Computational Method for Quantifying Growth Patterns at the Adaxial Leaf Surface in Three Dimensions1[W][OA]

Growth patterns vary in space and time as an organ develops, leading to shape and size changes. Quantifying spatiotemporal variations in organ growth throughout development is therefore crucial to understand how organ shape is controlled. We present a novel method and computational tools to quantify spatial patterns of growth from three-dimensional data at the adaxial surface of leaves. Growth patterns are first calculated by semiautomatically tracking microscopic fluorescent particles applied to the leaf surface. Results from multiple leaf samples are then combined to generate mean maps of various growth descriptors, including relative growth, directionality, and anisotropy. The method was applied to the first rosette leaf of Arabidopsis (Arabidopsis thaliana) and revealed clear spatiotemporal patterns, which can be interpreted in terms of gradients in concentrations of growth-regulating substances. As surface growth is tracked in three dimensions, the method is applicable to young leaves as they first emerge and to nonflat leaves. The semiautomated software tools developed allow for a high throughput of data, and the algorithms for generating mean maps of growth open the way for standardized comparative analyses of growth patterns.

[1]  E. Coen,et al.  Genetic Control of Surface Curvature , 2003, Science.

[2]  R. Maksymowych QUANTITATIVE ANALYSIS OF LEAF DEVELOPMENT IN XANTHIUM PENSYLVANICUM , 1959 .

[3]  M. M. Christ,et al.  Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. , 2007, The New phytologist.

[4]  U. Schurr,et al.  Environmental effects on spatial and temporal patterns of leaf and root growth. , 2009, Annual review of plant biology.

[5]  Y. Couder,et al.  Developmental Patterning by Mechanical Signals in Arabidopsis , 2009 .

[6]  G. S. Avery, STRUCTURE AND DEVELOPMENT OF THE TOBACCO LEAF , 1933 .

[7]  J. Micol Leaf development: time to turn over a new leaf? , 2009, Current opinion in plant biology.

[8]  J. Possingham,et al.  Studies on the Growth of Spinach Leaves (Spinacea oleracea) , 1970 .

[9]  M. M. Christ Temporal and spatial patterns of growth and photosynthesis in leaves of dicotyledonous plants under long-term CO2- and O3-exposure , 2005 .

[10]  AN ANALYSIS OF LEAF ELONGATION IN XANTHIUM PENSYLVANICUM PRESENTED IN RELATIVE ELEMENTAL RATES , 1962 .

[11]  Hirokazu Tsukaya,et al.  Mechanism of leaf-shape determination. , 2006, Annual review of plant biology.

[12]  U. Schurr,et al.  Glycine max leaflets lack a base-tip gradient in growth rate , 2005, Journal of Plant Research.

[13]  David Strutt Organ Shape: Controlling Oriented Cell Division , 2005, Current Biology.

[14]  Stijn Dhondt,et al.  Whole organ, venation and epidermal cell morphological variations are correlated in the leaves of Arabidopsis mutants. , 2011, Plant, cell & environment.

[15]  Konrad Walus,et al.  Delivering high-resolution landmarks using inkjet micropatterning for spatial monitoring of leaf expansion , 2011, Plant Methods.

[16]  D. Leister,et al.  Large-scale evaluation of plant growth in Arabidopsis thaliana by non-invasive image analysis , 1999 .

[17]  V. Ntziachristos Going deeper than microscopy: the optical imaging frontier in biology , 2010, Nature Methods.

[18]  U. Schurr,et al.  Expansion kinematics are an intrinsic property of leaf development and are scaled from cell to leaf level at different nutrient availabilities , 2003 .

[19]  C. Granier,et al.  Spatial and temporal analyses of expansion and cell cycle in sunflower leaves. A common pattern of development for all zones of a leaf and different leaves of a plant , 1998, Plant physiology.

[20]  H. Tsukaya,et al.  The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. , 2010, Plant & cell physiology.

[21]  R. O. Erickson,et al.  Relative Elemental Rates and Anisotropy of Growth in Area: a Computer Programme , 1966 .

[22]  Y. Couder,et al.  Constitutive property of the local organization of leaf venation networks. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[23]  J. Dumais,et al.  Analysis of surface growth in shoot apices. , 2002, The Plant journal : for cell and molecular biology.

[24]  Anne-Gaëlle Rolland-Lagan,et al.  Quantifying leaf venation patterns: two-dimensional maps. , 2009, The Plant journal : for cell and molecular biology.

[25]  D. Cosgrove Growth of the plant cell wall , 2005, Nature Reviews Molecular Cell Biology.

[26]  Richard Kennaway,et al.  Generation of Diverse Biological Forms through Combinatorial Interactions between Tissue Polarity and Growth , 2011, PLoS Comput. Biol..

[27]  R. Plant,et al.  Quantitative patterns of leaf expansion: comparison of normal and malformed leaf growth in Vitis vinifera cv. Ruby Red , 1986 .

[28]  P. B. Green,et al.  Quantitative Analysis of Surface Growth , 1986, Botanical Gazette.

[29]  Jens Timmer,et al.  Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. , 2007, Developmental cell.

[30]  Q. Cronk The Molecular Organography of Plants , 2009 .

[31]  U. Schurr,et al.  The modular character of growth in Nicotiana tabacum plants under steady-state nutrition , 1999 .

[32]  H. Tsukaya,et al.  Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. , 1996, Development.

[33]  B. Jähne,et al.  Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis , 1998 .

[34]  P. Prusinkiewicz,et al.  The genetics of geometry. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Derek W. R. White,et al.  PEAPOD regulates lamina size and curvature in Arabidopsis , 2006, Proceedings of the National Academy of Sciences.

[36]  P. Piazza,et al.  Evolution of leaf developmental mechanisms. , 2005, The New phytologist.

[37]  Oscar W. Richards,et al.  The Analysis of the Relative Growth Gradients and Changing Form of Growing Organisms: Illustrated by the Tobacco Leaf , 1943, The American Naturalist.

[38]  I. Sussex,et al.  The developmental morphology and growth dynamics of the tobacco leaf , 1985, Planta.

[39]  F. Miglietta,et al.  Spatial and Temporal Effects of Free-Air CO2Enrichment (POPFACE) on Leaf Growth, Cell Expansion, and Cell Production in a Closed Canopy of Poplar1 , 2003, Plant Physiology.

[40]  Arezki Boudaoud,et al.  In silico leaf venation networks: growth and reorganization driven by mechanical forces. , 2009, Journal of theoretical biology.

[41]  Bernd Rinn,et al.  Probing the Reproducibility of Leaf Growth and Molecular Phenotypes: A Comparison of Three Arabidopsis Accessions Cultivated in Ten Laboratories1[W] , 2010, Plant Physiology.

[42]  Markus Langhans,et al.  Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis , 2003, Planta.

[43]  T. Sebo,et al.  Digital image analysis. , 1995, Mayo Clinic proceedings.

[44]  T. Baskin Anisotropic expansion of the plant cell wall. , 2005, Annual review of cell and developmental biology.

[45]  J. Friml,et al.  Control of leaf vascular patterning by polar auxin transport. , 2006, Genes & development.