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Using the Cap Analysis of Gene Expression (CAGE) technology, the FANTOM5 consortium provided one of the most comprehensive maps of transcription start sites (TSSs) in several species. Strikingly, ~72% of them could not be assigned to a specific gene and initiate at unconventional regions, outside promoters or enhancers. Here, we probe these unassigned TSSs and show that, in all species studied, a significant fraction of CAGE peaks initiate at microsatellites, also called short tandem repeats (STRs). To confirm this transcription, we develop Cap Trap RNA-seq, a technology which combines cap trapping and long read MinION sequencing. We train sequence-based deepmore » learning models able to predict CAGE signal at STRs with high accuracy. These models unveil the importance of STR surrounding sequences not only to distinguish STR classes, but also to predict the level of transcription initiation. Importantly, genetic variants linked to human diseases are preferentially found at STRs with high transcription initiation level, supporting the biological and clinical relevance of transcription initiation at STRs. Together, our results extend the repertoire of non-coding transcription associated with DNA tandem repeats and complexify STR polymorphism.« less

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

Plants constantly experience attack from surrounding organisms. Because they cannot escape from the environment, plants have evolved a sophisticated immune system to defend themselves against pests and pathogens. However, mounting a defense response is often accompanied by a decrease in growth. The antagonistic relationship between growth and defense has been interpreted as the plant's “dilemma” of how to distribute limited resources between these two fundamental processes. Jasmonic acid (JA) and its derivatives are a class of lipid‐derived hormones that mediate plant immunity against insect herbivores and necrotrophic pathogens, as well as growth, reproduction, and several other physiological processes. JA ismore » perceived by its receptor CORONATINE INSENSITIVE 1 (COI1), which mediates the degradation of the JASMONATE ZIM DOMAIN (JAZ) transcriptional repressors by the 26S proteasome. JAZ degradation releases JA‐responsive transcription factors such as MYC2 from repression, thereby initiating JA responses. Despite the importance of JA in mediating growth‐defense tradeoffs, the mechanism by which JA effects carbon resource allocation between growth and defense is poorly understood. In this study we demonstrate strong constitutive activation of JA signaling pathway in an Arabidopsis mutant ( jazD ) that lacks ten members of JASMONATE ZIM DOMAIN (JAZ) family proteins. This mutant displayed elevated defense against insect herbivores, stunted growth of vegetative tissues, as well as compromised seed reproduction. Metabolic phenotypes of jazD discerned from global protein and transcript profiling were indicative of elevated carbon allocation to protein‐ and amino acid‐based defense compounds. The strong defense sink in jazD leaves was linked to increased respiration and hallmarks of carbon starvation, whereas area‐based photosynthetic efficiency was unaffected. These findings establish a role for JAZ proteins in promoting growth and reproductive success through restraint of transcriptional programs that link primary metabolism to specialized metabolism. Our data suggest that JAZs adjust growth‐defense balance to match anticipated changes in carbon availability, potentially avoiding detrimental effects of carbon limitation that arise during growth‐to‐defense transitions. Support or Funding Information This research was funded by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy through grant DE–FG02–91ER20021. This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal .« less

The plant hormone jasmonate (JA) promotes the degradation of JASMONATE ZIM-DOMAIN (JAZ) proteins to relieve repression on diverse transcription factors (TFs) that execute JA responses. However, little is known about how combinatorial complexity among JAZ–TF interactions maintains control over myriad aspects of growth, development, reproduction, and immunity. We used loss-of-function mutations to define epistatic interactions within the core JA signaling pathway and to investigate the contribution of MYC TFs to JA responses in Arabidopsis thaliana. Constitutive JA signaling in a jaz quintuple mutant (jazQ) was largely eliminated by mutations that block JA synthesis or perception. Comparison of jazQ and amore » jazQ myc2 myc3 myc4 octuple mutant validated known functions of MYC2/3/4 in root growth, chlorophyll degradation,and susceptibility to the pathogen Pseudomonas syringae. We found that MYC TFs also control both the enhanced resistance of jazQ leaves to insect herbivory and restricted leaf growth of jazQ. Epistatic transcriptional profiles mirrored these phenotypes and further showed that triterpenoid biosynthetic and glucosinolate catabolic genes are up-regulated in jazQ independently of MYC TFs. Lastly, our study highlights the utility of genetic epistasis to unravel the complexities of JAZ–TF interactions and demonstrates that MYC TFs exert master control over a JAZ-repressible transcriptional hierarchy that governs growth–defense balance.« less

Plants resist infection and herbivory with innate immune responses that are often associated with reduced growth. Despite the importance of growth-defense tradeoffs in shaping plant productivity in natural and agricultural ecosystems, the molecular mechanisms that link growth and immunity are poorly understood. Here, we demonstrate that growth-defense tradeoffs mediated by the hormone jasmonate are uncoupled in an Arabidopsis mutant (jazQ phyB) lacking a quintet of Jasmonate ZIM-domain transcriptional repressors and the photoreceptor phyB. Analysis of epistatic interactions between jazQ and phyB reveal that growth inhibition associated with enhanced anti-insect resistance is likely not caused by diversion of photoassimilates from growthmore » to defense but rather by a conserved transcriptional network that is hardwired to attenuate growth upon activation of jasmonate signalling. Furthermore, the ability to unlock growth-defense tradeoffs through relief of transcription repression provides an approach to assemble functional plant traits in new and potentially useful ways.« less

Summary JAsmonate ZIM‐domain (JAZ) proteins repress the activity of transcription factors that execute responses to the plant hormone jasmonoyl‐L‐isoleucine (JA‐Ile). The ZIM protein domain recruits the co‐repressors NINJA and TOPLESS to JAZ‐bound transcription factors, and contains a highly conserved TIF[F/Y]XG motif that defines the larger family of TIFY proteins to which JAZs belong. Here, we report that diverse plant species contain genes encoding putative non‐TIFY JAZ proteins, including a previously unrecognized JAZ repressor in Arabidopsis (JAZ13, encoded by At3g22275). JAZ13 is most closely related to JAZ8 and includes divergent EAR, TIFY/ZIM, and Jas motifs. Unlike JAZ8, however, JAZ13 contains amore » Ser‐rich C‐terminal tail that is a site for phosphorylation. Overexpression of JAZ13 resulted in reduced sensitivity to JA, attenuation of wound‐induced expression of JA‐response genes, and decreased resistance to insect herbivory. JAZ13 interacts with the bHLH transcription factor MYC2 and the co‐repressor TOPLESS but, consistent with the absence of a TIFY motif, neither NINJA nor other JAZs. Analysis of single and higher‐order T‐DNA insertion jaz null mutants provided further evidence that JAZ13 is a repressor JA signaling. Our results demonstrate that proteins outside the TIFY family are functional JAZ repressors and further suggest that this expansion of the JAZ family allows fine‐tuning of JA‐mediated transcriptional responses.« less