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  1. Jasmonate activates secondary cell wall biosynthesis through MYC2–MYB46 module

    Formation of secondary cell wall (SCW) is tightly regulated spatiotemporally by various developmental and environmental signals. Successful fine-tuning of the trade-off between SCW biosynthesis and stress responses requires a better understanding of how plant growth is regulated under environmental stress conditions. However, the current understanding of the interplay between environmental signaling and SCW formation is limited. The lipid-derived plant hormone jasmonate (JA) and its derivatives are important signaling components involved in various physiological processes including plant growth, development, and abiotic/biotic stress responses. Recent studies suggest that JA is involved in SCW formation but the signaling pathway has not been studiedmore » for how JA regulates SCW formation. We tested this hypothesis using the transcription factor MYB46, a master switch for SCW biosynthesis, and JA treatments. Both the transcript and protein levels of MYB46, a master switch for SCW formation, were significantly increased by JA treatment, resulting in the upregulation of SCW biosynthesis. We then show that this JA-induced upregulation of MYB46 is mediated by MYC2, a central regulator of JA signaling, which binds to the promoter of MYB46. We conclude that this MYC2-MYB46 module is a key component of the plant response to JA in SCW formation.« less
  2. Pith–specific lignification in Nicotiana attenuata as a defense against a stem–boring herbivore

    Plants have developed tissue-specific defense strategies in response to various herbivores with different feeding habits. Although defense responses to leaf-chewing insects have been well studied, little is known about stem-specific responses, particularly in the pith, to stem-boring herbivores. To understand the stem-specific defense, we first conducted a comparative transcriptomic analysis of the wild tobacco Nicotiana attenuata before and after attack by the leaf-chewing herbivore Manduca sexta and the stem borer Trichobaris mucorea. When the stem-boring herbivore attacked, lignin-associated genes were upregulated specifically in the inner parenchymal cells of the stem, the pith; lignin also accumulated highly in the attacked pith.more » Silencing the lignin biosynthetic gene cinnamyl alcohol dehydrogenase enhanced the performance of the stem-boring herbivore but had no effect on the growth of the leaf-chewing herbivore. Two-dimensional nuclear magnetic resonance results revealed that lignified pith contains feruloyltyramine as an unusual lignin component in the cell wall, as a response against stem-boring herbivore attack. Pith-specific lignification induced by the stem-boring herbivore was modulated by both jasmonate and ethylene signaling. Furthermore, these results suggest that lignin provides a stem-specific inducible barrier, protecting plants against stem-boring insects.« less
  3. The Role of Chloroplast Membrane Lipid Metabolism in Plant Environmental Responses

    Plants are nonmotile life forms that are constantly exposed to changing environmental conditions during the course of their life cycle. Fluctuations in environmental conditions can be drastic during both day–night and seasonal cycles, as well as in the long term as the climate changes. Plants are naturally adapted to face these environmental challenges, and it has become increasingly apparent that membranes and their lipid composition are an important component of this adaptive response. Plants can remodel their membranes to change the abundance of different lipid classes, and they can release fatty acids that give rise to signaling compounds in responsemore » to environmental cues. Chloroplasts harbor the photosynthetic apparatus of plants embedded into one of the most extensive membrane systems found in nature. In part one of this review, we focus on changes in chloroplast membrane lipid class composition in response to environmental changes, and in part two, we will detail chloroplast lipid-derived signals.« less
  4. Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato

    As global climate change brings elevated average temperatures and more frequent and extreme weather events, pressure from biotic stresses will become increasingly compounded by harsh abiotic stress conditions. The plant hormone jasmonate (JA) promotes resilience to many environmental stresses, including attack by arthropod herbivores whose feeding activity is often stimulated by rising temperatures. How wound-induced JA signaling affects plant adaptive responses to elevated temperature (ET), however, remains largely unknown. In this study, we used the commercially important crop plantSolanum lycopersicum (cultivated tomato) to investigate the interaction between simulated heat waves and wound-inducible JA responses. We provide evidence that the heatmore » shock protein HSP90 enhances wound responses at ET by increasing the accumulation of the JA receptor, COI1. Wound-induced JA responses directly interfered with short-term adaptation to ET by blocking leaf hyponasty and evaporative cooling. Specifically, leaf damage inflicted by insect herbivory or mechanical wounding at ET resulted in COI1-dependent stomatal closure, leading to increased leaf temperature, lower photosynthetic carbon assimilation rate, and growth inhibition. Pharmacological inhibition of HSP90 reversed these effects to recapitulate the phenotype of a JA-insensitive mutant lacking the COI1 receptor. As climate change is predicted to compound biotic stress with larger and more voracious arthropod pest populations, our results suggest that antagonistic responses resulting from a combination of insect herbivory and moderate heat stress may exacerbate crop losses.« less
  5. An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

    The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. In this work, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography-tandem massmore » spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone-treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid-stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling play multifaceted roles in poplar L. bicolor ectomycorrhizal development.« less
  6. An important role of L–fucose biosynthesis and protein fucosylation genes in Arabidopsis immunity

    Plants mount coordinated immune responses to defend against pathogens. However, the cellular components required for plant immunity are not fully understood. The jasmonatemimicking coronatine (COR) toxin produced by Pseudomonas syringae pv. tomato (Pst) DC3000 functions to overcome plant immunity. We previously isolated eight Arabidopsis (scord) mutants that exhibit increased susceptibility to a COR-deficient mutant of Pst DC3000. Among them, the scord6 mutant exhibits defects both in stomatal closure response and in restricting bacterial multiplication inside the apoplast. However, the identity of SCORD6 remained elusive. In this study, we aim to identify the SCORD6 gene. Here, we identified SCORD6 via next-generationmore » sequencing and found it to be MURUS1 (MUR1), which is involved in the biosynthesis of GDP-L Discovery of SCORD6 as MUR1 led to a series of experiments that revealed a multifaceted role of -fucose. L-fucose biosynthesis in stomatal and apoplastic defenses as well as in pattern-triggered immunity and effector-triggered immunity, including glycosylation of pattern-recognition receptors. Furthermore, compromised stomatal and/or apoplastic defenses were observed in mutants of several fucosyltransferases with specific substrates (e.g., O-glycan, N-glycan or the DELLA transcriptional repressors). Collectively, these results uncover a novel and broad role of L-fucose and protein fucosylation in plant immuinity.« less
  7. JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis

    Plant immune responses mediated by the hormone jasmonoyl-L-isoleucine (JA-Ile) are metabolically costly and often linked to reduced growth. Although it is known that JA-Ile activates defense responses by triggering the degradation of JASMONATE ZIM DOMAIN (JAZ) transcriptional repressor proteins, expansion of the JAZ gene family in vascular plants has hampered efforts to understand how this hormone impacts growth and other physiological tasks over the course of ontogeny. Here, we combined mutations within the 13-member Arabidopsis JAZ gene family to investigate the effects of chronic JAZ deficiency on growth, defense, and reproductive output. A higher-order mutant (jaz decuple, jazD) defective inmore » 10 JAZ genes (JAZ1–7, -9, -10, and -13) exhibited robust resistance to insect herbivores and fungal pathogens, which was accompanied by slow vegetative growth and poor reproductive performance. Metabolic phenotypes of jazD discerned from global transcript and protein profiling were indicative of elevated carbon partitioning to amino acid-, protein-, and endoplasmic reticulum body-based defenses controlled by the JA-Ile and ethylene branches of immunity. Resource allocation to a strong defense sink in jazD leaves was associated with increased respiration and hallmarks of carbon starvation but no overt changes in photosynthetic rate. Depletion of the remaining JAZ repressors in jazD further exaggerated growth stunting, nearly abolished seed production and, under extreme conditions, caused spreading necrotic lesions and tissue death. Our results demonstrate that JAZ proteins promote growth and reproductive success at least in part by preventing catastrophic metabolic effects of an unrestrained immune response.« less
  8. Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor

    Significance Pathogen infections can cause significant crop losses worldwide and major disturbances in natural ecosystems. Understanding the molecular basis of plant disease susceptibility is important for the development of new strategies to prevent disease outbreaks. Recent studies have identified the plant jasmonate (JA) hormone receptor as one of the common targets of pathogen virulence factors. In this study, we modified the JA receptor and showed that transgenic Arabidopsis plants with the modified JA receptor gained resistance to bacterial pathogens that secrete a potent JA-mimicking toxin to promote infection. Our results suggest that host target modification may be developed as amore » new strategy to protect the disease-vulnerable components of the susceptible plant against highly evolved pathogens.« less
  9. Plant chemical biology: are we meeting the promise?

    As an early adopter of plant chemical genetics to the study of endomembrane trafficking, we have observed the growth of small molecule approaches. Within the field, we often describe the strengths of the approach in a broad, generic manner, such as the ability to address redundancy and lethality. But, we are now in a much better position to evaluate the demonstrated value of the approach based on examples. In this perspective, we offer an assessment of chemical genetics in plants and where its applications may be of particular utility from the perspective of the cell biologist. Beyond this, we suggestmore » areas to be addressed to provide broader access and enhance the effectiveness of small molecule approaches in plant biology.« less
  10. Social Network: JAZ Protein Interactions Expand Our Knowledge of Jasmonate Signaling

    Members of the family of JASMONATE ZIM-DOMAIN (JAZ) proteins are key regulators of the jasmonate (JA) hormonal response. The 12-member family is characterized by three conserved domains, an N-terminal domain, a TIFY-containing ZINC-FINGER EXPRESSED IN INFLORESCENCE MERISTEM domain, and a C-terminal Jas domain. JAZ proteins regulate JA-responsive gene transcription by inhibiting DNA-binding transcription factors in the absence of JA. JAZ proteins interact in a hormone-dependent manner with CORONATINE INSENSITIVE 1 (COI1), the recognition component of the E3 ubiquitin ligase, SCFCOI1, resulting in the ubiquitination and subsequent degradation of JAZs via the 26S proteasome pathway. Since their discovery in 2007, JAZmore » proteins have been implicated in protein–protein interactions with multiple transcription factors. These studies have shed light on the mechanism by which JAZs repress transcription, are targeted for degradation, modulate the JA signaling response, and participate in crosstalk with other hormone signaling pathways. In this review, we will take a close look at the recent discoveries made possible by the characterization JAZ protein–protein interactions.« less
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