Enhancing inositol pyrophosphate accumulation in plants alters growth, phosphate homeostasis, and insect herbivory.

Plants never had it easy. When their ancestors colonized the land about 460 M years ago during the Ordovician period, they were immediately followed by crustaceans—which eventually developed into insects—that found plants a ready source of food. Ever since plants have been at the bottom of the food chain for pathogens and predators from viruses to mammalian herbivores. Unlike animals, plants cannot run away, having given up motility to maximize their surface exposed to sunlight. In lieu, they became masters in chemical warfare and communication to recognize and fend off pathogens and herbivores. Their “claws and teeth” are a dazzling arsenal of chemicals, metabolic and regulatory pathways, producing sensing and communication molecules that attract increasing interest from chemists and biologists for their potential use in medicine and agriculture. > Humans have also learned to use toxic compounds such as digitalis, atropine, opium or nicotine for medicinal, cosmetic or recreational use. Among these molecules are many spices, including the pungent piperine and capsaicin from peppers, or the glucosinolates from mustard and horseradish, and the bitter polyphenols, flavonoids or terpenes from red grapes, coffee beans, tea or cabbage. Humans have long come to appreciate these tastes—that originally evolved as a warning signal to herbivores—for centuries, spices were the most valuable commodity in global trade. Humans have also learned to use toxic compounds such as digitalis, atropine, opium or nicotine for medicinal, cosmetic or recreational use. The alkaloid taxol from the bark of the Pacific yew is a potent chemotherapeutic drug for cancer treatment; artemisinin, isolated from the plant Artemisia annua, or sweet wormwood, has long been employed in Chinese herbal medicine and been refined into a treatment for malaria. The metabolic pathways of plant compounds with medicinal value are therefore an active field of research with the objective of engineering these into E. coli or …

The pathway mediated by jasmonic acid (JA), biosynthesized via 13-lipoxygenases (LOX), plays a central role in both plant development and defense. In rice, there are at least fourteen 13-LOXs. Yet, only two 13-LOXs have been known to be involved in the biosynthesis of JA and plant defenses in rice. Here we cloned a chloroplast-localized 13-LOX gene from rice, OsRCI-1, whose transcripts were upregulated following infestation by brown planthopper (BPH, Nilaparvata lugens), one of the most important pests in rice. Overexpression of OsRCI-1 (oeRCI lines) increased levels of BPH-induced JA, jasmonate-isoleucine, trypsin protease inhibitors and three volatile compounds, 2-heptanone, 2-heptanol and α-thujene. BPHs showed a decreased colonization, fecundity and mass, and developed slowly on oeRCI plants compared with wild-type (WT) plants. Moreover, BPH-infested oeRCI plants were more attractive to the egg parasitoid of BPH, Anagrus nilaparvatae than equally treated WT plants. The decreased attractiveness to BPH and enhanced attractiveness to the parasitoid of oeRCI plants correlated with higher levels of BPH-induced 2-heptanone and 2-heptanol, and 2-heptanone, respectively. Compared with oeRCI plants, WT plants had higher plant height and 1000-grain weight. These results indicate that OsRCI-1 is involved in herbivore-induced JA bursts and plays a role in plant defense and growth.

Jasmonic acid (JA) is a plant hormone that plays important roles in regulating plant defenses against necrotrophic pathogens and herbivorous insects, but the role of JA in mediating the plant responses to root-knot nematodes has been unclear. Here we show that an application of either methyl jasmonate (MeJA) or the JA-mimic coronatine (COR) on Arabidopsis significantly reduced the number of galls caused by the root-knot nematode Meloidogyne hapla. Interestingly, the MeJA-induced resistance was independent of the JA-receptor COI1 (CORONATINE INSENSITIVE 1). The MeJA-treated plants accumulated the JA precursor cis-(+)-12-oxo-phytodienoic acid (OPDA) in addition to JA/JA-Isoleucine, indicating a positive feedback loop in JA biosynthesis. Using mutants in the JA-biosynthetic pathway, we found that plants deficient in the biosynthesis of JA and OPDA were hyper-susceptible to M. hapla. However, the opr3 mutant, which cannot convert OPDA to JA, exhibited wild-type levels of nematode galling. In addition, mutants in the JA-biosynthesis and perception which lie downstream of opr3 also displayed wild-type levels of galling. The data put OPR3 (OPDA reductase 3) as the branch point between hyper-susceptibility and wild-type like levels of disease. Overall, the data suggests that the JA precursor, OPDA, plays a role in regulating plant defense against nematodes.

Jasmonic acid (JA) is a critical hormonal regulator of plant growth and defense. To advance our understanding of the architecture and dynamic regulation of the JA gene regulatory network, we performed a high-resolution RNA-seq time series of methyl JA-treated Arabidopsis thaliana at 15 time points over a 16-h period. Computational analysis showed that methyl JA (MeJA) induces a burst of transcriptional activity, generating diverse expression patterns over time that partition into distinct sectors of the JA response targeting specific biological processes. The presence of transcription factor (TF) DNA binding motifs correlated with specific TF activity during temporal MeJA-induced transcriptional reprogramming. Insight into the underlying dynamic transcriptional regulation mechanisms was captured in a chronological model of the JA gene regulatory network. Several TFs, including MYB59 and bHLH27, were uncovered as early network components with a role in pathogen and insect resistance. Analysis of subnetworks surrounding the TFs ORA47, RAP2.6L, MYB59, and ANAC055, using transcriptome profiling of overexpressors and mutants, provided insights into their regulatory role in defined modules of the JA network. Collectively, our work illuminates the complexity of the JA gene regulatory network, pinpoints and validates previously unknown regulators, and provides a valuable resource for functional studies on JA signaling components in plant defense and development.

Jasmonic acid (JA) regulates plant defenses against necrotrophic pathogens and insect herbivores. Salicylic acid (SA) and abscisic acid (ABA) can antagonize JA‐regulated defenses, thereby modulating pathogen or insect resistance. We performed a genome‐wide association (GWA) study on natural genetic variation in Arabidopsis thaliana for the effect of SA and ABA on the JA pathway. We treated 349 Arabidopsis accessions with methyl JA (MeJA), or a combination of MeJA and either SA or ABA, after which expression of the JA‐responsive marker gene PLANT DEFENSIN1.2 (PDF1.2) was quantified as a readout for GWA analysis. Both hormones antagonized MeJA‐induced PDF1.2 in the majority of the accessions but with a large variation in magnitude. GWA mapping of the SA‐ and ABA‐affected PDF1.2 expression data revealed loci associated with crosstalk. GLYI4 (encoding a glyoxalase) and ARR11 (encoding an Arabidopsis response regulator involved in cytokinin signalling) were confirmed by T‐DNA insertion mutant analysis to affect SA–JA crosstalk and resistance against the necrotroph Botrytis cinerea. In addition, At1g16310 (encoding a cation efflux family protein) was confirmed to affect ABA–JA crosstalk and susceptibility to Mamestra brassicae herbivory. Collectively, this GWA study identified novel players in JA hormone crosstalk with potential roles in the regulation of pathogen or insect resistance.

Melatonin plays a crucial role in the mitigation of plant biotic stress through induced defense responses and pathogen attenuation. Utilizing the current knowledge of signaling and associated mechanism of this phytoprotectant will be invaluable in sustainable plant disease management. Biotic stress in plants involves complex regulatory networks of various sensory and signaling molecules. In this context, the polyfunctional, ubiquitous-signaling molecule melatonin has shown a regulatory role in biotic stress mitigation in plants. The present review conceptualized the current knowledge concerning the melatonin-mediated activation of the defense signaling network that leads to the resistant or tolerant phenotype of the infected plants. Fundamentals of signaling networks involved in melatonin-induced reactive oxygen species (ROS) or reactive nitrogen species (RNS) scavenging through enzymatic and non-enzymatic antioxidants have also been discussed. Increasing evidence has suggested that melatonin acts upstream of mitogen-activated proteinase kinases in activation of defense-related genes and heat shock proteins that provide immunity against pathogen attack. Besides, the direct application of melatonin on virulent fungi and bacteria showed disrupted spore morphology, destabilization of cell ultrastructure, reduced biofilm formation, and enhanced mortality that led to attenuate disease symptoms on melatonin-treated plants. The transcriptome analysis has revealed the down-regulation of pathogenicity genes, metabolism-related genes, and up-regulation of fungicide susceptibility genes in melatonin-treated pathogens. The activation of melatonin-mediated systemic acquired resistance (SAR) through cross-talk with salicylic acid (SA), jasmonic acid (JA) has been essential for viral disease management. The high endogenous melatonin concentration has also been correlated with the up-regulation of genes involved in pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI). The present review highlights the versatile functions of melatonin towards direct inhibition of pathogen propagule along with active participation in mediating oxidative burst and simulating PTI, ETI and SAR responses. The hormonal cross-talk involving melatonin mediated biotic stress tolerance through defense signaling network suggests its suitability in a sustainable plant protection system.

Molecular mechanisms associated with biochar-elicited suppression of soilborne plant diseases and improved plant performance are not well understood. A stem base inoculation approach was used to explore the ability of biochar to induce systemic resistance in tomato plants against crown rot caused by a soilborne pathogen, Fusarium oxysporum f. sp. radicis lycopersici. RNA-seq transcriptome profiling of tomato, and experiments with jasmonic and salycilic acid deficient tomato mutants, were performed to elucidate the in planta molecular mechanisms involved in induced resistance. Biochar (produced from greenhouse plant wastes) was found to mediate systemic resistance against Fusarium crown rot and to simultaneously improve tomato plant growth and physiological parameters by up to 63%. Transcriptomic analysis (RNA-seq) of tomato demonstrated that biochar had a priming effect on gene expression and upregulated the pathways and genes associated with plant defense and growth such as jasmonic acid, brassinosteroids, cytokinins, auxin and synthesis of flavonoid, phenylpropanoids and cell wall. In contrast, biosynthesis and signaling of the salicylic acid pathway was downregulated. Upregulation of genes and pathways involved in plant defense and plant growth may partially explain the significant disease suppression and improvement in plant performance observed in the presence of biochar.

Linking development to defense: auxin in plant–pathogen interactions

Unraveling molecular mechanisms underlying plant defense in response to dual insect attack : studying density-dependent effects

Genome-wide analysis of the WRKY family in Nicotiana benthamiana reveals key members regulating lignin synthesis and Bemisia tabaci resistance

A putative 12-oxophytodienoate reductase gene CsOPR3 from Camellia sinensis, is involved in wound and herbivore infestation responses

Plant fatty acids (FAs) and lipids are essential in storing energy and act as structural components for cell membranes and signaling molecules for plant growth and stress responses. Acyl carrier proteins (ACPs) are small acidic proteins that covalently bind the fatty acyl intermediates during the elongation of FAs. The Arabidopsis thaliana ACP family has eight members. Through reverse genetic, molecular, and biochemical approaches, we have discovered that ACP1 localizes to the chloroplast and limits the magnitude of pattern-triggered immunity (PTI) against the bacterial pathogen Pseudomonas syringae pv. tomato. Mutant acp1 plants have reduced levels of linolenic acid (18:3), which is the primary precursor for biosynthesis of the phytohormone jasmonic acid (JA), and a corresponding decrease in the abundance of JA. Consistent with the known antagonistic relationship between JA and salicylic acid (SA), acp1 mutant plants also accumulate a higher level of SA and display corresponding shifts in JA- and SA-regulated transcriptional outputs. Moreover, methyl JA and linolenic acid treatments cause an apparently enhanced decrease of resistance against P. syringae pv. tomato in acp1 mutants than that in WT plants. The ability of ACP1 to prevent this hormone imbalance likely underlies its negative impact on PTI in plant defense. Thus, ACP1 links FA metabolism to stress hormone homeostasis to be negatively involved in PTI in Arabidopsis plant defense. [Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

The jasmonic acid (JA) pathway plays a central role in plant defense responses against insects. Some phloem-feeding insects also induce the salicylic acid (SA) pathway, thereby suppressing the plant's JA response. These phenomena have been well studied in dicotyledonous plants, but little is known about them in monocotyledons. We cloned a chloroplast-localized type 2 13-lipoxygenase gene of rice, OsHI-LOX, whose transcripts were up-regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis and the rice brown planthopper (BPH) Niaparvata lugens, as well as by mechanical wounding and treatment with JA. Antisense expression of OsHI-LOX (as-lox) reduced SSB- or BPH-induced JA and trypsin protease inhibitor (TrypPI) levels, improved the larval performance of SBB as well as that of the rice leaf folder (LF) Cnaphalocrocis medinalis, and increased the damage caused by SSB and LF larvae. In contrast, BPH, a phloem-feeding herbivore, showed a preference for settling and ovipositing on WT plants, on which they consumed more and survived better than on as-lox plants. The enhanced resistance of as-lox plants to BPH infestation correlated with higher levels of BPH-induced H(2)O(2) and SA, as well as with increased hypersensitive response-like cell death. These results imply that OsHI-LOX is involved in herbivore-induced JA biosynthesis, and plays contrasting roles in controlling rice resistance to chewing and phloem-feeding herbivores. The observation that suppression of JA activity results in increased resistance to an insect indicates that revision of the generalized plant defense models in monocotyledons is required, and may help develop novel strategies to protect rice against insect pests.

Ever since their discovery as key regulators of the jasmonate (JA) signaling pathway, repressor proteins of the JASMONATE ZIM-domain (JAZ) family are rising stars in research on hormonal regulation of plant growth and defense. In plant cells, JAZ repressor proteins interact with an E3 ubiquitin ligase complex (SCFCOI1) that together functions as a JA receptor. In uninduced cells, JAZs block the activity of transcriptional regulators of JA responses by physically binding to them. Upon perception of bioactive JAs, JAZ proteins are rapidly degraded via the ubiquitin/26S proteasome-dependent proteolytic pathway. This releases the JAZ-bound transcription factors, resulting in the activation of downstream JA responses. JAs play a dominant role in regulating defense responses against herbivorous insects and necrotrophic pathogens, and in adaptive responses to beneficial soil-borne microbes. In addition, JAs have a signal function in a myriad of other processes, including abiotic stress reactions and plant growth responses to environmental cues. The JA pathway functions in the context of a complex network of hormone-regulated signaling pathways that, depending on the environmental or developmental condition, can act antagonistically or synergistically on each other to finely balance resource allocation between growth and defense and minimize fitness tradeoffs. In the process of balancing plant growth and defense, gibberellins (GAs) emerged as dominant antagonists of the JA signaling output. GAs regulate different aspects of plant growth via DELLA repressor proteins that block the activity of transcriptional regulators of GA responses by physically binding to them. Analogous to the role of JAZs in the JA pathway, DELLAs are degraded upon perception of GAs, resulting in the activation of downstream growth responses. Interestingly, DELLAs also interact with JAZs, thereby mutually limiting the cellular binding capacity to their cognate transcription factors. Consequently, GA-mediated degradation of DELLAs enhances the cellular binding capacity of JAZs to their cognate transcription factors, thus reducing the potential JA signaling output. This GA-mediated antagonistic effect on the JA pathway becomes apparent during the shade-avoidance response of plants that grow in dense vegetation stands. Shade-intolerant plant species respond to competition for light by increasing apical dominance and accelerating stem and petiole elongation. These growth and developmental responses occur in response to a drop in the red:far-red (R:FR) light ratio that is sensed by the phytochrome photoreceptors, predominantly phyB, and are GA-dependent through GA-mediated degradation of DELLA proteins. This allows them to outgrow neighboring plants, but at the cost of a reduced defensive capacity against necrotrophic pathogens and insect herbivores. In this issue of New Phytologist, Leone and co-workers zoomed in on the specific role of the Arabidopsis thaliana (Arabidopsis) JAZ10 protein in this process and shed light on the involvement of DELLAs in GA-JA crosstalk during the shade avoidance response. Besides growth-related hormones, also effector proteins of pathogens and plant growth-promoting mycorrhizal fungi have recently been shown to target JAZ repressor proteins, thereby changing the defense-related signaling circuitry for their own benefit. Hence, JAZ repressor proteins are emerging as central targets in the rewiring of the hormone-regulated signaling circuitry that regulates growth and defense.

Understanding the host response to Ascochyta fabae in faba bean ( Vicia faba L.), is crucial to elucidate the biology of host resistance. In an attempt to unravel the faba bean – A. fabae interaction, we performed genome-wide transcriptome profiling by deepSuperSAGE that quantified the early transcriptional changes elicited by the fungus in the resistant 29H faba bean genotype. The total number of 26 bp tags obtained was 1,313,009, of which 51,484 were unique sequences (UniTags) and 161 of them corresponded to fungal sequences. Sequences with a full match of the 26 bp revealed 2,222 tags with a significant P-value that were expressed differentialy between inoculated and control leaves. After gene ontology (GO) annotation, 2,143 of these matched to databases sequences (approximately 1/3 into each GO domain). At a 2.7-fold change threshold, 1,197 sequences were significantly differentially expressed in infected as compared to control leaves. Of these, nearly half were up- and the other downregulated. The most enriched GO terms corresponded to tags related with photosynthesis metabolism or structural components. Ten of them can be associated with plant defense, due to their association with responses to the jasmonic acid pathway, pectin esterase activity or gene silencing. Validation of the SuperSAGE data by qPCR of ten differentially expressed UniTags confirmed a rapid increase or decrease in mRNA 8 to 12 hours after inoculation in most of the up-regulated tags and, less consistently, in the downregulated ones. This study represents the most comprehensive analysis of the Ascochyta-response transcriptome of faba bean available to date. The applicability of these tags will increase as more faba bean genomic and cDNA sequences become available.