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1. Cell‐type‐aware regulatory landscapes governing monoterpene indole alkaloid biosynthesis in the medicinal plant Catharanthus roseus

   https://doi.org/10.1111/nph.20208  

   Li, Chenxin; Colinas, Maite; Wood, Joshua_C; Vaillancourt, Brieanne; Hamilton, John_P; Jones, Sophia_L; Caputi, Lorenzo; O'Connor, Sarah_E; Buell, C_Robin (October 2024, New Phytologist)

   Summary In plants, the biosynthetic pathways of some specialized metabolites are partitioned into specialized or rare cell types, as exemplified by the monoterpenoid indole alkaloid (MIA) pathway ofCatharanthus roseus(Madagascar Periwinkle), the source of the anticancer compounds vinblastine and vincristine. In the leaf, theC. roseusMIA biosynthetic pathway is partitioned into three cell types with the final known steps of the pathway expressed in the rare cell type termed idioblast. How cell‐type specificity of MIA biosynthesis is achieved is poorly understood.We generated single‐cell multi‐omics data fromC. roseusleaves. Integrating gene expression and chromatin accessibility profiles across single cells, as well as transcription factor (TF)‐binding site profiles, we constructed a cell‐type‐aware gene regulatory network for MIA biosynthesis.We showcased cell‐type‐specific TFs as well as cell‐type‐specificcis‐regulatory elements. Using motif enrichment analysis, co‐expression across cell types, and functional validation approaches, we discovered a novel idioblast‐specific TF (Idioblast MYB1,CrIDM1) that activates expression of late‐stage MIA biosynthetic genes in the idioblast.These analyses not only led to the discovery of the first documented cell‐type‐specific TF that regulates the expression of two idioblast‐specific biosynthetic genes within an idioblast metabolic regulon but also provides insights into cell‐type‐specific metabolic regulation. 

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2. Long‐term nitrogen isotope dynamics in Encelia farinosa reflect plant demographics and climate

   https://doi.org/10.1111/nph.17668  

   Driscoll, Avery W.; Kannenberg, Steven A.; Ehleringer, James R. (August 2021, New Phytologist)

   Summary While plant δ¹⁵N values have been applied to understand nitrogen (N) dynamics, uncertainties regarding intraspecific and temporal variability currently limit their application. We used a 28 yr record of δ¹⁵N values from two Mojave Desert populations ofEncelia farinosato clarify sources of population‐level variability.We leveraged > 3500 foliar δ¹⁵N observations collected alongside structural, physiological, and climatic data to identify plant and environmental contributors to δ¹⁵N values. Additional sampling of soils, roots, stems, and leaves enabled assessment of the distribution of soil N content and δ¹⁵N, intra‐plant fractionations, and relationships between soil and plant δ¹⁵N values.We observed extensive within‐population variability in foliar δ¹⁵N values and found plant age and foliar %N to be the strongest predictors of individual δ¹⁵N values. There were consistent differences between root, stem, and leaf δ¹⁵N values (spanningc. 3‰), but plant and bulk soil δ¹⁵N values were unrelated.Plant‐level variables played a strong role in influencing foliar δ¹⁵N values, and interannual relationships between climate and δ¹⁵N values were counter to previously recognized spatial patterns. This long‐term record provides insights regarding the interpretation of δ¹⁵N values that were not available from previous large‐scale syntheses, broadly enabling more effective application of foliar δ¹⁵N values. 

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3. Metabolomics-guided discovery of cytochrome P450s involved in pseudotropine-dependent biosynthesis of modified tropane alkaloids

   https://doi.org/10.1038/s41467-022-31653-1  

   Sadre, Radin; Anthony, Thilani M.; Grabar, Josh M.; Bedewitz, Matthew A.; Jones, A. Daniel; Barry, Cornelius S. (July 2022, Nature Communications)

   Abstract Plant alkaloids constitute an important class of bioactive chemicals with applications in medicine and agriculture. However, the knowledge gap of the diversity and biosynthesis of phytoalkaloids prevents systematic advances in biotechnology for engineered production of these high-value compounds. In particular, the identification of cytochrome P450s driving the structural diversity of phytoalkaloids has remained challenging. Here, we use a combination of reverse genetics with discovery metabolomics and multivariate statistical analysis followed byin plantatransient assays to investigate alkaloid diversity and functionally characterize two candidate cytochrome P450s genes fromAtropa belladonnawithout a priori knowledge of their functions or information regarding the identities of key pathway intermediates. This approach uncovered a largely unexplored root localized alkaloid sub-network that relies on pseudotropine as precursor. The two cytochrome P450s catalyzeN-demethylation and ring-hydroxylation reactions within the early steps in the biosynthesis of diverseN-demethylated modified tropane alkaloids. 

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4. Soil microenvironmental variation drives below‐ground trait variation and interacts with macroclimate to structure above‐ground trait variation of arctic shrubs

   https://doi.org/10.1111/1365-2745.14278  

   Fraterrigo, Jennifer M; Chen, Weile; Loyal, Joshua; Euskirchen, Eugénie S (April 2024, Journal of Ecology)

   Henn, J (Ed.)

   Abstract Intraspecific trait variation can influence plant performance in different environments and may thereby determine the ability of individual plants to respond to climate change. However, our understanding of its patterns and environmental drivers across different spatial scales is incomplete, especially in understudied regions like the Arctic.To fill this knowledge gap, we examined above‐ground and below‐ground traits from three shrub taxa expanding across the tundra biome and evaluated their relationships with multiple microenvironmental and macroclimatic factors. The traits reflected plant size and structure (plant height, leaf area and root to shoot ratio), leaf economics (specific leaf area, nitrogen content), and root economics and collaboration with mycorrhizal fungi (specific root length, root tissue density, nitrogen content, and ectomycorrhizal colonisation intensity). We also measured leaf and root δ¹⁵N and leaf δ¹³C to characterise nitrogen source and acquisition pathways and plant water stress. Traits were measured in replicated plots (N = 135) varying in soil microclimate, thaw depth and organic layer thickness established across five sites spanning a macroclimate gradient in northern Alaska. This hierarchical design allowed us to disentangle the independent and combined effects of fine‐scale and broad‐scale factors on intraspecific trait variation.We found substantial intraspecific variation at fine spatial scales for most traits and less variation along the macroclimate gradient and between shrub taxa. Consistent with these patterns, microenvironmental factors, mainly soil moisture and thaw depth, interacted with macroclimate, mainly climatic water deficit, to structure size‐structural and leaf trait variation. In contrast, most root traits responded additively to thaw depth and macroclimate.Synthesis. Our results demonstrate that above‐ground and below‐ground tundra shrub traits respond differently to microenvironmental and macroclimatic variation. These differing responses contribute to substantial trait variation at fine spatial scales and may decouple above‐ground and below‐ground trait responses to climate change. 

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5. Integrated metabolic strategy: A framework for predicting the evolution of carbon‐water tradeoffs within plant clades

   https://doi.org/10.1111/1365-2745.13204  

   Goud, Ellie M.; Sparks, Jed P.; Fishbein, Mark; Agrawal, Anurag A.; Shefferson, ed., Richard (May 2019, Journal of Ecology)

   Abstract The fundamental tradeoff between carbon gain and water loss has long been predicted as an evolutionary driver of plant strategies across environments. Nonetheless, challenges in measuring carbon gain and water loss in ways that integrate over leaf lifetime have limited our understanding of the variation in and mechanistic bases of this tradeoff. Furthermore, the microevolution of plant traits within species versus the macroevolution of strategies among closely related species may not be the same, and accordingly, the latter must be addressed using comparative phylogenetic analyses.Here we introduce the concept of ‘integrated metabolic strategy’ (IMS) to describe the ratio between carbon isotope composition (δ¹³C) and oxygen isotope composition above source water (Δ¹⁸O) of leaf cellulose. IMS is a measure of leaf‐level conditions that integrate several mechanisms contributing to carbon gain (δ¹³C) and water loss (Δ¹⁸O) over leaf lifespan, with larger values reflecting higher metabolic efficiency and hence less of a tradeoff. We tested how IMS evolves among closely related yet ecologically diverse milkweed species, and subsequently addressed phenotypic plasticity in response to water availability in species with divergent IMS.Integrated metabolic strategy varied strongly among 20Asclepiasspecies when grown under controlled conditions, and phylogenetic analyses demonstrate species‐specific tradeoffs between carbon gain and water loss. Larger IMS values were associated with species from dry habitats, with larger carboxylation capacity, smaller stomatal conductance and smaller leaves; smaller IMS was associated with wet habitats, smaller carboxylation capacity, larger stomatal conductance and larger leaves. The evolution of IMS was dominated by changes in species’ demand for carbon (δ¹³C) more so than water conservation (Δ¹⁸O). Although some individual physiological traits showed phylogenetic signal, IMS did not.In response to experimental decreases in soil moisture, three species maintained similar IMS across levels of water availability because of proportional increases inδ¹³C and Δ¹⁸O (or little change in either), while one species increased IMS due to disproportional changes inδ¹³C relative to Δ¹⁸O.Synthesis.IMS is a broadly applicable mechanistic tool; IMS variation among and within species may shed light on unresolved questions relating to the evolution and ecology of plant ecophysiological strategies. 

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