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Structural assessment of the impact of environmental constraints on arabidopsis thaliana leaf growth: A 3D approach

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Wuyts, Nathalie [UCL] Massonnet, Catherine [Laboratoire d'Ecophysiologie des Plantes sous Stress Environnementaux, INRA-SupAgro, Montpellier, France] Dauzat, Myriam [Laboratoire d'Ecophysiologie des Plantes sous Stress Environnementaux, INRA-SupAgro, Montpellier, France] Granier, Christine [Laboratoire d'Ecophysiologie des Plantes sous Stress Environnementaux, INRA-SupAgro, Montpellier, France]

Light and soil water content affect leaf surface area expansion through modifications in epidermal cell numbers and area, while effects on leaf thickness and mesophyll cell volumes are far less documented. Here, three-dimensional imaging was applied in a study of Arabidopsis thaliana leaf growth to determine leaf thickness and the cellular organization of mesophyll tissues under moderate soil water deficit and two cumulative light conditions. In contrast to surface area, thickness was highly conserved in response to water deficit under both low and high cumulative light regimes. Unlike epidermal and palisade mesophyll tissues, no reductions in cell number were observed in the spongy mesophyll; cells had rather changed in volume and shape. Furthermore, leaf features of a selection of genotypes affected in leaf functioning were analysed. The low-starch mutant pgm had very thick leaves because of unusually large palisade mesophyll cells, together with high levels of photosynthesis and stomatal conductance. By means of an open stomata mutant and a 9-cis-epoxycarotenoid dioxygenase overexpressor, it was shown that stomatal conductance does not necessarily have a major impact on leaf dimensions and cellular organization, pointing to additional mechanisms for the control of CO2 diffusion under high and low stomatal conductance, respectively. © 2012 Blackwell Publishing Ltd.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2012
Language Anglais
Journal information "Plant, Cell and Environment" - Vol. 35, no. 9, p. 1631-1646 (2012)
Peer reviewed yes
Publisher Wiley-Blackwell Publishing Ltd.
e-issn 1365-3040
issn 0140-7791
Publication status Publié
Affiliation UCL - SST/ELI/ELIA - Agronomy
Links
  1. AGUIRREZABAL LUIS, BOUCHIER-COMBAUD SANDRINE, RADZIEJWOSKI AMANDINE, DAUZAT MYRIAM, COOKSON SARAH JANE, GRANIER CHRISTINE, Plasticity to soil water deficit in Arabidopsis thaliana: dissection of leaf development into underlying growth dynamic and cellular variables reveals invisible phenotypes, 10.1111/j.1365-3040.2006.01595.x
  2. Bogeat-Triboulot M.-B., Brosche M., Renaut J., Jouve L., Le Thiec D., Fayyaz P., Vinocur B., Witters E., Laukens K., Teichmann T., Altman A., Hausman J.-F., Polle A., Kangasjarvi J., Dreyer E., Gradual Soil Water Depletion Results in Reversible Changes of Gene Expression, Protein Profiles, Ecophysiology, and Growth Performance in Populus euphratica, a Poplar Growing in Arid Regions, 10.1104/pp.106.088708
  3. Boyes D. C., Growth Stage-Based Phenotypic Analysis of Arabidopsis: A Model for High Throughput Functional Genomics in Plants, 10.1105/tpc.13.7.1499
  4. Caspar T., Huber S. C., Somerville C., Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity, 10.1104/pp.79.1.11
  5. Casson Stuart, Gray Julie E., Influence of environmental factors on stomatal development, 10.1111/j.1469-8137.2007.02351.x
  6. Casson Stuart A, Hetherington Alistair M, Environmental regulation of stomatal development, 10.1016/j.pbi.2009.08.005
  7. COOKSON SARAH J., VAN LIJSEBETTENS MIEKE, GRANIER CHRISTINE, Correlation between leaf growth variables suggest intrinsic and early controls of leaf size in Arabidopsis thaliana, 10.1111/j.1365-3040.2005.01368.x
  8. COOKSON S. J., A Dynamic Analysis of the Shade-induced Plasticity in Arabidopsis thaliana Rosette Leaf Development Reveals New Components of the Shade-adaptative Response, 10.1093/aob/mcj047
  9. Cookson Sarah Jane, Chenu Karine, Granier Christine, Day Length Affects the Dynamics of Leaf Expansion and Cellular Development in Arabidopsis thaliana Partially through Floral Transition Timing, 10.1093/aob/mcm005
  10. Cornic Gabriel, Drought stress inhibits photosynthesis by decreasing stomatal aperture – not by affecting ATP synthesis, 10.1016/s1360-1385(00)01625-3
  11. Davies William J., Wilkinson Sally, Loveys Brian, Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture, 10.1046/j.0028-646x.2001.00345.x
  12. Dengler Nancy G., Comparative histological basis of sun and shade leaf dimorphism in Helianthus annuus, 10.1139/b80-092
  13. Evans J. R., Kaldenhoff R., Genty B., Terashima I., Resistances along the CO2 diffusion pathway inside leaves, 10.1093/jxb/erp117
  14. Fabre Juliette, Dauzat Myriam, Nègre Vincent, Wuyts Nathalie, Tireau Anne, Gennari Emilie, Neveu Pascal, Tisné Sébastien, Massonnet Catherine, Hummel Irène, Granier Christine, PHENOPSIS DB: an Information System for Arabidopsis thaliana phenotypic data in an environmental context, 10.1186/1471-2229-11-77
  15. FLEXAS J., Drought-inhibition of Photosynthesis in C3 Plants: Stomatal and Non-stomatal Limitations Revisited, 10.1093/aob/mcf027
  16. Flexas J., Bota J., Loreto F., Cornic G., Sharkey T. D., Diffusive and Metabolic Limitations to Photosynthesis under Drought and Salinity in C3Plants, 10.1055/s-2004-820867
  17. Flexas J., Ribas-Carbo M., Bota J., Galmes J., Henkle M., Martinez-Canellas S., Medrano H., Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration, 10.1111/j.1469-8137.2006.01794.x
  18. Giakountis A., Cremer F., Sim S., Reymond M., Schmitt J., Coupland G., Distinct Patterns of Genetic Variation Alter Flowering Responses of Arabidopsis Accessions to Different Daylengths, 10.1104/pp.109.140772
  19. Granier Christine, Tardieu François, Water Deficit and Spatial Pattern of Leaf Development. Variability in Responses Can Be Simulated Using a Simple Model of Leaf Development, 10.1104/pp.119.2.609
  20. Granier Christine, Aguirrezabal Luis, Chenu Karine, Cookson Sarah Jane, Dauzat Myriam, Hamard Philippe, Thioux Jean-Jacques, Rolland Gaëlle, Bouchier-Combaud Sandrine, Lebaudy Anne, Muller Bertrand, Simonneau Thierry, Tardieu François, PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit inArabidopsis thalianapermitted the identification of an accession with low sensitivity to soil water deficit, 10.1111/j.1469-8137.2005.01609.x
  21. GRANIER CHRISTINE, TARDIEU FRANÇOIS, Multi-scale phenotyping of leaf expansion in response to environmental changes: the whole is more than the sum of parts, 10.1111/j.1365-3040.2009.01955.x
  22. Hoffmann-Benning S., Willmitzer L., Fisahn J., Analysis of growth, composition and thickness of the cell walls of transgenic tobacco plants expressing a yeast-derived invertase, 10.1007/bf01283290
  23. Hummel Irène, Pantin Florent, Sulpice Ronan, Piques Maria, Rolland Gaëlle, Dauzat Myriam, Christophe Angélique, Pervent Marjorie, Bouteillé Marie, Stitt Mark, Gibon Yves, Muller Bertrand, Arabidopsis Plants Acclimate to Water Deficit at Low Cost through Changes of Carbon Usage: An Integrated Perspective Using Growth, Metabolite, Enzyme, and Gene Expression Analysis, 10.1104/pp.110.157008
  24. Jung G., Wernicke W., Cell shaping and microtubules in developing mesophyll of wheat (Triticum aestivum L.), 10.1007/bf01353998
  25. Kaiser Werner M., Effects of water deficit on photosynthetic capacity, 10.1111/j.1399-3054.1987.tb04631.x
  26. Kampstra, Journal of Statistical Software, Code Snippets, 28, 1 (2008)
  27. Keller Ruth, Brearley Charles A., Trethewey Richard N., Muller-Rober Bernd, Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol 3-phosphate synthase, 10.1046/j.1365-313x.1998.00309.x
  28. Kim Gyung-Tae, Yano Satoshi, Kozuka Toshiaki, Tsukaya Hirokazu, Photomorphogenesis of leaves: shade-avoidance and differentiation of sun and shade leaves, 10.1039/b418440h
  29. Lee, Journal of the American Society for Horticultural Science, 116, 646 (1991)
  30. Lee David W., Oberbauer Steven F., Johnson Paulette, Krishnapilay Baskaran, Mansor Marzalina, Mohamad Haris, Yap Son Kheong, Effects of Irradiance and Spectral Quality on Leaf Structure and Function in Seedlings of Two Southeast Asian Hopea (Dipterocarpaceae) Species, 10.2307/2656588
  31. Lefebvre Valérie, North Helen, Frey Anne, Sotta Bruno, Seo Mitsunori, Okamoto Masanori, Nambara Eiji, Marion-Poll Annie, Functional analysis of ArabidopsisNCED6andNCED9genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy, 10.1111/j.1365-313x.2005.02622.x
  32. Marcotrigiano M., A role for leaf epidermis in the control of leaf size and the rate and extent of mesophyll cell division, 10.3732/ajb.0900102
  33. Merlot Sylvain, Mustilli Anna-Chiara, Genty Bernard, North Helen, Lefebvre Valerie, Sotta Bruno, Vavasseur Alain, Giraudat Jerome, Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation, 10.1046/j.1365-313x.2002.01322.x
  34. Merlot Sylvain, Leonhardt Nathalie, Fenzi Francesca, Valon Christiane, Costa Miguel, Piette Laurie, Vavasseur Alain, Genty Bernard, Boivin Karine, Müller Axel, Giraudat Jérôme, Leung Jeffrey, Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure, 10.1038/sj.emboj.7601750
  35. Morillon R., Chrispeels M. J., The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells, 10.1073/pnas.231471998
  36. Panteris Emmanuel, Galatis Basil, The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filaments : Research review, 10.1111/j.1469-8137.2005.01464.x
  37. Parent B., Hachez C., Redondo E., Simonneau T., Chaumont F., Tardieu F., Drought and Abscisic Acid Effects on Aquaporin Content Translate into Changes in Hydraulic Conductivity and Leaf Growth Rate: A Trans-Scale Approach, 10.1104/pp.108.130682
  38. Rasband, ImageJ (19972011)
  39. R Development Core Team, R: A Language and Environment for Statistical Computing (2010)
  40. Sack Lawren, Holbrook N. Michele, LEAF HYDRAULICS, 10.1146/annurev.arplant.56.032604.144141
  41. Sancho-Knapik Domingo, Álvarez-Arenas Tomás Gómez, Peguero-Pina José Javier, Fernández Victoria, Gil-Pelegrín Eustaquio, Relationship between ultrasonic properties and structural changes in the mesophyll during leaf dehydration, 10.1093/jxb/err065
  42. Savaldi-Goldstein Sigal, Chory Joanne, Growth coordination and the shoot epidermis, 10.1016/j.pbi.2007.10.009
  43. Scippa G. S., The histone-like protein H1-S and the response of tomato leaves to water deficit, 10.1093/jxb/erh022
  44. Skirycz Aleksandra, Vandenbroucke Korneel, Clauw Pieter, Maleux Katrien, De Meyer Bjorn, Dhondt Stijn, Pucci Anna, Gonzalez Nathalie, Hoeberichts Frank, Tognetti Vanesa B, Galbiati Massimo, Tonelli Chiara, Van Breusegem Frank, Vuylsteke Marnik, Inzé Dirk, Survival and growth of Arabidopsis plants given limited water are not equal, 10.1038/nbt.1800
  45. Streb S., Egli B., Eicke S., Zeeman S. C., The Debate on the Pathway of Starch Synthesis: A Closer Look at Low-Starch Mutants Lacking Plastidial Phosphoglucomutase Supports the Chloroplast-Localized Pathway, 10.1104/pp.109.144931
  46. TARDIEU FRANÇOIS, PARENT BORIS, SIMONNEAU THIERRY, Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes?, 10.1111/j.1365-3040.2009.02091.x
  47. Thompson A. J., Andrews J., Mulholland B. J., McKee J. M.T., Hilton H. W., Horridge J. S., Farquhar G. D., Smeeton R. C., Smillie I. R.A., Black C. R., Taylor I. B., Overproduction of Abscisic Acid in Tomato Increases Transpiration Efficiency and Root Hydraulic Conductivity and Influences Leaf Expansion, 10.1104/pp.106.093559
  48. Tisne S., Reymond M., Vile D., Fabre J., Dauzat M., Koornneef M., Granier C., Combined Genetic and Modeling Approaches Reveal That Epidermal Cell Area and Number in Leaves Are Controlled by Leaf and Plant Developmental Processes in Arabidopsis, 10.1104/pp.108.124271
  49. TISNÉ SÉBASTIEN, SCHMALENBACH INGA, REYMOND MATTHIEU, DAUZAT MYRIAM, PERVENT MARJORIE, VILE DENIS, GRANIER CHRISTINE, Keep on growing under drought: genetic and developmental bases of the response of rosette area using a recombinant inbred line population : Leaf development and drought stress, 10.1111/j.1365-3040.2010.02191.x
  50. Volkenburgh E. Van, Leaf expansion - an integrating plant behaviour : Leaf expansion, 10.1046/j.1365-3040.1999.00514.x
  51. VILE D., Specific Leaf Area and Dry Matter Content Estimate Thickness in Laminar Leaves, 10.1093/aob/mci264
  52. VILE DENIS, PERVENT MARJORIE, BELLUAU MICHAËL, VASSEUR FRANÇOIS, BRESSON JUSTINE, MULLER BERTRAND, GRANIER CHRISTINE, SIMONNEAU THIERRY, Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? : Plant responses to high temperature and water deficit, 10.1111/j.1365-3040.2011.02445.x
  53. Vrábl D., Vašková M., Hronková M., Flexas J., Šantrůček J., Mesophyll conductance to CO2 transport estimated by two independent methods: effect of variable CO2 concentration and abscisic acid, 10.1093/jxb/erp115
  54. Wuyts Nathalie, Palauqui Jean-Christophe, Conejero Genevieve, Verdeil Jean-Luc, Granier Christine, Massonnet Catherine, High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll, 10.1186/1746-4811-6-17
  55. Yano Satoshi, Terashima Ichiro, Separate Localization of Light Signal Perception for Sun or Shade Type Chloroplast and Palisade Tissue Differentiation in Chenopodium album, 10.1093/pcp/pce183
  56. YANO S., TERASHIMA I., Developmental process of sun and shade leaves in Chenopodium album L., 10.1111/j.1365-3040.2004.01182.x
  57. Terashima I., Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion, 10.1093/jxb/erj014
Bibliographic reference Wuyts, Nathalie ; Massonnet, Catherine ; Dauzat, Myriam ; Granier, Christine. Structural assessment of the impact of environmental constraints on arabidopsis thaliana leaf growth: A 3D approach. In: Plant, Cell and Environment, Vol. 35, no. 9, p. 1631-1646 (2012)
Permanent URL http://hdl.handle.net/2078.1/161132