skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Cuticle development and the underlying transcriptome–metabolome associations during early seedling establishment
Abstract The plant cuticle is a complex extracellular lipid barrier that has multiple protective functions. This study investigated cuticle deposition by integrating metabolomics and transcriptomics data gathered from six different maize seedling organs of four genotypes, the inbred lines B73 and Mo17, and their reciprocal hybrids. These datasets captured the developmental transition of the seedling from heterotrophic skotomorphogenic growth to autotrophic photomorphogenic growth, a transition that is highly vulnerable to environmental stresses. Statistical interrogation of these data revealed that the predominant determinant of cuticle composition is seedling organ type, whereas the seedling genotype has a smaller effect on this phenotype. Gene-to-metabolite associations assessed by integrated statistical analyses identified three gene networks associated with the deposition of different elements of the cuticle: cuticular waxes; monomers of lipidized cell wall biopolymers, including cutin and suberin; and both of these elements. These gene networks reveal three metabolic programs that appear to support cuticle deposition, including processes of chloroplast biogenesis, lipid metabolism, and molecular regulation (e.g. transcription factors, post-translational regulators, and phytohormones). This study demonstrates the wider physiological metabolic context that can determine cuticle deposition and lays the groundwork for new targets for modulating the properties of this protective barrier.  more » « less
Award ID(s):
2238942 2212799
PAR ID:
10555412
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Editor(s):
Nakamura, Yuki
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Journal of Experimental Botany
Volume:
75
Issue:
20
ISSN:
0022-0957
Page Range / eLocation ID:
6500 to 6522
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary Isogenic individuals can display seemingly stochastic phenotypic differences, limiting the accuracy of genotype‐to‐phenotype predictions. The extent of this phenotypic variation depends in part on genetic background, raising questions about the genes involved in controlling stochastic phenotypic variation.Focusing on early seedling traits inArabidopsis thaliana, we found that hypomorphs of the cuticle‐related geneLIPID TRANSFER PROTEIN 2(LTP2) greatly increased variation in seedling phenotypes, including hypocotyl length, gravitropism and cuticle permeability. Manyltp2hypocotyls were significantly shorter than wild‐type hypocotyls while others resembled the wild‐type.Differences in epidermal properties and gene expression betweenltp2seedlings with long and short hypocotyls suggest a loss of cuticle integrity as the primary determinant of the observed phenotypic variation. We identified environmental conditions that reveal or mask the increased variation inltp2hypomorphs and found that increased expression of its closest paralogLTP1is necessary forltp2phenotypes.Our results illustrate how decreased expression of a single gene can generate starkly increased phenotypic variation in isogenic individuals in response to an environmental challenge. 
    more » « less
  2. Abstract Global warming has been shifting climatic envelopes of many tree species to higher latitudes and elevations across the globe; however, unsuitable soil biota may inhibit tree migrations into these areas of suitable climate. Specifically, the role of mycorrhizal fungi in facilitating tree seedling establishment beyond natural species range limits has not been fully explored within forest ecosystems. We used three experiments to isolate and quantify the effects of mycorrhizal colonization and common mycorrhizal networks (CMN) on tree seedling survival and growth across (within and beyond) the elevational ranges of two dominant tree species in northeastern North America, which were associated with either arbuscular mycorrhiza (AMF,Acer saccharum) or ectomycorrhiza (EMF,Fagus grandifolia). In order to quantify the influence of mycorrhiza on seedling establishment independent of soil chemistry and climate, we grew seedlings in soils from within and beyond our study species ranges in a greenhouse experiment (GE) as well as in the field using a soil translocation experiment (STE) and another field experiment manipulating seedling connections to potential CMNs (CMNE). Root length colonized, seedling survival and growth, foliar nutrients, and the presence of potential root pathogens were examined as metrics influencing plant performance across species' ranges. Mycorrhizal inoculum from within species ranges, but not from outside, increased seedling survival and growth in a greenhouse setting; however, only seedling survival, and not growth, was significantly improved in field studies. Sustained potential connectivity to AMF networks increased seedling survival across the entire elevational range ofA. saccharum. Although seedlings disconnected from a potential CMN did not suffer decreased foliar nutrient levels compared with connected seedlings, disconnected AM seedlings, but not EM seedlings, had significantly higher aluminum concentrations and more potential pathogens present. Our results indicate that mycorrhizal fungi may facilitate tree seedling establishment beyond species range boundaries in this forested ecosystem and that the magnitude of this effect is modulated by the dominant mycorrhizal type present (i.e., AM vs. EM). Thus, despite changing climate conditions beyond species ranges, a lack of suitable mutualists can still limit successful seedling establishment and stall adaptive climate‐induced shifts in tree species distributions. 
    more » « less
  3. Abstract The fungusMagnaporthe oryzaecauses blast, the most devastating disease of cultivated rice. After penetrating the leaf cuticle,M. oryzaegrows as a biotroph in intimate contact with living rice epidermal cells before necrotic lesions develop. Biotrophic growth requires maintaining metabolic homeostasis while suppressing plant defenses, but the metabolic connections and requirements involved are largely unknown. Here, we characterized theM. oryzaenucleoside diphosphate kinase‐encoding geneNDK1and discovered it was essential for facilitating biotrophic growth by suppressing the host oxidative burst—the first line of plant defense. NDK enzymes reversibly transfer phosphate groups from tri‐ to diphosphate nucleosides. Correspondingly, intracellular nucleotide pools were perturbed inM. oryzaestrains lackingNDK1through targeted gene deletion, compared to WT. This affected metabolic homeostasis: TCA, purine and pyrimidine intermediates, and oxidized NADP+, accumulated in Δndk1. cAMP and glutathione were depleted. ROS accumulated in Δndk1hyphae. Functional appressoria developed on rice leaf sheath surfaces, but Δndk1invasive hyphal growth was restricted and redox homeostasis was perturbed, resulting in unsuppressed host oxidative bursts that triggered immunity. We conclude Ndk1 modulates intracellular nucleotide pools to maintain redox balance via metabolic homeostasis, thus quenching the host oxidative burst and suppressing rice innate immunity during biotrophy. 
    more » « less
  4. null (Ed.)
    Changes in cis-regulatory elements play important roles in adaptation and phenotypic evolution. However, their contribution to metabolic adaptation of organisms is less understood. Here we have utilized a unique vertebrate model, Astyanax mexicanus, different morphotypes of which survive in nutrient-rich surface and nutrient-deprived cave water to uncover gene regulatory networks in metabolic adaptation. We performed genome-wide epigenetic profiling in the liver tissue of one surface and two independently derived cave populations. We find that many cis-regulatory elements differ in their epigenetic status/chromatin accessibility between surface fish and cavefish, while the two independently derived cave populations have evolved remarkably similar regulatory signatures. These differentially accessible regions are associated with genes of key pathways related to lipid metabolism, circadian rhythm and immune system that are known to be altered in cavefish. Using in vitro and in vivo functional testing of the candidate cis-regulatory elements, we find that genetic changes within them cause quantitative expression differences. We characterized one cis-regulatory element in the hpdb gene and found a genomic deletion in cavefish that abolishes binding of the transcriptional repressor IRF2 in vitro and derepresses enhancer activity in reporter assays. Genetic experiments further validated a cis-mediated role of the enhancer and suggest a role of this deletion in the upregulation of hpdb in wild cavefish populations. Selection of this mutation in multiple independent cave populations supports its importance in the adaptation to the cave environment, providing novel molecular insights into the evolutionary trade-off between loss of pigmentation and adaptation to a food-deprived cave environment. 
    more » « less
  5. Gambino, Michela (Ed.)
    ABSTRACT Bacterial growth substrates influence a variety of biological functions, including the biosynthesis and regulation of lipid intermediates. The extent of this rewiring is not well understood nor has it been considered in the context of virally infected cells. Here, we used a one-host-two-temperate phage model system to probe the combined influence of growth substrate and phage infection on host carbon and lipid metabolism. Using untargeted metabolomics and lipidomics, we reported the detection of a suite of metabolites and lipid classes for two Sulfitobacter lysogens provided with three growth substrates of differing complexity and nutrient composition (yeast extract/tryptone [complex], glutamate and acetate). The growth medium led to dramatic differences in the detectable intracellular metabolites, with only 15% of 175 measured metabolites showing overlap across the three growth substrates. Between-strain differences were most evident in the cultures grown on acetate, followed by glutamate then complex medium. Lipid distribution profiles were also distinct between cultures grown on different substrates as well as between the two lysogens grown in the same medium. Five phospholipids, three aminolipid, and one class of unknown lipid-like features were identified. Most (≥94%) of these 75 lipids were quantifiable in all samples. Metabolite and lipid profiles were strongly determined by growth medium composition and modestly by strain type. Because fluctuations in availability and form of carbon substrates and nutrients, as well as virus pressure, are common features of natural systems, the influence of these intersecting factors will undoubtedly be imprinted in the metabolome and lipidome of resident bacteria. IMPORTANCE Community-level metabolomics approaches are increasingly used to characterize natural microbial populations. These approaches typically depend upon temporal snapshots from which the status and function of communities are often inferred. Such inferences are typically drawn from lab-based studies of select model organisms raised under limited growth conditions. To better interpret community-level data, the extent to which ecologically relevant bacteria demonstrate metabolic flexibility requires elucidation. Herein, we used an environmentally relevant model heterotrophic marine bacterium to assess the relationship between growth determinants and metabolome. We also aimed to assess the contribution of phage activity to the host metabolome. Striking differences in primary metabolite and lipid profiles appeared to be driven primarily by growth regime and, secondarily, by phage type. These findings demonstrated the malleable nature of metabolomes and lipidomes and lay the foundation for future studies that relate cellular composition with function in complex environmental microbial communities. 
    more » « less