Mechano-eco-evo-devo of plant shoot structure
Plant development is amazingly plastic. Being stuck in one location, plants need to cope with ever changing environment by adapting themselves to sustain their structural and physiological integrity. They do so remarkably well. For example, when encountering repetitive mechanical challenges (e.g. touch, strong unidirectional wind, even their own self-weight), plant shoots alter their body structure - both morphology and anatomy - to stay intact, often making their stems shorter and stiffer. Although the self-stabilisation of plant shoot is widely accepted, little is known about how plants sense mechanical distress and respond to alter their developmental decisions. In this integrative project, we aim to comprehend how plants achieve the robust structural stability via active mechano-sensing and response, taking both the top-down and bottom-up approaches, as well as zooming in and out at multi-scales in experimental focus.
How well do plants maintain their structural integrity? |
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It has been long established that plants auto-adjust its body (shoot and root - through development and physiology) to remain structurally sound. However, how well - quantitatively speaking - they maintain stability in face of mechanical challenges remains as yet unresolved.
In order to reveal how robust self-stabilization of plant shoot structure is, we are developing capturing the dynamic response of plant development and structural remodelling with the model plant Arabidopsis, The measured data will be input to a computational model of growing shoot, which adjusts its own stem structure as it grows, develops, and faces mechanical challenges. The structural stability will be calculated using a Finite Element Method-based engineering model, which is linked to a model of the plant shoot that can switch among different developmental outputs. |
Collaborators: Taku Komura (University of Edinburgh) Thomas Speck (University of Freiburg, Germany) Olga Speck (University of Freiburg, Germany) |
How do cells sense mechanical cues?
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In parallel, cell cultures that are given specific cell-type identities are created employing synthetic biology technology.
Cells react to their mechanical environment by changing cell division, expansion, and differentiation programmes, but how they sense and trigger such responses are just starting to be unravelled. We are developing single-cell & live-imaging platforms to examine cellular behaviours over time and responses to chemical and/or physical stimuli. A series of bespoke microfluidic devices is made to hold cells and apply chemical or mechanical treatments with high spatio-temporal precision. In parallel, cell cultures that are given specific cell-type identities are created employing synthetic biology technology. These two powerful resources will allow us to quantitatively visualise dynamic cellular responses to mechanical cues. It will also enable us to dissect key sensing and response mechanisms, in conjunction with mutant backgrounds, cell biological inhibitors and other chemical agents. |
Collaborators: Teuta Pilizota (University of Edinburgh) |
Molecular mechanisms underlying the structural remodelling
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From the sensing of the mechanical stimuli to ultimate changes in structural properties of the stem, we will connect the dots of key regulatory factors underlying the whole process, taking two approaches: candidate-based and a priori (longitudinal RNA-seq analysis). Once we understand the molecular pathways involved in the mechanically induced developmental and physiological responses leading to the structural remodelling, candidate key regulators will be tested by synthetic biology-based pathway engineering approaches. |
Form-function relationship of hair-like structures
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Collaborators: Ignazio Maria Viola (University of Edinburgh) Enrico Mastropaolo (University of Edinburgh) Arezki Boudaoud (ENS de Lyon/Ecole Polytechnique Paris, France) Angela Busse (University of Glasgow) Hossein Zare-Behtash (University of Glasgow) Mike Blatt (University of Glasgow) Merel Soons (Utrecht University, Netherlands) James Bullock (Centre for Ecology and Hydrology, UK) |
Nature invented numerous strategies to fly. Unlike animals that carry out muscle-based flight, plants (especially their fruits and seeds) travel in air with clever structural designs that increase air drag. A great example is the dandelion, for which a bundle of intricate hairs called pappus carry the seed over miles of distance with only a little help from wind. As familiar as the flight of dandelion is, we actually didn't know how it works.
We have characterising the structural engineering and fluid dynamics of the diaspore (the seed and the rest of the dispersal unit), in order to reveal the engineering underpinning of the flying seed. What we found was a previously unobserved ring vortex (wind wheel), which is separated but stays at a constant distance right downstream of the pappus. It creates a domain of low pressure and likely act to suck the seed upwards, helping to keep it aloft. |
Our research deciphering the flight mechanism of the dandelion has captured much public interest.
Examples of great videos made by the media:
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Synthetic Biology Engineering of Plant Regenerative Cultures
Developing synthetic biology tools for plant systems
Establishing plant regenerative cultures
Cellular agriculture of plant-driven food and materials
Thanks to the fundings from:
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Publications
R Ohlendorf, NHY Tan, N Nakayama. (2023)
Engineering themes in plant forms and functions.
Annual Review of Plant Biology. 74: 777-801.
EG Kocaoglan, D Radhakrishnan, N Nakayama. (2023)
Synthetic developmental biology: Molecular tools to re-design plant shoots and roots.
Journal of Experimental Botany. 13: 3864-76.
M Seale, O Zhdanov, C Cummins, E Kroll, M Blatt, H Zare-Behtash, A Busse, E Mastropaolo, IM Viola, N Nakayama. (2022)
Environmental morphing enables informed dispersal of the dandelion seeds.
eLife. 11: e81962.
T Wight, S Robinson, K Assefa, S Chanyalew, Z Tadele, N Nakayama*. (2022)
Morphology, development and phenotypic plasticity in Tef.
Textbook on the biology and agriculture of Tef, Eragrostis tef.
Ethiopian Institute of Agricultural Research Press. DOI: 10.48350/176287
M Seale, A Kiss, S Bovio, IM Viola, E Mastropaolo, A Boudaoud*, N Nakayama*. (2022)
Dandelion pappus morphing is actuated by radially patterned material swelling.
Nature Communications. 13: 2498. DOI:10.1038/s41467-022-30245-3
*Co-corresponding authors
Plant Cell Atlas Consortium, SG Jha, P Agarwal, AH Ahkami, ….., N Nakayama, .…, DW Ehrhardt, KD Birnbaum, SY Rhee. (2021)
A roadmap for plant cell atlas.
eLife. 10: e66877. DOI:10.7554/eLife.66877.
D Autran, G Bassel, E Chae, D Ezer, A Ferjani, , ..., N Nakayama, ..., M Ueda, S Wolf. (2021)
What is quantitative plant biology?
Quantitative Plant Biology. 2: E10. DOI:10.1017/qpb.2021.8.
D Certini, L Fazan, N Nakayama, IM Viola, G Kozlowski. (2020)
Velocity of the falling dispersal units in Zelkova abelicea: remarkable conservatism within the relict tree genus.
American Journal of Botany. 107: 1831. DOI:10.1002/ajb2.1581.
P Khumsupan, MA Kozlowska, D Orr, AI Andreou, NJ Patron, N Nakayama, E Carmo-Silva, and A McCormick. (2020)
Generating and characterising single- and multi-gene mutants of the Rubisco small subunit family in Arabidopsis.
Journal of Experimental Botany. 71: 5963. DOI:10.1093/jxb/eraa316.
M Seale*, N Nakayama*. (2019)
From passive to informed: mechanical mechanisms of seed dispersal.
New Phytologist. 225: 653.
*Co-corresponding authors
C Cummins, M Seale, A Macente, D Certini, E Mastropaolo, IM Viola*, N Nakayama*. (2018)
A separated vortex ring underlies the flight of the dandelion.
Nature. 562: 414-18.
*Co-corresponding authors
M Seale*, C Cummins, IM Viola, E Mastropaolo*, N Nakayama*. (2018)
Design principles of hair-like structures as biological machines.
Journal of Royal Society Interface. DOI:10.1098/rsif.2018.0206
*Co-corresponding authors
V Hernández-Hernández, RA Barrio, M Benítez, N Nakayama, JR Romero-Arias, C Villarreal. (2018)
A physico-genetic module for the polarisation of auxin efflux carriers PIN-FORMED (PIN).
Physical Biology. 15: 036002.
G Cannarozzi, S Chanyalew, K Assefa, A Bekele, .... N Nakayama, M Robinson, I Barker, S Zeeman, Z Tadele. (2018)
Technology generation to dissemination: lessons learned from the tef improvement project.
Euphytica. 214: 31.
AI Andreou*, N Nakayama*. (2018)
Mobius Assembly: a versatile Golden-Gate framework towards universal DNA assembly.
PLoS ONE. 13: e0189892.
*Co-corresponding authors
C Cummins*, IM Viola*, E Mastropaolo, N Nakayama. (2017)
The effect of permeability on the flow past porous disks at low Reynolds numbers.
Physics of Fluids. 29: 097103.
*Co-corresponding authors
J Reimegård, S Kundu, A Pendle, VF Irish, P Shaw, N Nakayama*, JF Sundstrom*, O Emanuelsson*. (2017)
Genome-wide identification of physically clustered genes suggests chromatin-level co-regulation in male reproductive development in Arabidopsis thaliana.
Nucleic Acid Research. 6: 3253-65.
*Co-corresponding authors
LCT Scorza, N Nakayama. (2016)
Right place right time: heterogeneity-driven organ geometry.
Developmental Cell. 38: 5-7.
YB Sinai, JD Julien, E Sharon, S Armon, N Nakayama, M Adda-Bedia, A Boudaoud. (2016)
Mechanical stresss induces remodeling of vascular networks in growing leaves.
PLoS Computational Biology. 12: e1004819.
P Barbier de Reuille, AL Rourier-Kierzkowska, D Kierzkowski, GW Bassel, .......,, N Nakayama, M Tsiantis, A Hay, D Kwiatkowska, I Xenarios, C Kuhlemeier, and RS Smith. (2015)
MorphoGraphX: a platform for quantifying morphogenesiss in 4D.
eLife. 05864.
H Nakayama, N Nakayama, S Seiki, M Kojima, H Sakakibara, N Sinha, and S Kimura. (2014)
Regulation of KNOX-GA gene module induces heterophyllic alteration in North American lake cress.
Plant Cell. 26: 4733-48.
A Nakamasu, H Nakayama, N Nakayama, NJ Suematsu, S Kimura. (2014)
A developmental model for branching morphogenesis of lake cress compound leaf.
PLoS One. 9: e111615.
L Beauzamy, N Nakayama*, and A Boudaoud.* (2014)
Flowers under pressure: ins and outs of turgor regulation in development.
Annual of Botany. 114: 1517-33.
*Co-corresponding authors
S Robinson*, A Burian, E Couturier, B Landrein, M Louveaux, ED Neumann, A Peaucelle, A Weber, and N Nakayama.* (2013) Mechanical control of morphogenesis at the shoot apex.
Journal of Experimental Botany. 64: 4729-4744.
*Co-corresponding authors
N Nakayama. (2013)
メリステム内の力学 (Mechanics of the meristems).
In 植物細胞壁 (Plant Cell Wall), edited by Kazuhiko Nishitani and Toshiaki Umesawa. Kodansha Scientific (Tokyo, Japan).
E Couturier, N Brunel, S Douady, and N Nakayama. (2012)
Abaxial growth and steric constraints guide leaf folding and shape in Acer pseudoplatanus.
American Journal of Botany. 99: 1289-99.
N Nakayama, RS Smith, T Mandel, S Robinson, S Kimura, A Boudaoud, and C Kuhlemeier. (2012)
Mechanical regulation of auxin-mediated growth.
Current Biology. 22: 1468-76.
Featured in Dispatch: Current Biology, 22: R635-637.
H Nakayama, N Nakayama, A Nakamasu, N Sinha, and S Kimura. (2012)
Toward elucidating the mechanisms that regulate heterophylly.
Plant Morphology. 24: 57-63.
N Nakayama. (2012)
生体組織のマテリアル解析から形態制御を探る (Morphogenic regulation through tissue material properties).
First Author’s ライフサイエンス新着論文レヴュー. http://first.lifesciencedb.jp/archives/4598
D Kierzkowski*, N Nakayama*, AL Rouiter-Kierzkowski*, A Weber*, EM Bayer, M Schorderet, D Reinhardt, C Kuhlemeier, and RS Smith. (2012)
Elastic domains regulate growth and organogenesis in the plant shoot apical meristem.
Science. 335: 1096-9.
*Co-first authors
Featured in Editor’s Choice: Science Signal, 5: ec73.
N Lugassi, N Nakayama, R Bochnik, and M Zik. (2010)
A novel allele of FILAMENTOUS FLOWER reveals new insights on the link between inflorescence and floral meristem organization and flower morphogenesis.
BMC Plant Biology. 10:131-44.
N Nakayama and C Kuhlemeier. (2009)
Leaf development: untangling the spirals.
Current Biology. 19: R71-4.
EM Bayer, RS Smith, T Mandel, N Nakayama, M Sauer, P Prusinkiewics, C Kuhlemeier. (2009)
Integration of transport-based model for phyllotaxis and midvein formation.
Genes and Development. 23: 373-84.
J Sundström, N Nakayama, K Glimelius, and VF Irish. (2006)
Direct regulation of the floral homeotic APETALA1 gene by APETALA3 and PISTILLATA in Arabidopsis.
Plant Journal. 46: 593-600.
N Nakayama, JM Arroyo, J Simorowski, B May, R Martienssen, and VF Irish. (2005)
Gene trap lines define domains of gene regulation in Arabidopsis petals and stamens.
Plant Cell. 17: 2486-506.
Press released by Plant Cell.
Y Liu*, N Nakayama*, M Schiff, A Litt, VF Irish, SP Dinesh-Kumar. (2004)
Virus induced gene silencing of a DEFICIENS ortholog in Nicotiana benthamiana.
Plant Molecular Biology. 54: 701-11.
*Co-first authors
X Wang, S Feng, N Nakayama, WL Crosby, VF Irish, XW Deng, and N Wei. (2003)
The COP9 signalosome interacts with SCFUFO and participates in Arabidopsis flower development.
Plant Cell. 15: 1071-82.
Engineering themes in plant forms and functions.
Annual Review of Plant Biology. 74: 777-801.
EG Kocaoglan, D Radhakrishnan, N Nakayama. (2023)
Synthetic developmental biology: Molecular tools to re-design plant shoots and roots.
Journal of Experimental Botany. 13: 3864-76.
M Seale, O Zhdanov, C Cummins, E Kroll, M Blatt, H Zare-Behtash, A Busse, E Mastropaolo, IM Viola, N Nakayama. (2022)
Environmental morphing enables informed dispersal of the dandelion seeds.
eLife. 11: e81962.
T Wight, S Robinson, K Assefa, S Chanyalew, Z Tadele, N Nakayama*. (2022)
Morphology, development and phenotypic plasticity in Tef.
Textbook on the biology and agriculture of Tef, Eragrostis tef.
Ethiopian Institute of Agricultural Research Press. DOI: 10.48350/176287
M Seale, A Kiss, S Bovio, IM Viola, E Mastropaolo, A Boudaoud*, N Nakayama*. (2022)
Dandelion pappus morphing is actuated by radially patterned material swelling.
Nature Communications. 13: 2498. DOI:10.1038/s41467-022-30245-3
*Co-corresponding authors
Plant Cell Atlas Consortium, SG Jha, P Agarwal, AH Ahkami, ….., N Nakayama, .…, DW Ehrhardt, KD Birnbaum, SY Rhee. (2021)
A roadmap for plant cell atlas.
eLife. 10: e66877. DOI:10.7554/eLife.66877.
D Autran, G Bassel, E Chae, D Ezer, A Ferjani, , ..., N Nakayama, ..., M Ueda, S Wolf. (2021)
What is quantitative plant biology?
Quantitative Plant Biology. 2: E10. DOI:10.1017/qpb.2021.8.
D Certini, L Fazan, N Nakayama, IM Viola, G Kozlowski. (2020)
Velocity of the falling dispersal units in Zelkova abelicea: remarkable conservatism within the relict tree genus.
American Journal of Botany. 107: 1831. DOI:10.1002/ajb2.1581.
P Khumsupan, MA Kozlowska, D Orr, AI Andreou, NJ Patron, N Nakayama, E Carmo-Silva, and A McCormick. (2020)
Generating and characterising single- and multi-gene mutants of the Rubisco small subunit family in Arabidopsis.
Journal of Experimental Botany. 71: 5963. DOI:10.1093/jxb/eraa316.
M Seale*, N Nakayama*. (2019)
From passive to informed: mechanical mechanisms of seed dispersal.
New Phytologist. 225: 653.
*Co-corresponding authors
C Cummins, M Seale, A Macente, D Certini, E Mastropaolo, IM Viola*, N Nakayama*. (2018)
A separated vortex ring underlies the flight of the dandelion.
Nature. 562: 414-18.
*Co-corresponding authors
M Seale*, C Cummins, IM Viola, E Mastropaolo*, N Nakayama*. (2018)
Design principles of hair-like structures as biological machines.
Journal of Royal Society Interface. DOI:10.1098/rsif.2018.0206
*Co-corresponding authors
V Hernández-Hernández, RA Barrio, M Benítez, N Nakayama, JR Romero-Arias, C Villarreal. (2018)
A physico-genetic module for the polarisation of auxin efflux carriers PIN-FORMED (PIN).
Physical Biology. 15: 036002.
G Cannarozzi, S Chanyalew, K Assefa, A Bekele, .... N Nakayama, M Robinson, I Barker, S Zeeman, Z Tadele. (2018)
Technology generation to dissemination: lessons learned from the tef improvement project.
Euphytica. 214: 31.
AI Andreou*, N Nakayama*. (2018)
Mobius Assembly: a versatile Golden-Gate framework towards universal DNA assembly.
PLoS ONE. 13: e0189892.
*Co-corresponding authors
C Cummins*, IM Viola*, E Mastropaolo, N Nakayama. (2017)
The effect of permeability on the flow past porous disks at low Reynolds numbers.
Physics of Fluids. 29: 097103.
*Co-corresponding authors
J Reimegård, S Kundu, A Pendle, VF Irish, P Shaw, N Nakayama*, JF Sundstrom*, O Emanuelsson*. (2017)
Genome-wide identification of physically clustered genes suggests chromatin-level co-regulation in male reproductive development in Arabidopsis thaliana.
Nucleic Acid Research. 6: 3253-65.
*Co-corresponding authors
LCT Scorza, N Nakayama. (2016)
Right place right time: heterogeneity-driven organ geometry.
Developmental Cell. 38: 5-7.
YB Sinai, JD Julien, E Sharon, S Armon, N Nakayama, M Adda-Bedia, A Boudaoud. (2016)
Mechanical stresss induces remodeling of vascular networks in growing leaves.
PLoS Computational Biology. 12: e1004819.
P Barbier de Reuille, AL Rourier-Kierzkowska, D Kierzkowski, GW Bassel, .......,, N Nakayama, M Tsiantis, A Hay, D Kwiatkowska, I Xenarios, C Kuhlemeier, and RS Smith. (2015)
MorphoGraphX: a platform for quantifying morphogenesiss in 4D.
eLife. 05864.
H Nakayama, N Nakayama, S Seiki, M Kojima, H Sakakibara, N Sinha, and S Kimura. (2014)
Regulation of KNOX-GA gene module induces heterophyllic alteration in North American lake cress.
Plant Cell. 26: 4733-48.
A Nakamasu, H Nakayama, N Nakayama, NJ Suematsu, S Kimura. (2014)
A developmental model for branching morphogenesis of lake cress compound leaf.
PLoS One. 9: e111615.
L Beauzamy, N Nakayama*, and A Boudaoud.* (2014)
Flowers under pressure: ins and outs of turgor regulation in development.
Annual of Botany. 114: 1517-33.
*Co-corresponding authors
S Robinson*, A Burian, E Couturier, B Landrein, M Louveaux, ED Neumann, A Peaucelle, A Weber, and N Nakayama.* (2013) Mechanical control of morphogenesis at the shoot apex.
Journal of Experimental Botany. 64: 4729-4744.
*Co-corresponding authors
N Nakayama. (2013)
メリステム内の力学 (Mechanics of the meristems).
In 植物細胞壁 (Plant Cell Wall), edited by Kazuhiko Nishitani and Toshiaki Umesawa. Kodansha Scientific (Tokyo, Japan).
E Couturier, N Brunel, S Douady, and N Nakayama. (2012)
Abaxial growth and steric constraints guide leaf folding and shape in Acer pseudoplatanus.
American Journal of Botany. 99: 1289-99.
N Nakayama, RS Smith, T Mandel, S Robinson, S Kimura, A Boudaoud, and C Kuhlemeier. (2012)
Mechanical regulation of auxin-mediated growth.
Current Biology. 22: 1468-76.
Featured in Dispatch: Current Biology, 22: R635-637.
H Nakayama, N Nakayama, A Nakamasu, N Sinha, and S Kimura. (2012)
Toward elucidating the mechanisms that regulate heterophylly.
Plant Morphology. 24: 57-63.
N Nakayama. (2012)
生体組織のマテリアル解析から形態制御を探る (Morphogenic regulation through tissue material properties).
First Author’s ライフサイエンス新着論文レヴュー. http://first.lifesciencedb.jp/archives/4598
D Kierzkowski*, N Nakayama*, AL Rouiter-Kierzkowski*, A Weber*, EM Bayer, M Schorderet, D Reinhardt, C Kuhlemeier, and RS Smith. (2012)
Elastic domains regulate growth and organogenesis in the plant shoot apical meristem.
Science. 335: 1096-9.
*Co-first authors
Featured in Editor’s Choice: Science Signal, 5: ec73.
N Lugassi, N Nakayama, R Bochnik, and M Zik. (2010)
A novel allele of FILAMENTOUS FLOWER reveals new insights on the link between inflorescence and floral meristem organization and flower morphogenesis.
BMC Plant Biology. 10:131-44.
N Nakayama and C Kuhlemeier. (2009)
Leaf development: untangling the spirals.
Current Biology. 19: R71-4.
EM Bayer, RS Smith, T Mandel, N Nakayama, M Sauer, P Prusinkiewics, C Kuhlemeier. (2009)
Integration of transport-based model for phyllotaxis and midvein formation.
Genes and Development. 23: 373-84.
J Sundström, N Nakayama, K Glimelius, and VF Irish. (2006)
Direct regulation of the floral homeotic APETALA1 gene by APETALA3 and PISTILLATA in Arabidopsis.
Plant Journal. 46: 593-600.
N Nakayama, JM Arroyo, J Simorowski, B May, R Martienssen, and VF Irish. (2005)
Gene trap lines define domains of gene regulation in Arabidopsis petals and stamens.
Plant Cell. 17: 2486-506.
Press released by Plant Cell.
Y Liu*, N Nakayama*, M Schiff, A Litt, VF Irish, SP Dinesh-Kumar. (2004)
Virus induced gene silencing of a DEFICIENS ortholog in Nicotiana benthamiana.
Plant Molecular Biology. 54: 701-11.
*Co-first authors
X Wang, S Feng, N Nakayama, WL Crosby, VF Irish, XW Deng, and N Wei. (2003)
The COP9 signalosome interacts with SCFUFO and participates in Arabidopsis flower development.
Plant Cell. 15: 1071-82.