Plant-insect interactions: an evolutionary arms race between two distinct defense mechanisms

A CROSS-TALK BETWEEN PLANTS AND INSECTS MINIREVIEW 71 Plant-insect interactions: an evolutionary arms race between two distinct defense mechanisms Marcia O. Mello and Marcio C. Silva-Filho* Departamento de Genética, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, Av. Pádua Dias, 11, CP 83, 13.400-970 Piracicaba, SP, Brazil; *Corresponding author: Received: 22/04/2002, Accepted: 05/07/2002 In this review, plant-insect interaction is discussed as a dynamic system, subjected to continual variation and change. Plants developed different mechanisms to reduce insect attack, including specific responses that activate different metabolic pathways which considerably alter their chemical and physical aspects. On the other hand, insects developed several strategies to overcome plant defense barriers, allowing them to feed, grow and reproduce on their host plants. This review foccuses on several aspects of this complex interaction between plants and insects, including chemical-derived substances, protein-derived molecules and volatile compounds of plants whereas metabolization, sequestration or avoidance are in turn employed by the insects. Key words: adaptation, co-evolution, herbivory. Interação planta-inseto: uma disputa evolutiva entre dois mecanismos de defesa distintos: Nesta revisão, a interação planta-inseto é abordada como um sistema dinâmico, sujeito a contínuas variações e mudanças. As plantas desenvolveram diferentes mecanismos para reduzir o ataque de insetos, incluindo respostas específicas que ativam diferentes vias metabólicas as quais alteram consideravelmente suas características químicas e físicas. Por outro lado, os insetos desenvolveram várias estratégias para superar as barreiras defensivas das plantas, permitindo a sua alimentação, desenvolvimento e reprodução em seus hospedeiros. Esta revisão enfoca vários aspectos desta complexa interação entre plantas e insetos, incluindo substâncias derivadas de compostos químicos, moléculas produzidas a partir do processamento de proteínas e compostos voláteis das plantas, enquanto que a metabolização, seqüestro ou fuga são empregados em contrapartida pelos insetos. Palavras-chave: adaptação, co-evolução, herbivoria. INTRODUCTION The evolution of plants transformed the terrestrial environment into a highly valuable resource for the herbivore community. In natural ecosystems, plants and insects are just some of the living organisms that are continuously interacting in a complex way. These two organisms are intimately associated since insects have several beneficial activities including defense and pollination while plants provide shelter, oviposition sites and food, the three main factors requested for insect proliferation (Panda and Khush, 1995). On the other hand, depending on the intensity of insect attack, herbivores might be extremely harmful to plants leading them to death. Plant-insect interaction is a dynamic system, subjected to continual variation and change. In order to reduce insect attack, plants developed different defense mechanisms including chemical and physical barriers such as the induction of defensive proteins (Haruta et al., 2001), volatiles that attract predators of the insect herbivores (Birkett et al., 2000), secondary metabolites (Baldwin, 2001 and references herein; Kliebenstein et al., 2001) and trichome density (Fordyce and Agrawal, 2001) (figure 1). In parallel, insects developed strategies to overcome plant barriers such as detoxification of toxic compounds (Scott and Wen, 2001), avoidance mechanisms (Zangerl, 1990), sequestration of poison (Nishida, 2002 and references herein) and alteration of gene expression pattern (Silva et al., 2001) (figure 1). Braz. J. Plant Physiol., 14(2):71-81, 2002 Braz. J. Plant Physiol., 14(2):71-81, 2002 Gene Activation PLANT SIGNAL Inhibitors increased activity heterogeneous set high specificity bifunctionality high complexity Nutritional hurdle I Secondary metabolites and Proteins L A N G S volatiles from an attacked plant Physical Barriers Direct Responses Figure 1. Interactions between plants and insects. Leaf shape Plant architecture Secondary metabolites Volatiles Indirect Responses volatiles parasitoids predators HERBIVORY A c t i v a t i o n G e n e Wound Insect elicitors Improved digestive enzymes high activity modified spectrum low sensitivity to PIs Proteinases to destroy PIs Utilization of alternative hosts Increase the consumption rate Modify the nutritive quality of the host plant tissue Establish associations with microorganisms Temporal / spatial avoidance Detoxification Sequestration of the poisons Avoidance New metabolites INSECT 72 M. O. MELLO AND M. C. SILVA-FILHO A CROSS-TALK BETWEEN PLANTS AND INSECTS This is the base of the co-evolution theory proposed by Ehrlich and Raven in 1964. Even though this theory has been accepted by researchers, it is important to stress that certain plant defense compounds experience opposing selection pressure by different enemies and that major defensive barriers evolve in response to a diverse assemblage of herbivores and other biotic and abiotic factors (Stowe, 1998). Moreover, both organisms are under environmental pressures that have an important impact on this interaction system (Panda and Khush, 1995 and references herein). According to Stowe (1998), herbivores and other natural enemies challenge the plant resistance characters in multiple ways. On the other hand, plant populations counteract the facing mechanisms with a wide potential to respond to this selection pressure. Figure 1 summarizes the aspects that will be discussed in this review as well as the mechanisms involved in plant-insect interaction. Plant responses to insect attack Plants produce chemicals for defense purposes in two different ways; first, as constitutive substances to repel herbivores through direct toxicity or by reducing the digestibility of plant tissues and second, as inducible substances synthesized in response to tissue damage by herbivores. These strategies are able to prevent most of the herbivores although there are a reduced number of insects that are able to adapt to specific plant species. Secondary metabolites perform useful functions for the plant acting either in an inducible or constitutive manner. Some compounds are plant growth regulators while others act as chemical signals in the ecosystem, antibiosis agents, transport and storage of carbon and nitrogen molecules which are directly involved in the plant primary metabolism (Panda and Khush, 1995). Secondary plant compounds are involved in plant defense against insect herbivores acting as insect repellents, feeding inhibitors and/or toxins. In this paper, we have classified these toxic compounds into chemical-derived substances (table 1) and protein-derived molecules (table 2). Glucosinolates are an example of secondary metabolites involved in plant/insect interactions. This class of molecu (...truncated)