Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle.

Leaf growth dynamics are driven by diel rhythms. The analysis of spatio-temporal leaf growth patterns in Arabidopsis thaliana wild type and mutants of interest is a promising approach to elucidate molecular mechanisms controlling growth. The diel availability of carbohydrates is thought to affect diel growth. A digital image sequence processing (DISP)-based noninvasive technique for visualizing and quantifying highly resolved spatio-temporal leaf growth was adapted for the model plant A. thaliana. Diel growth patterns were analysed for the wild type and for a mutant with altered diel carbohydrate metabolism. A. thaliana leaves showed highest relative growth rates (RGRs) at dawn and lowest RGRs at the beginning of the night. Along the lamina, a clear basipetal gradient of growth rate distribution was found, similar to that in many other dicotyledonous species. The starch-free 1 (stf1) mutant revealed changed temporal growth patterns with reduced nocturnal, and increased afternoon, growth activity. The established DISP technique is presented as a valuable tool to detect altered temporal growth patterns in A. thaliana mutants. Endogenous changes in the diel carbohydrate availability of the starch-free mutant clearly affected its diel growth rhythms.

[1]  Gerrit T.S. Beemster,et al.  Variation in Growth Rate between Arabidopsis Ecotypes Is Correlated with Cell Division and A-Type Cyclin-Dependent Kinase Activity1 , 2002, Plant Physiology.

[2]  F. Tardieu,et al.  Temperature Affects Expansion Rate of Maize Leaves without Change in Spatial Distribution of Cell Length (Analysis of the Coordination between Cell Division and Cell Expansion) , 1995, Plant physiology.

[3]  J. Keurentjes,et al.  Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[4]  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 .

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

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

[7]  Xiao-Ming Yu,et al.  Photosynthetic Carbon Metabolism and Translocation in Wild-Type and Starch-Deficient Mutant Nicotiana sylvestris L , 1995, Plant physiology.

[8]  J. Fisahn,et al.  Transgenic plants changed in carbon allocation pattern display a shift in diurnal growth pattern. , 1998, The Plant journal : for cell and molecular biology.

[9]  François Tardieu,et al.  Root elongation rate is accounted for by intercepted PPFD and source‐sink relations in field and laboratory‐grown sunflower , 1994 .

[10]  Y. Fujiki,et al.  Multiple signaling pathways in gene expression during sugar starvation. Pharmacological analysis of din gene expression in suspension-cultured cells of Arabidopsis. , 2000, Plant physiology.

[11]  E. Baena-González,et al.  Sugar sensing and signaling in plants: conserved and novel mechanisms. , 2006, Annual review of plant biology.

[12]  R. H. Goodwin,et al.  GROWTH AND DIFFERENTIATION IN THE ROOT TIP OF PHLEUM PRATENSE , 1945 .

[13]  O. H. Lowry,et al.  Enzymic Assay of 10−7 to 10−14 Moles of Sucrose in Plant Tissues , 1977 .

[14]  Ulrich Schurr,et al.  Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth , 2006, Planta.

[15]  Gerrit T.S. Beemster,et al.  Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L.): kinematic analysis of leaf elongation , 1996 .

[16]  U. Schurr,et al.  Restriction of nyctinastic movements and application of tensile forces to leaves affects diurnal patterns of expansion growth. , 2002, Functional plant biology : FPB.

[17]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[18]  Ulrich Schurr,et al.  Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity. , 2006, Plant, cell & environment.

[19]  F. Tardieu,et al.  Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots , 1998 .

[20]  S. Huber,et al.  Carbon Partitioning and Growth of a Starchless Mutant of Nicotiana sylvestris. , 1992, Plant physiology.

[21]  K. Nakamura,et al.  Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for beta-amylase and on the accumulation of anthocyanin that are inducible by sugars. , 1997, The Plant journal : for cell and molecular biology.

[22]  P. Prusinkiewicz.  Modeling plant growth and development. , 2004, Current opinion in plant biology.

[23]  Yves Gibon,et al.  Sugars and Circadian Regulation Make Major Contributions to the Global Regulation of Diurnal Gene Expression in Arabidopsis[W][OA] , 2005, The Plant Cell Online.

[24]  Ulrich Schurr,et al.  Dynamics of leaf and root growth: endogenous control versus environmental impact. , 2005, Annals of botany.

[25]  K. Chenu,et al.  PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. , 2006, The New phytologist.

[26]  H. Tsukaya,et al.  Cell cycling and cell enlargement in developing leaves of Arabidopsis. , 1999, Developmental biology.

[27]  Sjef Smeekens,et al.  SUGAR-INDUCED SIGNAL TRANSDUCTION IN PLANTS. , 2000, Annual review of plant physiology and plant molecular biology.

[28]  Donald R. Geiger,et al.  Diurnal Regulation of Photosynthetic Carbon Metabolism in C3 Plants , 1994 .

[29]  T. Okita,et al.  Interactions of Nitrate and CO2 Enrichment on Growth, Carbohydrates, and Rubisco in Arabidopsis Starch Mutants. Significance of Starch and Hexose1 , 2002, Plant Physiology.

[30]  S. Zeeman,et al.  A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. , 1998, The Plant journal : for cell and molecular biology.

[31]  J. Preiss,et al.  Mutants of Arabidopsis with altered regulation of starch degradation. , 1991, Plant physiology.

[32]  D. Inzé,et al.  Genome-Wide Analysis of Gene Expression Profiles Associated with Cell Cycle Transitions in Growing Organs of Arabidopsis1[w] , 2005, Plant Physiology.

[33]  Filip Rolland,et al.  Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling , 2003, Science.

[34]  Hanno Scharr,et al.  Dynamics of leaf and root growth , 2001 .

[35]  P. León,et al.  Hexokinase as a sugar sensor in higher plants. , 1997, The Plant cell.

[36]  J. Fisahn,et al.  Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. , 2004, The Plant journal : for cell and molecular biology.

[37]  E. Schulze,et al.  A Quantification of the Significance of Assimilatory Starch for Growth of Arabidopsis thaliana L. Heynh. , 1991, Plant physiology.

[38]  W. Silk,et al.  Quantitative Descriptions of Development , 1984 .

[39]  T. Baskin,et al.  Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. , 1998, Plant physiology.

[40]  A. Weber,et al.  Molecular characterisation of a new mutant allele of the plastid phosphoglucomutase in Arabidopsis, and complementation of the mutant with the wild-type cDNA , 2000, Molecular and General Genetics MGG.

[41]  M. M. Christ,et al.  The effect of elevated CO2 on diel leaf growth cycle, leaf carbohydrate content and canopy growth performance of Populus deltoides , 2005 .

[42]  C. Somerville,et al.  Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity. , 1985, Plant physiology.

[43]  Loren L Looger,et al.  Conversion of a Putative Agrobacterium Sugar-binding Protein into a FRET Sensor with High Selectivity for Sucrose* , 2006, Journal of Biological Chemistry.

[44]  P. Perata,et al.  Digital Object Identifier (DOI) 10.1007/s10265-005-0251-1 REGULAR PAPER , 2022 .

[45]  R. O. Erickson,et al.  Kinematics of plant growth. , 1979, Journal of theoretical biology.