Plants have evolved a complicated resistance system to defend against damages from various types of attackers. Based on many studies devoted to plant defense signal transduction, three main plant defense hormones have been identified. They are salicylic acid (SA), jasmonic acid (JA), and ethylene (ET), which are the key signal molecules involved in defense against pathogens, insects, and fungi, respectively [1–3]. It has recently been shown, however, that these signals are correlated in a very complex fashion; sometimes they conflict, while at other times they cooperate [4, 5], indicating that plants express various defense patterns when damaged by different attackers. The factors determining these plant response patterns are still not clear, however.
Plant responses to chewing insects and phloem-feeding insects are significantly different [6, 7]. The two types of insects not only produce different elicitors, but also have different feeding guides. For example, wounding leads to leakage of plant cellular liquids, stimulating the mobilization of many defense pathways ; insect feeding causes similar damage to plants, but the elicitors in insect saliva can induce special plant defense proteins  or conversely suppress plant defense signals . Phloem-feeding insects cause little wounding but have long damage durations, and plant defenses to these insects are thus slight [11, 12]. In comparison to chewing insects and phloem-feeding insects, little is known about molecular responses to leafminers, which are insects with special feeding guides.
Pea leafminers (Liriomyza huidobrensis) feed on over 100 species in 22 plant families, including the model plant Arabidopsis thaliana. During the adult stage, the female fly uses her ovipositor to penetrate the epidermis of host plant leaves; she then either lays eggs inside the leaves or feeds at the wound site, which can greatly reduce photosynthesis and eventually kill young plants . Although male flies are unable to puncture leaves, they occasionally feed at the wounds and oviposition punctures made available by females . Plant cells around the oviposition holes usually die and form ayellow necrotic spot, which is similar to necrotic spots created by pathogens . The leafminer is thus a special insect with a damage pattern in plants somewhat similar to pathogens, and is a good model to test relationships between insect damage patterns and plant defense patterns. In addition to its importance as a model insect in plant defense studies, this pest can cause economic losses to host plant crops, as mining larvae consume foliage while dwelling inside leaves . Leafminer larvae consume mesophyll both in palisade and spongy tissues [13, 17]. Leafminer plant damage is very serious, but the insects are difficult to detect at early stages because they are well-hidden in the leaves; it is therefore important to explore the inherent defenses of plants to this insect. Consequently, our study of leafminer-plant interactions is not only important for exploring the mechanisms of plant-insect interactions, but also of value for leafminer pest management.
In this study, we used an Affymetrix ATH1 A. thaliana microarray, from an organism with a well-understood genomic background and thus capable of comprehensively representing transcriptome response, to study expression pattern changes in A. thaliana in response to both local (LI) and systemic (SI) pea leafminer damage. We found that more than 3000 genes were induced in the locally-damaged tissue, and that these genes could be divided into two categories: metabolic processes and stimulus response. Systemic defense of A. thaliana to pea leafminer was very similar to local defense, and the SI-induced genes were almost the same as LI-induced genes, but fewer in number and with lower fold changes. Our analysis of defense signal pathways to leafminer in A. thaliana revealed that signal responses to insects, bacteria, and fungi were all greatly induced. We then downloaded data from online databases and used hierarchical clustering to explore the relationships among A. thaliana expression patterns induced by different types of predators. Interestingly, two different types of data provided evidence that the response to pea leafminer in A. thaliana is more similar to that induced by pathogens than by insects, supporting our hypothesis that plant response patterns are closely related to the damage pattern of attackers.