ABSTRACT
Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these patterns remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlated with the average abiotic characteristics of each species' contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.
Subject(s)
Vitis , Phylogeny , Biological Evolution , Plant Leaves , Plants , HerbivoryABSTRACT
Plants produce chemical defenses that poison insect herbivores or deter their feeding, but herbivores are also accompanied by microbial endosymbionts crucial for their nutrition, reproduction, and fitness. Hence, plant defenses could target a herbivore's beneficial endosymbionts, but this has not yet been demonstrated. Here, we studied flavonoids that are induced when rice is attacked by a phloem-feeding pest, the brown planthopper (BPH), which harbors beneficial yeast-like symbionts (YLS) essential for insect nutrition, such as by remedying deficiencies in sterols. BPH attack dramatically increased sakuranetin accumulations in leaf sheaths and phloem exudates. Sakuranetin is an antifungal phytoalexin derived from the antibacterial precursor, naringenin, via catalysis of naringenin-O-methyltransferase (NOMT). When added to artificial diets, sakuranetin decreased BPH survivorship, suggesting that it functions as an induced defense. Mutation of NOMT abolished sakuranetin accumulation and increased BPH oviposition and hatching rates. High-throughput amplicon sequencing revealed that BPH fed on sakuranetin-deficient nomt lines were enriched in YLS with only minor changes in the bacterial endosymbionts, compared to those feeding on sakuranetin-rich wild-type (WT) plants. In-vitro feeding of sakuranetin suggested that this flavonoid directly inhibited the growth of YLS. BPH feeding on nomt lines accumulated higher cholesterol levels, which might be attributed to increases in the supply of sterol precursors from the YLS, while nomt lines suffered more damage than WT plants did from BPH herbivory. BPH-elicited accumulation of sakuranetin requires intact jasmonate (JA) signaling. This study reveals that rice uses a JA-induced antifungal flavonoid phytoalexin in defense against BPH by inhibiting its beneficial endosymbionts.
Subject(s)
Hemiptera , Oryza , Animals , Female , Antifungal Agents , Flavonoids/pharmacology , Gene Expression Regulation, Plant , Oryza/geneticsABSTRACT
BACKGROUND: Resistance to insect pests is an important self-defense characteristic of pepper plants. However, the resistance of different pepper cultivars to Spodoptera litura larvae, one of the main insect pest species on pepper, is not well understood. RESULTS: Among seven pepper cultivars evaluated, cayenne pepper 'FXBX' showed the highest repellency to third instar S. litura larvae, Chao tian chili pepper 'BLTY2' showed the lowest repellency. Plant volatiles (1-hexene, hexanal, ß-ionone, (E,E)-2,6-nonadienal, and methyl salicylate) affected host selection by S. litura. Among these, 1-hexene, hexanal, and ß-ionone at concentrations naturally-released by pepper leaves were found to repel S. litura. Interestingly, S. litura larvae fed on the larva-attracting pepper cultivar, (BLTY2) had an extended developmental period, which was about 13 days longer than larvae fed on FXBX. Besides, the survival rate of larvae fed on BLTY2 was 22.5 ± 0.0%, indicating that the leaves of BLTY2 can kill S. litura larvae. Correlation analysis showed that larval survival rate, emergence rate, female adult longevity, and pupal weight were positively correlated with the vitamin C, amino acids, protein, cellulose, and soluble sugar contents, but were negatively correlated with wax and flavonoids contents. CONCLUSION: We identified two different modes of direct defense exhibited by pepper cultivars against S. litura. One involves the release of repellent volatiles to avoid been fed on (FXBX cultivar). The other involves the inhibition of the growth and development or the direct killing of S. litura larvae which feeds on it (BLTY2 cultivar). © 2022 Society of Chemical Industry.
Subject(s)
Flavonoids , Sugars , Aldehydes , Alkenes , Amino Acids , Animals , Ascorbic Acid , Cellulose , Larva , Norisoprenoids , SpodopteraABSTRACT
Plants protect themselves against pest attack utilizing both direct and indirect modes of defense. The direct mode of defense includes morphological, biochemical, and molecular barriers that affect feeding, growth, and survival of herbivores whereas the indirect mode of defense includes release of a blend of volatiles that attract natural enemies of the pests. Both of these strategies adopted by plants are reinforced if the plants are supplied with one of the most abundant metalloids, silicon (Si). Plants absorb Si as silicic acid (Si(OH)4) and accumulate it as phytoliths, which strengthens their physical defense. This deposition of Si in plant tissue is up-regulated upon pest attack. Further, Si deposited in the apoplast, suppresses pest effector molecules. Additionally, Si up-regulates the expression of defense-related genes and proteins and their activity and enhances the accumulation of secondary metabolites, boosting induced molecular and biochemical defenses. Moreover, Si plays a crucial role in phytohormone-mediated direct and indirect defense mechanisms. It is also involved in the reduction of harmful effects of oxidative stress resulting from herbivory by accelerating the scavenging process. Despite increasing evidence of its multiple roles in defense against pests, the practical implications of Si for crop protection have received less attention. Here, we highlight recent developments in Si-mediated improved plant resistance against pests and its significance for future use in crop improvement.
Subject(s)
Herbivory , Silicon , Plant Defense Against Herbivory , Plant Growth Regulators , PlantsABSTRACT
MAIN CONCLUSION: Metabolite profiling, biochemical assays, and transcript analysis revealed differential modulation of specific induced defense responses in local, older, and younger systemic leaves in Solanum lycopersicum upon Spodoptera litura herbivory. Plants reconfigure their metabolome upon herbivory to induce production of defense metabolites involved in both direct and indirect defenses against insect herbivores. Herbivory mediated leaf-to-leaf systemic induction pattern of primary and non-volatile secondary metabolites is not well studied in tomato. Here, we show that, in cultivated tomato Solanum lycopersicum herbivory by generalist insect, Spodoptera litura results in differential alteration of primary metabolites, majorly sugars and amino acids and specific secondary metabolites in local, younger, and older systemic leaves. Cluster analysis of 55 metabolites identified by GC-MS showed correlation between local and younger systemic leaves. Re-allocation of primary metabolites like glucose and amino acids from the local to systemic leaf was observed. Secondary metabolites chlorogenic acid, caffeic acid, and catechin were significantly induced during herbivory in systemic leaves. Among specific secondary metabolites, chlorogenic acid and catechin significantly inhibits S. litura larval growth in all stages. Local leaf exhibited increased lignin accumulation upon herbivory. Differential alteration of induced defense responses like reactive oxygen species, polyphenol oxidase activity, proteinase inhibitor, cell wall metabolites, and lignin accumulation was observed in systemic leaves. The metabolite alteration also resulted in increased defense in systemic leaves. Thus, comparative analysis of metabolites in local and systemic leaves of tomato revealed a constant re-allocation of primary metabolites to systemic leaves and differential induction of secondary metabolites and induced defenses upon herbivory.
Subject(s)
Herbivory , Plant Leaves/chemistry , Plant Leaves/metabolism , Solanum lycopersicum/physiology , Spodoptera/physiology , Animals , Catechin/metabolism , Catechol Oxidase , Cell Wall/metabolism , Chlorogenic Acid/analysis , Chlorogenic Acid/metabolism , Gas Chromatography-Mass Spectrometry , Hydrogen Peroxide/analysis , Hydrogen Peroxide/metabolism , Larva/growth & development , Lignin/metabolism , Solanum lycopersicum/chemistry , Metabolome , Pupa/physiology , Secondary Metabolism , Signal TransductionABSTRACT
Numerous plant species emit volatile nitriles upon herbivory, but the biosynthesis as well as the relevance of these nitrogenous compounds in plant-insect interactions remains unknown. Populus trichocarpa has been shown to produce a complex blend of nitrogenous volatiles, including aldoximes and nitriles, after herbivore attack. The aldoximes were previously reported to be derived from amino acids by the action of cytochrome P450 enzymes of the CYP79 family. Here we show that nitriles are derived from aldoximes by another type of P450 enzyme in P. trichocarpa. First, feeding of deuterium-labeled phenylacetaldoxime to poplar leaves resulted in incorporation of the label into benzyl cyanide, demonstrating that poplar volatile nitriles are derived from aldoximes. Then two P450 enzymes, CYP71B40v3 and CYP71B41v2, were characterized that produce aliphatic and aromatic nitriles from their respective aldoxime precursors. Both possess typical P450 sequence motifs but do not require added NADPH or cytochrome P450 reductase for catalysis. Since both enzymes are expressed after feeding by gypsy moth caterpillars, they are likely to be involved in herbivore-induced volatile nitrile emission in P. trichocarpa. Olfactometer experiments showed that these volatile nitriles have a strong repellent activity against gypsy moth caterpillars, suggesting they play a role in induced direct defense against poplar herbivores.
Subject(s)
Gene Expression Regulation, Plant , Moths/drug effects , Nitriles/metabolism , Oximes/metabolism , Populus/enzymology , Volatile Organic Compounds/pharmacology , Animals , Cytochrome P-450 Enzyme System/genetics , Cytochrome P-450 Enzyme System/metabolism , Herbivory , Larva , Moths/physiology , Oximes/chemistry , Phylogeny , Plant Leaves/enzymology , Plant Leaves/genetics , Plant Leaves/immunology , Plant Proteins/genetics , Plant Proteins/metabolism , Populus/genetics , Populus/immunology , Sequence Analysis, DNA , Volatile Organic Compounds/metabolismABSTRACT
Ethylene is a stress hormone with contrasting effects on herbivore resistance. However, it remains unknown whether these differences are plant- or herbivore-specific. We cloned a rice 1-aminocyclopropane-1-carboxylic acid (ACC) synthase gene, OsACS2, whose transcripts were rapidly up-regulated in response to mechanical wounding and infestation by two important pests: the striped stem borer (SSB) Chilo suppressalis and the brown planthopper (BPH) Nilaparvata lugens. Antisense expression of OsACS2 (as-acs) reduced elicited ethylene emission, SSB-elicited trypsin protease inhibitor (TrypPI) activity, SSB-induced volatile release, and SSB resistance. Exogenous application of ACC restored TrypPI activity and SSB resistance. In contrast to SSB, BPH infestation increased volatile emission in as-acs lines. Accordingly, BPH preferred to feed and oviposit on wild-type (WT) plants--an effect that could be attributed to two repellent volatiles, 2-heptanone and 2-heptanol, that were emitted in higher amounts by as-acs plants. BPH honeydew excretion was reduced and natural enemy attraction was enhanced in as-acs lines, resulting in higher overall resistance to BPH. These results demonstrate that ethylene signaling has contrasting, herbivore-specific effects on rice defense responses and resistance against a chewing and a piercing-sucking insect, and may mediate resistance trade-offs between herbivores of different feeding guilds in rice.