ANNUAL REVIEWS Further Quick links to online content Ann Rev Plant Physiol 1977 28:479-501 Copyright © 1977 by Annual Reviews Inc All rights reserved SECONDARY COMPOUNDS +7639 Annu Rev Plant Physiol 1977.28:479-501 Downloaded from www.annualreviews.org by Stanford University - Main Campus - Lane Medical Library on 02/19/13 For personal use only AS PROTECTIVE AGENTS Tony Swain Department of Biology, Boston University, Boston, Massachusetts 02215 CONTENTS Introduction Distribution of Secondary Compounds in Space and Time Function of Secondary Compounds Secondary Compounds as Waste Products Secondary Compounds as Protective Agents 479 480 480 481 483 483 484 Introduction Defenses on the Surface of Plants Defensive Function of the Cell Wall Che"1ical Defenses within the Cell The Role of Tannins The Role of Phytoalexins 485 485 485 486 486 487 488 SECONDARY COMPOUNDS AND ALLELOPATHY Introduction 489 489 489 490 490 INTRODUCTION THE NATURE OF SECONDARY COMPOUNDS SECONDARY COMPOUNDS AND PLANT DISEASES The Complexity of Allelopathy Allelopathic Activity of Secondary Compounds Nonprotein Amino A cids and A llelopathy SECONDARY COMPOUNDS AS INSECT DETERRENTS Introduction Insect Chemoreceptors Insect-deterrent Properties of Secondary Compounds 490 490 491 492 SECONDARY COMPOUNDS AS PROTECTiVE AGENTS AGAINST OTHER HERBIVORES Introduction The Role of Cyanogenesis The Role of Alkaloids The Role of Tannins CONCLUSIONS 493 493 494 494 495 495 INTRODUCTION We live in a chemical world a world dominated by color, by scent, and by taste (67, 135) Many animal phyla have developed a discriminatory acuity in these latter 479 Annu Rev Plant Physiol 1977.28:479-501 Downloaded from www.annualreviews.org by Stanford University - Main Campus - Lane Medical Library on 02/19/13 For personal use only 480 SWAIN two senses which rivals their sight (180, 181) Even ourselves, who possess the most sophisticated means of aural and visual communication, depend on our olfactory and gustatory senses in our overall perception of the living world For the majority of living organisms, however, chemical signals are the main means of communica tion Such signals have the virtue of persistance, of being unaffected by most spatial barriers, and of denoting absolutely whether the organism from which they originate is benign or hostile to the receiver (1S0) The majority of chemical signals are complex They contain mixtures of many different compounds, the majority of which belong to the heterogeneous collection of so-called "secondary products" (lOS) These compounds were so named because they have no obvious metabolic function and their very diversity of structure and distribution among living organisms has led to the idea that they are waste products (117, lIS) The majority of known secondary products are of plant origin (64, 7S), but many are found in fungi, bacteria, or sessile marine animals (3S, 148, 169) A large number are present in arthropods (46), but fewer are found in the chordates, whose diversity mainly depends on variation in size, shape, and, above all, behavioral patterns (55, l SI) What is the value to the plant of the varied secondary products it contains? Are they merely a result of the capricious whims of evolution, leading towards unneces sary diversity, or are they perhaps the counterpart of behavior in animals? It is the purpose of this review to try to answer these questions-to show that all the varied types of secondary products present in plants have a most important function, a function shaped by evolution (159-161) They are present to maintain the overall integrity of the plant against competitors, predators, and pathogens The enormous variety of chemical structures found determines the infinite number of signals which are required to maintain the complexity of the differing ecosystems found in nature (27, 36, 5S-60, 65, 72, 79, 87, 131, 132, 154, 176) To illustrate what I mean by ecological complexity, consider a temperate-zone meadow in the height of summer On average, each 100 square meters will contain 150,000 individual plants Associated with these will be several hundred guilds of herbivores and carnivores: diverse populations of insects, birds, and mammals total ing about 30,000 Above and below ground will exist 1,000 billion bacteria, fungi, algae, and protozoa The soil around the plants' roots will contain a billion nema todes, million microarthropods, million oligochaete worms, and 30,000 earth worms (132) A formidable array indeed! This is why one requires an enormous diversity of chemical signals which attract or deter, nourish or kill THE NATURE OF SECONDARY COMPOUNDS Introduction There are over 10,000 known low-molecular weight secondary metabolites in higher plants and fungi (19, 56, 64, 70, 73, 78, 81, 85, 125, 165) They are usually classed according to their chemical structures as shown in Table I and Figure (108) In addition, there are an unknown number of proteins, polysaccharides, and other SECONDARY COMPOUNDS AS PROTECTIVE AGENTS 48 Table Secondary products as protective agents No o f known Annu Rev Plant Physiol 1977.28:479-501 Downloaded from www.annualreviews.org by Stanford University - Main Campus - Lane Medical Library on 02/19/13 For personal use only Class Example structures Afford protection againsta Ref 74 Wyerone (I) Lupanine (II) Fungi M amma ls 250 300 Canavanine (III) (J-Carotene Insects Photoprotection 128 101 Coumarins Cyanogenic 150 Scopoletin (IV) Fungi 103 g lucosides Flavon oids 50 1200 Linamarin (V) Procyanidin tannins (VI) Sinigrin (VII) Molluscs 94 Insects 50 Acetylenes Alkalo id s Amino adds Carotenoids G l u cosin ola tes Lignans Lipids Phenolic acids Polyketides Quinones Terpene sb St eroid s Miscellaneous Proteins Polysaccharides Other polymers 750 4500 80 50 100 100 500 200 1100 600 500 ? ? Excelsin (VIII) Waxes Vanillic acid (IX) Hircinol (X) J uglone (Xl) Glaucolide-A (XII) Ecdysones Tuliposide (XIII) Lectins Acylated polysaccharides Cutin Insects 48 Insects Fungi Pla nt s Fungi P lan ts Insects 141a 159 120 54 175 25 Insects Fungi Insect Fungi 131 115 91 61 Fungi III a For other examples see text bExcluding carotenoids and steroids polymers which can be classed as secondary products insofar as they have no known metabolic function in plants (21, III, 124, 142, 166) The number of secondary metabolites presently known undoubtedly represents the tip of the iceberg In the majority of cases only the major components of a given structural class have been examined from any one plant species When a more intensive search is carried out, the number of isolated secondary compounds usually increases dramatically For example, detailed investigation of Vinca rosea, a source of antitumor indole alkaloids, showed the plant contains over 100 of these com pounds (149) Obviously it will also possess the expected complement of lipids, phytosterols, carotenoids, phenolic acids, and flavonoids (78) It seems possible, therefore, that the total number of all secondary products present in plants may well equal the 400, 000 known species ( 126) Distribution of Secondary Compounds in Space and Time Secondary metabolites are not distributed evenly throughout the plant, either quan titatively or qualitatively, in space and time (72, 1I2, 13, 117, 176) Usually the 482 SWAIN II H�, C-NH-O-(CHa)-CH-COOH a Annu Rev Plant Physiol 1977.28:479-501 Downloaded from www.annualreviews.org by Stanford University - Main Campus - Lane Medical Library on 02/19/13 For personal use only H N� I N Ha, CHP -?'jr ° '?O HO"� IV III OH OH HO HO v VI NOS03 � eH =CH_CH_e s