Control of Leaf Expansion: A Developmental Switch from Metabolics to Hydraulics1[W][OA]

Leaf expansion is the central process by which plants colonize space, allowing energy capture and carbon acquisition. Water and carbon emerge as main limiting factors of leaf expansion, but the literature remains controversial about their respective contributions. Here, we tested the hypothesis that the importance of hydraulics and metabolics is organized according to both dark/light fluctuations and leaf ontogeny. For this purpose, we established the developmental pattern of individual leaf expansion during days and nights in the model plant Arabidopsis (Arabidopsis thaliana). Under control conditions, decreases in leaf expansion were observed at night immediately after emergence, when starch reserves were lowest. These nocturnal decreases were strongly exaggerated in a set of starch mutants, consistent with an early carbon limitation. However, low-light treatment of wild-type plants had no influence on these early decreases, implying that expansion can be uncoupled from changes in carbon availability. From 4 d after leaf emergence onward, decreases of leaf expansion were observed in the daytime. Using mutants impaired in stomatal control of transpiration as well as plants grown under soil water deficit or high air humidity, we gathered evidence that these diurnal decreases were the signature of a hydraulic limitation that gradually set up as the leaf developed. Changes in leaf turgor were consistent with this pattern. It is concluded that during the course of leaf ontogeny, the predominant control of leaf expansion switches from metabolics to hydraulics. We suggest that the leaf is better armed to buffer variations in the former than in the latter.

[1]  Y. Gibon,et al.  Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. , 2011, Journal of experimental botany.

[2]  J. Kikuchi,et al.  The circadian clock modulates water dynamics and aquaporin expression in Arabidopsis roots. , 2011, Plant & cell physiology.

[3]  F. Tardieu,et al.  Floret initiation, tissue expansion and carbon availability at the meristem of the sunflower capitulum as affected by water or light deficits. , 2011, The New phytologist.

[4]  Robert Turgeon,et al.  The developmental dynamics of the maize leaf transcriptome , 2010, Nature Genetics.

[5]  M. Stitt,et al.  Arabidopsis Plants Acclimate to Water Deficit at Low Cost through Changes of Carbon Usage: An Integrated Perspective Using Growth, Metabolite, Enzyme, and Gene Expression Analysis1[C][W][OA] , 2010, Plant Physiology.

[6]  A. Nardini,et al.  Leafminers help us understand leaf hydraulic design. , 2010, Plant, cell & environment.

[7]  K. Al-Rasheid,et al.  Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. , 2010, The Plant journal : for cell and molecular biology.

[8]  Mark Stitt,et al.  Circadian control of carbohydrate availability for growth in Arabidopsis plants at night , 2010, Proceedings of the National Academy of Sciences.

[9]  Nima Yazdanbakhsh,et al.  Analysis of Arabidopsis thaliana root growth kinetics with high temporal and spatial resolution. , 2010, Annals of botany.

[10]  F. Tardieu,et al.  Dissection and modelling of abiotic stress tolerance in plants. , 2010, Current opinion in plant biology.

[11]  F. Tardieu,et al.  Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes? , 2010, Plant, cell & environment.

[12]  Ulrich Schurr,et al.  Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects , 2010, Journal of experimental botany.

[13]  M. R. Thorpe,et al.  Root cooling strongly affects diel leaf growth dynamics, water and carbohydrate relations in Ricinus communis. , 2010, Plant, cell & environment.

[14]  B. Usadel,et al.  Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis , 2009, Molecular systems biology.

[15]  M. Stitt,et al.  Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. , 2009, Plant, cell & environment.

[16]  Joachim Selbig,et al.  Starch as a major integrator in the regulation of plant growth , 2009, Proceedings of the National Academy of Sciences.

[17]  L. Poorter,et al.  Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. , 2009, The New phytologist.

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

[19]  François Tardieu,et al.  Aquaporin-Mediated Reduction in Maize Root Hydraulic Conductivity Impacts Cell Turgor and Leaf Elongation Even without Changing Transpiration1[W] , 2009, Plant Physiology.

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

[21]  Paul-Henry Cournède,et al.  A model-based analysis of the dynamics of carbon balance at the whole-plant level in Arabidopsis thaliana. , 2008, Functional plant biology : FPB.

[22]  André Lacointe,et al.  Modelling phloem and xylem transport within a complex architecture. , 2008, Functional plant biology : FPB.

[23]  Robert B. Heinen,et al.  The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation , 2008, Plant Molecular Biology.

[24]  J. Boyer,et al.  Xylem tension affects growth-induced water potential and daily elongation of maize leaves. , 2008, Journal of experimental botany.

[25]  M. Stitt,et al.  Coordination of carbon supply and plant growth. , 2007, Plant, cell & environment.

[26]  T. Brodribb,et al.  Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics1[W][OA] , 2007, Plant Physiology.

[27]  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.

[28]  M. Stitt,et al.  Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment. , 2007, Functional plant biology : FPB.

[29]  A. To,et al.  The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. , 2007, The Plant journal : for cell and molecular biology.

[30]  D. Bergmann,et al.  Stomatal development. , 2007, Annual review of plant biology.

[31]  L. Schreiber,et al.  Cuticular permeance in relation to wax and cutin development along the growing barley (Hordeum vulgare) leaf , 2007, Planta.

[32]  C. Granier,et al.  Plasticity to soil water deficit in Arabidopsis thaliana: dissection of leaf development into underlying growth dynamic and cellular variables reveals invisible phenotypes. , 2006, Plant, cell & environment.

[33]  Pierre Tocquin,et al.  Leaf carbohydrate controls over Arabidopsis growth and response to elevated CO2: an experimentally based model. , 2006, The New phytologist.

[34]  G. Kerstiens.  Water transport in plant cuticles: an update. , 2006, Journal of experimental botany.

[35]  F. Tardieu,et al.  Leaf growth and turgor in growing cells of maize (Zea mays L.) respond to evaporative demand under moderate irrigation but not in water-saturated soil. , 2006, Plant, cell & environment.

[36]  C. Granier,et al.  A dynamic analysis of the shade-induced plasticity in Arabidopsis thaliana rosette leaf development reveals new components of the shade-adaptative response. , 2006, Annals of botany.

[37]  E. Nambara,et al.  Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. , 2006, The Plant journal : for cell and molecular biology.

[38]  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.

[39]  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.

[40]  Anthony Hall,et al.  Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage , 2005, Science.

[41]  A. Nardini,et al.  Circadian regulation of leaf hydraulic conductance in sunflower (Helianthus annuus L. cv Margot) , 2005 .

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

[43]  Hervé Cochard,et al.  Hydraulic architecture of leaf blades: where is the main resistance? , 2004 .

[44]  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.

[45]  D. Thorneycroft,et al.  A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. , 2004, The Plant journal : for cell and molecular biology.

[46]  Alison M. Smith,et al.  A Previously Unknown Maltose Transporter Essential for Starch Degradation in Leaves , 2004, Science.

[47]  E. Schulze,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS , 1993, Planta.

[48]  E. Schulze,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS , 1992, Planta.

[49]  M. Pigliucci,et al.  Phenotypic plasticity to light intensity in Arabidopsis thaliana: invariance of reaction norms and phenotypic integration , 2004, Evolutionary Ecology.

[50]  T. Sharkey,et al.  The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells , 2004, Planta.

[51]  F. Tardieu,et al.  Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings , 2002 .

[52]  H. Griffiths,et al.  Plant responses to water stress. , 2002, Annals of botany.

[53]  M. Steup,et al.  The starch-related R1 protein is an α-glucan, water dikinase , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Karine Chenu,et al.  Individual leaf development in Arabidopsis thaliana: a stable thermal-time-based programme. , 2002, Annals of botany.

[55]  J. Boyer,et al.  Growth-induced water potentials and the growth of maize leaves. , 2002, Journal of experimental botany.

[56]  M. Steup,et al.  The starch-related R1 protein is an alpha -glucan, water dikinase. , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[57]  J. Durand,et al.  Quantitative Analysis of Vasculature in the Leaves of Festuca arundinacea (Poaceae): Implications for Axial Water Transport , 2001, International Journal of Plant Sciences.

[58]  F. Tardieu,et al.  The elongation rate at the base of a maize leaf shows an invariant pattern during both the steady-state elongation and the establishment of the elongation zone. , 2001, Journal of experimental botany.

[59]  J. Durand,et al.  Hydraulic architecture and water flow in growing grass tillers (Festuca arundinacea Schreb.) , 2001 .

[60]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[61]  E. Groot,et al.  Short‐Day‐Grown Arabidopsis thaliana Satisfies the Assumptions of the Plastochron Index as a Time Variable in Development , 2000, International Journal of Plant Sciences.

[62]  U. Schurr,et al.  Leaf development in Ricinus communis during drought stress: dynamics of growth processes, of cellular structure and of sink-source transition. , 2000, Journal of experimental botany.

[63]  F. Tardieu,et al.  Spatial distributions of expansion rate, cell division rate and cell size in maize leaves: a synthesis of the effects of soil water status, evaporative demand and temperature. , 2000, Journal of experimental botany.

[64]  J. Durand,et al.  Changes in axial hydraulic conductivity along elongating leaf blades in relation to xylem maturation in tall fescue. , 2000, The New phytologist.

[65]  Leaf expansion and cell division are affected by reducing absorbed light before but not after the decline in cell division rate in the sunflower leaf , 1999 .

[66]  E. Steudle,et al.  Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus , 1999, Planta.

[67]  E. Komor,et al.  Assimilate export by leaves of Ricinus communis L. growing under normal and elevated carbon dioxide concentrations: the same rate during the day, a different rate at night , 1999, Planta.

[68]  John Clifton-Brown,et al.  Alteration of transpiration rate, by changing air vapour pressure deficit, influences leaf extension rate transiently in Miscanthus , 1999 .

[69]  François Tardieu,et al.  Modelling leaf expansion in a fluctuating environment: are changes in specific leaf area a consequence of changes in expansion rate? , 1999 .

[70]  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.

[71]  F. Tardieu,et al.  Control of Leaf Expansion Rate of Droughted Maize Plants under Fluctuating Evaporative Demand (A Superposition of Hydraulic and Chemical Messages?) , 1997, Plant physiology.

[72]  F. Tardieu,et al.  Quantitative analysis of the combined effects of temperature, evaporative demand and light on leaf elongation rate in well-watered field and laboratory-grown maize plants , 1996 .

[73]  I. Rademacher,et al.  Drought effects on cellular and spatial parameters of leaf growth in tall fescue , 1995 .

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

[75]  M. R. Thorpe,et al.  A Simple Mechanistic Model of Phloem Transport which Explains Sink Priority , 1993 .

[76]  A. Pradet,et al.  Study of glucose starvation in excised maize root tips. , 1991, Plant physiology.

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

[78]  Robert Turgeon,et al.  The Sink-Source Transition in Leaves , 1989 .

[79]  J. Boyer.  Cell enlargement and growth-induced water potentials , 1988 .

[80]  C. J. Nelson,et al.  Diurnal growth of tall fescue leaf blades : I. Spatial distribution of growth, deposition of water, and assimilate import in the elongation zone. , 1988, Plant physiology.

[81]  J. E. Dale,et al.  The Control of Leaf Expansion , 1988 .

[82]  J. Rozema,et al.  An Ecophysiological Comparison of Measurements of the Diurnal Rhythm of the Leaf Elongation and Changes of the Leaf Thickness of Salt-resistant Dicotyledonae and Monocotyledonae , 1987 .

[83]  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.

[84]  Dale Je.  The carbon relations of the developing leaf. , 1985 .

[85]  N. J. Chatterton,et al.  Photosynthate Partitioning into Starch in Soybean Leaves: II. IRRADIANCE LEVEL AND DAILY PHOTOSYNTHETIC PERIOD DURATION EFFECTS. , 1981, Plant physiology.

[86]  J. M. Cutler,et al.  Dynamic aspects and enhancement of leaf elongation in rice. , 1980, Plant physiology.

[87]  R. A. Christ.  The Elongation Rate of Wheat Leaves II. EFFECT OF SUDDEN LIGHT CHANGE ON THE ELONGATION RATE , 1978 .

[88]  J. Monteith.  Climate and the efficiency of crop production in Britain , 1977 .

[89]  N. Boardman.  Comparative photosynthesis of sun and shade plants. , 1977 .

[90]  K. Brown,et al.  Leaf Age as a Determinant in Stomatal Control of Water Loss from Cotton during Water Stress. , 1975, Plant physiology.

[91]  D W Henderson,et al.  Immediate and subsequent growth responses of maize leaves to changes in water status. , 1971, Plant physiology.

[92]  J. Boyer,et al.  Relationship of water potential to growth of leaves. , 1968, Plant physiology.

[93]  J. Lockhart.  An analysis of irreversible plant cell elongation. , 1965, Journal of theoretical biology.

[94]  T. H. Honert,et al.  Water transport in plants as a catenary process , 1948 .