Localized growth and remodelling drives spongy mesophyll morphogenesis

Treado, John D.; Roddy, Adam B.; Théroux-Rancourt, Guillaume; Zhang, Liyong; Ambrose, Chris; Brodersen, Craig R.; Shattuck, Mark D.; O’Hern, Corey S.

doi:10.1098/rsif.2022.0602

Localized growth and remodelling drives spongy mesophyll morphogenesis

Journal Article · 01 December 2022 · Interface (Online)

DOI:https://doi.org/10.1098/rsif.2022.0602· OSTI ID:2422698

^[1]; Roddy, Adam B. ^[2]; ^[3]; Zhang, Liyong ^[4]; Ambrose, Chris ^[4]; ^[5]; Shattuck, Mark D. ^[6]; O’Hern, Corey S. ^[7]

Department of Mechanical Engineering and Materials Science and Integrated Graduate Program in Physical and Engineering Biology, Yale University, New Haven, CT 06520, USA
Institute of Environment, Department of Biological Sciences, Florida International University, Miami, FL 33199, USA
University of Natural Resources and Life Sciences, Vienna, Department of Integrative Biology and Biodiversity Research, Institute of Botany, 1180 Vienna, Austria
Department of Biology, College of Arts and Science, University of Saskatchewan, Saskatoon, Canada S7N 5E2
School of the Environment, Yale University, New Haven, CT 06520, USA
Department of Physics and Benjamin Levich Institute, City College of New York, NY 10031, USA
Department of Physics, Yale University, New Haven, CT 06520, USA; Department of Applied Physics, Yale University, New Haven, CT 06520, USA

The spongy mesophyll is a complex, porous tissue found in plant leaves that enables carbon capture and provides mechanical stability. Unlike many other biological tissues, which remain confluent throughout development, the spongy mesophyll must develop from an initially confluent tissue into a tortuous network of cells with a large proportion of intercellular airspace. How the airspace in the spongy mesophyll develops while the tissue remains mechanically stable is unknown. Here, we use computer simulations of deformable polygons to develop a purely mechanical model for the development of the spongy mesophyll tissue. By stipulating that cell wall growth and remodelling occurs only near void space, our computational model is able to recapitulate spongy mesophyll development observed inArabidopsis thalianaleaves. We find that robust generation of pore space in the spongy mesophyll requires a balance of cell growth, adhesion, stiffness and tissue pressure to ensure cell networks become porous yet maintain mechanical stability. The success of this mechanical model of morphogenesis suggests that simple physical principles can coordinate and drive the development of complex plant tissues like the spongy mesophyll.

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC02-05CH11231

OSTI ID:: 2422698

Journal Information:: Interface (Online), Journal Name: Interface (Online) Journal Issue: 197 Vol. 19; ISSN 1742-5662

Publisher:: The Royal Society

Country of Publication:: United States

Language:: English

References (57)

Cell and chloroplast anatomical features are poorly estimated from 2D cross‐sections Harwood, Richard; Goodman, Elinor; Gudmundsdottir, Marin New Phytologist, Vol. 225, Issue 6 https://doi.org/10.1111/nph.16219	journal	November 2019
Air-space tissue in plants Sifton, H. B. The Botanical Review, Vol. 11, Issue 2 https://doi.org/10.1007/BF02861138	journal	February 1945
Physical Forces Regulate Plant Development and Morphogenesis Sampathkumar, Arun; Yan, An; Krupinski, Pawel Current Biology, Vol. 24, Issue 10 https://doi.org/10.1016/j.cub.2014.03.014	journal	May 2014
Profiles of ¹⁴ C fixation through spinach leaves in relation to light absorption and photosynthetic capacity: Where in a leaf is light captured and CO ₂ fixed? Evans, J. R.; Vogelmann, T. C. Plant, Cell & Environment, Vol. 26, Issue 4 https://doi.org/10.1046/j.1365-3040.2003.00985.x	journal	April 2003
Three-dimensional patterns of cell division and expansion throughout the development of Arabidopsis thaliana leaves Kalve, S.; Fotschki, J.; Beeckman, T. Journal of Experimental Botany, Vol. 65, Issue 22 https://doi.org/10.1093/jxb/eru358	journal	September 2014
Why plants make puzzle cells, and how their shape emerges Sapala, Aleksandra; Runions, Adam; Routier-Kierzkowska, Anne-Lise eLife, Vol. 7 https://doi.org/10.7554/eLife.32794	journal	February 2018
Development and Structure of Drought-tolerant Leaves of the Mediterranean Shrub Capparis spinosa L. Rhizopoulou, S. Annals of Botany, Vol. 92, Issue 3 https://doi.org/10.1093/aob/mcg149	journal	July 2003
Watersheds in digital spaces: an efficient algorithm based on immersion simulations Vincent, L.; Soille, P. IEEE Transactions on Pattern Analysis and Machine Intelligence, Vol. 13, Issue 6 https://doi.org/10.1109/34.87344	journal	June 1991
Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins inArabidopsis Abe, Mitsutomo; Katsumata, Hiroshi; Komeda, Yoshibumi Development, Vol. 130, Issue 4 https://doi.org/10.1242/dev.00292	journal	February 2003
Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object Paganin, D.; Mayo, S. C.; Gureyev, T. E. Journal of Microscopy, Vol. 206, Issue 1 https://doi.org/10.1046/j.1365-2818.2002.01010.x	journal	April 2002
High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll Wuyts, Nathalie; Palauqui, Jean-Christophe; Conejero, Genevieve Plant Methods, Vol. 6, Issue 1 https://doi.org/10.1186/1746-4811-6-17	journal	January 2010
Generic rigidity percolation in two dimensions Jacobs, D. J.; Thorpe, M. F. Physical Review E, Vol. 53, Issue 4 https://doi.org/10.1103/PhysRevE.53.3682	journal	April 1996
Understanding airspace in leaves: 3D anatomy and directional tortuosity Harwood, Richard; Théroux‐Rancourt, Guillaume; Barbour, Margaret M. Plant, Cell & Environment, Vol. 44, Issue 8 https://doi.org/10.1111/pce.14079	journal	May 2021
Why are Sun Leaves Thicker than Shade Leaves? — Consideration based on Analyses of CO2 Diffusion in the Leaf Terashima, Ichiro; Miyazawa, Shin-Ichi; Hanba, Yuko T. Journal of Plant Research, Vol. 114, Issue 1 https://doi.org/10.1007/PL00013972	journal	March 2001
Of puzzles and pavements: a quantitative exploration of leaf epidermal cell shape Vőfély, Róza V.; Gallagher, Joseph; Pisano, Grace D. New Phytologist, Vol. 221, Issue 1 https://doi.org/10.1111/nph.15461	journal	October 2018
Riddled with holes: Understanding air space formation in plant leaves Whitewoods, Christopher D. PLOS Biology, Vol. 19, Issue 12 https://doi.org/10.1371/journal.pbio.3001475	journal	December 2021
A Computational Framework for 3D Mechanical Modeling of Plant Morphogenesis with Cellular Resolution Boudon, Frédéric; Chopard, Jérôme; Ali, Olivier PLoS Computational Biology, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pcbi.1003950	journal	January 2015
Frequency distribution of mechanically stable disk packings Gao, Guo-Jie; Bławzdziewicz, Jerzy; O’Hern, Corey S. Physical Review E, Vol. 74, Issue 6 https://doi.org/10.1103/PhysRevE.74.061304	journal	December 2006
Diurnal changes in xylem pressure and mesophyll cell turgor pressure of the lianaTetrastigma voinierianum: The role of cell turgor in long-distance water transport Th�rmer, F.; Zhu, J. J.; Gierlinger, N. Protoplasma, Vol. 206, Issue 1-3 https://doi.org/10.1007/BF01279262	journal	March 1999
Cell water potential, osmotic potential, and turgor in the epidermis and mesophyll of transpiring leaves Nonami, Hiroshi; Schulze, E. -D. Planta, Vol. 177, Issue 1 https://doi.org/10.1007/BF00392152	journal	January 1989
The Scaling of Genome Size and Cell Size Limits Maximum Rates of Photosynthesis with Implications for Ecological Strategies Roddy, Adam B.; Théroux-Rancourt, Guillaume; Abbo, Tito International Journal of Plant Sciences, Vol. 181, Issue 1 https://doi.org/10.1086/706186	journal	January 2020
Structural Relaxation Made Simple Bitzek, Erik; Koskinen, Pekka; Gähler, Franz Physical Review Letters, Vol. 97, Issue 17 https://doi.org/10.1103/PhysRevLett.97.170201	journal	October 2006
Mesophyll structure during leaf development in Ballota acetabulosa Psaras, G. K.; Rhizopoulou, S. New Phytologist, Vol. 131, Issue 3 https://doi.org/10.1111/j.1469-8137.1995.tb03066.x	journal	November 1995
Shape matters: the pitfalls of analyzing mesophyll anatomy Théroux‐Rancourt, Guillaume; Voggeneder, Klara; Tholen, Danny New Phytologist, Vol. 225, Issue 6 https://doi.org/10.1111/nph.16360	journal	December 2019
Jamming of Deformable Polygons Boromand, Arman; Signoriello, Alexandra; Ye, Fangfu Physical Review Letters, Vol. 121, Issue 24 https://doi.org/10.1103/PhysRevLett.121.248003	journal	December 2018
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
Pathways of Cellular Morphogenesis Green, Paul B. The Journal of Cell Biology, Vol. 27, Issue 2 https://doi.org/10.1083/jcb.27.2.343	journal	November 1965
Bridging particle deformability and collective response in soft solids Treado, John D.; Wang, Dong; Boromand, Arman Physical Review Materials, Vol. 5, Issue 5 https://doi.org/10.1103/PhysRevMaterials.5.055605	journal	May 2021
Structural organization of the spongy mesophyll Borsuk, Aleca M.; Roddy, Adam B.; Théroux‐Rancourt, Guillaume New Phytologist, Vol. 234, Issue 3 https://doi.org/10.1111/nph.17971	journal	February 2022
The effect of humidity and light on cellular water relations and diffusion conductance of leaves ofTradescantia virginiana L. Frensch, J�rgen; Schulze, Ernst-Detlef Planta, Vol. 173, Issue 4 https://doi.org/10.1007/BF00958969	journal	January 1988
A Re-examination of the Root Cortex in Wetland Flowering Plants With Respect to Aerenchyma Seago, James L.; Marsh, Leland C.; Stevens, Kevin J. Annals of Botany, Vol. 96, Issue 4 https://doi.org/10.1093/aob/mci211	journal	August 2005
Hydraulic traits are more diverse in flowers than in leaves Roddy, Adam B.; Jiang, Guo‐Feng; Cao, Kunfang New Phytologist, Vol. 223, Issue 1 https://doi.org/10.1111/nph.15749	journal	March 2019
CLASP balances two competing cell division plane cues during leaf development Zhang, Liyong; Ambrose, Chris Nature Plants, Vol. 8, Issue 6 https://doi.org/10.1038/s41477-022-01163-5	journal	June 2022
Regulator or Driving Force? The Role of Turgor Pressure in Oscillatory Plant Cell Growth Kroeger, Jens H.; Zerzour, Rabah; Geitmann, Anja PLoS ONE, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pone.0018549	journal	April 2011
Structure and Development of the Tobacco leaf Avery, George S. American Journal of Botany, Vol. 20, Issue 9 https://doi.org/10.1002/j.1537-2197.1933.tb08913.x	journal	November 1933
Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity Lehmeier, Christoph; Pajor, Radoslaw; Lundgren, Marjorie R. The Plant Journal, Vol. 92, Issue 6 https://doi.org/10.1111/tpj.13727	journal	November 2017
Hydrodynamics and Cell Volume Oscillations in the Pollen Tube Apical Region are Integral Components of the Biomechanics of Nicotiana tabacum Pollen Tube Growth Zonia, Laura; Müller, Michiel; Munnik, Teun Cell Biochemistry and Biophysics, Vol. 46, Issue 3 https://doi.org/10.1385/CBB:46:3:209	journal	January 2006
Development, Cell Shape, Suberization of Internal Surface, and Abscission in the Leaf of the Valencia Orange, Citrus sinensis Scott, Flora Murray; Schroeder, Mary R.; Turrell, Franklin M. Botanical Gazette, Vol. 109, Issue 4 https://doi.org/10.1086/335493	journal	June 1948
Live imaging of microtubule organization, cell expansion, and intercellular space formation in Arabidopsis leaf spongy mesophyll cells Zhang, Liyong; McEvoy, Delanie; Le, Yen The Plant Cell, Vol. 33, Issue 3 https://doi.org/10.1093/plcell/koaa036	journal	December 2020
Developmental Patterning by Mechanical Signals in Arabidopsis Hamant, O.; Heisler, M. G.; Jonsson, H. Science, Vol. 322, Issue 5908 https://doi.org/10.1126/science.1165594	journal	December 2008
Getting into shape: the mechanics behind plant morphogenesis Eng, Ryan Christopher; Sampathkumar, Arun Current Opinion in Plant Biology, Vol. 46 https://doi.org/10.1016/j.pbi.2018.07.002	journal	December 2018
Relating the mechanics of the primary plant cell wall to morphogenesis Bidhendi, Amir J.; Geitmann, Anja Journal of Experimental Botany, Vol. 67, Issue 2 https://doi.org/10.1093/jxb/erv535	journal	December 2015
Plant cell shape: modulators and measurements Ivakov, Alexander; Persson, Staffan Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00439	journal	January 2013
A lower content of de-methylesterified homogalacturonan improves enzymatic cell separation and isolation of mesophyll protoplasts in Arabidopsis Lionetti, Vincenzo; Cervone, Felice; De Lorenzo, Giulia Phytochemistry, Vol. 112 https://doi.org/10.1016/j.phytochem.2014.07.025	journal	April 2015
Underconstrained jammed packings of nonspherical hard particles: Ellipses and ellipsoids Donev, Aleksandar; Connelly, Robert; Stillinger, Frank H. Physical Review E, Vol. 75, Issue 5 https://doi.org/10.1103/PhysRevE.75.051304	journal	May 2007
Microtubule organization, mesophyll cell morphogenesis, and intercellular space formation inAdiantum capillus veneris leaflets Panteris, E.; Apostolakos, P.; Galatis, B. Protoplasma, Vol. 172, Issue 2-4 https://doi.org/10.1007/BF01379367	journal	June 1993
The Puzzle of the Walnut Shell: A Novel Cell Type with Interlocked Packing Antreich, Sebastian J.; Xiao, Nannan; Huss, Jessica C. Advanced Science, Vol. 6, Issue 16 https://doi.org/10.1002/advs.201900644	journal	June 2019
How to let go: pectin and plant cell adhesion Daher, Firas Bou; Braybrook, Siobhan A. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00523	journal	July 2015
The structural, vibrational, and mechanical properties of jammed packings of deformable particles in three dimensions Wang, Dong; Treado, John D.; Boromand, Arman Soft Matter, Vol. 17, Issue 43 https://doi.org/10.1039/D1SM01228B	journal	January 2021
FluoRender: An application of 2D image space methods for 3D and 4D confocal microscopy data visualization in neurobiology research Wan, Yong; Otsuna, Hideo; Chien, Chi-Bin 2012 IEEE Pacific Visualization Symposium https://doi.org/10.1109/PacificVis.2012.6183592	conference	February 2012
The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging Théroux-Rancourt, Guillaume; Earles, J. Mason; Gilbert, Matthew E. New Phytologist, Vol. 215, Issue 4 https://doi.org/10.1111/nph.14687	journal	July 2017
The epidermal-growth-control theory of stem elongation: An old and a new perspective Kutschera, U.; Niklas, K. J. Journal of Plant Physiology, Vol. 164, Issue 11 https://doi.org/10.1016/j.jplph.2007.08.002	journal	November 2007
Mesophyll porosity is modulated by the presence of functional stomata Lundgren, Marjorie R.; Mathers, Andrew; Baillie, Alice L. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10826-5	journal	June 2019
The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filaments Panteris, Emmanuel; Galatis, Basil New Phytologist, Vol. 167, Issue 3 https://doi.org/10.1111/j.1469-8137.2005.01464.x	journal	June 2005
Direct turgor pressure measurements in individual leaf cells of Tradescantia virginiana Zimmermann, U.; H�sken, D.; Schulze, E. -D. Planta, Vol. 149, Issue 5 https://doi.org/10.1007/BF00385746	journal	October 1980
Maximum CO ₂ diffusion inside leaves is limited by the scaling of cell size and genome size Théroux-Rancourt, Guillaume; Roddy, Adam B.; Earles, J. Mason Proceedings of the Royal Society B: Biological Sciences, Vol. 288, Issue 1945 https://doi.org/10.1098/rspb.2020.3145	journal	February 2021
Computational morphodynamics of plants: integrating development over space and time Roeder, Adrienne H. K.; Tarr, Paul T.; Tobin, Cory Nature Reviews Molecular Cell Biology, Vol. 12, Issue 4 https://doi.org/10.1038/nrm3079	journal	March 2011

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