Disentangling the Potato Tuber Moth-Induced Early-Defense Response by Simulated Herbivory in Potato Plants

Abstract

Plants rely on the perception of a multitude of herbivory-associated cues (HACs) to activate their defense response to insect herbivores. These stimuli are mainly derived from three functional components, namely, mechanical damage, insect-associated microbe, and insect’s chemical cues. While simulated herbivory integrating these stimuli is widely exploited for complementing actual herbivory in clarifying the details of plant–herbivore interaction, breaking down these stimuli and identifying the mechanisms of plant responses associated with them have been less explored. In this study, the components of potato tuber moth (Phthorimaea operculella, PTM) herbivory were reorganized in a cumulative way and their impacts on the early defense responses of potato leaf were characterized. We found that simulated and actual herbivory of PTM triggered similar patterns of phytohormonal and transcriptomic responses in potato leaf. Moreover, the microbe in the PTM herbivory stimuli is associated with the regulation of the phytohormones jasmonic acid (JA) and abscisic acid (ABA) since reducing the microbe in HAC could reduce JA while increasing ABA. In addition, seven robust gene modules were identified to illustrate how potato plants respond to different PTM herbivory stimuli when herbivory components increased. Significantly, we found that mechanical damage mainly activated JA-mediated signaling; PTM-derived HACs contributed much more to potato early-defense response and induced signaling molecules such as multiple protein kinases; orally secreted bacteria stimuli could antagonize PTM-derived HACs and modulate plant defense, including repressing phenylpropanoid biosynthesis. Our study broadened the understanding of how potato plants integrate the responses to a multitude of stimuli upon PTM herbivory and evidenced that insect-associated microbes greatly modulated the plants response to insect herbivory.

Functional characterization of a terpene synthase responsible for (E)-β-ocimene biosynthesis identified in Pyrus betuleafolia transcriptome after herbivory

“…In addition, 24 genes associated with the biosynthetic pathways of volatile terpenoids and HPL-derived green leaf volatiles were upregulated after S. litura infestation, highlighting their potential roles in S. litura-induced pear defenses. Unlike defense-related nonvolatile and volatile secondary metabolites, growth-related photosynthesis was suppressed in S. litura-infested P. betuleafolia (Table S7), which is similar to the findings reported in the defense response of potato (Mao et al, 2022), cotton (Zhang et al, 2022), rice (Wang et al, 2020;Satturu et al, 2021), wheat (Zhang et al, 2020) and tomato (Ke et al, 2021) plants induced by herbivores. In herbivoredamaged plants, suppression of photosynthesis might be a Behavioral preference of Spodoptera litura larvae for (E)-b-ocimene.…”

“…Plants, especially perennial fruit trees such as pear, are frequently subject to attack by a variety of insect pests. In response to insect herbivore attack, plants have evolved highly sophisticated strategies allowing them to perceive various herbivory-associated molecules from insects’ oral secretions (or regurgitant), oviposition fluids or larval frass and trigger complex defense systems ( Mao et al., 2022 ; Zhang et al., 2022 ). After the recognition of herbivores, plant initiate a series of early signaling events such as V m variation, Ca 2+ elevation, production of reactive oxygen species and activation of MAP kinases, as well as phytohormone-centered regulatory networks to broad transcriptional reprogramming, ultimately leads to the synthesis and accumulation of defensive proteins and defense-associated secondary metabolites ( Erb and Reymond, 2019 ).…”

Comparative Transcriptome Analysis of Defense Response of Potato to Phthorimaea operculella Infestation

“…In the study of Mao et al [20], ROS signaling was activated by PTM-derived herbivoryrelated cues as early as 1 h after treatment. In general, the process of ROS generation occurs within seconds to minutes of stress initiation [58,59], whereas it is possible that the subsequent results might be different in response to the age of PTMs or depending on treatment time.…”

“…Numerous studies have shown that JA plays a central role in regulating plant responses to phytophagous insects, while other hormones act in concert or antagonize the JA signaling pathway [1,12]. The selective activation of downstream-related pathways or signals by plants depends on the insect and plant species, and time differences in insect infestation can also lead to dramatic changes in plant defense responses [18][19][20]. Transcription factors play a key regulatory role in the global defense deployment of plants [12].…”

“…[11,13]. Thus, at the plant-insect interface, mechanical damage and insect oral secretion stimuli OS are two main herbivory-associated stimuli [19,20]. Mechanical damage is often used as a control in experiments to investigate plant defense responses against herbivory.…”