Solanaceae and Convolvulaceae: Secondary Metabolites

Eckart Eich

Solanaceaeand Convolvulaceae: Secondary Metabolites

Biosynthesis, Chemotaxonomy, Biological and Economic Significance (A Handbook)

Prof. Dr. Eckart EichFreie Universität BerlinInstitut für Pharmazie- Pharmazeutische Biologie -Königin-Luise-Str. 2 + 414195 BerlinGermanyE-mail: eckeich@zedat.fu-berlin.de

ISBN 978-3-540-74540-2 e-ISBN 978-3-540-74541-9

The Library of Congress Control Number: 2007933490

© 2008 Springer-Verlag Berlin Heidelberg

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Cover illustration: Flowers of Ipomoea purpurea (L.) Roth [cultivar; Convolvulaceae] (left)and Solandra maxima (Sessé & Mocino) P.S. Green [Solanaceae] (right). Plotted on the photographs are corresponding constituents: the major anthocyanin pigment and the major alkaloid hyoscyamine, respectively.

„Was du ererbt von deinen Vätern hast, Erwirb es, um es zu besitzen.“

(All that you have, bequeathed you by your fathers,Earn it in order to possess it.)

Johann Wolfgang von Goethe (Faust I)

This book is based on a multitude of results obtained in botany, phytochemistry, and other biological sciences from all over the world since the beginning of modern research two hundred years ago. It is dedicated to all the scientists who have contributed to these results.

Acknowledgments

This interdisciplinary book is a result of my long-standing fascination for the bot-any of solanaceous and convolvulaceous plants as well as their ability to synthesize a multitude of chemical species with their biological activities. However, this book would not have been realized without the support of the following individuals to whom I express my sincere gratitude:

• For conscientious reading and competent commenting on the manuscript of the book: Priv.-Doz. Dr. Kristina Jenett-Siems and Prof. Dr. Heinz H. Pertz, Freie Universität Berlin, Germany (Chaps. 3–8), Priv.-Doz. Dr. Michael Stech, Universiteit Leiden, The Netherlands (Chap. 2), and my daughter, Dr. Susanne Eich-Greatorex, Universitet for miljø- og biovitenskap, Ås, Norway (Chap. 1)

• For introducing me, an ignoramus in computer affairs until 2003, to the secrets of the personal computer and its various functions with patience and unremitting efforts: Dr. Thomas Schimming, Berlin

• For rescue of my personal computer in severe cases of crashes: Dr. Colja Schubert, Heinrich Hertz Institut Berlin

• For long-term botanical advice and information: Daniel F. Austin, Ph.D., Emeritus Professor at Florida Atlantic University, Boca Raton, and Research Associate of the Arizona-Sonora Desert Museum, Tucson, USA

• For the excellent advice and guidance as well as for the generous acceptance of my requests: the life sciences editorial staff of Springer, especially Dr. Jutta Lindenborn and Dr. Dieter Czeschlik, Heidelberg, Germany and the copyeditor, John Kirby, Malvern, UK

• For the contribution of 53 photographs to the Colour Plates of this book taken during our common journeys through predominantly tropical countries, for the essential support in many different respects, e.g., by proof-reading, discussions, excellent organizing, and last but not least for the forbearance of my preoccupation with the book and long-term encouragement: my wife, Elisabeth Bäumel-Eich, Berlin

Berlin, August 2007 Eckart Eich

vii

Contents

1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

1.1 Philosophy and Aims of this Book . . . . . . . . . . . . . . . . . . . . . . . . . . 1 1.1.1 The Large Solanales Families as a Topic . . . . . . . . . . . . . . . 1 1.1.2 General Role of the Secondary Metabolism

for a Specific Characterization and Classification of Plant Taxa . . . . . . . . . . . . . . . . . . . . . . 1

1.1.3 Bird’s-Eye View of Two Centuries of Phytochemical Research on Solanaceae and Convolvulaceae. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

1.2 Secondary Metabolism of the Large Solanales Families . . . . . . . . . 3 1.2.1 Historical Background. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 1.2.2 Common Ground and Differences

of the Solanales Families. . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 1.2.3 Similar Secondary Metabolism of the Large

Solanales Families . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 1.3 Strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 1.4 Criteria for Selection of Secondary Metabolites Based

on their Specific Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 1.5 Accumulation or Low-Level Occurrence

of Secondary Metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 1.6 Significance of Chemotaxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 1.7 Principal Nomenclatural Points . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 1.7.1 Species Names. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 1.7.2 Chemical Trivial Names . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

2 Classification and System in Solanales . . . . . . . . . . . . . . . . . . . . . . . . . 11

2.1 Position of the Order Solanales and its Families . . . . . . . . . . . . . . . 11 2.1.1 Traditional Systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 2.1.2 Phylogenetic Classification Based on Predominantly

(Macro)molecular Data Sets . . . . . . . . . . . . . . . . . . . . . . . . . 12

ix

2.2 Solanaceae A.L. de Jussieu: Delimitation, Intrafamilial Circumscription and Relationships . . . . . . . . . . . . . . . 15

2.2.1 Traditional Systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 2.2.2 Phylogenetic Classification Based on Predominantly

(Macro)molecular Data Sets . . . . . . . . . . . . . . . . . . . . . . . . . 16 2.3 Convolvulaceae A.L. de Jussieu: Delimitation, Intrafamilial

Circumscription and Relationships . . . . . . . . . . . . . . . . . . . . . . . . . . 21 2.3.1 Traditional Systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 2.3.2 Phylogenetic Classification Based on Predominantly

(Macro)molecular Data Sets . . . . . . . . . . . . . . . . . . . . . . . . . 22 2.4 Uncharted Territory with Regard to Secondary

Metabolites of the Solanales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

3 Ornithine-Derived Alkaloids. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33

3.1 Simple Pyrrolidines. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3.1.1 Discovery and Structural Elucidation . . . . . . . . . . . . . . . . . . 65 3.1.2 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 68 3.1.3 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 70 3.1.4 Biosynthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73 3.1.5 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74 3.2 N-Acylpyrrolidines (Pyrrolidides, Pyrrolidine Amides). . . . . . . . . . 74 3.2.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 75 3.2.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 75 3.2.3 Biosynthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76 3.2.4 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76 3.3 Nicotinoids (Tobacco Alkaloids) . . . . . . . . . . . . . . . . . . . . . . . . . . . 77 3.3.1 Discovery and Structure Elucidation. . . . . . . . . . . . . . . . . . . 77 3.3.2 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 87 3.3.3 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 94 3.3.4 Biosynthesis of Pyrrolidine-Type

Nicotinoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94 3.3.5 Biosynthesis of Piperidine-/Piperideine-Type

Nicotinoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 3.3.6 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98 3.4 Tropanes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109 3.4.1 Discovery and Structure Elucidation. . . . . . . . . . . . . . . . . . . 109 3.4.2 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 114 3.4.3 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 130 3.4.4 Biosynthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150 3.4.5 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153 3.5 Calystegines (Polyhydroxylated Nortropanes) . . . . . . . . . . . . . . . . . 160 3.5.1 Discovery and Structure Elucidation. . . . . . . . . . . . . . . . . . . 160 3.5.2 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 164

x Contents

3.5.3 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 165 3.5.4 Biosynthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175 3.5.5 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176 3.6 Indolizidines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177 3.7 Pyrrolizidines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 3.7.1 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 180 3.7.2 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188

4 Tryptophan-derived Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213

4.1 β-Carbolines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213 4.1.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 213 4.1.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 214 4.2 Ergolines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215 4.2.1 Discovery and Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215 4.2.2 Biosynthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218 4.2.3 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 222 4.2.4 Location and Origin of Ergoline Alkaloids. . . . . . . . . . . . . . 241 4.2.5 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 245 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252

5 Miscellaneous Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261

5.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261 5.1.1 Fabianine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261 5.1.2 2-Methoxy-3-isobutylpyrazine . . . . . . . . . . . . . . . . . . . . . . . 261 5.1.3 Nicotianamine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 5.1.4 Solamines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 5.1.5 Pyrrole Alkaloids. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 5.1.6 Benzodiazepines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 5.1.7 Catecholamines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 5.1.8 Betaines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 5.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . . . . . . . 264 5.2.1 Benzylisoquinolines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 5.2.2 Animartinines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266 5.2.3 Lolines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266 5.2.4 Betaines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267 5.2.5 N,N-Diacylspermidines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268

6 Phenylalanine-derived Metabolites / Phenylpropanoids . . . . . . . . . . . 271

6.1 N-Acylphenylethylamines and Derivatives. . . . . . . . . . . . . . . . . . . . 272 6.1.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 272 6.1.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 272

Contents xi

6.2 Cyanogenic Glycosides. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274 6.2.1 Discovery, Distribution in the Plant Kingdom,

Ecological Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274 6.2.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 274 6.3 Cinnamate, Hydroxycinnamates and their Derivatives

(Phenylpropanoids Sensu Latiore) . . . . . . . . . . . . . . . . . . . . . . . . . . 275 6.3.1 Phenylpropanoids Sensu Stricto (C

6C

3 Skeleton) . . . . . . . . . 277

6.3.2 Phenylethanoids (C6C

2 Skeleton) . . . . . . . . . . . . . . . . . . . . . 278

6.3.3 Phenylmethanoids (C6C

1 Skeleton): Benzoates,

Hydroxybenzoates, and their Derivatives . . . . . . . . . . . . . . . 279 6.4 Capsaicinoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 282 6.4.1 Discovery and Structure Elucidation. . . . . . . . . . . . . . . . . . . 282 6.4.2 Botanical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 284 6.4.3 Occurrence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285 6.4.4 Biosynthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 286 6.4.5 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287 6.5 Hydroxycoumarins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292 6.5.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 292 6.5.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 293 6.6 Hydroxycinnamate Conjugates/Caffeic Acid Derivatives . . . . . . . . 294 6.6.1 Long Chain Alkyl Esters

of Hydroxycinnamic Acids . . . . . . . . . . . . . . . . . . . . . . . . . . 294 6.6.2 Hydroxycinnamoyl Glucose Esters

and O-Glucosides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295 6.6.3 Chlorogenic Acid, Dicaffeoylquinic Acids,

and Related Caffeic Acid Derivatives . . . . . . . . . . . . . . . . . . 295 6.6.4 Hydroxycinnamic Acid Amides . . . . . . . . . . . . . . . . . . . . . . 298 6.7 Flavonoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303 6.7.1 Flavones, Flavonols, and their Derivatives . . . . . . . . . . . . . . 304 6.7.2 Flavonoid Sulfates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307 6.7.3 Anthocyanins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 308 6.7.4 Isoflavonoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 319 6.8 Lignans and Neolignans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 321 6.8.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 323 6.8.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 326 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329

7 Terpenoids (Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343

7.1 Hemiterpenoids (C5 Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . . . . . 344

7.1.1 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 344 7.2 Monoterpenoids (C

10 Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . . . . 345

7.2.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 345 7.2.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 347

xii Contents

7.3 Sesquiterpenoids (C15

Isoprenoids). . . . . . . . . . . . . . . . . . . . . . . . . 348 7.3.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . 348 7.3.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . 356 7.4 Diterpenoids (C

20 Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . . . . . . 359

7.4.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . 361 7.4.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . 365 7.5 Triterpenoids (C

30 Isoprenoids). . . . . . . . . . . . . . . . . . . . . . . . . . . . 366

7.5.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . 366 7.5.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . 368 7.6 Phytosterols (C

27–C

29 Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . . . 368

7.6.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . 370 7.6.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . 372 7.7 Steroidal Sapogenins/Saponins (C

27 Isoprenoids) . . . . . . . . . . . . . 372

7.7.1 Discovery and Structure Elucidation . . . . . . . . . . . . . . . . 376 7.7.2 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . 386 7.7.3 Biosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393 7.7.4 Significance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395 7.8 Steroidal Alkaloids/Glycoalkaloids (C

27 Isoprenoids) . . . . . . . . . . 399

7.8.1 Discovery and Structure Elucidation . . . . . . . . . . . . . . . . 412 7.8.2 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . 425 7.8.3 Biosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441 7.8.4 Significance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 447 7.9 Miscellaneous Rare Steroidal Metabolites . . . . . . . . . . . . . . . . . . . 460 7.9.1 Homo-cholestane Glycosides (C

27 + C

2/C

3). . . . . . . . . . . 460

7.9.2 Cardenolides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 460 7.9.3 Cholecalciferol/Vitamin D

3 and Congeners

(C27

Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 461 7.9.4 Estrogens (C

18 Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . 464

7.9.5 Ecdysteroids and Antagonists . . . . . . . . . . . . . . . . . . . . . . 464 7.9.6 Brassinosteroids (C

27 + C

1/C

2 Isoprenoids) . . . . . . . . . . . 465

7.10 Withanolides/Withasteroids (C28

Isoprenoids) . . . . . . . . . . . . . . . . 466 7.10.1 Discovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 466 7.10.2 Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 471 7.10.3 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . 479 7.10.4 Biosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 480 7.10.5 Significance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 480 7.11 Petuniasteroids (C

28 Isoprenoids) . . . . . . . . . . . . . . . . . . . . . . . . . . 483

7.11.1 Discovery and Structures . . . . . . . . . . . . . . . . . . . . . . . . . 483 7.11.2 Ecological Significance. . . . . . . . . . . . . . . . . . . . . . . . . . . 486 7.12 Tetraterpenoids/Carotenoids (C

40 Isoprenoids) . . . . . . . . . . . . . . . . 486

7.12.1 Solanaceae. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487 7.12.2 Convolvulaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 493 7.12.3 Significance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 494 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 495

Contents xiii

8 Secondary Metabolites Derived from Fatty Acids and Carbohydrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525

8.1 Fatty Acids and Their Derivatives . . . . . . . . . . . . . . . . . . . . . . . . . . 525 8.1.1 Fatty Acids. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525 8.1.2 Fatty Acid Amides and Aliphatic Monoamines . . . . . . . . . . 527 8.2 Secondary Carbohydrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 529 8.2.1 Occurrence in the Solanaceae . . . . . . . . . . . . . . . . . . . . . . . . 529 8.2.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 531 8.3 Resin Glycosides (Glycoresins) . . . . . . . . . . . . . . . . . . . . . . . . . . . . 532 8.3.1 Discovery and Structural Elucidation . . . . . . . . . . . . . . . . . . 532 8.3.2 Occurrence in the Convolvulaceae . . . . . . . . . . . . . . . . . . . . 562 8.3.3 Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 564 8.3.4 Convolvulaceous Resin Glycosides versus

Solanaceous Steroidal Glycoalkaloids . . . . . . . . . . . . . . . . . 572 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 573

Appendix: Color Plates of Solanales Species . . . . . . . . . . . . . . . . . . . . . . . 583

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 607

Taxonomic Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 625

xiv Contents

1Introduction

1.1 Philosophy and Aims of this Book

1.1.1 The Large Solanales Families as a Topic

Solanales are from the Mid-Cretaceous (stem node age: 106 my; crown node age: 100 my) (Bremer et al. 2004). Solanaceae and Convolvulaceae are sisters represent-ing the two large families of this order. Their last common ancestor lived about 70 my ago (Durbin et al. 2000). The main objective of the author is to focus on aspects of our extensive knowledge of secondary metabolites in the plant kingdom in order to account for the specific competitiveness and productivity of these two large Solanales families. To this end, it has been necessary to take a bird’s-eye view of 200 years of phytochemical research on the Solanales, since first scientific reports with regard to both families were published in the early nineteenth century. Due to an almost complete lack of phytochemical reports (one single exception) on species of the three remaining, very small families of the order (see Chap. 2), they have not been considered.

1.1.2 General Role of the Secondary Metabolism for a Specific Characterization and Classification of Plant Taxa

While traditional systematics generally focused on morphologic-anatomical charac-ters of plants, in some cases chemotaxonomic aspects with regard to low molecular secondary metabolites were also considered. However, plant biochemistry and chemotaxonomy normally played a minor role in classification. In contrast, phylo-genetic approaches to plant systematics, based on (macro)molecular cladistic analy-ses, have received an extraordinary, increasing significance during the past 25 years (e.g., Judd et al. 1999). In the author’s opinion, our extensive knowledge of secondary metabolites has not yet been integrated into the characterization of plant families, genera, and species to an extent appropriate to its significance. There are enormous numbers of flora from all over the world which document and maintain in

Eckart Eich, Solanaceae and Convolvulaceae: Secondary Metabolites 1© Springer-Verlag Berlin Heidelberg 2008

2 1 Introduction

detail the morphologic-anatomical characters of the different taxa as well as their phytogeographic distribution. There are also extensive, daily growing databases available on specific DNA sequences of many plant species or even on their whole genome. These fields of botanical sciences have been used to characterize plants, especially on the species level.

On the other hand, plant biochemistry is still playing a minor role with regard to the specific characterization of plants. The primary metabolism of plants is more or less ubiquitously the same with few exceptions, e.g., C3 vs C4 plants. Therefore, it is of minor if any use for the characterization of the different taxa. The secondary metabolism as far as low-molecular constituents are concerned can add further important information to the characterization of taxa on different levels. Normal flora written for geographically restricted areas only occasionally included some information on secondary metabolites, e.g., “Flore de Madagascar et des Comores, famille 171, Convolvulaceae” on two pages (Deroin 2001). As a rare exception, the comprehensive monograph “Genera Solanacearum” (Hunziker 2001), based tradi-tionally on morphologic/anatomical characters plus detailed information on chromo-some numbers, also included aspects of the secondary metabolism – fortunately from the phytochemical point of view. As well as a short initial overview of the phytochemistry of the family, some limited but valuable information predomi-nantly on groups/subgroups of secondary metabolites nested within the correspond-ing genera sections – exactly documented by references – were given. However, this information is more genus-orientated, i.e., not species-specific.

1.1.3 Bird’s-Eye View of Two Centuries of Phytochemical Research on Solanaceae and Convolvulaceae

The author wants to place far greater emphasis on the integration of specific bio-chemistry into the individual characterization of taxa in the field of the two large Solanales families. In so doing, he is trying to contribute to a more interdisciplinary way of looking at things by combining botanical and chemical sciences. Chemical characters identified in single species in countless chemistry-oriented papers are not really noticed by botanists though they may be of additional value for the char-acterization of the respective species. It is of little use to note that a species or any other taxon contains, e.g., “alkaloids” or – slightly more specific – “tropane alka-loids”. There are tens of thousands of alkaloids and hundreds of tropane alkaloids. The presence or absence of any single alkaloid or any other metabolite is a specific character and may contribute to the characterization of a taxon.

Similar to other characters, e.g., morphological ones, it must be taken into account that there may be qualitative and quantitative differences in any species due to intraspecific, ontogenetic, and morphogenetic variability, respectively.

Furthermore, from the ecological point of view, differentiation is necessary; it is usually not a class/group of metabolites which is associated with a certain activity. In contrast, two structurally closely related compounds may show clearly different effects.

Every single alkaloid as well as any other metabolite is more or less “bioactive” but in individually diverging qualities (effects, mechanisms of action). Its individual potency and its content (high or low accumulation or presence in traces) in the living plant spe-cies are of considerable significance. To come back to the example of tropane alkaloids, only a small subgroup of them (3α-tropoyloxytropanes and closely related congeners such as hyoscyamine/atropine) is highly poisonous due to an anticholinergic potency. The vast majority of tropane alkaloids do not possess this property.

Due to their relationship with botany and chemistry, other disciplines, such as pharmacognosy, pharmacology/toxicology, agricultural and food sciences, ecology etc., also play a part in this interdisciplinary approach.

Therefore, the author’s objectives are to

● Document the secondary metabolites of the Solanaceae and Convolvulaceae discovered and structurally elucidated in 200 years of phytochemical research as far as low-molecular compounds (“small molecules”) are concerned

● Describe the peculiarities of their secondary metabolism as compared to other plants in the plant kingdom, with main focus on angiosperms

● Show common features in secondary metabolism of both families, as well as their chemotaxonomic relationships

● Demonstrate the special qualities of the family Solanaceae vs the family Convolvulaceae, i.e., their differences

● Compare the special qualities on different intrafamilial taxonomic levels (sub-families, tribes, genera, subgenera, species) of both families, in certain cases also on different intraspecific taxonomic levels (subspecies, sections) of both families

● Consider and integrate the ecological, pharmacological/toxicological, and eco-nomic significance of metabolites from both families

1.2 Secondary Metabolism of the Large Solanales Families

1.2.1 Historical Background

The discovery of morphine as the sleep-inducing principle (“principium somni-ferum”) of the opium poppy, Papaver somniferum L. (Papaveraceae), by the German apothecary Friedrich Wilhelm Sertürner (1783–1841) in 1805 is of par-ticular significance in the history of organic chemistry. It represented not only the first isolation of a basic plant metabolite, but also at least one of the first isolations of a secondary metabolite in the plant kingdom at all (Sertürner 1805; 1817). It was the initial and stimulating step in the search for further basic constituents. Particularly toxic plants have been screened for such compounds, which were named “alkaloids” (alkali-like) according to the proposal of Meissner (1819). It was therefore natural to look at poisonous species like the solanaceous herbs Solanum nigrum (black nightshade), Nicotiana tabacum L. (Virginian tobacco), and Atropa belladonna L. (deadly nightshade or poison black cherry). Thus, at the

1.2 Secondary Metabolism of the Large Solanales Families 3

4 1 Introduction

beginning of scientific research on secondary plant metabolism the relationship between natural compounds and their toxicological/pharmacological/ecological significance led to the isolation and – many decades later – structure elucidation of these compounds. Over the past two centuries this principle has revealed the majority of secondary plant metabolites, i.e., discoveries by “bioassay-guided fractionation/isolation”, the corresponding term in modern methodology of phyto-chemistry. Of course, this has been true not only for alkaloids – though they rep-resent a huge class of secondary metabolites which are especially suitable for this method due to their particularly distinctive biological activities – but also for all other classes of secondary metabolites. The isolation of solanine (Desfosses 1820, 1821), nicotine (Posselt and Reimann 1828), and atropine (Mein 1833; Geiger and Hesse 1833a, b) from the three species mentioned above represented the first alka-loids from the Solanaceae and also their first secondary metabolites in general. A century later, the very first alkaloid from the Convolvulaceae, the 3α- acyloxytropane convolvine, was discovered as a constituent of Convolvulus pseudocantabricusSchrenk. (Orechoff and Konowalowa 1933). Resin glycosides (glycoresins) belong to the early discoveries in this family, e.g., in Ipomoea purga (Wender.)Hayne, Mexican jalap (Cadet de Gassicourt 1817) and I. orizabensis, Mexican scammony (Pellet.) Led. ex Steud. (Johnston 1840). Again, pharmacological reasons led to the isolation of products from plant material, in this case a complex mixture of structurally related resin glycosides as was found later (Mexican jalap resin and Mexican scammonium resin, respectively).

1.2.2 Common Ground and Differences of the Solanales Families

Solanaceae and Convolvulaceae share a number of obvious characters, properties, and other factors, most of them not very surprising due to the fact that they are sisters and a few perhaps only by pure chance:

● Common phylogeny● Morphologic-anatomical similarities● Similar phytogeographic distribution● Similar secondary metabolism● Similar order of magnitude of species in the family (~2500 vs ~1800 species)● One genus dominating by far (Solanum ~1400 species vs Ipomoea ~650 species)● One economically very important food plant containing starch in the tuber

[Solanum tuberosum L. vs Ipomoea batatas (L.) Lam.]● A remarkable number of popular ornamentals – though not suitable as cut flow-

ers, e.g., from the genera Brugmansia, Brunfelsia, Petunia, Solandra, Solanumvs. Argyreia, Convolvulus, Evolvulus, Ipomoea, Merremia

Of course, the fourth point is the decisive one with respect to the objective of this book. Therefore, it shall be presented in more detail.

1.2.3 Similar Secondary Metabolism of the Large Solanales Families

Of course, classes/groups of metabolites which occur (almost) ubiquitously or at least frequently in the plant kingdom (“general secondary metabolites”) are also constituents of both large Solanales families: (i) phenolics such as simple cinnamic acid derivatives (Sect. 6.4), hydroxycoumarins (Sect. 6.6), hydroxycinnamate con-jugates (Sect. 6.7), flavonoids (Sect. 6.8), lignans (Sect. 6.9), (ii) sterols (Sect. 7.6), (iii) carotenoids (Sect. 7.12), (iv) fats/oils and fatty acids (Sect. 8.1), (v) carbohy-drates (Sect. 8.2) etc.

In addition, they share classes/groups of metabolites which occur rarely in the plant kingdom (“specific secondary metabolites”):

● The extensive class of ornithine-derived alkaloids such as hygrines, N- acylpyrrolidines, nicotinoids, tropanes, calystegines (Sects. 3.1–3.5)

● Sesquiterpenoid phytoalexins (Sect. 7.3)

On the other hand, they have in common the absence of the following classes although those are frequent constituents of closely related families also belonging to the lamiids (euasterids I):

● Iridoids (constituents of Apocynaceae, Gentianaceae, Lamiaceae, Rubiaceae)● Volatile oils (essential oils), complex mixtures of lipophilic mono-/ sesquiterpenes

and/or phenylpropanoids secreted in oil cells, secretion ducts/cavities or glandu-lar hairs (constituents of Lamiaceae)

● Condensed tannins (proanthocyanidins; constituents of Rubiaceae)

The following groups lacking in Convolvulaceae represent specific secondary metabolites of certain solanaceous taxa:

● Capsaicinoids (Sect. 6.5)● Steroidal saponins (Sect. 7.7)● Steroidal alkaloids (Sect. 7.8)● Withasteroids (Sect. 7.10)

On the other hand, the following groups lacking in Solanaceae represent specific secondary metabolites of certain convolvulaceous taxa:

● Indolizidine alkaloids (Sect. 3.6)● Pyrrolizidine alkaloids (Sect. 3.7)● Ergolines (Sect. 4.2)● Resin glycosides (glycoresins) (Sect. 8.3)

Erratically occurring specific secondary metabolites, e.g., (i) β-carbolines in both families (Sect. 4.1), (ii) cardenolides (Sect. 7.9.2), in the Solanaceae or (iii) 2-alkylpiperidines (animartinines; Sect. 5.2.2), serotonin-hydroxycinnamic acid amides (ipobscurines; Sect. 6.7.4) in the Convolvulaceae, are not taken into consideration here.

1.2 Secondary Metabolism of the Large Solanales Families 5

6 1 Introduction

1.3 Strategy

Phytochemical studies, published in thousands upon thousands of original reports over two centuries, have produced detailed knowledge on such a huge amount of metabolites in both families that it would be impossible to integrate it all into this monograph. Therefore, it is obvious to attach great significance to those phyto-chemical characters identified above as specific secondary metabolites (definition: Sect. 1.2.3). Such chapters/sections are the centre of attention in this book resulting in a correspondingly comprehensive treatment. Consequently, limitations were nec-essary as far as general secondary metabolites (definition: Sect. 1.2.3) were con-cerned. It has to be added that the existence or lack of recent reviews on a class/group of metabolites in the literature has been another point of consideration in the present book, i.e., a lack of recent reviews has stimulated a more extensive treatment.

1.4 Criteria for Selection of Secondary Metabolites Based on their Specific Significance

The author is well aware of the subjectivity of his selection. Nevertheless, he hopes that it is comprehensible. Due to the frequency of their occurrence, general secondary metabolites are of limited value for the characterization of any taxon independent on its level (family, genus, species) – in contrast to specific secondary metabolites. General secondary metabolites may be interpreted as plesiomorphic characters, whereas derived secondary metabolites apparently represent apomor-phic characters. Of course, this also implies that, from the evolutionary point of view, the former early products may have been lost in certain taxa during the evolu-tion of the plant kingdom. Thus, e.g., simple lignans – low-molecular congeners of lignin macromolecules – are frequent though not ubiquitous constituents of living angiosperms. From the phylogenetic point of view, loss of a plesiomorphic charac-ters may also be evaluated like an apomorphic character in cladistic analyses. This is – in a figurative way – also true for the phytochemical characterization of a taxon: Also absence of a general secondary metabolite or a class/group of such may contribute to the characterization of a certain taxon.

However, there is no doubt that the presence of specific secondary metabolites makes a much more valuable contribution. Consequently, the following criteria for the selection of secondary metabolites to receive a more detailed treatment in this book reflect this opinion. However, it is necessary to take into account additional aspects:

● Criteria of plant-characterizing and chemotaxonomic significance° Specific secondary metabolites or groups of such confined to certain taxa of

one or both large Solanales families (“unique secondary metabolites”), e.g., 3α-tropoyloxytropanes (Sect. 3.4), resin glycosides (Sect. 8.3), sesquiterpe-noid phytoalexins (Sect. 7.3)

° Specific secondary metabolites or groups of such occurring in certain taxa of one or both large Solanales families but also in a restricted number of taxa outside the Solanales, e.g., steroidal alkaloids (Sect. 7.8), pyrrolizidine alka-loids (Sect. 3.7), calystegines (Sect. 3.6)

° Specific secondary metabolites or groups of such derived from classes/groups of general secondary metabolites. Such specific secondary metabo-lites are confined to certain taxa of one or both Solanales families – in con-trast to their generally/frequently occurring congeners, e.g., certain lignanamides (jacpaniculines) in Jacquemontia paniculata or certain sesqui-lignans (bonaspectins) in Bonamia spectabilis (both Convolvulaceae; Sect. 6.9.3) in contrast to members of the same class which belong to general sec-ondary metabolites, i.e., frequently occurring in the plant kingdom, such as pinoresinol- or dibenzylbutyrolactone-type lignans

● The criterion of size of a special taxon (e.g., number of species of a certain genus) – though only if sufficient phytochemical data are available – e.g., genera Solanum/Nicotiana and Ipomoea/Convolvulus, respectively

● Criteria of ecological significance, e.g., nicotinoids (Sect. 3.3), calystegines (Sect. 3.5), ergolines (Sect. 4.2)

● Criteria of pharmacological/toxicological significance, e.g., hyoscyamine/atro-pine (Sect. 3.4), nicotine (Sect. 3.3)

● Criteria of economic significance (economically useful plants: food plants, safety of food plants, production of pure drugs, tobacco products etc.), e.g., cap-saicinoids (Sect. 6.5), steroidal alkaloids (Sect. 7.8), hyoscyamine/atropine (Sect. 3.4), nicotine (Sect. 3.3)

1.5 Accumulation or Low-Level Occurrence of Secondary Metabolites

Another important point with regard to characterization is the question of whether a certain constitutive metabolite or a group of such is accumulated in a certain species or whether it is only present in a very low concentration. Accumulation of constitu-tive metabolites is advantageous, e.g., for defence against herbivores, microorgan-isms, viruses, or plant competitors. However, modern analytical methods such as GC/MS elucidated that many metabolites are present in very low concentrations in one taxon in contrast to their accumulation in another, closely related one. Such cases demonstrate that the principal ability to synthesize a certain compound is given for, e.g., an individual species though this metabolite is not really “used” due to differen-tial expression of the corresponding genes. A species may be rendered poisonous only by accumulation of, e.g., a major alkaloid. However, both accumulation as well as the principal ability to synthesize a certain metabolite – even if only in low amounts – contributes to the phytochemical characterization of a taxon. Accumulation

1.5 Accumulation or Low-Level Occurrence of Secondary Metabolites 7

8 1 Introduction

is another character exceeding a simple low-level presence; therefore, it may be con-sidered as an additional contribution to the characterization of a taxon.

1.6 Significance of Chemotaxonomy

According to Cronquist, cited by Spring and Buschmann (1998) “….. chemical characters are like other characters: they work when they work, and they don’t work when they don’t work. Like all taxonomic characters, they attain their value through correlation with other characters, and perfect correlations are the exception rather than the rule.” Based on comprehensive studies with regard to Fabaceae, Solanaceae, and Lamiaceae, Wink (2003) concluded “The inconsistent secondary metabolite profiles mean that the systematic value of chemical characters become a matter of interpretation in the same way as traditional morphological markers. Thus, the distribution of secondary metabolites has some value for taxonomy but their occurrence apparently reflects adaptations and particular life strategies embedded in a given framework.”

1.7 Principal Nomenclatural Points

1.7.1 Species Names

“Worldwide, not all authors of research papers use the currently accepted name, so caution is necessary and botanical sources should be checked” (Trease and Evans 2002). The author of the present book has tried to meet these requirements to the best of his knowledge. Apparently invalid names used in original reports have been supplied by valid ones, e.g., the species termed in the original reference Lycopersicon esculentum is cited as Solanum lycopersicum L. sub nom. Lycopersicon esculentumMill. Unfortunately, species epithetons lack the respective authorities in the major-ity of phytochemical reports. This sometimes led to equivocal situations. As far as possible the corresponding authorities have been added to each species. If species are listed in tables, the authorities are added there but not in the corresponding part of the text.

1.7.2 Chemical Trivial Names

For practical reasons, trivial names for secondary metabolites rather than names according to systematic rules of the IUPAC or Chemical Abstracts have been widely accepted in plant biochemistry. This is also the case for Chemical Abstracts

and the corresponding SciFinder Scholar™ 2006. However, such systematic names can easily be taken from the latter. In very rare cases, original research reports avoided trivial names for novel secondary metabolites, thus forcing the author to use names according to the systematic rules.

References

Bremer K, Friis EM, Bremer B (2004) Molecular phylogenetic dating of asterid flowering plants shows Early Cretaceous diversification. Syst Biol 53:496–505

Cadet de Gassicourt L (1817) J Pharmacie 3:495; fide Shellard EJ (1961a)Deroin T (2001) Flore de Madagascar et des Comores, famille 171, Convolvulaceae. Muséum

National d’Histoire Naturelle, ParisDesfosses M (1820) Extrait d’une lettre. J Pharmacie 6:374–376Desfosses M (1821) Extrait d’une lettre. J Pharmacie 7:414–417Durbin ML, McCaig B, Clegg MT (2000) Molecular evolution of the chalcone synthase multigene

family in the morning glory genome. Plant Mol Biol 42:79–92Geiger PL, Hesse (1833a) Darstellung des Atropins. Liebigs Ann Chem 5:43–81Geiger PL, Hesse (1833b) Fortgesetzte Versuche ueber Atropin. Liebigs Ann Chem 6:44–65Hunziker AT (2001) Genera Solanacearum – the genera of Solanaceae illustrated, arranged

according to a new system. A.R.G.Gantner Verlag, Ruggell, LiechtensteinJohnston JFW (1840) Philos Trans R Soc, London A 341; fide Noda et al. (1990)Judd WS, Campbell CS, Kellogg EA, Stevens PF (1999) Plant Systematics – a phylogenetic

approach. Sinauer Associates, Inc, Sunderland, MA, USAMein (1833) Ueber die Darstellung des Atropins in weißen Krystallen. Liebigs Ann Chem

6:67–72Meissner CFW (1819) Ueber ein neues Pflanzenalkali (Alkaloid). J Chem Phys 25:381Noda N, Kogetsu H, Kawasaki T, Miyahara K (1990) Resin glycosides. VI. Scammonins I and II,

the resin glycosides of Radix Scammoniae from Convolvulus scammonia. Phytochemistry 29:3565–3569

Orechoff A, Konowalowa R (1933) Über die Alkaloide von Convolvulus pseudocantabricusSchrenk. (1.Mitt.) Arch Pharm 271:145–148

Posselt W, Reimann L (1828) Chemische Untersuchung des Tabaks und Darstellung eines eigenthümlich wirksamen Prinzips dieser Pflanze. Poggend Ann Phys Chem 8:399–410

Sertürner FW (1805) Darstellung der reinen Mohnsäure (Opiumsäure) nebst einer chemischen Untersuchung des Opiums mit vorzüglicher Hinsicht auf einen darin neu entdeckten Stoff und die dahin gehörigen Bemerkungen. J Pharmacie 14:47–93

Sertürner FW (1817) Über das Morphium, eine neue salzfähige Grundlage, und die Mekonsäure, als Hauptbestandteile des Opiums. Ann Phys 55 (neue Folge 25):56–89

Shellard EJ (1961a) The chemistry of some convolvulaceous resins. Part I. Vera Cruz Jalap. Planta Med 9:102–116

Spring O, Buschmann H (1998) Grundlagen und Methoden der Pflanzensystematik. Quelle & Meyer Verlag, Wiesbaden, Germany

Trease D, Evans WC (2002) Pharmacognosy, 15th edn. W.B. Saunders, Edinburgh, UKWink (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic

perspective. Phytochemistry 64:3–19

References 9

2Classification and System in Solanales

2.1 Position of the Order Solanales and its Families

Traditional classifications predominantly based on morphological characters have already taken into account – with increasing effort – the significance of interrela-tionships reflecting the evolutionary history of taxa. However, only the exciting developments during the past two decades, resulting from huge advances in molec-ular biology, have achieved a phylogeny-based classification of broad scientific acceptance. Concerning the role of morphology in phylogeny reconstruction / sys-tematics, a passionate summing-up has recently been published by Scotland et al. (2003): “We disagree that morphology offers any hope for the future to resolve phylogeny at lower or higher taxonomic levels. In other words, just because there are enough morphological synapomorphies for careful observers to recognize many monophyletic groups over the years in traditional taxonomic studies, further dissec-tion of morphology by present or future scientists may still not be able to resolve the full branch structure of the tree of life. Molecular phylogenetics holds several orders of magnitude more hope for that end, even though an honest observer would have to agree that even whole genomes for all species will probably not yield a fully resolved, highly confident tree.” An updated phylogenetic classification includes the order Solanales Dumortier comprising five families with altogether 165 genera and 4080 species (Table 2.1; Stevens 2001 onwards). An alternative esti-mate has taken 140 genera and 4800 species as a basis (Albach et al. 2001). The two large families Solanaceae and Convolvulaceae are both characterized by an almost world-wide distribution whereas the minor families Hydroleaceae, Montiniaceae, and Sphenocleaceae are limited to the tropics.

2.1.1 Traditional Systematics

Above the rank of order, Solanales have been nested traditionally within subclass Asteridae s.l. (e.g., Takhtajan 1964) which comprised all former Sympetalae Tetracyclicae or alternatively within subclass Lamiidae (e.g., Ehrendorfer 1991),

Eckart Eich, Solanaceae and Convolvulaceae: Secondary Metabolites 11© Springer-Verlag Berlin Heidelberg 2008

12 2 Classification and System in Solanales

a more restricted taxon with, e.g., Gentianales, Boraginales, Scrophulariales, Lamiales, although excluding Campanulales and Lamiales, i.e., Asteridae s.str. According to other views Solanaceae, Nolanaceae (nowadays included in Solanaceae), Convolvulaceae, Cuscutaceae, and Dichondraceae (both nowadays included in Convolvulaceae) have been ranked together with, e.g., Boraginaceae, Hydrophyllaceae, Polemoniaceae among the order Polemoniales (Takhtajan 1959, 1973; Heywood 1978), whereas Ehrendorfer has integrated Polemoniaceae into Solanales. Though many authors have placed Convolvulaceae in the order Solanales (e.g., Cronquist 1988; Dahlgren 1989; Thorne 1992) the family has been segregated alternatively into its own order, Convolvulales; this opinion was based on a number of characteristics not shared with other Solanales, e.g. presence of articulated latex canals and latex cells (Takhtajan 1997).

2.1.2 Phylogenetic Classification Based on Predominantly (Macro)molecular Data Sets

Macromolecular data have revolutionized the view of phylogenetic relationships not only in the plant kingdom. “The big difference is that there are simply many more molecular (DNA) characters available (than morphological) and their inter-pretation is generally easier – an adenine is an adenine, whereas compound leaves, for example, can form in quite different ways in different plants. As a result, molecular data are now widely used for generating phylogenetic hypotheses” (Judd et al. 1999).

Table 2.1 Families of the order Solanales Dumortier according to the Angiosperm Phylogeny Website (Stevens 2001 onwards; version May 2006)Family Authority Genera Species Distribution

Convolvulaceae (morning glory or bindweed family)

A.L. de Jussieu 57 (55)a 1601 (1930)a World-wide (most diverse in tropical and subtropicalregions)

Hydroleaceae Berchtold & J. Presl

1 12 Tropical

Montiniaceae Nakai 3 5 Africa / MadagascarSolanaceae

(nightshade or potato family)

A.L. de Jussieu 102 (147)a (92)b 2460 (2930)a

(2300)b

World-wide (overwhelmingly Neotropics)

Sphenocleaceae (Lindley)Baskerville

1 2 Pantropical

a Numbers in brackets show one alternative point of view: Judd et al. (1999)b Numbers in brackets show another alternative point of view: Hunziker (2001)

2.1.2.1 Angiosperms, Asterids

A number of recent cladistic analyses predominantly based on molecular data have extraordinarily improved the understanding of phylogenetic relationships among angiosperms, e.g., studies inferred from chloroplast rbcL sequences (Chase et al. 1993), nuclear 18S rDNA sequences (Soltis et al. 1997), and a combination of chloroplast atpB and rbcL sequences (Savolainen et al. 2000). Moreover, a com-bined cladistic analysis including molecular, morphological, and even chemical characters, i.e., small molecules, was published (Nandi et al. 1998). Another study comprised a combined data set for 560 angiosperms and 7 outgroups based on sequences of three genes (18S rDNA, rbcL, atpB; Soltis et al. 2000). In this case stronger support could be received from the jackknife consensus tree than from bootstrap or jackknife analyses in previous studies based only on single genes. The asterid clade (99% support) was one of six subclades of the core eudicots (core tri-colpates). Monophyly of the core eudicots and the subclades, respectively, was also strongly supported (100%). This asterid clade showed trichotomy comprising Ericales, Cornales, and euasterids I / II (core asterids), each also with strong sup-port (89–98%). Basal interrelationships among Cornales, Ericales, and core asterids could be resolved with strong support in a more recent study (Bremer et al. 2002; see below). An ordinal classification for the families of flowering plants has been published (Angiosperm Phylogeny Group 1998).

2.1.2.2 Core Asterids, Euasterids I (Lamiids)

The core asterid clade includes the euasterid I clade (renamed as lamiids sensu Bremer et al. 2002; Fig. 2.1) and the euasterid II clade (renamed as campanulids sensu Bremer et al. 2002). In contrast to the euasterid II clade (88% support) the euasterid I clade was only weakly supported (56%) in the study of Soltis et al. (2000); it comprised a trichotomy: (1) Oncothecaceae, (2) Garryales, and (3) a large well-supported monophyletic group (99%) consisting primarily of three again well-supported orders, Lamiales (99%), Gentianales (100%), Solanales (100%). Moreover, two families, Vahliaceae and Boraginaceae (100%), were left unassigned to an order. This was in contrast to certain previous studies based on sequences of only single genes which placed Boraginaceae as part of Solanales (e.g., Chase et al. 1993). However, the third large subclade in the study of Soltis et al. still included polytomy.

One phylogenetic analysis focused on asterids only, with an expanded number of species, based on sequences of the three genes mentioned above combined with those of a fourth, chloroplast ndhF, and a high number of asterid-specific parsimony-informative characters led to further elucidation (Albach et al. 2001). The Solanales constitute a subclade including again Solanaceae, Convolvulaceae, Hydroleaceae, and Montiniaceae. Relationships within Solanaceae were congruent with results from a previous study (Olmstead and Sweere 1994; see below). Moreover, a recent phylogenetic study of asterids based on three coding and three

2.1 Position of the Order Solanales and its Families 13

14 2 Classification and System in Solanales

non-coding chloroplast DNA markers proved that the three noncoding markers are almost equally useful as the three coding genes in phylogenetic reconstruction at the high level of orders and families in asterids (Bremer et al. 2002). In general this study has provided increased support for resolution within the asterids. Thus, the strict consensus tree from the combined analysis of all of the six markers also shows strong support (100%) for the lamiids (new name replacing euasterids I) in contrast to the study of Soltis et al. (2000; see above). However, the nodes repre-senting interrelationships among the orders of the lamiids are more or less sup-ported by jackknife analysis: Garryales/Gentianales/Vahliaceae, Boraginaceae are successive sister groups to Solanales/Lamiales though mainly with low support (<50%). Only the resolution of Gentianales and the remaining lamiids (including Solanales) is strongly supported (100%).

Molecular phylogenetic dating – based on the data matrix from Bremer et al. (2002) – showed diversification of lamiids like other major subgroups of the

Montiniaceae(incl. Kaliphora)

Sphenocleaceae

Hydroleaceae

Solanaceae

Convolvulaceae

Lamiales

Solanales

Boraginaceae

Vahliaceae

Gentianales

Garryales

Icacinaceae

Oncothecaceae

Campanulids

Fig. 2.1 Phylogenetic tree of the lamiids sensu Bremer et al. (2002) (syn.: Euasterids I) established by cladistic analyses based on molecular data sets; outgroup: Campanulids sensu Bremer et al. (2002) (syn.: Euasterids II); for details and further references see text

asterids during the Early Cretaceous; Solanales are from the Mid-Cretaceous (stem node age: 106 my; crown node age: 100 my) (Bremer et al. 2004).

2.1.2.3 Solanales and Families Belonging to this Order

In the study of Soltis et al. (2000) the Solanales genera Solanum, Nolana, Nicotiana,Petunia, Schizanthus, and Duckeodendron (Solanaceae), Ipomoea and Convolvulus(Convolvulaceae), Montinia (Montiniaceae), and Hydrolea (Hydroleaceae) were integrated into a jackknife consensus tree of the euasterid I clade (lamiids) with predominantly excellent support: Montiniaceae/Hydroleaceae were sister to Convolvulaceae/Solanaceae (96%); Montiniaceae were sister to Hydroleaceae (99%), Convolvulaceae was sister to Solanaceae (99%). Within the Solanaceae subclade (100%), there was a trichotomy comprising Duckeodendron, Schizanthus,and a clade with the remaining genera (97%); Petunia is sister to Nicotiana/Nolana/Solanum (99%). Only the Nolana/Solanum subclade showed low support (58%). The study of Bremer et al. (2002) included representatives of all five Solanales families, i.e., the four families mentioned above and in addition Sphenocleaceae. For the first time these families were supported as a monophyletic group (90%). Solanaceae/Convolvulaceae together formed the sister of the three remaining fami-lies (Montiniaceae, Sphenocleaceae, Hydroleaceae). The relationship between Solanaceae and Convolvulaceae again received 100% jackknife support. The time of divergence between this two families is – assuming molecular clock arguments – about 70 my ago (Durbin et al. 2000).

2.2 Solanaceae A.L. de Jussieu: Delimitation, Intrafamilial Circumscription and Relationships

Fossil palynomorphs belonging to the genus Solanaceaepollenites from the Eocene (55–38 my ago) were found in Taiwan (Shaw 1999).

2.2.1 Traditional Systematics

Already in the famous New Kreüterbuch (The New Herbal) by Leonhart Fuchs (1501–1566), a pioneer of modern Botany, eight solanaceous species from seven genera were described scientifically and depicted in excellent plant illustrations (col-oured woodcuts; Fuchs 1543): Atropa belladonna L. (deadly nightshade); Capsicum annuum L. (paprika, red and green sweet pepper); Datura metel L. (downy thorn-apple); Hyoscyamus niger L. (henbane); Mandragora officinarum L. (mandrake); Physalis alkekengi L. (Chinese or Japanese lantern); Solanum melongena L. (auber-gine, eggplant), S. nigrum L. (black nightshade). Linnaeus (1707–1778) recognized

2.2 Solanaceae A.L. de Jussieu: Delimitation, Intrafamilial Circumscription 15

16 2 Classification and System in Solanales

13 genera still accepted nowadays in his Species Plantarum (1753) and Genera Plantarum (1754), respectively (Panzer 1788): Atropa (3 spp. including A. mandragora= Mandragora officinarum), Browallia (3), Brunfelsia (1), Capsicum (3), Cestrum(3), Datura (5), Hyoscyamus (7), Lycium (4), Nicotiana (7), Nolana (1), Physalis(12), Schwenckia (1), Solanum (34). The long history of the classification of the Solanaceae before and after Linnaeus has been summarized in a comprehensive paper by D’Arcy (1979).

Recently, Hunziker (2001) has published a synopsis of the family as “… the first attempt, in the last 110 years after Wettstein (1891), to coordinate the profusion of available information on every genus of Solanaceae, integrating it critically in a system of classification”. He divided the nightshade family in 6 subfamilies com-posed of 92 genera and ca. 2300 species according to Table 2.2. Hunziker excluded the related genera Duckeodendron, Goetzea, and Nolana from Solanaceae as inde-pendent families.

2.2.2 Phylogenetic Classification Based on Predominantly (Macro)molecular Data Sets

In early attempts to reconstruct phylogeny certain prominent genera have been subjected to analyses by assessing chloroplast DNA restriction site variation: Nicotiana (Kung et al. 1982; Olmstead et al. 1990), Lycopersicon (Palmer and Zamir 1982), Solanum sect. Tuberosum (Hosaka et al. 1984), Capsicum (Mitchell et al. 1989). Meanwhile, a number of further studies on single genera, especially those which include economically important cultivated species, have been pub-lished integrating, e.g., a chloroplast atpB-rbcL noncoding spacer region, ITS nrDNA, and different loci of plastid DNA, respectively in case of, e.g., Capsicum(Walsh and Hoot 2001), Nicotiana (Chase et al. 2003; Knapp et al. 2004a; Clarkson et al. 2004). For other genera see certain chapters/sections, e.g., Solanum in connection with steroid alkaloids (Sect. 7.8). A first higher-level chloroplast DNA analysis including 42 species, representing 12 of the 14 tribes recognized by D’Arcy (1991), with Ipomoea coccinea L. (Convolvulaceae) as the outgroup representative had already been published a few years later (Olmstead and Palmer 1992). This phylogenetic study revealed the important insight that the Cestroideae are the ancestral subfamily and not the Solanoideae as considered traditionally.

As a matter of priority this book is intended to document the occurrence as well as the distribution of secondary metabolites within the Solanales and to demonstrate relationships of chemotaxonomic relevance resulting from this documentation. In this connection a provisional phylogenetic tree of the Solanaceae (Fig. 2.2) has been established by theoretical combination of different cladistic analyses. This has been based on (i) restriction site analysis of the entire chloroplast genome and (ii) on chlo-roplast rbcL and ndhF gene sequences, respectively (Olmstead et al. 1998, 1999; Garcia and Olmstead 2003; Santiago-Valentin and Olmstead 2003) or on chloroplast rbcL and matK gene sequences (Gemeinholzer and Wink 2001; Wink 2003).

Table 2.2 Classification and geographic distribution of the Solanaceae based on data of Hunziker (2001)

Genera in bold = significant for this book (studies on secondary metabolites published); genera in standard type = no phytochemical results available; underlined genera = classification different from the phylogenetic tree based on (DNA) molecular analysis (see Fig. 2.2)

Subfamily Tribe Subtribe Genus Species Distributiona

Cestroideae Cestreae Cestrum 175 NeotropicsVestia 1 ChileSessea 28 Neotropics

Metternichieae Metternichia 1 BrazilLatueae Latua 1 ChileNicotianeae Nicotianinae Nicotiana 66 AM/AUS

Petunia 34 S-AMFabiana 15 S-AM

Nierembergiinae Nierembergia 21 S-AMBouchetia 3 AM

Leptoglossinae Leptoglossis 7 S-AMHunzikeria 3 AMPlowmania 1 C-AM

Benthamielleae Benthamiella 12 Chile/Argent.Pantacantha 1 ArgentinaCombera 2 Chile/Argent.

Francisceae Brunfelsia 46 NeotropicsBrowallieae Browallia 17? AM

Streptosolen 1 S-AMSchwenckieae Schwenckia 25 AM

Melananthus 5 AMProtoschwenckia 1 Boliv./BrazilHeteranthia 1 Brazil

Juanulloideae Juanulloeae Juanulloa 8 NeotropicsDyssochroma 2 BrazilEctozoma 1 S-AMHawkesiophyton 3 NeotropicsMarkea 17 S-AMMerinthopodium 2 NeotropicsRahowardiana 2 Panama/Col.Schultesianthus 5 NeotropicsTrianaea 2 S-AM

Solanoideae Nicandreae Nicandra 1 Peru/Argent.Mandragoreae Mandragora 2 E-Mediterr.Datureae Datura 11 N/C-AM

Brugmansia 6 S-AMLycieae Lycium 81 Cosmopol.

Phrodus 1 ChileGrabowskia 4 Neotropics

Solaneae Witheringinae Witheringia 28 NeotropicsBrachistus 3 C-AMCuatresia 11 NeotropicsDeprea 7 NeotropicsDiscopodium 1 trop. AfricaExodeconus 6 S-AMJaltomata 50 NeotropicsNothocestrum 6 HawaiiAcnistus 1 Neotropics

(continued)

Physalinae Physalis 90 AMQuincula 1 N-/C-AMLeucophysalis 3 AMChaemasaracha 10 N-/C-AM

Iochrominae Iochroma 16 S-AMSaracha 2 S-AMOryctes 1 N-AMTubocapsicum 1 E-/SE-AS

Capsicinae Capsicum 20 C-/S-AMAureliana 5 S-AMAthenaea 7 BrazilDarcyanthus 1 Peru/Boliv.Eriolarynx 3 Argent./Boliv.Vassobia 2 S-AMLarnax 12 S-AMDunalia 5 S-AMWithania 20 Old World

Solaninae Solanum 1033 Cosmopol.Cyphomandra 41 NeotropicsLycopersicon 7 S-AMLycianthes 150 Neotropicsb

Triguera 1 SW-Mediterr.Normanna 2 Macronesia

Atropeae Atropa 2 EUR/ASc

Jaboroseae Jaborosa 23 S-AMSalpichroa 15 S-AMNectouxia 1 Mexico

Solandreae Solandra 10 NeotropicsHyoscyameae Hyoscyamus 23 Old World

Anisodus 4 China/NepalAtropanthe 1 ChinaPhysochlaina 8 ASPrzewalskia 1 ChinaScopolia 2 EUR/AS

Salpiglossoideae Salpiglossideae Salpiglossis 2 Chile/Argent.Reyesia 4 Chile/Argent.

Schizanthoideae Schizantheae Schizanthus 12 Chile/Argent.Anthocercidoideae Anthocercideae Anthocercis 10 W/S-AUS

Anthotroche 3 W-AUSCyphanthera 9 W/S-AUSCrenidium 1 W-AUSDuboisia 4 AUSd

Grammosolen 2 S-AUSSymonanthus 2 W-AUS

a Abbreviations: capital letters for the four points of the compass (C = Central) and continents (e.g.: AM = America), respectively; Medit. = Mediterraneanb 20 species native to South-East Asiac Distribution of A. belladonna L.; A. baetica Willk.: SE-Spain/N-Moroccod D. myoporoides R.Br. additionally in New Caledonia

Table 2.2 Classification and geographic distribution of the Solanaceae based on data of Hunziker (2001) (continued)

Genera in bold = significant for this book (studies on secondary metabolites published); genera in standard type = no phytochemical results available; underlined genera = classification different from the phylogenetic tree based on (DNA) molecular analysis (see Fig. 2.2)Subfamily Tribe Subtribe Genus Species Distributiona

Nicotianoideae

Crenidium, Cyphanthera, Duboisia

(Cyphanthera clade)

Bouchetia, Brunfelsia, Fabiana,

Hunzikeria, Nierembergia, Petunia,

(Appendix: Leptoglossis ?)

Metternichia, Coeloneurum,

Henoonia, Espadaea, Goetzea

(Goetzeae clade)

Schizanthus

Schwenckia

Convolvulaceae

Cestroideae s.s.

Anthotroche

(Anthotroche clade)

Grammosolen

(Grammosolen clade)

Anthocercis

(Anthocercis clade)

Symonanthus

(Symonanthus clade)

Nicotiana

(Nicotianeae clade)

Browallia, Streptosolen

(Browallieae clade)

Cestrum, Sessea, Vestia

(Cestreae clade)

(Appendix: Latua ?)

Salpiglossis

Solanoideae

(tradit.: Anthocercioideae)

Duckeodendron

Petunioideae

Goetzeoideae

Schizanthoideae

Schwenckioideae

(tradit.: Cestroideae s.l.)

(tradit.: Cestroideae s.l.)

(tradit.: Cestroideae s.l.)

(tradit.: Goetzeaceae)

(tradit.: Duckeodendraceae)

(tradit.: Cestroideae s.l.)

(tradit.: Salpiglossoideae)

A

Fig. 2.2 Provisional phylogenetic tree of the Solanaceae established by theoretical combination of different cladistic analyses; outgroup: Convolvulaceae; for details and references see text. Genera in bold indicate the significance for this book (presence of phytochemical data in the lit-erature for this specific genus); genera in standard type indicate that there are no data available. Genera with a question mark listed under “Appendix” have been nested within a clade according to the traditional classification of Hunziker (2001) due to the lack of molecular data for this spe-cific genus. The genera Schultesianthus and Markea have to be added in bold as an “Appendix” to the Juanulloinae subclade with a question mark; this is also true for the genus Eriolarynx to the Iochrominae subclade. Genera without molecular data and without phytochemical reports are not listed

2.2 Solanaceae A.L. de Jussieu: Delimitation, Intrafamilial Circumscription 19

20 2 Classification and System in Solanales

Nicotianoideae

Aureliana, Tubocapsicum, Withania (Withaninae subclade; Physaleae clade)

Chamaesaracha, Leucophysalis, Physalis,Witheringia (Physalinae subclade; Physaleae clade)(Appendix: Brachistus ?, Cuatresia ?, Deprea ?,Discopodium ?)

Salpichroa (Salpichroinae subclade; Physaleae clade)

Capsicum, Lycianthes (Capsiceae clade)

Jaltomata, Solanum (incl. Cyphomandra,Lycopersicon) (Solaneae clade)

Brugmansia, Datura (Datureae clade)

Dyssochroma, Hawkesiophyton, Juanulloa(Juanulloinae subclade; Solandreae clade)(tradit.: Juanulloideae)

x =

12 c

lade

Acnistus, Dunalia, Iochroma, Saracha, Vassobia(Iochrominae subclade; Physaleae clade)(Appendix: Oryctes ?)

Exodeconus, Nicandra (Nicandreae clade)

Solandra (Solandrinae subclade; Solandreae clade)

Mandragora (Mandragoreae clade)

Grabowskia, Lycium (Lycieae clade)(Appendix: Phrodus ?)

Nolana, Sclerophylax (Nolaneae clade)(tradit.: Nolanaceae)

Jaborosa (Jaboroseae clade)

Anisodus, Atropa, Atropanthe, Hyoscyamus,Physochlaina, Przewalskia, Scopolia(Hyoscyameae clade)

Solanoideae B

Fig. 2.2 (continued)