ESAU’S PLANT ANATOMYMeristems, Cells, and Tissues of the Plant Body:Their Structure, Function, and Development

Third Edition

RAY F. EVERTKatherine Esau Professor of Botany and Plant Pathology, EmeritusUniversity of Wisconsin, Madison

With the assistance ofSusan E. Eichhorn

University of Wisconsin, Madison

A John Wiley & Sons, Inc., Publication

Innodata0470047372.jpg

Esau’s Plant Anatomy

ESAU’S PLANT ANATOMYMeristems, Cells, and Tissues of the Plant Body:Their Structure, Function, and Development

Third Edition

RAY F. EVERTKatherine Esau Professor of Botany and Plant Pathology, EmeritusUniversity of Wisconsin, Madison

With the assistance ofSusan E. Eichhorn

University of Wisconsin, Madison

A John Wiley & Sons, Inc., Publication

Copyright © 2006 by John Wiley & Sons, Inc. All rights reserved.

Published by John Wiley & Sons, Inc., Hoboken, New Jersey.Published simultaneously in Canada.

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Library of Congress Cataloging-in-Publication Data:

Evert, Ray Franklin. Esau’s Plant anatomy : meristems, cells, and tissues of the plant body : their structure, function, and development / Ray F. Evert.—3rd ed. p. cm. Rev. ed. of: Plant anatomy / Katherine Esau. 2nd. ed. 1965. ISBN-13: 978-0-471-73843-5 (cloth) ISBN-10: 0-471-73843-3 (cloth) 1. Plant anatomy. 2. Plant morphology. I. Esau, Katherine, 1898- Plant anatomy. II. Title. QK671.E94 2007 571.3'2—dc22

2006022118

Printed in the United States of America.

10 9 8 7 6 5 4 3 2 1

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Dedicated to the late Katherine Esau, mentor and close friend“In recognition of her distinguished service to the American community of plant biologists, and for the excellence of her pioneering research, both basic and applied, on plant structure and development, which has spanned more than six decades; for her superlative performance as an educator, in the classroom and through her books; for the encouragement and inspiration she has given a legion of young, aspiring plant biologists; for providing a special role model for women in science.”

Citation, National Medal of Science, 1989

Katherine Esau

Contents

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xv

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xvii

General References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xix

Chapter 1 Structure and Development of the Plant Body—An Overview . . . . . . . . . . . . . . . . . . . . . . . . 1

Internal Organization of the Plant Body . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 The Body of a Vascular Plant Is Composed of Three Tissue Systems . . . . . . . . . . . . . . . . . . . . . 3 Structurally Stem, Leaf, and Root Differ Primarily in the Relative

Distribution of the Vascular and Ground Tissues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Summary of Types of Cells and Tissues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Development of the Plant Body . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 The Body Plan of the Plant Is Established during Embryogenesis . . . . . . . . . . . . . . . . . . . . . . . . 7 With Germination of the Seed, the Embryo Resumes Growth and Gradually Develops into

an Adult Plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

Chapter 2 The Protoplast: Plasma Membrane, Nucleus, and Cytoplasmic Organelles . . . . . . . . . . . . . 15

Prokaryotic and Eukaryotic Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 Cytoplasm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 Plasma Membrane . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 Cell Cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 Plastids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25 Chloroplasts Contain Chlorophyll and Carotenoid Pigments . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

vii

viii | Contents

Chromoplasts Contain Only Carotenoid Pigments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 Leucoplasts Are Nonpigmented Plastids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28 All Plastids Are Derived Initially from Proplastids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28 Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31 Peroxisomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33 Vacuoles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34 Ribosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

Chapter 3 The Protoplast: Endomembrane System, Secretory Pathways, Cytoskeleton,

and Stored Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45

Endomembrane System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 The Endoplasmic Reticulum Is a Continuous, Three-dimensional

Membrane System That Permeates the Entire Cytosol . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 The Golgi Apparatus Is a Highly Polarized Membrane System Involved in Secretion . . . . . . . . . 48 Cytoskeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49 Microtubules Are Cylindrical Structures Composed of Tubulin Subunits . . . . . . . . . . . . . . . . . . 49 Actin Filaments Consist of Two Linear Chains of Actin Molecules in the Form of a Helix . . . . 50 Stored Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52 Starch Develops in the Form of Grains in Plastids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52 The Site of Protein Body Assembly Depends on Protein Composition . . . . . . . . . . . . . . . . . . . . 53 Oil Bodies Bud from Smooth ER Membranes by an Oleosin-mediated Process . . . . . . . . . . . . . . 54 Tannins Typically Occur in Vacuoles but Also Are Found in Cell Walls . . . . . . . . . . . . . . . . . . . 55 Crystals of Calcium Oxalate Usually Develop in Vacuoles but

Also Are Found in the Cell Wall and Cuticle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56 Silica Most Commonly Is Deposited in Cell Walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58

Chapter 4 Cell Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65

Macromolecular Components of the Cell Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 Cellulose Is the Principal Component of Plant Cell Walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 The Cellulose Microfi brils Are Embedded in a Matrix of Noncellulosic Molecules . . . . . . . . . . 67 Principal Hemicelluoses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67 Pectins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68 Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68 Callose Is a Widely Distributed Cell Wall Polysaccharide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Lignins Are Phenolic Polymers Deposited Mainly in Cell Walls of Supporting and Conducting

Tissues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Cutin and Suberin Are Insoluble Lipid Polymers Found Most

Commonly in the Protective Surface Tissues of the Plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71 Cell Wall Layers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71 The Middle Lamella Frequently Is Diffi cult to Distinguish from the Primary Wall . . . . . . . . . . . 72 The Primary Wall Is Deposited While the Cell Is Increasing in Size . . . . . . . . . . . . . . . . . . . . . . 72 The Secondary Wall Is Deposited inside the Primary Wall Largely, If Not Entirely, after the

Primary Wall Has Stopped Increasing in Surface Area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72 Pits and Primary Pit-Fields . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74 Origin of Cell Wall during Cell Division . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76 Cytokinesis Occurs by the Formation of a Phragmoplast and Cell Plate . . . . . . . . . . . . . . . . . . . 76 Initially Callose Is the Principal Cell Wall Polysaccharide Present

in the Developing Cell Plate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78 The Preprophase Band Predicts the Plane of the Future Cell Plate . . . . . . . . . . . . . . . . . . . . . . . 78 Growth of the Cell Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80 The Orientation of Cellulose Microfi brils within the Primary Wall Infl uences the

Direction of Cell Expansion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82 When Considering the Mechanism of Wall Growth, It Is Necessary to Distinguish

between Growth in Surface (Wall Expansion) and Growth in Thickness . . . . . . . . . . . . . . . . . . 83

Contents | ix

Expansion of the Primary Cell Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83 Cessation of Wall Expansion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84 Intercellular Spaces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84 Plasmodesmata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85 Plasmodesmata May Be Classifi ed as Primary or Secondary According to Their Origin . . . . . . . 85 Plasmodesmata Contain Two Types of Membranes: Plasma Membrane and Desmotubule . . . . . 87 Plasmodesmata Enable Cells to Communicate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88 The Symplast Undergoes Reorganization throughout the Course of Plant Growth and

Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91

Chapter 5 Meristems and Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103

Meristems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103 Classifi cation of Meristems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104 A Common Classifi cation of Meristems Is Based on Their Position in the Plant Body . . . . . . 104 Meristems Are Also Classifi ed According to the Nature of

Cells That Give Origin to Their Initial Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106 Characteristics of Meristematic Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106 Growth Patterns in Meristems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107 Meristematic Activity and Plant Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108 Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110 Terms and Concepts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110 Senescence (Programmed Cell Death) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111 Cellular Changes in Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113 A Cytologic Phenomenon Commonly Observed in Differentiating

Cells of Angiosperms Is Endopolyploidy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113 One of the Early Visible Changes in Differentiating Tissues Is the

Unequal Increase in Cell Size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113 Intercellular Adjustment in Differentiating Tissue Involves

Coordinated and Intrusive Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 114 Causal Factors in Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115 Tissue Culture Techniques Have Been Useful for the Determination

of Requirements for Growth and Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115 The Analysis of Genetic Mosaics Can Reveal Patterns of Cell Division

and Cell Fate in Developing Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117 Gene Technologies Have Dramatically Increased Our Understanding of Plant Development . . . 117 Polarity Is a Key Component of Biological Pattern Formation and

Is Related to the Phenomenon of Gradients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119 Plant Cells Differentiate According to Position . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119 Plant Hormones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120 Auxins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121 Cytokinins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122 Ethylene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 Abscisic Acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 Gibberellins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Chapter 6 Apical Meristems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133

Evolution of the Concept of Apical Organization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134 Apical Meristems Originally Were Envisioned as Having a Single Initial Cell . . . . . . . . . . . . . . . 134 The Apical-Cell Theory Was Superseded by the Histogen Theory . . . . . . . . . . . . . . . . . . . . . . . . 134 The Tunica-Corpus Concept of Apical Organization Applies Largely to Angiosperms . . . . . . . . 135

The Shoot Apices of Most Gymnosperms and Angiosperms Show a Cytohistological Zonation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136

Inquiries into the Identity of Apical Initials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136 Vegetative Shoot Apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138

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The Presence of an Apical Cell Is Characteristic of Shoot Apices in Seedless Vascular Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139

The Zonation Found in the Ginkgo Apex Has Served as a Basis for the Interpretation of Shoot Apices in Other Gymnosperms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140

The Presence of a Zonation Superimposed on a Tunica-Corpus Confi guration Is Characteristic of Angiosperm Shoot Apices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141

The Vegetative Shoot Apex of Arabidopsis thaliana . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143 Origin of Leaves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145 Throughout the Vegetative Period the Shoot Apical Meristem Produces Leaves in a

Regular Order . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145 The Initiation of a Leaf Primordium Is Associated with an Increase

in the Frequency of Periclinal Divisions at the Initiation Site . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147 Leaf Primordia Arise at Sites That Are Correlated with the Phyllotaxis of the Shoot . . . . . . . . . 149 Origin of Branches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149 In Most Seed Plants Axillary Meristems Originate from Detached Meristems . . . . . . . . . . . . . . . 150 Shoots May Develop from Adventitious Buds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152 Root Apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152 Apical Organization in Roots May Be either Open or Closed . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153 The Quiescent Center Is Not Completely Devoid of Divisions under Normal Conditions . . . . . 157 The Root Apex of Arabidopsis thaliana . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160 Growth of the Root Tip . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165

Chapter 7 Parenchyma and Collenchyma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175

Parenchyma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175 Parenchyma Cells May Occur in Continuous Masses as Parenchyma Tissue or Be

Associated with Other Cell Types in Morphologically Heterogeneous Tissues . . . . . . . . . . . . . . 176 The Contents of Parenchyma Cells Are a Refl ection of the Activities of the Cells . . . . . . . . . . . 177 The Cell Walls of Parenchyma Cells May Be Thick or Thin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 Some Parenchyma Cells—Transfer Cells—Contain Wall Ingrowths . . . . . . . . . . . . . . . . . . . . . . . 179 Parenchyma Cells Vary Greatly in Shape and Arrangement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181

Some Parenchyma Tissue—Aerenchyma—Contains Particularly Large Intercellular Spaces . . . . . 182 Collenchyma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183 The Structure of the Cell Walls of Collenchyma Is the Most Distinctive Characteristic of

This Tissue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184 Collenchyma Characteristically Occurs in a Peripheral Position . . . . . . . . . . . . . . . . . . . . . . . . . 185 Collenchyma Appears to Be Particularly Well Adapted for Support of

Growing Leaves and Stems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

Chapter 8 Sclerenchyma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191

Fibers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192 Fibers Are Widely Distributed in the Plant Body . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192 Fibers May Be Divided into Two Large Groups, Xylary and Extraxylary . . . . . . . . . . . . . . . . . . . 194 Both Xylary and Extraxylary Fibers May Be Septate or Gelatinous . . . . . . . . . . . . . . . . . . . . . . . 196 Commercial Fibers Are Separated into Soft Fibers and Hard Fibers . . . . . . . . . . . . . . . . . . . . . . . 197 Sclereids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198 Based on Shape and Size, Sclereids May Be Classifi ed into a Number of Types . . . . . . . . . . . . . 198 Sclereids Like Fibers Are Widely Distributed in the Plant Body . . . . . . . . . . . . . . . . . . . . . . . . . . 199 Sclereids in Stems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200 Sclereids in Leaves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200 Sclereids in Fruits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201 Sclereids in Seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201 Origin and Development of Fibers and Sclereids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202 Factors Controlling Development of Fibers and Sclereids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207

Contents | xi

Chapter 9 Epidermis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211

Ordinary Epidermal Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 214 Epidermal Cell Walls Vary in Thickness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 214 The Most Distinctive Feature of the Outer Epidermal Wall Is the Presence of a Cuticle . . . . . . 215 Stomata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218 Stomata Occur on All Aerial Parts of the Primary Plant Body . . . . . . . . . . . . . . . . . . . . . . . . . . . 218 Guard Cells Are Generally Kidney-shaped . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221 Guard Cells Typically Have Unevenly Thickened Walls with Radially Arranged

Cellulose Microfi brils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 222 Blue Light and Abscisic Acid Are Important Signals in the Control of

Stomatal Movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224 Development of Stomatal Complexes Involves One or More Asymmetric Cell Divisions . . . . . . 225 Different Developmental Sequences Result in Different

Confi gurations of Stomatal Complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228 Trichomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229 Trichomes Have a Variety of Functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229 Trichomes May Be Classifi ed into Different Morphological Categories . . . . . . . . . . . . . . . . . . . . 230 A Trichome Is Initiated as a Protuberance from an Epidermal Cell . . . . . . . . . . . . . . . . . . . . . . . 230 The Cotton Fiber . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230 Root Hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234 The Arabidopsis Trichome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235 Cell Patterning in the Epidermis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237 The Spatial Distribution of Stomata and Trichomes in Leaves Is Nonrandom . . . . . . . . . . . . . . . 237 There Are Three Main Types of Patterning in the Epidermis of Angiosperm Roots . . . . . . . . . . 238 Other Specialized Epidermal Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239 Silica and Cork Cells Frequently Occur Together in Pairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239 Bulliform Cells Are Highly Vacuolated Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241 Some Epidermal Hairs Contain Cystoliths . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 242 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243

Chapter 10 Xylem: Cell Types and Developmental Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255

Cell Types of the Xylem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256 Tracheary Elements—Tracheids and Vessel Elements—Are the Conducting Cells of the

Xylem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256 The Secondary Walls of Most Tracheary Elements Contain Pits . . . . . . . . . . . . . . . . . . . . . . . . . . 260 Vessels Are More Effi cient Conduits of Water Than Are Tracheids . . . . . . . . . . . . . . . . . . . . . . . . 263 Fibers Are Specialized as Supporting Elements in the Xylem . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266 Living Parenchyma Cells Occur in Both the Primary and Secondary Xylem . . . . . . . . . . . . . . . . 266 In Some Species the Parenchyma Cells Develop Protrusions—Tyloses—That Enter the

Vessels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267 Phylogenetic Specialization of Tracheary Elements and Fibers . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268 The Major Trends in the Evolution of the Vessel Element Are Correlated with Decrease in

Vessel Element Length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268 Deviations Exist in Trends of Vessel Element Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270 Like Vessel Elements and Tracheids, Fibers Have Undergone a Phylogenetic Shortening . . . . . 271 Primary Xylem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271 Some Developmental and Structural Differences Exist between the Earlier and Later Formed

Parts of the Primary Xylem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271 The Primary Tracheary Elements Have a Variety of Secondary Wall Thickenings . . . . . . . . . . . 273 Tracheary Element Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276 Plant Hormones Are Involved in the Differentiation of Tracheary Elements . . . . . . . . . . . . . . . . 280 Isolated Mesophyll Cells in Culture Can Transdifferentiate Directly into

Tracheary Elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283

xii | Contents

Chapter 11 Xylem: Secondary Xylem and Variations in Wood Structure . . . . . . . . . . . . . . . . . . . . . . . . . 291

Basic Structure of Secondary Xylem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293 The Secondary Xylem Consists of Two Distinct Systems of Cells, Axial and Radial . . . . . . . . . . 293 Some Woods Are Storied and Others Are Nonstoried . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 294 Growth Rings Result from the Periodic Activity of the Vascular Cambium . . . . . . . . . . . . . . . . 294 As Wood Becomes Older, It Gradually Becomes Nonfunctional in Conduction and Storage . . . 297 Reaction Wood Is a Type of Wood That Develops in Branches

and Leaning or Crooked Stems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 299 Woods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302 The Wood of Conifers Is Relatively Simple in Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302 The Axial System of Conifer Woods Consists Mostly or Entirely of Tracheids . . . . . . . . . . . . . . 302 The Rays of Conifers May Consist of Both Parenchyma Cells and Tracheids . . . . . . . . . . . . . . . 303 The Wood of Many Conifers Contains Resin Ducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 304 The Wood of Angiosperms Is More Complex and Varied Than That of Conifers . . . . . . . . . . . . 306 On the Basis of Porosity, Two Main Types of Angiosperm Wood Are Recognized: Diffuse-

porous and Ring-porous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307 The Distribution of Axial Parenchyma Shows Many Intergrading Patterns . . . . . . . . . . . . . . . . . 309 The Rays of Angiosperms Typically Contain Only Parenchyma Cells . . . . . . . . . . . . . . . . . . . . . 310 Intercellular Spaces Similar to the Resin Ducts of Gymnosperms

Occur in Angiosperm Woods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 312 Some Aspects of Secondary Xylem Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 312 Identifi cation of Wood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 316

Chapter 12 Vascular Cambium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 323

Organization of the Cambium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 323 The Vascular Cambium Contains Two Types of Initials: Fusiform Initials and Ray Initials . . . . 323 The Cambium May Be Storied or Nonstoried . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 325 Formation of Secondary Xylem and Secondary Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 326 Initials Versus Their Immediate Derivatives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 327 Developmental Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 Formation of New Ray Initials from Fusiform Initials or Their Segments Is a Common

Phenomenon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Domains Can Be Recognized within the Cambium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335 Seasonal Changes in Cambial Cell Ultrastructure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 336 Cytokinesis of Fusiform Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 338 Seasonal Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 341 The Size of the Xylem Increment Produced during One Year Generally Exceeds That of the

Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343 A Distinct Seasonality in Cambial Activity Also Occurs in Many Tropical Regions . . . . . . . . . . . 344 Causal Relations in Cambial Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 346 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 348

Chapter 13 Phloem: Cell Types and Developmental Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357

Cell Types of the Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 359 The Angiospermous Sieve-Tube Element . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 360 In Some Taxa the Sieve-Tube Element Walls Are Remarkably Thick . . . . . . . . . . . . . . . . . . . . . . 361 Sieve Plates Usually Occur on End Walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 364 Callose Apparently Plays a Role in Sieve-Pore Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . 364 Changes in the Appearance of the Plastids and the Appearance of P-protein Are Early

Indicators of Sieve-Tube Element Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 365 Nuclear Degeneration May Be Chromatolytic or Pycnotic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 372 Companion Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 372 The Mechanism of Phloem Transport in Angiosperms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 379 The Source Leaf and Minor Vein Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 382

Contents | xiii

Several Types of Minor Veins Occur in Dicotyledonous Leaves . . . . . . . . . . . . . . . . . . . . . . . . . . 384 Type 1 Species with Specialized Companion Cells, Termed Intermediary Cells, Are

Symplastic Loaders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 384 Species with Type 2 Minor Veins Are Apoplastic Loaders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385 The Collection of Photoassimilate by the Minor Veins in Some Leaves May Not Involve an

Active Step . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385 Some Minor Veins Contain More Than One Kind of Companion Cell . . . . . . . . . . . . . . . . . . . . . 385 The Minor Veins in Leaf Blades of the Poaceae Contain Two Types of Metaphloem Sieve

Tubes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 386 The Gymnospermous Sieve Cell . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 386 The Walls of Sieve Cells Are Characterized as Primary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 387 Callose Does Not Play a Role in Sieve-Pore Development in Gymnosperms . . . . . . . . . . . . . . . . 387 Little Variation Exists in Sieve-Cell Differentiation among Gymnosperms . . . . . . . . . . . . . . . . . 388 Strasburger Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 390 The Mechanism of Phloem Transport in Gymnosperms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 390 Parenchyma Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 391 Sclerenchyma Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 391 Longevity of Sieve Elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 391 Trends in Specialization of Sieve-Tube Elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 392 Sieve Elements of Seedless Vascular Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393 Primary Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 398

Chapter 14 Phloem: Secondary Phloem and Variations in Its Structure . . . . . . . . . . . . . . . . . . . . . . . . . . 407

Conifer Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 409 Angiosperm Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412 The Patterns Formed by the Fibers Can Be of Taxonomic Signifi cance . . . . . . . . . . . . . . . . . . . . 413 Secondary Sieve-Tube Elements Show Considerable Variation in Form and Distribution . . . . . . 415 Differentiation in the Secondary Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417 Sclerenchyma Cells in the Secondary Phloem Commonly Are Classifi ed as Fibers, Sclereids,

and Fiber-Sclereids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418 The Conducting Phloem Constitutes Only a Small Part of the Inner Bark . . . . . . . . . . . . . . . . . 420 Nonconducting Phloem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422 The Nonconducting Phloem Differs Structurally from the Conducting Phloem . . . . . . . . . . . . . 423 Dilatation Is the Means by Which the Phloem Is Adjusted to the Increase in Circumference

of the Axis Resulting from Secondary Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424

Chapter 15 Periderm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427

Occurrence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427 Characteristics of the Components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429 The Phellogen Is Relatively Simple in Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429 Several Kinds of Phellem Cells May Arise from the Phellogen . . . . . . . . . . . . . . . . . . . . . . . . . . . 429 Considerable Variation Exists in the Width and Composition of Phelloderm . . . . . . . . . . . . . . . 431 Development of Periderm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 433 The Sites of Origin of the Phellogen Are Varied . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 433 The Phellogen Is Initiated by Divisions of Various Kinds of Cells . . . . . . . . . . . . . . . . . . . . . . . . 434 The Time of Appearance of the First and Subsequent Periderms Varies . . . . . . . . . . . . . . . . . . . 434 Morphology of Periderm and Rhytidome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 437 Polyderm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438 Protective Tissue in Monocotyledons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438 Wound Periderm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438 Lenticels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440 Three Structural Types of Lenticels Are Recognized in Woody Angiosperms . . . . . . . . . . . . . . . 441 The First Lenticels Frequently Appear under Stomata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 442 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 442

xiv | Contents

Chapter 16 External Secretory Structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 447

Salt Glands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449 Salt Bladders Secrete Ions into a Large Central Vacuole . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449 Other Glands Secrete Salt Directly to the Outside . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449 The Two-celled Glands of the Poaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449 The Multicellular Glands of Eudicotyledons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 450 Hydathodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 451 Nectaries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 452 The Nectaries of Lonicera japonica Exude Nectar from Unicellular Trichomes . . . . . . . . . . . . 455 The Nectaries of Abutilon striatum Exude Nectar from Multicellular Trichomes . . . . . . . . . . . 456 The Nectaries of Vicia faba Exude Nectar via Stomata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 456 The Most Common Sugars in Nectar Are Sucrose, Glucose, and Fructose . . . . . . . . . . . . . . . . . 456 Structures Intermediate between Nectaries and Hydathodes Also Exist . . . . . . . . . . . . . . . . . . . 459 Colleters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 459 Osmophores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 461 Glandular Trichomes Secreting Lipophilic Substances . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 462 Glandular Trichome Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 463 The Glandular Structures of Carnivorous Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 465 Stinging Hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 466 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 466

Chapter 17 Internal Secretory Structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 473

Internal Secretory Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 473 Oil Cells Secrete Their Oils into an Oil Cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 475 Mucilage Cells Deposit Their Mucilage between the Protoplast and the Cellulosic Cell

Wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 476 Tannin Is the Most Conspicuous Inclusion in Numerous Secretory Cells . . . . . . . . . . . . . . . . . . 477 Secretory Cavities and Ducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478 The Best-Known Secretory Ducts Are the Resin Ducts of Conifers . . . . . . . . . . . . . . . . . . . . . . . 478 Development of Secretory Cavities Appears to Be Schizogenous . . . . . . . . . . . . . . . . . . . . . . . . . 479 Secretory Ducts and Cavities May Arise under the Stimulus of Injury . . . . . . . . . . . . . . . . . . . . . 481 Kino Veins Are a Special Type of Traumatic Duct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 482 Laticifers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 483 On the Basis of Their Structure, Laticifers Are Grouped in Two Major Classes: Articulated

and Nonarticulated . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 484 Latex Varies in Appearance and in Composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 486 Articulated and Nonarticulated Laticifers Apparently Differ from One Another

Cytologically . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487 Laticifers Are Widely Distributed in the Plant Body, Refl ecting Their Mode of

Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 489 Nonarticulated Laticifers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 489 Articulated Laticifers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 491

The Principal Source of Commercial Rubber Is the Bark of the Para Rubber Tree, Hevea brasiliensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 493

The Function of Laticifers Is Not Clear . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 495 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 495

Addendum: Other Pertinent References Not Cited in the Text . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 503

Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521

Author Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 541

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 567

Preface

It has been over 40 years since the second edition of Esau’s Plant Anatomy was completed. The enormous expansion of biological knowledge that has taken place during this period is unprecedented. In 1965, electron microscopy was just beginning to have an impact on plant research at the cellular level. Since then, new approaches and techniques, particularly those used in molecular-genetic research, have resulted in emphasis and direction toward the molecular realm of life. Old concepts and principles are being challenged at virtu-ally every level, often, however, without a clear under-standing of the bases upon which those concepts and principles were established.

A biologist, regardless of his or her line of specializa-tion, cannot afford to lose sight of the whole organism, if his or her goal is an understanding of the organic world. Knowledge of the grosser aspects of structure is basic for effective research and teaching at every level of specialization. The ever-increasing trend toward a reduction of emphasis on factual information in contem-porary teaching and the apparent diminution of plant anatomy and plant morphology courses at many col-leges and universities make a readily accessible source of basic information on plant structure more important than ever. One consequence of these phenomena is a less precise use of terminology and an inappropriate adoption of animal terms for plant structures.

Research in plant structure has benefi ted greatly from the new approaches and techniques now available. Many plant anatomists are participating effectively in the interdisciplinary search for integrated concepts of growth and morphology. At the same time comparative plant anatomists continue to create new concepts on the relationships and evolution of plants and plant tissues with the aid of molecular data and cladistic analy-ses. The integration of ecological and systematic plant anatomy—ecophyletic anatomy—is bringing about a clearer understanding of the driving forces behind evolutionary diversifi cations of wood and of leaf attributes.

A thorough knowledge of the structure and develop-ment of cells and tissues is essential for a realistic inter-pretation of plant function, whether the function concerned is photosynthesis, the movement of water, the transport of food, or the absorption of water and minerals by roots. A full understanding of the effects of pathogenetic organisms on the plant body can only be achieved if one knows the normal structure of the plant concerned. Such horticultural practices as grafting, pruning, vegetative propagation, and the associated phenomena of callus formation, wound healing, regen-eration, and development of adventitious roots and buds are more meaningful if the structural features underly-ing these phenomena are properly understood.

xv

xvi | Preface

A common belief among students and many research-ers alike is that we know virtually all there is to know about the anatomy of plants. Nothing could be further from the truth. Although the study of plant anatomy dates back to the last part of the 1600s, most of our knowledge of plant structure is based on temperate, often agronomic, plants. The structural features of plants growing in subtropical and tropical environments are frequently characterized as exceptions or anomalies rather than as adaptations to different environments. With the great diversity of plant species in the tropics, there is a wealth of information to be discovered on the structure and development of such plants. In addition, as noted by Dr. Esau in the preface of the fi rst edition of Anatomy of Seed Plants (John Wiley & Sons, 1960) “ . . . plant anatomy is interesting for its own sake. It is a gratifying experience to follow the ontogenetic and evolutionary development of structural features and gain the realization of the high degree of complexity and the remarkable orderliness in the organization of the plant.”

A major goal of this book is to provide a fi rm founda-tion in the meristems, cells, and tissues of the plant body, while at the same time nothing some of the many advances being made in our understanding of their function and development through molecular research. For example, in the chapter on apical meristems, which have been the object of considerable molecular-genetic research, a historical review of the concept of apical organization is presented to provide the reader with an understanding of how that concept has evolved with the availability of more sophisticated methodology. Through-out the book, greater emphasis is made on structure-function relationships than in the previous two editions. As in the previous editions, angiosperms are empha-

sized, but some features of the vegetative parts of gymnosperms and seedless vascular plants are also considered.

These are exciting times for plant biologists. This is refl ected, in part, in the enormity of literature output. The references cited in this book represent but a frac-tion of the total number of articles read in preparation of the third edition. This is particularly true of the molecular-genetic literature, which is cited most selec-tively. It was important not to lose focus on the anatomy. A great many of the references cited in the second edition were read anew, in part to insure continuity between the second and third editions. A large number of selected references are listed to support descriptions and interpretations and to direct the interested person toward wider reading. Undoubtedly, some pertinent papers were inadvertently overlooked. A number of review articles, books, and chapters in books with helpful reference lists are included. Additional pertinent references are listed in the addendum.

This book has been planned primarily for advanced students in various branches of plant science, for researchers (from molecular to whole plant), and for teachers of plant anatomy. At the same time, an effort has been made to attract the less-advanced student by presenting the subject in an inviting style, with numerous illustrations, and by explaining and analyzing terms and concepts as they appear in the text. It is my hope that this book will enlighten many and inspire numerous others to study plant structure and development.

R. F. E.Madison, Wisconsin

July, 2006

Acknowledgments

Illustrations form an important part of a book in plant anatomy. I am indebted to various persons who kindly provided illustrations of one kind or another for inclu-sion in the book and to others, along with publishers and scientifi c journals, for permission to reproduce in one form or another their published illustrations. Illus-trations whose source(s) are not indicated in the fi gure captions are original. Numerous fi gures are from research articles by me or coauthored with colleagues, including my students. A great many of the illustrations are the superb work—line art and micrographs—of Dr. Esau. Some fi gures are expertly rendered electronic illustrations by Kandis Elliot.

Sincere thanks are extended to Laura Evert and Mary Evert for their able assistance with the process of obtain-ing permissions.

I am grateful to the following people, who so gener-ously gave of their time to review parts of the manu-

script: Drs. Veronica Angyalossy, Pieter Baas, Sebastian Y. Bednarek, C. E. J. Botha, Anne-Marie Catesson, Judith L. Croxdale, Nigel Chaffey, Abraham Fahn, Donna Fernandez, Peter K. Helper, Nels R. Lersten, Edward K. Merrill, Regis B. Miller, Thomas L. Rost, Alexander Schulz, L. Andrew Staehelin, Jennifer Thorsch, and Joseph E. Varner. Two of the reviewers, Judith L. Croxdale, who reviewed Chapter 9 (Epidermis), and Joseph E. Varner, who reviewed an early draft of Chapter 4 (Cell Wall), are now deceased. The reviewers offered valuable suggestions for improve-ment. The fi nal responsibility for the contents of the book, including all errors and omissions, however, is mine.

Very special acknowledgment is accorded Susan E. Eichhorn. Without her assistance it would not have been possible for me to revise the second edition of Esau’s Plant Anatomy.

xvii

ALEKSANDROV, V. G. 1966. Anatomiia Rastenii (Anatomy of Plants), 4th ed. Izd. Vysshaia Shkola, Moscow.

BAILEY, I. W. 1954. Contributions to Plant Anatomy. Chronica Botanica, Waltham, MA.

BIEBL, R., and H. GERM. 1967. Praktikum der Pfl anzenanatomie, 2nd ed. Springer-Verlag, Vienna.

BIERHORST, D. W. 1971. Morphology of Vascular Plants. Macmillan, New York.

BOLD, H. C. 1973. Morphology of Plants, 3rd ed. Harper and Row, New York.

BOUREAU, E. 1954–1957. Anatomie végétale: l’appareil végétatif des phanérogrames, 3 vols. Presses Universitaires de France, Paris.

BOWES, B. G. 2000. A Color Atlas of Plant Structure. Iowa State University Press, Ames, IA.

BOWMAN, J., ed. 1994. Arabidopsis: An Atlas of Morphology and Development. Springer-Verlag, New York.

BRAUNE, W., A. LEMAN, and H. TAUBERT. 1971 (© 1970). Pfl an-zenanatomisches Praktikum: zur Einführung in die Anatomie der Vegetationsorgane der höheren Pfl anzen, 2nd ed. Gustav Fischer, Stuttgart.

BUCHANAN, B. B., W. GRUISSEM, and R. L. JONES, eds. 2000. Bio-chemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD.

CARLQUIST, S. 1961. Comparative Plant Anatomy: A Guide to Taxo-nomic and Evolutionary Application of Anatomical Data in Angio-sperms. Holt, Rinehart and Winston, New York.

CARLQUIST, S. 2001. Comparative Wood Anatomy: Systematic, Eco-logical, and Evolutionary Aspects of Dicotyledon Wood, 2nd ed. Springer-Verlag, Berlin.

CHAFFEY, N. 2002. Wood Formation in Trees: Cell and Molecular Biology Techniques. Taylor and Francis, London.

CUTLER, D. F. 1969. Anatomy of the Monocotyledons, vol. IV, Jun-cales. Clarendon Press, Oxford.

CUTLER, D. F. 1978. Applied Plant Anatomy. Longman, London.

CUTTER, E. G. 1971. Plant Anatomy: Experiment and Interpretation,part 2, Organs. Addison-Wesley, Reading, MA.

CUTTER, E. G. 1978. Plant Anatomy, part 1, Cells and Tissues, 2nd ed. Addison-Wesley, Reading, MA.

DAVIES, P. J., ed. 2004. Plant Hormones: Biosynthesis, Signal Trans-duction, Action!, 3rd ed. Kluwer Academic, Dordrecht.

DE BARY, A. 1884. Comparative Anatomy of the Vegetative Organs of the Phanerogams and Ferns. Clarendon Press, Oxford.

DICKISON, W. C. 2000. Integrative Plant Anatomy. Harcourt/Aca-demic Press, San Diego.

DIGGLE, P. K., and P. K. ENDRESS, eds. 1999. Int. J. Plant Sci. 160 (6, suppl.: Development, Function, and Evolution of Symmetry in Plants), S1–S166.

General References

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EAMES, A. J. 1961. Morphology of Vascular Plants: Lower Groups.McGraw-Hill, New York.

EAMES, A. J., and L. H. MACDANIELS. 1947. An Introduction to Plant Anatomy, 2nd ed. McGraw-Hill, New York.

ESAU, K. 1965. Plant Anatomy, 2nd ed. Wiley, New York.

ESAU, K. 1977. Anatomy of Seed Plants, 2nd ed. Wiley, New York.

ESCHRICH, W. 1995. Funktionelle Pfl anzenanatomie. Springer, Berlin.

FAHN, A. 1990. Plant Anatomy, 4th ed. Pergamon Press, Oxford.

GIFFORD, E. M., and A. S. FOSTER. 1989. Morphology and Evolution of Vascular Plants, 3rd ed. Freeman, New York.

HABERLANDT, G. 1914. Physiological Plant Anatomy. Macmillan, London.

Handbuch der Pfl anzenanatomie (Encyclopedia of Plant Anatomy). 1922–1943; 1951– . Gebrüder Borntraeger, Berlin.

HARTIG, R. 1891. Lehrbuch der Anatomie und Physiologie der Pfl an-zen unter besonderer Berücksichtigung der Forstgewächse.Springer, Berlin.

HAYWARD, H. E. 1938. The Structure of Economic Plants. Macmillan, New York.

HIGUCHI, T. 1997. Biochemistry and Molecular Biology of Wood.Springer, Berlin.

HOWELL, S. H. 1998. Molecular Genetics of Plant Development.Cambridge University Press, Cambridge.

HUBER, B. 1961. Grundzüge der Pfl anzenanatomie. Springer-Verlag, Berlin.

IQBAL, M., ed. 1995. The Cambial Derivatives. Gebrüder Borntrae-ger, Berlin.

JANE, F. W. 1970. The Structure of Wood, 2nd ed. Adam and Charles Black, London.

JEFFREY, E. C. 1917. The Anatomy of Woody Plants. University of Chicago Press, Chicago.

JURZITZA, G. 1987. Anatomie der Samenpfl anzen. Georg Thieme Verlag, Stuttgart.

KAUSSMANN, B. 1963. Pfl anzenanatomie: unter besonderer Berücksichtigung der Kultur- und Nutzpfl anzen. Gustav Fischer, Jena.

KAUSSMANN, B., and U. SCHIEWER. 1989. Funktionelle Morphologie und Anatomie der Pfl anzen. Gustav Fischer, Stuttgart.

LARSON, P. R. 1994. The Vascular Cambium. Development and Structure. Springer-Verlag, Berlin.

MANSFIELD, W. 1916. Histology of Medicinal Plants. Wiley, New York.

MAUSETH, J. D. 1988. Plant Anatomy. Benjamin/Cummings, Menlo Park, CA.

METCALFE, C. R. 1960. Anatomy of the Monocotyledons, vol. I, Gra-mineae. Clarendon Press, Oxford.

METCALFE, C. R. 1971. Anatomy of the Monocotyledons, vol. V, Cyperaceae. Clarendon Press, Oxford.

METCALFE, C. R., and L. CHALK. 1950. Anatomy of the Dicotyledons: Leaves, Stems, and Wood in Relation to Taxonomy with Notes on Economic Uses, 2 vols. Clarendon Press, Oxford.

METCALFE, C. R., and L. CHALK, eds. 1979. Anatomy of the Dicotyledons, 2nd ed., vol. I. Systematic Anatomy of Leaf and Stem, with a Brief History of the Subject. Clarendon Press, Oxford.

METCALFE, C. R., and L. CHALK, eds. 1983. Anatomy of the Dicoty-ledons, 2nd ed., vol. II. Wood Structure and Conclusion of the General Introduction. Clarendon Press, Oxford.

RAUH, W. 1950. Morphologie der Nutzpfl anzen. Quelle und Meyer, Heidelberg.

ROMBERGER, J. A. 1963. Meristems, Growth, and Development in Woody Plants: An Analytical Review of Anatomical, Physiological, and Morphogenic Aspects. Tech. Bull. No. 1293. USDA, Forest Service, Washington, DC.

ROMBERGER, J. A., Z. HEJNOWICZ, and J. F. HILL. 1993. Plant Struc-ture: Function and Development: A Treatise on Anatomy and Veg-etative Development, with Special Reference to Woody Plants.Springer-Verlag, Berlin.

RUDALL, P. 1992. Anatomy of Flowering Plants: An Introduction to Structure and Development, 2nd ed. Cambridge University Press, Cambridge.

SACHS, J. 1875. Text-Book of Botany, Morphological and Physiological. Clarendon Press, Oxford.

SINNOTT, E. W. 1960. Plant Morphogenesis. McGraw-Hill, New York.

SOLEREDER, H. 1908. Systematic Anatomy of the Dicotyledons: A Handbook for Laboratories of Pure and Applied Botany, 2 vols. Clarendon Press, Oxford.

SOLEREDER, H., and F. J. MEYER. 1928–1930, 1933. Systematische Anatomie der Monokotyledonen, No. 1 (Pandales, Helobiae, Triu-ridales), 1933; No. 3 (Principes, Synanthae, Spathifl orae), 1928; No. 4 (Farinosae), 1929; No. 6 (Scitamineae, Microspermae), 1930. Gebrüder Borntraeger, Berlin.

SRIVASTAVA, L. M. 2002. Plant Growth and Development: Hormones and Environment. Academic Press, Amsterdam.

STEEVES, T. A., and I. M. SUSSEX. 1989. Patterns in Plant Develop-ment, 2nd ed. Cambridge University Press, Cambridge.

STRASBURGER, E. 1888–1909. Histologische Beiträge, nos. 1–7. Gustav Fisher, Jena.

TOMLINSON, P. B. 1961. Anatomy of the Monocotyledons, vol. II. Palmae. Clarendon Press, Oxford.

TOMLINSON, P. B. 1969. Anatomy of the Monocotyledons, vol. III. Commelinales—Zingiberales. Clarendon Press, Oxford.

TROLL, W. 1954. Praktische Einführung in die Pfl anzenmorphologie,vol. 1, Der vegetative Aufbau. Gustav Fischer, Jena.

TROLL, W. 1957. Praktische Einführung in die Pfl anzenmorphologie,vol. 2, Die blühende Pfl anze. Gustav Fischer, Jena.

WARDLAW, C. W. 1965. Organization and Evolution in Plants.Longmans, Green and Co., London.

xx | General References

Structure and Development of the Plant Body—An Overview

CHAPTER ONE

The complex multicellular body of a vascular plant is a result of evolutionary specialization of long duration—specialization that followed the transition of multicellu-lar organisms from an aquatic habitat to a terrestrial one (Niklas, 1997). The requirements of the new and harsher environments led to the establishment of morphological and physiological differences among the parts of the plant body so that they became more or less strongly specialized with reference to certain functions. The rec-ognition of these specializations by botanists became embodied in the concept of plant organs (Troll, 1937; Arber, 1950). At fi rst, botanists visualized the existence of many organs, but later as the interrelationships among the plant parts came to be better understood, the number of vegetative organs was reduced to three: stem, leaf, and root (Eames, 1936). In this scheme, stem and leaf are commonly treated together as a mor-phological and functional unit, the shoot.

Researchers in evolution postulate that the organiza-tion of the oldest vascular plants was extremely simple, perhaps resembling that of the leafl ess and rootless Devonian plant Rhynia (Gifford and Foster, 1989; Kenrick and Crane, 1997). If the seed plants have evolved from rhyniaceous types of plants, which con-

sisted of dichotomously branched axes without append-ages, the leaf, the stem, and the root would be closely interrelated through phylogenetic origin (Stewart and Rothwell, 1993; Taylor and Taylor, 1993; Raven, J. A. and Edwards, 2001). The common origin of these three organs is even more obvious in their ontogeny (develop-ment of an individual entity), for they are initiated together in the embryo as the latter develops from the unicellular zygote into a multicellular organism. At the apex of the shoot the leaf and stem increments are formed as a unit. At maturity, too, the leaf and stem imperceptibly merge with one another both externally and internally. In addition, the root and the stem consti-tute a continuum—a continuous structure—and have many common features in form, anatomy, function, and method of growth.

As the embryo grows and becomes a seedling, stem and root increasingly deviate from one another in their organization (Fig. 1.1). The root grows as a more or less branched cylindrical organ; the stem is composed of nodes and internodes, with leaves and branches attached at the nodes. Eventually the plant enters the reproductive stage when the shoot forms infl orescences and fl owers (Fig. 1.2). The fl ower is sometimes called

1

Esau’s Plant Anatomy, Third Edition, By Ray F. Evert.Copyright © 2006 John Wiley & Sons, Inc.

2 | Esau’s Plant Anatomy, Third Edition

A

B

C

D

epicotyl

cotyledons

FIGURE 1.1

Some stages in development of the fl ax (Linum usitatis-simum) seedling. A, germinating seed. The taproot (below interrupted line) is the fi rst structure to pene-trate the seed coat. B, the elongating hypocotyl (above interrupted line) has formed a hook, which subsequently will straighten out, pulling the cotyledons and shoot apex above ground. C, after emergence above ground, the cotyledons, which in fl ax persist for about 30 days, enlarge and thicken. The developing epicotyl—the stem-like axis or shoot above the cotyledons—is now apparent between the cotyledons. D, the developing epicotyl has given rise to several foliage leaves, and the taproot to several branch roots. (From Esau, 1977; drawn by Alva D. Grant.)

sepals

petals

A

B

C

FIGURE 1.2

Infl orescence and fl owers of fl ax (Linum usitatissimum).A, infl orescence, a panicle, with intact fl owers showing sepals and petals. B, fl ower, from which the sepals and petals have been removed, to show the stamens and gynoecium. Flax fl owers usually have fi ve fertile stamens. The gynoecium consists of fi ve united carpels, with fi ve distinct styles and stigmas. C, mature fruit (capsule) and persistent sepals. (Drawn by Alva D. Grant.)

Structure and Development of the Plant Body—An Overview | 3

an organ, but the classical concept treats the fl ower as an assemblage of organs homologous with the shoot. This concept also implies that the fl oral parts—some of which are fertile (stamens and carpels) and others sterile (sepals and petals)—are homologous with the leaves. Both the leaves and the fl oral parts are thought to have originated from the kind of branch systems that charac-terized the early, leafl ess and rootless vascular plants (Gifford and Foster, 1989).

Despite the overlapping and intergrading of charac-ters between plant parts, the division of the plant body into morphological categories of stem, leaf, root, and fl ower (where present) is commonly resorted to because it brings into focus the structural and the functional specialization of parts, the stem for support and conduc-tion, the leaf for photosynthesis, and the root for anchor-age and absorption. Such division must not be emphasized to the degree that it might obscure the essential unity of the plant body. This unity is clearly perceived if the plant is studied developmentally, an approach that reveals the gradual emergence of organs and tissues from a relatively undifferentiated body of the young embryo.

❙ INTERNAL ORGANIZATION OF THE PLANT BODYThe plant body consists of many different types of cell, each enclosed in its own cell wall and united with other cells by means of a cementing intercellular sub-stance. Within this united mass certain groupings of cells are distinct from others structurally or function-ally or both. These groupings are referred to as tissues.The structural variations of tissues are based on differ-ences in the component cells and their type of attach-ment to each other. Some tissues are structurally relatively simple in that they consist of one cell type; others, containing more than one cell type, are complex.

The arrangement of tissues in the plant as a whole and in its major organs reveals a defi nite structural and functional organization. Tissues concerned with con-duction of food and water—the vascular tissues—form a coherent system extending continuously through each organ and the entire plant. These tissues connect places of water intake and food synthesis with regions of growth, development, and storage. The nonvascular tissues are similarly continuous, and their arrangements are indicative of specifi c inter-relations (e.g., between storage and vascular tissues) and of specialized functions (e.g., support or storage). To emphasize the organization of tissues into large entities showing topographic continuity, and reveal-ing the basic unity of the plant body, the expres-sion tissue system has been adopted (Sachs, 1875; Haberlandt, 1914; Foster, 1949).

Although the classifi cation of cells and tissues is a somewhat arbitrary matter, for purposes of orderly description of plant structure the establishment of cat-egories is necessary. Moreover, if the classifi cations issue from broad comparative studies, in which the vari-ability and the intergrading of characters are clearly revealed and properly interpreted, they not only are descriptively useful but also refl ect the natural relation of the entities classifi ed.

The Body of a Vascular Plant Is Composed of Three Tissue Systems

According to Sachs’s (1875) convenient classifi cation based on topographic continuity of tissues, the body of a vascular plant is composed of three tissue systems, the dermal, the vascular, and the fundamental (or ground). The dermal tissue system comprises the epidermis,that is, the primary outer protective covering of the plant body, and the periderm, the protective tissue that supplants the epidermis, mainly in plants that undergo a secondary increase in thickness. The vascular tissue system contains two kinds of conducting tissues, the phloem (food conduction) and the xylem (water con-duction). The epidermis, periderm, phloem, and xylem are complex tissues.

The fundamental tissue system (or ground tissue system) includes the simple tissues that, in a sense, form the ground substance of the plant but at the same time show various degrees of specialization. Paren-chyma is the most common of ground tissues. Paren-chyma cells are characteristically living cells, capable of growth and division. Modifi cations of parenchyma cells are found in the various secretory structures, which may occur in the ground tissue as individual cells or as smaller or larger cell complexes. Collenchyma is a living thick-walled tissue closely related to parenchyma; in fact, it is commonly regarded as a form of paren-chyma specialized as supporting tissue of young organs. The fundamental tissue system often contains highly specialized mechanical elements—with thick, hard, often lignifi ed walls—combined into coherent masses as sclerenchyma tissue or dispersed as individual or as small groups of sclerenchyma cells.

Structurally Stem, Leaf, and Root Differ Primarily in the Relative Distribution of the Vascular and Ground Tissues

Within the plant body the various tissues are distributed in characteristic patterns depending on plant part or plant taxon or both. Basically the patterns are alike in that the vascular tissue is embedded in ground tissue and the dermal tissue forms the outer covering. The principal differences in the structure of stem, leaf, and root lie in the relative distribution of the vascular and ground tissues (Fig. 1.3). In the stems of eudicotyledons

4 | Esau’s Plant Anatomy, Third Edition

leaf bases

stem inprimary growth

stem insecondary growth

root inroot insecondary growthsecondary growth

root insecondary growth

leaf subtendingthe axillary shoot

primary phloem

primary xylem

axillary shoot

vascular rays

phellem (cork)pericyclevascular cambium

secondary xylem

root apex

rootcap

epidermisvascular cylinder

lateral vein

midvein

vascular bundles

mesophyll

epidermis

cortex

procambiumpith

leaf trace gap

shoot apex young leaves

cortex

primary xylemepidermis

cortex

endodermis

secondary phloem

primary phloem

vascular cylinder

primary phloem

pericycle

epidermis

cortexpith

vascular bundles

primary phloem

primary xylem

vascular cambiumsecondary xylem

primary phloem fiberssecondary phloem

primary xylem

epidermis

cortex

pith

A

B

C

E

H

G

F

root in primary growth

leaf blade

D

FIGURE 1.3

Organization of a vascular plant. A, habit sketch of fl ax (Linum usitatissimum) in vegetative state. Transverse sec-tions of stem at B, C, and of root at D, E. F, longitudinal section of terminal part of shoot with shoot apex and devel-oping leaves. G, transverse section of leaf blade. H, longitudinal section of terminal part of root with root apex (covered by rootcap) and subjacent root regions. (A, ×2/5; B, E, F, H, ×50; C, ×32; D, ×7; G, ×19. A, drawn by R. H. Miller.)

Structure and Development of the Plant Body—An Overview | 5

FIGURE 1.4

Types of stem anatomy in angiosperms. A, transverse section of stem of Helianthus, a eudicot, with discrete vascular bundles forming a single ring around a pith. B, transverse section of stem of Zea, a monocot, with the vascular bundles scattered throughout the ground tissue. The bundles are more numerous near the periphery. (From Esau, 1977.)

(eudicots), for example, the vascular tissue forms a “hollow” cylinder, with some ground tissue enclosed by the cylinder (pith, or medulla) and some located between the vascular and dermal tissues (cortex) (Figs. 1.3B, C and 1.4A). The primary vascular tissues may appear as a more or less continuous cylinder within the ground tissue or as a cylinder of discrete strands, or bundles, separated from one another by ground tissue. In the stems of most monocotyledons (monocots) the vascular bundles occur in more than one ring or appear scattered throughout the ground tissue (Fig. 1.4B). In the latter instance the ground tissue often cannot be distinguished as cortex and pith. In the leaf the vascular tissue forms an anastomosing system of veins, which thoroughly permeate the mesophyll, the ground tissue of the leaf that is specialized for photosynthesis (Fig. 1.3G).

The pattern formed by the vascular bundles in the stem refl ects the close structural and developmental relationship between the stem and its leaves. The term “shoot” serves not only as a collective term for these two vegetative organs but also as an expression of their intimate physical and developmental association. At each node one or more vascular bundles diverge from the strands in the stem and enter the leaf or leaves attached at that node in continuity with the vasculature

of the leaf (Fig. 1.5). The extensions from the vascular system in the stem toward the leaves are called leaf traces, and the wide gaps or regions of ground tissue in the vascular cylinder located above the level where leaf traces diverge toward the leaves are called leaf trace gaps (Raven et al., 2005) or interfascicular regions (Beck et al., 1982). A leaf trace extends from its connection with a bundle in the stem (called a stem bundle, or an axial bundle), or with another leaf trace, to the level at which it enters the leaf (Beck et al., 1982).

Compared with the stem, the internal structure of the root is usually relatively simple and closer to that of the ancestral axis (Raven and Edwards, 2001). Its rela-tively simple structure is due in large part to the absence of leaves and the corresponding absence of nodes and internodes. The three tissue systems in the primary stage of root growth can be readily distinguished from one another. In most roots, the vascular tissues form a solid cylinder (Fig. 1.3E), but in some they form a hollow cylinder around a pith. The vascular cylinder comprises the vascular tissues and one or more layers of nonvas-cular cells, the pericycle, which in seed plants arises from the same part of the root apex as the vascular tissues. In most seed plants branch, or lateral, roots arise in the pericycle. A morphologically differentiated

A B

1 m

m

1 m

m

6 | Esau’s Plant Anatomy, Third Edition

peridermcollenchyma

leaf tracegap

leaf trace

sympodium

median trace lateral trace

A B

5

75

64

86

4

68

46

57

1 1 1 1

2 2 2

3 3 33

4 8 6 4 6 8 4 6 5 7 56575

FIGURE 1.5

Diagrams illustrating primary vascular system in the stem of elm (Ulmus), a eudicot. A, transverse section of stem showing the discrete vascular bundles encircling the pith. B, longitudinal view showing the vascular cylinder as though cut through median leaf trace 5 and spread out in one plane. The transverse section (A) corresponds to the topmost view in B. The numbers in both views indicate leaf traces. Three leaf traces—a median and two lateral traces—connect the vascular system of the stem with that of the leaf. A stem bundle and its associated leaf traces are called a sympodium. (From Esau, 1977; after Smithson, 1954, with permission of the Council of the Leeds Philo-sophical and Literary Society.)

endodermis (the innermost, and compactly arranged, layer of cells of the cortex in seed plants) typically sur-rounds the pericycle. In the absorbing region of the root the endodermis is characterized by the presence of Cas-parian strips in its anticlinal walls (the radial and trans-verse walls, which are perpendicular to the surface of the root) (Fig. 1.6). In many roots the outermost layer of cortical cells is differentiated as an exodermis,which also exhibits Casparian strips. The Casparian strip is not merely a wall thickening but an integral band-like portion of the wall and intercellular substance that is impregnated with suberin and sometimes lignin. The presence of this hydrophobic region precludes the passage of water and solutes across the endodermis and exodermis via the anticlinal walls (Lehmann et al., 2000).

❙ SUMMARY OF TYPES OF CELLS AND TISSUESAs implied earlier in this chapter, separation of cells and tissues into categories is, in a sense, contrary to the fact that structural features vary and intergrade with each other. Cells and tissues do, however, acquire differential

properties in relation to their positions in the plant body. Some cells undergo more profound changes than others. That is, cells become specialized to varied degrees. Cells that are relatively little specialized retain living proto-plasts and have the capacity to change in form and func-tion during their lifetimes (various kinds of parenchyma cells). More highly specialized cells may develop thick, rigid cell walls, become devoid of living protoplasts, and cease to be capable of structural and functional changes (tracheary elements and various kinds of sclerenchyma cells). Between these two extremes are cells at varying levels of metabolic activity and degrees of structural and functional specialization. Classifi cations of cells and tissues serve to deal with the phenomena of differentia-tion—and the resultant diversifi cation of plant parts—in a manner that allows making generalizations about common and divergent features among related and unre-lated taxa. They make possible treating the phenomena of ontogenetic and phylogenetic specialization in a com-parative and systematic way.

Table 1.1 summarizes information on the generally recognized cate