Combined Genetic and Modeling Approaches Reveal That Epidermal Cell Area and Number in Leaves Are Controlled by Leaf and Plant Developmental Processes in Arabidopsis1[W]

Both leaf production and leaf expansion are tightly linked to cell expansion and cell division, but the functional relationships between all these variables are not clearly established. To get insight into these relationships, a quantitative genetic analysis was performed in 118 recombinant inbred lines derived from a cross between the Landsberg erecta and Antwerp accessions and was combined with a structural equation modeling approach. Main effects and epistatic interactions at the quantitative trait locus (QTL) level were detected for rosette area, rosette leaf number, leaf 6 area, epidermal cell area and number. A QTL at ERECTA marker (ER) controlled cell expansion and cell division, in interaction with two other QTLs at SNP295 and SNP21 markers. Moreover, both the screening for marker association involved in the variation of the relationships between leaf growth variables and the test of alternative functional models by structural equation modeling revealed that the allelic value at ER controlled epidermal cell area and epidermal cell number in a leaf. These effects are driven both by a whole plant mechanism associated with leaf production and by a single leaf mechanism associated with leaf expansion. The complex effects of the QTL at ER were validated in selected heterogeneous inbred families. The ERECTA gene, which is mutated in the Landsberg erecta parental line, was found to be a putative candidate responsible for these mapped effects by phenotyping mutants of this gene at the cellular level. Together, these results give insight into the complex determination of leaf epidermal cell number and area.

[1]  P. Robles,et al.  A mutational analysis of leaf morphogenesis in Arabidopsis thaliana. , 1999, Genetics.

[2]  F. Tardieu,et al.  Co-Ordination of Cell Division and Tissue Expansion in Sunflower, Tobacco, and Pea Leaves: Dependence or Independence of Both Processes? , 2000, Journal of Plant Growth Regulation.

[3]  D. Inzé,et al.  Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. , 1995, The EMBO journal.

[4]  C. Granier,et al.  Correlation between leaf growth variables suggest intrinsic and early controls of leaf size in Arabidopsis thaliana , 2005 .

[5]  E. Ashby STUDIES IN THE MORPHOGENESIS OF LEAVES. II. THE AREA, CELL SIZE AND CELL NUMBER OF LEAVES OF IPOMOEA IN RELATION TO THEIR POSITION ON THE SHOOT , 1948 .

[6]  T. Mackay,et al.  Quantitative trait loci for floral morphology in Arabidopsis thaliana. , 2000, Genetics.

[7]  K. Torii,et al.  Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation , 2004, Development.

[8]  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.

[9]  B. Mangin,et al.  ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. , 2003, The Plant journal : for cell and molecular biology.

[10]  R. Amasino,et al.  Natural allelic variation identifies new genes in the Arabidopsis circadian system. , 1999, The Plant journal : for cell and molecular biology.

[11]  Franky R. G. Terras,et al.  Functional Analysis of Cyclin-Dependent Kinase Inhibitors of Arabidopsis , 2001, The Plant Cell Online.

[12]  J. Murray,et al.  Cyclin D control of growth rate in plants , 2022 .

[13]  J. E. Dale,et al.  How Do Leaves Grow?Advances in cell and molecular biology are unraveling some of the mysteries of leaf development , 1992 .

[14]  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.

[15]  G. Rédei Single locus heterosis , 1962, Zeitschrift für Vererbungslehre.

[16]  K. Chase,et al.  Epistat : a computer program for identifying and testing interactions between pairs of quantitative trait loci , 1997, Theoretical and Applied Genetics.

[17]  Bill Shipley,et al.  Cause and Correlation in Biology: A User''s Guide to Path Analysis , 2016 .

[18]  K. Torii,et al.  Dominant-Negative Receptor Uncovers Redundancy in the Arabidopsis ERECTA Leucine-Rich Repeat Receptor–Like Kinase Signaling Pathway That Regulates Organ Shape Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010413. , 2003, The Plant Cell Online.

[19]  J. V. Ooijen,et al.  Software for the mapping of quantitative trait loci in experimental populations , 2004 .

[20]  G. L. Wilson Studies on the Expansion of the Leaf Surface: V. CELL DIVISION AND EXPANSION IN A DEVELOPING LEAF AS INFLUENCED BY LIGHT AND UPPER LEAVES , 1966 .

[21]  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.

[22]  G. Farquhar,et al.  The ERECTA gene regulates plant transpiration efficiency in Arabidopsis , 2005, Nature.

[23]  J. Murray,et al.  Altered Cell Cycle Distribution, Hyperplasia, and Inhibited Differentiation in Arabidopsis Caused by the D-Type Cyclin CYCD3 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004838. , 2003, The Plant Cell Online.

[24]  John Fox,et al.  TEACHER'S CORNER: Structural Equation Modeling With the sem Package in R , 2006 .

[25]  M. Koornneef,et al.  New Arabidopsis Recombinant Inbred Line Populations Genotyped Using SNPWave and Their Use for Mapping Flowering-Time Quantitative Trait Loci , 2006, Genetics.

[26]  D. Francis The cell cycle in plant development. , 1992, The New phytologist.

[27]  Hans Lambers,et al.  Genetic and Physiological Architecture of Early Vigor in Aegilops tauschii, the D-Genome Donor of Hexaploid Wheat. A Quantitative Trait Loci Analysis1[w] , 2005, Plant Physiology.

[28]  K. Torii,et al.  Stomatal Patterning and Differentiation by Synergistic Interactions of Receptor Kinases , 2005, Science.

[29]  A. Fleming Cell Cycle Control during Leaf Development , 2007 .

[30]  N. Mitsukawa,et al.  The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. , 1996, The Plant cell.

[31]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

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

[33]  Karine Chenu,et al.  Day length affects the dynamics of leaf expansion and cellular development in Arabidopsis thaliana partially through floral transition timing. , 2007, Annals of botany.

[34]  G. Horiguchi,et al.  Analysis of Leaf Development in fugu Mutants of Arabidopsis Reveals Three Compensation Modes That Modulate Cell Expansion in Determinate Organs1[W] , 2007, Plant Physiology.

[35]  H. Tsukaya Organ shape and size: a lesson from studies of leaf morphogenesis. , 2003, Current opinion in plant biology.

[36]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .

[37]  P. Green Growth and Cell Pattern Formation on an Axis: Critique of Concepts, Terminology, and Modes of Study , 1976, Botanical Gazette.

[38]  José Luis Micol,et al.  Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. , 2002, Genetics.

[39]  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.