Latex: A Model for Understanding Mechanisms, Ecology, and Evolution of Plant Defense Against Herbivory

Latex is a sticky emulsion that exudes upon damage from specialized canals in about 10% of flowering plant species. Latex has no known primary metabolic function and has been strongly implicated in defense against herbivorous insects. Here we review historical hypotheses about the function of latex, evidence that it serves as a potent defense, and the chemistry and mode of action of the major constituent defense chemicals and proteins across a diversity of plant species. We further attempt to synthesize the characteristics of latex as a coordinated plant defense system. Herbivores that feed on latex-bearing plants typically evade contact with latex by severing the laticifers or feeding intercellularly, or may possess physiological adaptations. Convergent evolution appears to be rampant both in plants with latex and insects that exploit latex-bearing plants. Because latex shows phenotypic plasticity, heritability, and macoevolutionary lability, it is an ideal system to study plant-herbivore interactions using evolutionary approaches. 311 A nn u. R ev . E co l. E vo l. Sy st . 2 00 9. 40 :3 11 -3 31 . D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by 7 1. 12 7. 18 2. 15 8 on 1 1/ 19 /0 9. F or p er so na l u se o nl y. ANRV393-ES40-15 ARI 1 October 2009 11:56 Mandibulate: refers to insects that have mandibles for biting or chewing leaf tissue (as opposed to having a proboscis or stylet for sucking) Latex: a milky suspension or emulsion of particles in an aqueous fluid, usually held under pressure in living plant cells (lacticifers) Hevea brasiliensis or Pará rubber tree (Euphorbiaceae): native to the Amazon, and perhaps the best-studied latexproducing species because of the economic importance of rubber Asclepias: a genus of herbaceous perennial plants with ≈140 species in the Americas and named for their exuding milky latex, commonly called milkweeds INTRODUCTION About 10% of all flowering plant species (angiosperms) exude latex upon tissue damage and this latex has no known function in primary metabolism (in terms of plant resource acquisition and allocation) (Farrell et al. 1991, Hunter 1994, Lewinsohn 1991, Metcalf 1967). Over the past 20 years, a growing literature has emerged on latex, its biochemistry, and its ecological and evolutionary consequences. Both circumstantial and experimental evidence points to latex as a potent plant defense against mandibulate herbivores. Here we review various aspects of the chemical ecology and evolutionary biology of latex with special reference to plant-herbivore interactions. We use latex as a model to address general conceptually motivated questions that scientists might ask about any plant defense (Sidebar: A set of conceptually motivated questions addressing the mechanisms, ecology, and evolution of any plant defense trait). Not unlike the blood of animals, when the tissues of latex-bearing plants are damaged, latex oozes out, becomes sticky when exposed to air, and quickly coagulates. Sometimes latex exudation can be remarkably abundant, like a squirt of toxic white glue, whereas at other times it may be difficult to detect because it is clear or barely exudes (Agrawal et al. 2008, Metcalf 1967, Shukla & Krishna Murti 1971). Latex is sometimes colored yellow, orange, or red, such as that of Cannabis (Cannabaceae). Latex is well known for its sticky properties, which have been used to produce rubber (from Hevea brasiliensis Euphorbiaceae and other species), chicle from Manilkara spp. (Sapotaceae) used in chewing gum, and lacquers from phenols in the latex of plants in the Anacardiaceae. Latex from various plant species contains bioactive compounds including alkaloids such as morphine in Papaver spp. (Papaveraceae); cardiac glycosides in Asclepias spp. (Apocynaceae); terpenes such as the sesquiterpene lactone, lactucin, from lettuce (Lactuca spp. Asteraceae); and digestive cysteine proteases in Carica papaya (Caricaceae) and Ficus spp. (Moraceae) (see section on Biochemistry and Mode of Action). As evidenced from the above list of plant families with latex-bearing species, latex is extraordinarily common. Among flowering plants, over 20,000 species (from over 40 families in multiple lineages) contain latex (Farrell et al. 1991, Hunter 1994, Lewinsohn 1991, Metcalf 1967). Latex is found in dicotyledonous and monocotyledonous (e.g., Liliaceae) plants. This finding, that nearly 10% of families and species produce latex, implies that latex is a highly convergent trait (that is, A SET OF CONCEPTUALLY MOTIVATED QUESTIONS ADDRESSING THE MECHANISMS, ECOLOGY, AND EVOLUTION OF ANY PLANT DEFENSE TRAIT What is the mode of action? Are the constituents that make up the defense redundant, additive, or synergistic? Is this defense tied into primary plant metabolism, protection from abiotic stress, energy storage, or waste? How specific are the effects of the defense against a diversity of attackers? Does this defense interact with predation? How do resources and abiotic environment modulate expression of the trait? Are there ontogenetic shifts in the expression of this trait? Is the defense inducible by herbivory? Which plant hormones regulate defense investment? Is there specificity in the elicitation of the induced response? How do herbivores cope with this defense? In what sorts of communities is this defense present, and what are the consequences of herbivory at the community level? Is there heritable variation for the expression of the defense? What maintains this heritable variation (allocation or ecological costs, spatial or temporal variation in the benefits)? How does this defense trait covary with other defense traits within the species? Do herbivores impose natural selection on this trait? How evolutionarily conserved is the defense in a clade of related plants? Is the defense adapted to particular populations or habitat types? Does this defense show phylogenetic patterns or trends? Any evidence for this defense as a key innovation? 312 Agrawal · Konno A nn u. R ev . E co l. E vo l. Sy st . 2 00 9. 40 :3 11 -3 31 . D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by 7 1. 12 7. 18 2. 15 8 on 1 1/ 19 /0 9. F or p er so na l u se o nl y. ANRV393-ES40-15 ARI 1 October 2009 11:56 Resin: plant exudates common in conifers and some angiosperms (e.g., Anacardiaceae), rich in terpenoids and phenolics, and stored in intercelluar spaces Mucilage: plantproduced sticky polysaccharides that are often clear and exude from the phloem following damage (common in cucurbits) Gum: distinct from latex, resin, or mucilage; these water soluble polysaccharides exude from cellular cavities or bark (as in Rosaceous fruit trees) Laticifer: an elongated cell with two main morphological types (articulated or nonarticulated) produced in any plant part, serving to transport latex David Dussourd: American biologist at the University of Central Arkansas who has been the leading scientist unraveling the mechanisms of latex as a plant defense has evolved independently multiple times) and that latex is likely encountered by many herbivore species. In addition, latex has been reported in mushrooms (e.g., Lactarius spp.), conifers (e.g., Gnetum spp.) and pteridophytes (Metcalf 1967). Both in terms of absolute and proportional estimates, tropical plant families (and species overall) are more likely to produce latex than are temperate groups (Lewinsohn 1991). Indeed, some 14% of tropical plant species produced latex compared to 6% of temperate species, and this distribution is not independent of plant phylogeny (Lewinsohn 1991). Latex is phylogenetically conserved in the above-mentioned plant families, and these and other latex-bearing families may be overrepresented in the tropics.