Foliar and Axial Aspects of Vascular Differentiation: Hypotheses and Evidence

A comparison is made between foliar and axial vascular differentiation. Current thoughts and new evidence are presented on the role of hormones in controlling the differentiation of vascular tissues in organized and tumorous tissues, focusing on the role of auxin and cytokinin in controlling phloem and xylem relationships, vessel size and density, cambium sensitivity, vascular adaptation and xylem evolution in deciduous hardwood trees. The possible role of wounding is also considered. A new hypothesis, namely, the leaf-venation hypothesis, is proposed to explain the hormonal control of vascular differentiation in leaves of dicotyledonous plants. Experimental evidence in support of the hypothesis is presented showing that hydathodes, the watersecreting glands, are the primary sites of auxin synthesis during leaf morphogenesis. Vessel element patterns similar to those found in hydathodes were experimentally induced by exogenous auxin application.

[1]  T. Sachs.  The development of vascular networks during leaf development , 1989 .

[2]  S. Carlquist.  Ecological strategies of xylem evolution , 1975 .

[3]  R. Aloni,et al.  Vascularization is a general requirement for growth of plant and animal tumours. , 2000, Journal of experimental botany.

[4]  F. Carland,et al.  LOP1: a gene involved in auxin transport and vascular patterning in Arabidopsis. , 1996, Development.

[5]  R. Aloni.  The Induction of Vascular Tissues by Auxin and Cytokinin , 1995 .

[6]  J. Curtis,et al.  PARAVEINAL MESOPHYLL IN CALLIANDRA TWEEDII AND C. EMARGINATA (LEGUMINOSAE; MIMOSOIDEAE). , 1993, American journal of botany.

[7]  B. Sundberg,et al.  Indole-3-acetic acid controls cambial growth in scots pine by positional signaling , 1998, Plant physiology.

[8]  I. Somssich,et al.  Developmental and auxin-induced expression of the Arabidopsis prha homeobox gene. , 1997, The Plant journal : for cell and molecular biology.

[9]  T. Nelson,et al.  Genetic Regulation of Vascular Tissue Patterning in Arabidopsis , 1999, Plant Cell.

[10]  Elliot M. Meyerowitz,et al.  Arabidopsis, a useful weed , 1989, Cell.

[11]  L. Sieburth,et al.  The SCARFACE gene is required for cotyledon and leaf vein patterning. , 2000, Development.

[12]  M. Tyree,et al.  Natural and experimentally altered hydraulic architecture of branch junctions in Acer saccharum Marsh. and Quercus velutina Lam. trees , 1997, Trees.

[13]  R. Aloni,et al.  The never ripe mutant provides evidence that tumor-induced ethylene controls the morphogenesis of agrobacterium tumefaciens-induced crown galls on tomato stems , 1998, Plant physiology.

[14]  C. Peterson,et al.  Role of Cytokinin in Vessel Regeneration in Wounded Coleus Internodes , 1991 .

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

[16]  P. Wareing,et al.  The Effect of Applied Growth Hormones on Cambial Division and the Differentiation of the Cambial Derivatives , 1966 .

[17]  R. Poethig.  Leaf morphogenesis in flowering plants. , 1997, The Plant cell.

[18]  C. Hardtke,et al.  Vascular continuity and auxin signals. , 2000, Trends in plant science.

[19]  T. Kozlowski,et al.  Effect of Ethrel on Stem Anatomy of Ulmus Americana Seedlings , 1987 .

[20]  R. Savidge,et al.  Cell and molecular biology of wood formation , 2000 .

[21]  E. Ashby,et al.  STUDIES IN THE MORPHOGENESIS OF LEAVES , 1951 .

[22]  J L Micol,et al.  Venation pattern formation in Arabidopsis thaliana vegetative leaves. , 1999, Developmental biology.

[23]  E. Ashby.  STUDIES IN THE MORPHOGENESIS OF LEAVES. I. AN ESSAY ON LEAF SHAPE , 1948 .

[24]  T. Berleth,et al.  Responses of plant vascular systems to auxin transport inhibition. , 1999, Development.

[25]  G. Sandberg,et al.  Auxin-Cytokinin Interactions in Wild-Type and Transgenic Tobacco , 1997 .

[26]  T. Sachs.  The Control of the Differentiation of Vascular Networks , 1975 .

[27]  C. Brubaker,et al.  Paraveinal mesophyll, and its relationship to vein endings, in Solidago canadensis (Asteraceae) , 1989 .

[28]  A. ALLSOPP,et al.  Plant Anatomy , 1966, Nature.

[29]  L. Sieburth,et al.  Auxin is required for leaf vein pattern in Arabidopsis. , 1999, Plant physiology.

[30]  J. J. Taylor,et al.  Transformation of the collateral vascular bundles into amphivasal vascular bundles in an Arabidopsis mutant. , 1999, Plant physiology.

[31]  S. Carlquist.  Comparative Wood Anatomy: Systematic, Ecological, and Evolutionary Aspects of Dicotyledon Wood , 1990 .

[32]  N. Lersten.  SIEVE TUBES IN FOLIAR VEIN ENDINGS: REVIEW AND QUANTITATIVE SURVEY OF RUDBECKIA LACINIATA (ASTERACEAE) , 1990 .

[33]  H. Klee,et al.  Inactivation of auxin in tobacco transformed with the indoleacetic acid-lysine synthetase gene of Pseudomonas savastanoi. , 1991, Genes & development.

[34]  ACROPETAL LEAF DIFFERENTIATION IN QUERCUS RUBRA (FAGACEAE) , 1991 .

[35]  Pea Compound Leaf Architecture Is Regulated by Interactions among the Genes UNIFOLIATA, COCHLEATA, AFILA, and TENDRIL-LESS , 2000, Plant Cell.

[36]  T. Berleth,et al.  Vascular development: tracing signals along veins. , 2000, Current opinion in plant biology.

[37]  T. Sachs.  Pattern Formation in Plant Tissues: Callus and tumor development , 1991 .

[38]  Prof. Dr. Lorin W. Roberts,et al.  Vascular Differentiation and Plant Growth Regulators , 1988, Springer Series in Wood Science.

[39]  W. P. Jacobs.  THE ROLE OF AUXIN IN DIFFERENTIATION OF XYLEM AROUND A WOUND , 1952 .

[40]  E. Groot,et al.  Comparison of Leaf Plastochron Index and Allometric Analyses of Tooth Development in Arabidopsis thaliana , 2000, Journal of Plant Growth Regulation.

[41]  R. Poethig,et al.  15 Leaf Development in Arabidopsis , 1994 .

[42]  K. Esau.  Vascular differentiation in plants , 1966 .

[43]  R. Aloni.  The Role of Cytokinin in Organised Differentiation of Vascular Tissues , 1993 .

[44]  T. Nelson,et al.  Leaf Vascular Pattern Formation. , 1997, The Plant cell.

[45]  R. Aloni,et al.  Differentiation of Vascular Tissues , 1987 .

[46]  Peter H. Raven,et al.  Biology of plants , 1976 .

[47]  M. Tyree,et al.  Natural and experimentally altered hydraulic architecture of branch junctions in , 1997 .

[48]  P. Baas,et al.  A Survey of the Fossil Record for Dicotiledonous Wood and its Significance for Evolutionary and Ecological Wood Anatomy , 1991 .

[49]  R. Aloni.  Hormonal control of vascular differentiation in plants: the physiological basis of cambium ontogeny and xylem evolution , 2000 .

[50]  A. Trewavas,et al.  Sensitivity Thresholds and Variable Time Scales in Plant Hormone Action , 1994, Plant physiology.

[51]  K. Koizumi,et al.  A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. , 2000, Development.

[52]  B. Sundberg,et al.  Auxin as a positional signal in pattern formation in plants. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[53]  N. Lersten,et al.  Quantitative survey of sieve tube distribution in foliar terminal veins of ten dicot species , 1994 .

[54]  M. Estelle,et al.  The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. , 2000, Development.

[55]  M. Zimmermann,et al.  The control of vessel size and density along the plant axis: a new hypothesis , 1983 .

[56]  E. Njoku.  STUDIES IN THE MORPHOGENESIS OF LEAVES , 1956 .

[57]  Y. Eshed,et al.  The Making of a Compound Leaf: Genetic Manipulation of Leaf Architecture in Tomato , 1996, Cell.

[58]  T. Sachs.  Integrating cellular and organismic aspects of vascular differentiation. , 2000, Plant & cell physiology.

[59]  K. Fischer,et al.  Ethylene production and ACC‐accumulation in Agrobacterium tumefaciens‐induced plant tumours and their impact on tumour and host stem structure and function , 1999 .

[60]  A. Trewavas,et al.  Is plant development regulated by changes in the concentration of growth substances or by changes in the sensitivity to growth substances , 1983 .

[61]  C. Peterson,et al.  The role of cytokinin in sieve tube regeneration and callose production in wounded coleus internodes. , 1990, Plant physiology.

[62]  Mitsuo Suzuki,et al.  Phenological Comparison of the Onset of Vessel Formation Between Ring-Porous and Diffuse-Porous Deciduous Trees in a Japanese Temperate Forest , 1996 .

[63]  B. Sundberg,et al.  A Microscale Technique for Gas Chromatography-Mass Spectrometry Measurements of Picogram Amounts of Indole-3-Acetic Acid in Plant Tissues , 1995, Plant physiology.

[64]  T. Sachs.  The Control of the Patterned Differentiation of Vascular Tissues , 1981 .