Cytokinins (CKs) are well-established as important phytohormonal regulators of plant growth and development. An increasing number of studies have also revealed the function of these hormones in plant responses to biotic and abiotic stresses. While the function of certain CK classes, including trans-zeatin and isopentenyladenine-type CKs, have been studied in detail, the role of cis-zeatin-type CKs (cZs) in plant development and in mediating environmental interactions is less well defined. Here we provide a comprehensive summary of the current knowledge about abundance, metabolism and activities of cZs in plants. We outline the history of their analysis and the metabolic routes comprising cZ biosynthesis and degradation. Further we provide an overview of changes in the pools of cZs during plant development and environmental interactions. We summarize studies that investigate the role of cZs in regulating plant development and defence responses to pathogen and herbivore attack and highlight their potential role as 'novel' stress-response markers. Since the functional roles of cZs remain largely based on correlative data and genetic manipulations of their biosynthesis, inactivation and degradation are few, we suggest experimental approaches using transgenic plants altered in cZ levels to further uncover their roles in plant growth and environmental interactions and their potential for crop improvement.
BackgroundPlant metabolites are commonly functionally classified, as defense- or growth-related phytohormones, primary and specialized metabolites, and so forth. Analytical procedures for the quantifications of these metabolites are challenging because the metabolites can vary over several orders of magnitude in concentrations in the same tissues and have very different chemical characteristics. Plants clearly adjust their metabolism to respond to their prevailing circumstances in very sophisticated ways that blur the boundaries among these functional or chemically defined classifications. But if plant biologists want to better understand the processes that are important for a plant’s adaptation to its environment, procedures are needed that can provide simultaneous quantifications of the large range of metabolites that have the potential to play central roles in these adjustments in a cost and time effective way and with a low sample consumption.ResultsHere we present a method that combines well-established methods for the targeted analysis of phytohormones, including jasmonates, salicylic acid, abscisic acid, gibberellins, auxins and cytokinins, and extends it to the analysis of inducible and constitutive defense compounds, as well as the primary metabolites involved in the biosynthesis of specialized metabolites and responsible for nutritional quality (e.g., sugars and amino acids). The method is based on a single extraction of 10–100 mg of tissue and allows a broad quantitative screening of metabolites optimized by their chemical characteristics and concentrations, thereby providing a high throughput analysis unbiased by the putative functional attributes of the metabolites. The tissues of Nicotiana attenuata which accumulate high levels of nicotine and diterpene glycosides, provide a challenging matrix that thwarts quantitative analysis; the analysis of various tissues of this plant are used to illustrate the robustness of the procedure.ConclusionsThe method described has the potential to unravel various, until now overlooked interactions among different sectors of plant metabolism in a high throughput manner. Additionally, the method could be particularly beneficial as screening method in forward genetic approaches, as well as for the investigation of plants from natural populations that likely differ in metabolic traits.Electronic supplementary materialThe online version of this article (doi:10.1186/s13007-016-0130-x) contains supplementary material, which is available to authorized users.
Abstract1. Plants emit volatile blends specific to particular herbivore interactions, which predators and parasitoids learn to associate with prey, increasing herbivore mortality and thereby plant fitness in a phenomenon termed indirect defence.2. Herbivore-induced plant volatile blends commonly include both rapid, transient green leaf volatiles (GLVs) and delayed, enduring sesquiterpenes. A few laboratory studies indicate that insects can use plant volatiles to time behaviour, but it is not known whether and how the temporal dynamics of plant volatile blends influence their function in indirect defence.3. We characterized the activity of the native herbivores Manduca sexta and Tupiocoris notatus and their predators, Geocoris spp., on their host plant Nicotiana attenuata in their natural habitat. Diurnal predator activity only partially overlapped with variable herbivore activity, and herbivore attack at the beginning or end of the photophase elicited plant volatile blends with distinct GLV and sesquiterpene profiles.4. In field trials, day-active Geocoris spp. predators preferred morning-over eveningtypical GLV blends. Using plants genetically transformed so as to be unable to produce specific volatiles, we found that GLVs increased predation after dawn elicitations, whereas sesquiterpenes increased predation after dusk elicitations in field trials.5. We conclude that predators respond to temporal differences in plant volatile blends, and that the different dynamics of specific volatiles permit effective indirect defence despite variable herbivore activity in nature. K E Y W O R D SGeocoris sp., green leaf volatiles, herbivore-induced plant volatiles, Manduca sexta, Nicotiana attenuata, sesquiterpenes, temporal dynamics, Tupiocoris notatus | INTRODUCTIONFlowering plants (angiosperms) and the insect herbivores that attack them are among the most diverse groups of multicellular life on Earth.Perhaps it is not surprising that plants can induce defences with great specificity in response to attack by particular insect herbivores (reviewed in Schuman & Baldwin, 2016), as exemplified by the specificity of herbivore-induced plant volatiles (HIPVs, reviewed e.g. in Howe & Jander, 2008). Much work on plant-insect interactions is done under controlled conditions required to dissect intricate mechanisms of specificity in elicitation and response. However, to be useful for wild plants, responses must keep functioning in the face of environmental disturbances: they must be robust (Kitano, 2004). Most plant and insect communities in nature are unevenly distributed over space andtime (Agrawal, Lau, & Hambäck, 2006) and changes in spatiotemporal co-occurrence may alter the course of plant-insect interactions (Brown, 2003;Kolasa & Rollo, 1991;López-Carretero, Díaz-Castelazo, Boege, & Rico-Gray, 2014). Thus it is important to ask how robust are plant defences when faced with the variable herbivore communities that characterize natural interactions.Plant indirect defences are perhaps more susceptible to disturbance by shifts in t...
Nearly half a century ago insect herbivores were found to induce the formation of green islands by manipulating cytokinin (CK) levels. However, the response of the CK pathway to attack by chewing insect herbivores remains unclear. Here, we characterize the CK pathway of Nicotiana attenuata (Torr. ex S. Wats.) and its response to wounding and perception of herbivore-associated molecular patterns (HAMPs). We identified 44 genes involved in CK biosynthesis, inactivation, degradation, and signaling. Leaf wounding rapidly induced transcriptional changes in multiple genes throughout the pathway, as well as in the levels of CKs, including isopentenyladenosine and cis-zeatin riboside; perception of HAMPs present in the oral secretions (OS) of the specialist herbivore Manduca sexta amplified these responses. The jasmonate pathway, which triggers many herbivore-induced processes, was not required for these HAMP-triggered changes, but rather suppressed the CK responses. Interestingly CK pathway changes were observed also in systemic leaves in response to wounding and OS application indicating a role of CKs in mediating long distance systemic processes in response to herbivory. Since wounding and grasshopper OS elicited similar accumulations of CKs in Arabidopsis thaliana L., we propose that CKs are integral components of wounding and HAMP-triggered responses in many plant species.
BackgroundThe evolutionary arms race between plants and insects has driven the co-evolution of sophisticated defense mechanisms used by plants to deter herbivores and equally sophisticated strategies that enable phytophagous insects to rapidly detoxify the plant’s defense metabolites. In this study, we identify the genetic determinants that enable the mirid, Tupiocoris notatus, to feed on its well-defended host plant, Nicotiana attenuata, an outstanding model for plant-insect interaction studies.ResultsWe used an RNAseq approach to evaluate the global gene expression of T. notatus after feeding on a transgenic N. attenuata line which does not accumulate jasmonic acid (JA) after herbivory, and consequently accumulates very low levels of defense metabolites. Using Illumina sequencing, we generated a de novo assembled transcriptome which resulted in 63,062 contigs (putative transcript isoforms) contained in 42,610 isotigs (putative identified genes). Differential expression analysis based on RSEM-estimated transcript abundances identified 82 differentially expressed (DE) transcripts between T. notatus fed on wild-type and the defenseless plants. The same analysis conducted with Corset-estimated transcript abundances identified 59 DE clusters containing 85 transcripts. In both analyses, a larger number of DE transcripts were found down-regulated in mirids feeding on JA-silenced plants (around 70%). Among these down-regulated transcripts we identified seven transcripts possibly involved in the detoxification of N. attenuata defense metabolite, specifically, one glutathione-S-transferase (GST), one UDP-glucosyltransferase (UGT), five cytochrome P450 (P450s), and six serine proteases. Real-time quantitative PCR confirmed the down-regulation for six transcripts (encoding GST, UGT and four P450s) and revealed that their expression was only slightly decreased in mirids feeding on another N. attenuata transgenic line specifically silenced in the accumulation of diterpene glycosides, one of the many classes of JA-mediated defenses in N. attenuata.ConclusionsThe results provide a transcriptional overview of the changes in a specialist hemimetabolous insect associated with feeding on host plants depleted in chemical defenses. Overall, the analysis reveals that T. notatus responses to host plant defenses are narrow and engages P450 detoxification pathways. It further identifies candidate genes which can be tested in future experiments to understand their role in shaping the T. notatus-N. attenuata interaction.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3348-0) contains supplementary material, which is available to authorized users.
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