Numerous plants protect themselves from attackers by using specialized metabolites. The biosynthesis of these deterrent, often toxic metabolites is costly, as their synthesis diverts energy and resources on account of growth and development. How plants diversify investments into growth and defense is explained by the optimal defense theory. The central prediction of the optimal defense theory is that plants maximize growth and defense by concentrating specialized metabolites in tissues that are decisive for fitness. To date, supporting physiological evidence relies on the correlation between plant metabolite presence and animal feeding preference. Here, we use glucosinolates as a model to examine the effect of changes in chemical defense distribution on feeding preference. Taking advantage of the uniform glucosinolate distribution in transporter mutants, we show that high glucosinolate accumulation in tissues important to fitness protects them by guiding larvae of a generalist herbivore to feed on other tissues. Moreover, we show that the mature leaves of Arabidopsis thaliana supply young leaves with glucosinolates to optimize defense against herbivores. Our study provides physiological evidence for the central hypothesis of the optimal defense theory and sheds light on the importance of integrating glucosinolate biosynthesis and transport for optimizing plant defense.
Glucosinolates constitute the primary defense metabolites in Arabidopsis thaliana (Arabidopsis). Indole and aliphatic glucosinolates, biosynthesized from tryptophan and methionine, respectively, are known to serve distinct biological functions. Although all genes in the biosynthetic pathways are identified, and it is known where glucosinolates are stored, it has remained elusive where glucosinolates are produced at the cellular and tissue level. To understand how the spatial organization of the different glucosinolate biosynthetic pathways contributes to their distinct biological functions, we investigated the localization of enzymes of the pathways under constitutive conditions and, for indole glucosinolates, also under induced conditions, by analyzing the spatial distribution of several fluorophore-tagged enzymes at the whole plant and the cellular level. We show that key steps in the biosynthesis of the different types of glucosinolates are localized in distinct cells in separate as well as overlapping vascular tissues. The presence of glucosinolate biosynthetic enzymes in parenchyma cells of the vasculature may assign new defense-related functions to these cell types. The knowledge gained in this study is an important prerequisite for understanding the orchestration of chemical defenses from site of synthesis to site of storage and potential (re)mobilization upon attack.
In the phloem cap region of Arabidopsis plants, sulfur-rich cells (S-cells) accumulate >100 mM glucosinolates (GLS), but are biosynthetically inactive. The source and route of S-cell-bound GLS remain elusive. In this study, using single-cell sampling and scanning electron microscopy with energy-dispersive X-ray analysis we show that two GLS importers, NPF2.10/GTR1 and NPF2.11/GTR2, are critical for GLS accumulation in S-cells, although they are not localized in the S-cells. Comparison of GLS levels in S-cells in multiple combinations of homo-and heterografts of gtr1 gtr2, biosynthetic null mutant and wild-type plants indicate that S-cells accumulate GLS via symplasmic connections either directly from neighboring biosynthetic cells or indirectly to non-neighboring cells expressing GTR1/2. Distinct sources and transport routes exist for different types of GLS, and vary depending on the position of S-cells in the inflorescence stem. Based on these findings, we propose a model illustrating the GLS transport routes either directly from biosynthetic cells or via GTR-mediated import from apoplastic space radially into a symplasmic domain, wherein the S-cells are the ultimate sink. Similarly, we observed accumulation of the cyanogenic glucoside defensive compounds in high-turgor cells in the phloem cap of Lotus japonicus, suggesting that storage of defensive compounds in high-turgor cells may be a general mechanism for chemical protection of the phloem cap.
The phloem cap of Arabidopsis thaliana accumulates glucosinolates that yield toxic catabolites upon damage-induced hydrolysis. These defence compounds are stored in high concentrations in millimetre long S-cells. At early stages of development, S-cells initiate a process indicative of programmed cell death. How these cells are maintained in a highly turgescent state following this process is currently unknown. Here, we show that S-cells undergo substantial morphological changes during early differentiation. Vacuolar collapse and rapid clearance of the cytoplasm did not occur until senescence. Instead, smooth endoplasmic reticulum, Golgi bodies, vacuoles, and undifferentiated plastids were observed. Lack of chloroplasts indicates that S-cells depend on metabolite supply from neighbouring cells. Interestingly, TEM revealed numerous plasmodesmata between S-cells and neighbouring cells. Photoactivation of a symplasmic tracer showed coupling with neighbouring cells that are involved in glucosinolate synthesis. Hence, symplasmic transport might contribute to glucosinolate storage in S-cells. To investigate the fate of S-cells, we traced them in flower stalks from the earliest detectable stages to senescence. At late stages, S-cells were shown to deposit thick secondary cell walls and transform into phloem fibres. Thus, phloem fibres in the herbaceous plant Arabidopsis pass a pronounced phase of chemical defence during early stages of development.
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