40. 44.

I ~'

A selection of Hartig's (1837) drawings illustrating his Vergleichende Untersuchungen iiber die Organisation des Stammes der einheimischen Waldbiiume: Fig. 23. Xylem element (species not mentioned); Fig.24. course of vascular bundles in a nodal area (species not mentioned); Fig. 40. sieve fibers ("Siebfasem") in a peripheral section of Pinus sylvestris; Fig. 41. sieve pores viewed from the ray side (Pinus sylvestris); Fig. 42. sieve pores in sieve fibers of Acer, Aesculus, Carpinus; a. sieve area of young sieve fiber of Carpinus; Fig. 43. part of a sieve tube of Acer; a. sieve-like perforated cross walls in sieve tubes of Acer, Robinia (from pp 157-158; Hartig did not provide legends)

H.-D. Behnke R. D. Sjolund (Eds.)

Sieve Elements Comparative Structure, Induction and Development

With 266 Figures

Springer-Verlag Berlin Heidelberg New York London Paris Tokyo Hong Kong

Professor Dr. H.-D. Behnke

Zellenlehre, Universitat Heidelberg 1m Neuenheimer Feld 230 0-6900 Heidelberg, FRO

Professor Dr. R. D. Sjolund

Department of Botany University of Iowa Iowa City, Iowa 52242, USA

Cover: Longitudinal section through the phloem of Cheiranthus cheiri with mature sieve element in center. (From Behnke 1981, Nordic J Bot 1: 381-400)

ISBN-13: 978-3-642-74447-1 e-ISBN-13: 978-3-642-74445-7 DO I: 10.1007/ 978-3-642-74445-7

This work is subject to copyright. All rights are reserved, whether the whole or part of the material is con­cerned, specifically the rights of translation, reprinting, re-use of illustrations, recitation, broadcasting, repro­duction on microfilms or in other ways, and storage in data banks. Duplication of this publication or parts thereof is only permitted under the provisions of the German Copyright Law of September 9, 1965, in its version of June 24, 1985, and a copyright fee must always be paid. Violations fall under the prosecution act of the German Copyright Law.

© Springer-Verlag Berlin Heidelberg 1990 Softcover reprint of the hardcover 1st edition 1990

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Typesetting : Appl, Wemding 213113145-543210 Printed on acid-free paper

Preface

As part of his Comparative Investigations of the Organization of the Trunk of the Native Forest Trees (Theodor Hartig 1837, Vergleichende Untersuchungen tiber die Organisation des Stammes der einheimischen Waldbaume. lahresberichte tiber die Fortschritte der Forstwissenschaften und forstlichen Naturkunde 1: 125-168) Hartig gives an anatomical description of the "composition and nature" of the then "completely uninvestigated elementary organs" of what he called the "sap skin" (Safthaut) of trees, a tissue for which Nageli later (1858) coined the term phloem. Within the "Safthaut" Hartig describes three cell types in detail, (1) "Siebfasern", (2) "Siebrohren", and (3) "keulenfOrmige Saftrohren" (club-shaped sap-tubes). While the description of the latter refers to laticifers in Euphorbia and resin ducts in Acer and Robinia. "Siebfasern" and "Siebrohren" comprise the sieve elements.

A literal translation of the more significant parts of the description of these cell types demonstrates that his "Siebrohren" entirely correspond to what has later been defined as "sieve tubes" but that his "Siebfasern" are less well­defined and in addition to what we call "sieve cells" also include small sieve tubes as well as spindle-shaped cells of cambium, phloem parenchyma and sclerenchyma. Both in his "Siebfasern" and "Siebrohren" Hartig describes sieve areas (his expression is "lense-shaped cavities") and sieve pores (Siebporen). from page 157: "1) Sieve fibers ... We are able to shortly characterize them, if we say that they correspond most to xylem fibers of the conifers both in form and in position. Comparable to these, they show on the sides facing the rays lense-shaped cavities in the inter­cellular space ... which are penetrated by a great number of smaller pores. Fig. 40 shows sieve fibers in a peripheral section from Pinus sylvestris. Fig. 41 shows sieve pores as viewed from the ray .... Their formation within conifers and deciduous trees basically is the same. In Alnus. Aesculus. Carpinus they are distinguished by size of both the sieve fibers and the sieve pores, Fig. 42. In Car­pinus it can be seen that in those sieve fibers which are closest to the wood the concavity of the cell wall, it is true, is already present, and even more depressed than at a later time, but no porosity is displayed, instead, however, the surface of the concavity appears to be occupied with small warts, Fig. 42 a. Are they perhaps small, in the pores lying vesicles? ... " from page 158: "2) Sieve tubes The sieve tube is to be paralleled to the xylem vessel as is the sieve fiber to the

VI Preface

xylem fiber. They are delicate tubes of considerable diameter which are densely covered by sieve pores at sides not adjacent to rays, while at sides facing the rays only roundish cavities, contoured by faint shadows, are shown; a detail by which they are distinguished from sieve fibers, the pores of which are always on the ray side. Their nature and their relationship to xylem vessels may best be seen in the chestnut and in the maple from which I have depicted a part of a tube, Fig.44." [This obviously is a misprint and should refer to Fig. 43, since according to Hartig's earlier description Fig. 44 refers to sieve fibers of Acer showing a "transition to pachydermal cells".] "At places where the sieve pores are arranged very densely, the tube looks like a netlike spiral vessel with pitted meshes; however, it can be distinctly recognized that the network is formed by the close proximity of the sieve pores only. Without any visible segmentation of the sieve tube into single members, sieve-like perforated cross walls can be seen within the inner lumen at rather wide distances, Fig. 43 a (Acer, Robinia). The pores are almost regularly hexagonal and sit so close together that the remain­ing cell wall looks like a network .... " (See frontispiece for reproduction of figures)

In the 150 years since the publication of Hartig's description of the phloem, our knowledge about the structure and the function of sieve elements has increased greatly. The improved resolution made possible initially by refinements in the light microscope, and more recently through the development of the electron microscope, has provided modem investigators a tool with which to extend Hartig's early and limited observations down to the current level of organelles, membranes and macromolecules. This book reviews the structure of the con­ducting elements of the major plant groups, from the algae to the flowering plants, from extant and extinct groups (Chaps. 1 to 7 and 14), revealing both common features and divergent solutions to the problem of nutrient transport. Additional information about phloem structure and function is provided in the coverage of special cases of phloem deVelopment (Chaps. 8 and 12), experi­mental systems that provide new insight in sieve element induction and forma­tion (Chaps. 9 to 11), and of specific phloem contents (Chap. 13).

From these pages it will become clear, however, that, despite 150 years of progress, many fundamental questions concerning sieve-element structure, development and function remain to be resolved.

Portions of this book were presented during the XIVth International Botani­cal Congress, Berlin 1987, in a symposium commemorating Theodor Hartig's first description of sieve elements, 150 years ago.

October, 1989 H.-Dietmar Behnke, Heidelberg and Richard D. Sjolund, Iowa City, Iowa

Contents

Preface. v

1 Algae ______________________________________________ ___

2

3

KLAUS SCHMITZ 1.1 Requirement for Medium-Distance and Long-Distance Transport

in Algae ........... . 1.2 Medium-Distance Transport .. 1.3 Long-Distance Transport . . . . 2 1.4 Conducting Cells of Red Algae. 2 1.5 Conducting Cells in Brown Algae 5

1.5.1 General Remarks ..... 5 1.5.2 Conducting Cells in Dictyotales, Scytosiphonales,

Desmarestiales and Fucales . . . 5 1.5.3 Sieve Elements in Laminariales. . . . . . . . . . .

Mosses DANIEL C. SCHEIRER 2.1 Introduction ..

2.1.1 Overview 2.1.2 Terminology

2.2 General Organization of Conducting Tissues in Mosses 2.2.1 The Gametophyte .. 2.2.2 The Sporophyte ...............

2.3 Structure of Sieve Elements . . . . . . . . . . . . . 2.3.1 General Features of Moss Sieve Elements . 2.3.2 Differentiating and Mature Sieve Elements

2.4 Associated Parenchyma . ..............

Seedless Vascular Plants RAy F. EVERT 3.1 Introduction . . . . . . . . . . 3.2 The Sieve-Element Protoplast

3.2.1 Nucleus ........ . 3.2.2 Endoplastic Reticulum 3.2.3 Plastids and Mitochondria 3.2.4 Dictyosomes . . . . . . . .

8

19 19 19 20 20 20 21 21 21 31

35 35 37 40 40 41

VIII Contents

3.2.5 Microtubules and Microfilaments 42 3.2.6 Plasmalemma and Tonoplast 42 3.2.7 Refractive Spherules. 43

3.3 The Wall . . . . . . . . . . . . . . . 48 3.4 The Sieve Areas . . . . . . . . . . . 51 3.5 Parenchymatous Cells Associated with the Sieve Elements 56 3.6 Longevity of the Sieve Elements 57 3.7 Comments on Terminology . . . . . . . . . . . . . . . . . . 57

4 Conifers _____________________________________________ ___

ALEXANDER SCHULZ

4.1 Introduction............... 63 4.2 General Description . . . . . . . . . . . 64

4.2.1 Primary and Secondary Phloem 64 4.2.2 Shape and Size of Sieve Cells . 65

4.3 Development of the Sieve Cell 67 4.3.1 The Nucleus 68 4.3.2 Plastids.... 70 4.3.3 Mitochondria 73 4.3.4 Dictyosomes 75 4.3.5 Endoplasmic Reticulum (ER) and Ribosomes 75 4.3.6 Vacuole and Ground Plasm. 79 4.3.7 Structural Proteins . . . . . . . 80 4.3.8 The Wall . . . . . . . . . . . . 80 4.3.9 Intercellular Communication . 81

4.4 Strasburger Cells. . . . . . . . . . . . 83

5 Cycads and Gnetophytes _____________________________ _ H.-DIETMAR BEHNKE

5.1 Introduction....................... 89 5.2 Cycads . . . . . . . . . . . . . . . . . . . . . . . . . . 91

5.2.1 Organization and Composition of the Phloem 91 5.2.2 Ultrastructure of the Sieve Elements . . . . . . 91 5.2.3 Parenchymatous Cells Associated with the Sieve Elements 95

5.3 Gnetophytes........................... 95 5.3.1 Organization and Composition of the Phloem ....... 95 5.3.2 Ontogeny and Structure of the Mature Sieve Element . .. 97 5.3.3 Parenchymatous Cells Associated with the Sieve Elements 100

6 Dicotyledons ____________________________________________ _ RAy F. EVERT

6.1 Introduction............. 103 6.2 The Sieve-Tube Member Protoplast 103

6.2.1 Nucleus............ 105

Contents IX

6.2.2 Endoplasmic Reticulum. . 106 6.2.3 Plastids and Mitochondria 107 6.2.4 Dictyosomes ........ 109 6.2.5 Microtubules and Microfilaments 110 6.2.6 Plasmalemma and Tonoplast 110 6.2.7 P-Protein 111

6.3 The Wall ......... 119 6.4 The Sieve Plate. . . . . . 121 6.5 The Lateral Sieve Areas . 124 6.6 Parenchymatous Cells Associated with Sieve-Tube Members 125 6.7 Longevity of Sieve-Tube Members . . . . . . . . . . . . . . . 130

7 Monocotyledons ELEFTHERIOS P. ELEFTHERIOU 7.1 Introduction 139 7.2 Ontogeny .... 139 7.3 The Protoplast . 141

7.3.1 Nucleus. 141 7.3.2 Plastids . 146 7.3.3 Endoplasmic Reticulum and Mitochondria 151 7.3.4 Microtubules and Dictyosomes . 151 7.3.5 P-Protein ......... 154 7.3.6 Vacuoles and Tonoplast . 154

7.4 Cell Wall ............ 155 7.5 Thick-Walled Sieve Elements. 155 7.6 Sieve Plates. . . . . . . . . . . 156

8 Sieve Elements in Internodal and Nodal Anastomoses of the Monocotyledon Liana Dioscorea ______________ _ H.-DIETMAR BEHNKE 8.1 Introduction.......................... 161 8.2 The Vascular Construction in the Aerial Stem of Dioscorea 163 8.3 The Specific Composition of Phloem Anastomoses . 168 8.4 Ultrastructure of the Sieve Elements of Anastomoses 170

8.4.1 Connecting Sieve-Tube Members (CST) . . . 170 8.4.2 Anastomosal Sieve-Tube Members (ANST) . . 173 8.4.3 Anastomosal Sieve Elements (ANSE) . . . . . 173

8.5 Parenchymatous Cells Associated with the Sieve Elements of Anastomoses. . . . . . . . . . . . . . . . . . . . . . . . . 175

8.6 Some Physiological Implications of Nodal Anastomoses ... 177

X Contents

9 Sieve Elements in Plant Tissue Cultures: Development, Freeze-Fracture, and Isolation RICHARD D. SJOLUND 9.1 Introduction ............... 179 9.2 Phloem Function in Vitro . . . . . . . . 180 9.3 Phloem Development in Callus Tissues 181 9.4 P-Protein, Callus Phloem and Wounding 181 9.5 Freeze-Fracture Studies Using Callus Sieve Elements 185 9.6 Sieve-Area Pores . . . . . . . . . . . . . . . . . . . . . 185 9.7 The Sieve-Element Reticulum (SER). . . . . . . . . . 187 9.8 Isolation and Partial Purification of Callus Sieve Elements 193 9.9 Antibody Formation Against Callus Sieve Elements .... 195

10 Wound-Sieve Elements __________________ _ ALEXANDER SCHULZ 10.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . 199 10.2 Tissue Changes During Wound-Phloem Development. 199

10.2.1 Tissue of Origin . . . . . . . . . . . . . . . 199 10.2.2 Developmental Pattern of Wound Phloem 201 10.2.3 Size and Shape of Wound-Sieve Elements. 203

10.3 Cytoplasm of Wound-Sieve Elements 205 10.3.1 Nucleus and Vacuole . . . . . . 205 10.3.2 Sieve-Element Plastids ..... 207 10.3.3 Mitochondria and Dictyosomes 208 10.3.4 Endoplasmic Reticulum and Ribosomes 208 10.3.5 P-Protein and Microtubules. . . . . . . . 209

10.4 Symplastic Connections of Wound-Sieve Elements. 210 10.4.1 Connections Between Sieve Elements . . . . 210 10.4.2 Connections from Sieve Elements to Other Cell Types 214

10.5 Companion Cells . . . . . . . . . . . . . . . . . . . . . . . 215 10.6 Comparison Between Wound- and Bundle-Sieve Elements . 215

11 Sieve Elements of Graft Unions _______________ _ RAINER KOLLMANN and CHRISTL GLOCKMANN 11.1 Introduction . . . . . . . . . . . . . . . . 219 11.2 Grafting Procedure ..... . . . . . . . 221 11.3 Histology and Cytology of the Graft Union . 221

11.3.1 General Aspects of Development .. 221 11.3.2 Sieve-Element Contact at the Graft Interface 224

11.4 Function of Phloem Connections in Graft Unions . 232 11.5 Questions Concerning the Mechanism of Sieve-Element

Formation in Graft Unions . . . . . . . . . . . . . . . . . ?33

12 Sieve Elements in Haustoria of Parasitic Angiosperms INGE DORR

Contents XI

12.1 Introduction . . . . . . . . . . . . . . . . . 239 12.2 Phloem in the Haustorium of Cuscuta . . . 239 12.3 Development of Haustorial Sieve Elements 243 12.4 The Contact Hypha of Cuscuta. . . . . . . 249 12.5 Phloem in the Haustoria of Different Parasitic Plants 251 12.6 Comparative Aspects . . . . . . . . . . . . . . . . . . 253

13 Phloem Proteins _____________________ _ JAMES CRONSHAW and DINKAR D. SABNIS

13.1 Introduction . . . . 257 13.2 P-Protein . . . . . . 258

13.2.1 Distribution 259 13.2.2 Morphology 259 13.2.3 Filamentous (Fibrillar) P-Proteins 259 13.2.4 Tubular P-Protein . . . . . . . . . 261 13.2.5 Crystalline P-Proteins . . . . . . . 262 13.2.6 P-Protein Bodies and Their Formation. 264 13.2.7 Dispersal of P-Protein Bodies. . . . 267 13.2.8 P-Protein in Mature Sieve Elements 268 13.2.9 P-Protein in Sieve-Plate Pores 268

13.3 Other Phloem-Specific Proteins 269 13.3.1 Nuclear Inclusions. . . . . . . 269 13.3.2 Plastid Inclusions . . . . . . . 269 13.3.3 Refractive Spherules and Other Vesicles . 270 13.3.4 Proteins Associated with the Endoplasmic Reticulum 270

13.4 Biochemistry of Phloem Proteins. . . . . . . . . . . . 270 13.4.1 Isolation and Chemical Properties . . . . . . . 270 13.4.2 Lectin Properties of Phloem-Specific Proteins. 273 13.4.3 Comparative Aspects . . . . . . . . . . . . . . 278

14 Phloem Evolution: An Appraisal Based on the Fossil Record ____ _ EDITH L. TAYLOR

14.1 Introduction . . . . . . . . . . . . . . . . 285 14.1.1 Phloem Phylogeny - Background 289

14.2 Phloem of Vascular Cryptogams . 290 14.3 Gymnosperm Phloem . . . . . . . 293 14.4 Conclusions - Phloem Phylogeny 294

Index ....................................... 299

Contributors

H.-DIETMAR BEHNKE

Zellenlehre Universitat Heidelberg 1m Neuenheimer Feld 230 0-6900 Heidelberg, FRG

JAMES CRONSHA W

Department of Biological Sciences University of California Santa Barbara, CA 93106 USA

INGE DORR

Botanisches Institut der Universitat Olshausenstr. 40 0-2300 Kiel, FRG

ELEFTHERIOS P. ELEFTHERIOU

Department of Botany University of Thessaloniki GR-540 06 Thessaloniki

RAy F. EVERT

Department of Botany University of Wisconsin 430 Lincoln Drive Madison, WI 53706, USA

CHRISTL GLOCKMANN

Botanisches Institut der Universitat Olshausenstr. 40 0-2300 Kiel, FRG

RAINER KOLLMANN

Botanisches Institut der Universitat Olshausenstr. 40 0-2300 Kiel, FRG

DINKAR D. SABNIS

Department of Plant Science University of Aberdeen St. Machar Drive Aberdeen AB9 2UD, UK

DANIEL C. SCHEIRER

Department of Biology Northeastern University 360 Huntington Avenue Boston, MA 02115, USA

KLAUS SCHMITZ

Botanisches Institut der Universitat Gyrhofstr. 15 0-5000 K6ln 41, FRG

AI,EXANDER SCHULZ

Zellenlehre Universitat Heidelberg 1m Neuenheimer Feld 230 0-6900 Heidelberg, FRG

RICHARD D. SJOLUND

Department of Botany University of Iowa Iowa City, Iowa 52242, USA

EDITH L. TAYLOR

Department of Botany Ohio State University Columbus, Ohio 43210, USA