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The titan arum (Amorphophallus titanum), commonly known as the corpse flower, produces the largest unbranched inflorescence in the world. Its rare blooms last only a few days and are notable both for their burst of thermogenic activity and for the odor of rotting flesh by which they attract pollinators. Studies on the titan arum can therefor lend insight into the mechanisms underlying thermogenesis as well as the production of sulfur-based volatiles, about which little is known in plants. Here, we made use of transcriptome and metabolite analyses to uncover underlying mechanisms that enable thermogenesis and volatile production in the titan arum. The ability to perform thermogenesis correlated with the expression of genes involved in bypass steps for the mitochondrial electron transport chain, in particular alternative oxidase expression, and through our analysis is placed within the context of sugar transport and metabolism. The major odorants produced by the titan arum are dimethyl disulfide and dimethyl trisulfide, and we identified pathways for sulfur transport and metabolism that culminate in the production of methionine, which our analysis identifies as the amino acid substrate for production of these odorants. Putrescine, derived from arginine, was identified as an additional and previously unrecognized component of the titan arum's odor. Levels of free methionine and putrescine were rapidly depleted during thermogenesis, consistent with roles in production of the titan arum's odor. Models for how tissues of the titan arum contribute to thermogenesis and volatile production are proposed. 

Abstract PremiseThe origin of diversity is a fundamental biological question. Gene duplications are one mechanism that provides raw material for the emergence of novel traits, but evolutionary outcomes depend on which genes are retained and how they become functionalized. Yet, following different duplication types (polyploidy and tandem duplication), the events driving gene retention and functionalization remain poorly understood. Here we usedCakile maritima, a species that is tolerant to salt and heavy metals and shares an ancient whole‐genome triplication with closely related salt‐sensitive mustard crops (Brassica), as a model to explore the evolution of abiotic stress tolerance following polyploidy. MethodsUsing a combination of ionomics, free amino acid profiling, and comparative genomics, we characterize aspects of salt stress response inC. maritimaand identify retained duplicate genes that have likely enabled adaptation to salt and mild levels of cadmium. ResultsCakile maritimais tolerant to both cadmium and salt treatments through uptake of cadmium in the roots. Proline constitutes greater than 30% of the free amino acid pool inC. maritimaand likely contributes to abiotic stress tolerance. We find duplicated gene families are enriched in metabolic and transport processes and identify key transport genes that may be involved inC. maritimaabiotic stress tolerance. ConclusionsThese findings identify pathways and genes that could be used to enhance plant resilience and provide a putative understanding of the roles of duplication types and retention on the evolution of abiotic stress response. 

Plants produce phylogenetically and spatially restricted, as well as structurally diverse specialized metabolites via multistep metabolic pathways. Hallmarks of specialized metabolic evolution include enzymatic promiscuity and recruitment of primary metabolic enzymes and examples of genomic clustering of pathway genes. Solanaceae glandular trichomes produce defensive acylsugars, with sidechains that vary in length across the family. We describe a tomato gene cluster on chromosome 7 involved in medium chain acylsugar accumulation due to trichome specific acyl-CoA synthetase and enoyl-CoA hydratase genes. This cluster co-localizes with a tomato steroidal alkaloid gene cluster and is syntenic to a chromosome 12 region containing another acylsugar pathway gene. We reconstructed the evolutionary events leading to this gene cluster and found that its phylogenetic distribution correlates with medium chain acylsugar accumulation across the Solanaceae. This work reveals insights into the dynamics behind gene cluster evolution and cell-type specific metabolite diversity. 

The target of rapamycin (TOR) kinase is an evolutionarily conserved hub of nutrient sensing and metabolic signaling. In plants, a functional connection of TOR activation with glucose availability was demonstrated, while it is yet unclear whether branched-chain amino acids (BCAAs) are a primary input of TOR signaling as they are in yeast and mammalian cells. Here, we report on the characterization of an Arabidopsis mutant over-accumulating BCAAs. Through chemical interventions targeting TOR and by examining mutants of BCAA biosynthesis and TOR signaling, we found that BCAA over-accumulation leads to up-regulation of TOR activity, which causes reorganization of the actin cytoskeleton and actin-associated endomembranes. Finally, we show that activation of TOR is concomitant with alteration of cell expansion, proliferation and specialized metabolism, leading to pleiotropic effects on plant growth and development. These results demonstrate that BCAAs contribute to plant TOR activation and reveal previously uncharted downstream subcellular processes of TOR signaling. 

Abstract Plant specialized metabolites mediate interactions between plants and the environment and have significant agronomical/pharmaceutical value. Most genes involved in specialized metabolism (SM) are unknown because of the large number of metabolites and the challenge in differentiating SM genes from general metabolism (GM) genes. Plant models like Arabidopsis thaliana have extensive, experimentally derived annotations, whereas many non-model species do not. Here we employed a machine learning strategy, transfer learning, where knowledge from A. thaliana is transferred to predict gene functions in cultivated tomato with fewer experimentally annotated genes. The first tomato SM/GM prediction model using only tomato data performs well (F-measure = 0.74, compared with 0.5 for random and 1.0 for perfect predictions), but from manually curating 88 SM/GM genes, we found many mis-predicted entries were likely mis-annotated. When the SM/GM prediction models built with A. thaliana data were used to filter out genes where the A. thaliana-based model predictions disagreed with tomato annotations, the new tomato model trained with filtered data improved significantly (F-measure = 0.92). Our study demonstrates that SM/GM genes can be better predicted by leveraging cross-species information. Additionally, our findings provide an example for transfer learning in genomics where knowledge can be transferred from an information-rich species to an information-poor one. 

Specialized metabolites are structurally diverse and cell‐ or tissue‐specific molecules produced in restricted plant lineages. In contrast, primary metabolic pathways are highly conserved in plants and produce metabolites essential for all of life, such as amino acids and nucleotides. Substrate promiscuity – the capacity to accept non‐native substrates – is a common characteristic of enzymes, and its impact is especially apparent in generating specialized metabolite variation. However, promiscuity only leads to metabolic diversity when alternative substrates are available; thus, enzyme cellular and subcellular localization directly influence chemical phenotypes. We review a variety of mechanisms that modulate substrate availability for promiscuous plant enzymes. We focus on examples where evolution led to modification of the ‘cellular context’ through changes in cell‐type expression, subcellular relocalization, pathway sequestration, and cellular mixing via tissue damage. These varied mechanisms contributed to the emergence of structurally diverse plant specialized metabolites and inform future metabolic engineering approaches. 

Plant specialized metabolism (SM) enzymes produce lineage-specific metabolites with important ecological, evolutionary, and biotechnological implications. UsingArabidopsis thalianaas a model, we identified distinguishing characteristics of SM and GM (general metabolism, traditionally referred to as primary metabolism) genes through a detailed study of features including duplication pattern, sequence conservation, transcription, protein domain content, and gene network properties. Analysis of multiple sets of benchmark genes revealed that SM genes tend to be tandemly duplicated, coexpressed with their paralogs, narrowly expressed at lower levels, less conserved, and less well connected in gene networks relative to GM genes. Although the values of each of these features significantly differed between SM and GM genes, any single feature was ineffective at predicting SM from GM genes. Using machine learning methods to integrate all features, a prediction model was established with a true positive rate of 87% and a true negative rate of 71%. In addition, 86% of known SM genes not used to create the machine learning model were predicted. We also demonstrated that the model could be further improved when we distinguished between SM, GM, and junction genes responsible for reactions shared by SM and GM pathways, indicating that topological considerations may further improve the SM prediction model. Application of the prediction model led to the identification of 1,220A. thalianagenes with previously unknown functions, each assigned a confidence measure called an SM score, providing a global estimate of SM gene content in a plant genome. 

Abstract l‐Tyrosine (Tyr) is an aromatic amino acid synthesized de novo in plants and microbes downstream of the shikimate pathway. In plants, Tyr and a Tyr pathway intermediate, 4‐hydroxyphenylpyruvate (HPP), are precursors to numerous specialized metabolites, which are crucial for plant and human health. Tyr is synthesized in the plastids by a TyrA family enzyme, arogenate dehydrogenase (ADH/TyrA_a), which is feedback inhibited by Tyr. Additionally, many legumes possess prephenate dehydrogenases (PDH/TyrA_p), which are insensitive to Tyr and localized to the cytosol. Yet the role of PDH enzymes in legumes is currently unknown. This study isolated and characterizedTnt1‐transposon mutants ofMtPDH1(pdh1) inMedicago truncatulato investigate PDH function. The pdh1mutants lackedPDHtranscript and PDH activity, and displayed little aberrant morphological phenotypes under standard growth conditions, providing genetic evidence thatMtPDH1is responsible for the PDH activity detected inM. truncatula. Though plant PDH enzymes and activity have been specifically found in legumes, nodule number and nitrogenase activity ofpdh1 mutants were not significantly reduced compared with wild‐type (Wt) during symbiosis with nitrogen‐fixing bacteria. Although Tyr levels were not significantly different between Wt and mutants under standard conditions, when carbon flux was increased by shikimate precursor feeding, mutants accumulated significantly less Tyr than Wt. These data suggest that MtPDH1 is involved in Tyr biosynthesis when the shikimate pathway is stimulated and possibly linked to unidentified legume‐specific specialized metabolism.