Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

Abstract

(A.H.); 0000-0002-9675-934X (G.J.).As a response to insect attack, maize (Zea mays) has inducible defenses that involve large changes in gene expression and metabolism. Piercing/sucking insects such as corn leaf aphid (Rhopalosiphum maidis) cause direct damage by acquiring phloem nutrients as well as indirect damage through the transmission of plant viruses. To elucidate the metabolic processes and gene expression changes involved in maize responses to aphid attack, leaves of inbred line B73 were infested with corn leaf aphids for 2 to 96 h. Analysis of infested maize leaves showed two distinct response phases, with the most significant transcriptional and metabolic changes occurring in the first few hours after the initiation of aphid feeding. After 4 d, both gene expression and metabolite profiles of aphid-infested maize reverted to being more similar to those of control plants. Although there was a predominant effect of salicylic acid regulation, gene expression changes also indicated prolonged induction of oxylipins, although not necessarily jasmonic acid, in aphid-infested maize. The role of specific metabolic pathways was confirmed using Dissociator transposon insertions in maize inbred line W22. Mutations in three benzoxazinoid biosynthesis genes, Bx1, Bx2, and Bx6, increased aphid reproduction. In contrast, progeny production was greatly decreased by a transposon insertion in the single W22 homolog of the previously uncharacterized B73 terpene synthases TPS2 and TPS3. Together, these results show that maize leaves shift to implementation of physical and chemical defenses within hours after the initiation of aphid feeding and that the production of specific metabolites can have major effects in maize-aphid interactions.

Combined transcriptome and metabolome analyses to understand the dynamic responses of rice plants to attack by the rice stem borer Chilo suppressalis (Lepidoptera: Crambidae)

“…This is consistent with previous findings concerning aphid-infested maize [7] and maize that was mechanically wounded and then treated with the oral secretions of Mythimna separata [9]. Similarly, more DEGs were up-regulated than down-regulated when Arabidopsis plants were individually infested with Myzus persicae , Brevicoryne brassicae , Spodoptera exigua , or Pieris rapae [40], or when cotton was damaged by the chewing insects Helicoverpa armigera or Anthonomus grandis [41].…”

“…We found that changes in gene expression induced by C. suppressalis in rice were positively correlated with changes induced by ABA treatment in Arabidopsis , which agrees with previous results in several plant-insect systems [5, 7, 9, 40, 44]. The role of ABA in regulating defense against pathogens in rice has been well documented [51], but its role in resistance to insects is much less understood.…”

“…Hormonometer program analyses [34] (http://hormonometer.weizmann.ac.il/) was used to assess the similarity of the expression of rice genes induced by C. suppressalis with indexed data sets of those elicited by exogenous application of phytohormones to Arabidopsis as previously described [7]. The rice genes were blasted to the Arabidopsis thaliana genome.…”

“…The integration of modern omics technologies such as transcriptomics, proteomics, and metabolics provides a great opportunity for a deeper understanding of the mechanisms of plant defence responses to herbivore feeding at molecular and cellular levels [7, 9–11]. Previous results have suggested that plant response to herbivore feeding is a dynamic process, and that the transcript patterns, protein and metabolite profiles are temporally and spatially regulated [1, 10, 12].…”

“…Previous results have suggested that plant response to herbivore feeding is a dynamic process, and that the transcript patterns, protein and metabolite profiles are temporally and spatially regulated [1, 10, 12]. This suggests that it is essential to investigate the dynamic at transcriptional, proteomic and metabolic changes associated to insect feeding [6, 7, 9, 11]. Transcriptomic and proteomic studies are only able to predict changes in gene expression and the protein level, while metabolomic studies investigate the changed functions exerted by these genes or proteins.…”