, Pervere LM, Bascom C et al (2018) Conditional genetic screen in Physcomitrella patens reveals a novel microtubule depolymerizing-end-tracking protein. PLoS Genet 14:e1007221. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Doonan JH, Cove DJ, Lloyd CW (1988) Microtubules and microfilaments in tip growth: evidence that microtubules impose polarity on protonemal growth in Physcomitrella patens. J Cell Sci 89:533–540Google Scholar
  11. Doonan JH, Cove DJ, Lloyd CW (1985) Immunofluorescence microscopy of microtubules in intact cell lineages of the moss I Normal and CIPC-treated tip cells. J Cell Sci 75:131–147Google Scholar
  12. Eng RC, Sampathkumar A (2018) Getting into shape: the mechanics behind plant morphogenesis. Curr Opin Plant Biol 46:25–31. CrossRefGoogle Scholar
  13. Erickson JL, Adlung N, Lampe C et al (2018) The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana. Plant J 93:856–870. CrossRefGoogle Scholar
  14. Facette MR, Rasmussen CG, Van Norman JM (2018) A plane choice: coordinating timing and orientation of cell division during plant development. Curr Opin Plant Biol 47:47–55. CrossRefGoogle Scholar
  15. Furt F, Lemoi K, Tüzel E, Vidali L (2012) Quantitative analysis of organelle distribution and dynamics in Physcomitrella patens protonemal cells. BMC Plant Biol 12:70. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Furt F, Liu Y-C, Bibeau JP et al (2013) Apical myosin XI anticipates F-actin during polarized growth of Physcomitrella patens cells. Plant J 73:417–428. CrossRefGoogle Scholar
  17. Gundersen GG, Worman HJ (2013) Nuclear positioning. Cell 152:1376–1389. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Harrison CJ, Roeder AHK, Meyerowitz EM, Langdale JA (2009) Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr Biol 19:461–471. CrossRefGoogle Scholar
  19. Heslop-Harrison J, Heslop-Harrison Y, Cresti M et al (1988) Cytoskeletal elements, cell shaping and movement in the angiosperm pollen tube. J Cell Sci 91:49–60Google Scholar
  20. Hiwatashi Y, Obara M, Sato Y et al (2008) Kinesins are indispensable for interdigitation of phragmoplast microtubules in the moss Physcomitrella patens. Plant Cell 20:3094–3106. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hiwatashi Y, Sato Y, Doonan JH (2014) Kinesins have a dual function in organizing microtubules during both tip growth and cytokinesis in Physcomitrella patens. Plant Cell 26:1256–1266. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jonsson E, Yamada M, Vale RD, Goshima G (2015) Clustering of a kinesin-14 motor enables processive retrograde microtubule-based transport in plants. Nature Plants
  23. Kadota A, Sato Y, Wada M (2000) Intracellular chloroplast photorelocation in the moss Physcomitrella patens is mediated by phytochrome as well as by a blue-light receptor. Planta 210:932–937. CrossRefPubMedGoogle Scholar
  24. Kadota A, Yamada N, Suetsugu N et al (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci U S A 106:13106–13111. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kawai H, Kanegae T, Christensen S et al (2003) Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421:287–290. CrossRefPubMedGoogle Scholar
  26. Kofuji R, Hasebe M (2014) Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Curr Opin Plant Biol 17:13–21. CrossRefPubMedGoogle Scholar
  27. Kong SG, Arai Y, Suetsugu N et al (2013) Rapid severing and motility of chloroplast-actin filaments are required for the chloroplast avoidance response in Arabidopsis. THE PLANT CELL ONLINE 25:572–590. CrossRefGoogle Scholar
  28. Kost B, Spielhofer P, Chua NH (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 16:393–401CrossRefPubMedGoogle Scholar
  29. Kumar AS, Park E, Nedo A, et al (2018) Stromule extension along microtubules coordinated with actin-mediated anchoring guides perinuclear chloroplast movement during innate immunity. elife
  30. Lee Y-RJ, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136:3877–3883. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Leong SY, Yamada M, Yanagisawa N, Goshima G (2018) SPIRAL2 stabilises endoplasmic microtubule minus ends in the moss Physcomitrella patens. Cell Struct Funct 43:53–60. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Loisel TP, Boujemaa R, Pantaloni D, Carlier M-F (1999) Reconstitution of actin-based motility of <i>Listeria</i> and <i>Shigella</i> using pure proteins. Nature 401:613–616. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lopez-Obando M, Hoffmann B, Géry C et al (2016) Simple and efficient targeting of multiple genes through CRISPR-Cas9 in Physcomitrella patens. G3 (Bethesda) 6:3647–3653. CrossRefGoogle Scholar
  34. MacVeigh-Fierro D, Tüzel E, Vidali L (2017) The Motor Kinesin 4II is important for growth and chloroplast light avoidance in the moss Physcomitrella patens. Am J Plant Sci 08:791–809. CrossRefGoogle Scholar
  35. Miki T, Naito H, Nishina M, Goshima G (2014) Endogenous localizome identifies 43 mitotic kinesins in a plant cell. Proc Natl Acad Sci U S A 111:E1053–E1061. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Miki T, Nishina M, Goshima G (2015) RNAi screening identifies the armadillo repeat-containing kinesins responsible for microtubule-dependent nuclear positioning in Physcomitrella patens. Plant Cell Physiol 56:737–749. CrossRefGoogle Scholar
  37. Moody LA, Kelly S, Rabbinowitsch E, Langdale JA (2018) Genetic regulation of the 2D to 3D growth transition in the moss Physcomitrella patens. Curr Biol 28:473–478.e5. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Müller S, Jürgens G (2016) Plant cytokinesis—no ring, no constriction but centrifugal construction of the partitioning membrane. Semin Cell Dev Biol 53:10–18. CrossRefGoogle Scholar
  39. Peremyslov VV, Mockler TC, Filichkin SA et al (2011) Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol 155:1191–1204. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Prigge MJ, Lavy M, Ashton NW, Estelle M (2010) Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxin-signaling pathway. Curr Biol 20:1907–1912. CrossRefGoogle Scholar
  41. Rasmussen CG, Bellinger M (2018) An overview of plant division-plane orientation. New Phytol 219:505–512. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Reddy AS, Day IS (2001a) Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2:2CrossRefPubMedPubMedCentralGoogle Scholar
  43. Reddy AS, Day IS (2001b) Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 2:RESEARCH0024CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rounds CM, Bezanilla M (2013) Growth mechanisms in tip-growing plant cells. Annu Rev Plant Biol 64:243–265. CrossRefGoogle Scholar
  45. Ryan JM, Nebenführ A (2018) Update on myosin motors: molecular mechanisms and physiological functions. Plant Physiol 176:119–127. CrossRefGoogle Scholar
  46. Sato Y, Wada M, Kadota A (2001) Choice of tracks, microtubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor. J Cell Sci 114:269–279Google Scholar
  47. Sauer B (1998) Inducible gene targeting in mice using the Cre/lox system. Methods 14:381–392. CrossRefGoogle Scholar
  48. Schaefer D, Zryd JP, Knight CD, Cove DJ (1991) Stable transformation of the moss <Emphasis Type=“Italic”>Physcomitrella patens</Emphasis>. Mol Gen Genet 226:418–424. CrossRefGoogle Scholar
  49. Schaefer DG, Zrÿd J-P (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206. CrossRefGoogle Scholar
  50. Schaefer E, Belcram K, Uyttewaal M et al (2017) The preprophase band of microtubules controls the robustness of division orientation in plants. Science 356:186–189. CrossRefPubMedGoogle Scholar
  51. Shen Z, Collatos AR, Bibeau JP et al (2012) Phylogenetic analysis of the Kinesin superfamily from physcomitrella. Front Plant Sci 3:230. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Shen Z, Liu YC, Bibeau JP et al (2015) The kinesin-like proteins, KAC1/2, regulate actin dynamics underlying chloroplast light-avoidance in Physcomitrella patens. J Integr Plant Biol 57:106–119. CrossRefPubMedGoogle Scholar
  53. Shimmen T (2007) The sliding theory of cytoplasmic streaming: fifty years of progress. J Plant Res 120:31–43. CrossRefPubMedGoogle Scholar
  54. Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Curr Opin Cell Biol 16:68–72. CrossRefPubMedGoogle Scholar
  55. Smertenko A, Assaad F, Baluška F et al (2017) Plant cytokinesis: terminology for structures and processes. Trends Cell Biol 27:885–894. CrossRefGoogle Scholar
  56. Stevenson SR, Kamisugi Y, Trinh CH et al (2016) Genetic analysis of Physcomitrella patens identifies ABSCISIC ACID NON-RESPONSIVE, a regulator of ABA responses unique to basal land plants and required for desiccation tolerance. Plant Cell 28:1310–1327. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Strepp R, Scholz S, Kruse S et al (1998) Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci U S A 95:4368–4373. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Suetsugu N, Sato Y, Tsuboi H et al (2012) The KAC family of kinesin-like proteins is essential for the association of chloroplasts with the plasma membrane in land plants. Plant Cell Physiol 53:1854–1865. CrossRefGoogle Scholar
  59. Suetsugu N, Yamada N, Kagawa T et al (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107:8860–8865. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Szymanski D, Staiger CJ (2018) The actin cytoskeleton: functional arrays for cytoplasmic organization and cell shape control. Plant Physiol 176:106–118. CrossRefPubMedGoogle Scholar
  61. Tamura K, Iwabuchi K, Fukao Y et al (2013) Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis. Curr Biol 23:1776–1781. CrossRefPubMedGoogle Scholar
  62. Vidali L, Augustine RC, Kleinman KP, Bezanilla M (2007) Profilin is essential for tip growth in the moss Physcomitrella patens. THE PLANT CELL ONLINE 19:3705–3722. CrossRefGoogle Scholar
  63. Vidali L, Bezanilla M (2012) Physcomitrella patens: a model for tip cell growth and differentiation. Curr Opin Plant Biol 15:625–631. CrossRefPubMedGoogle Scholar
  64. Vidali L, Burkart GM, Augustine RC et al (2010) Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell 22:1868–1882. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Vidali L, Rounds CM, Hepler PK, Bezanilla M (2009) Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS One 4:e5744–e5715. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wu J-Q, Pollard TD (2005) Counting cytokinesis proteins globally and locally in fission yeast. Science 310:310–314. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wu S-Z, Bezanilla M (2014) Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. Elife 3:e03498. CrossRefPubMedCentralGoogle Scholar
  68. Wu S-Z, Bezanilla M (2018) Actin and microtubule cross talk mediates persistent polarized growth. J Cell Biol 89:jcb.201802039–jcb.201802023. CrossRefGoogle Scholar
  69. Wu S-Z, Ritchie JA, Pan A-H et al (2011) Myosin VIII regulates protonemal patterning and developmental timing in the moss Physcomitrella patens. Mol Plant 4:909–921. CrossRefPubMedGoogle Scholar
  70. Yamada M, Goshima G (2018) The KCH kinesin drives nuclear transport and cytoskeletal coalescence to promote tip cell growth in Physcomitrella patens. Plant Cell 30:1496–1510. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yamada M, Tanaka-Takiguchi Y, Hayashi M, et al (2017) Multiple kinesin-14 family members drive microtubule minus end-directed transport in plant cells. J Cell Biol jcb.201610065.
  72. Yamashita H, Sato Y, Kanegae T et al (2011) Chloroplast actin filaments organize meshwork on the photorelocated chloroplasts in the moss Physcomitrella patens. Planta 233:357–368. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Zhou X, Graumann K, Evans DE, Meier I (2012) Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J Cell Biol 196:203–211. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Zurzycki J (1980) Blue light-induced intracellular movements. 50–68.

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesDartmouth CollegeHanoverUSA
  2. 2.Division of Biological Science, Graduate School of ScienceNagoya UniversityNagoyaJapan

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