Flavonoids are polyphenolic small molecules that are abundant in plant products and are largely recognized for their beneficial health effects. Possessing both antioxidant and prooxidant properties, flavonoids have complex behavior in biological systems. The presented work investigates the intersection between the biological activity of flavonoids and their interactions with copper ions. Copper is required for the proper functioning of biological systems. As such, dysregulation of copper is associated with metabolic disease states such as diabetes and Wilson’s disease. There is evidence that flavonoids bind copper ions, but the biological implications of their interactions remain unclear. Better understanding these interactions will provide insight into the mechanisms of flavonoids’ biological behavior and can inform potential therapeutic targets. We employed a variety of spectroscopic techniques to study flavonoid-Cu(II) binding and radical scavenging activities. We identified structural moieties important in flavonoid-copper interactions which relate to ring substitution but not the traditional structural subclassifications. The biological effects of the investigated flavonoids specifically on copper trafficking were assessed in knockout yeast models as well as in human hepatocytes. The copper modulating abilities of strong copper-binding flavonoids were largely influenced by the relative hydrophobicities. Combined, these spectroscopic and biological data help elucidate the intricate nature of flavonoids in affecting copper transport and open avenues to inform dietary recommendations and therapeutic development.
more »
« less
Soil organic matter attenuates the efficacy of flavonoid-based plant-microbe communication
Plant-microbe interactions are mediated by signaling compounds that control vital plant functions, such as nodulation, defense, and allelopathy. While interruption of signaling is typically attributed to biological processes, potential abiotic controls remain less studied. Here, we show that higher organic carbon (OC) contents in soils repress flavonoid signals by up to 70%. Furthermore, the magnitude of repression is differentially dependent on the chemical structure of the signaling molecule, the availability of metal ions, and the source of the plant-derived OC. Up to 63% of the signaling repression occurs between dissolved OC and flavonoids rather than through flavonoid sorption to particulate OC. In plant experiments, OC interrupts the signaling between a legume and a nitrogen-fixing microbial symbiont, resulting in a 75% decrease in nodule formation. Our results suggest that soil OC decreases the lifetime of flavonoids underlying plant-microbe interactions.
more »
« less
- Award ID(s):
- 1904865
- NSF-PAR ID:
- 10188233
- Date Published:
- Journal Name:
- Science Advances
- Volume:
- 6
- Issue:
- 5
- ISSN:
- 2375-2548
- Page Range / eLocation ID:
- eaax8254
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
SUMMARY Flavonoids are a well‐known class of specialized metabolites that play key roles in plant development, reproduction, and survival. Flavonoids are also of considerable interest from the perspective of human health, as both phytonutrients and pharmaceuticals. RNA sequencing analysis of an Arabidopsis null allele for chalcone synthase (CHS), which catalyzes the first step in flavonoid metabolism, has uncovered evidence that these compounds influence the expression of genes associated with the plant circadian clock. Analysis of promoter‐luciferase constructs further showed that the transcriptional activity of
CCA1 andTOC1 , two key clock genes, is altered in CHS‐deficient seedlings across the day/night cycle. Similar findings for a mutant line lacking flavonoid 3′‐hydroxylase (F3′H) activity, and thus able to synthesize mono‐ but not dihydroxylated B‐ring flavonoids, suggests that the latter are at least partially responsible; this was further supported by the ability of quercetin to enhanceCCA1 promoter activity in wild‐type and CHS‐deficient seedlings. The effects of flavonoids on circadian function were also reflected in photosynthetic activity, with chlorophyll cycling abolished in CHS‐ and F3′H‐deficient plants. Remarkably, the same phenotype was exhibited by plants with artificially high flavonoid levels, indicating that neither the antioxidant potential nor the light‐screening properties of flavonoids contribute to optimal clock function, as has recently also been demonstrated in animal systems. Collectively, the current experiments point to a previously unknown connection between flavonoids and circadian cycling in plants and open the way to better understanding of the molecular basis of flavonoid action. -
more » « less
Abstract Secondary chemistry often differs between sexes in dioecious plant species, a pattern attributed to its possible role in the evolution and/or maintenance of dioecy. We used GC-MS to measure floral volatiles emitted from, and LC-MS to quantitate non-volatile secondary compounds contained in, female and male Salix purpurea willow catkins from an F2 family. Using the abundance of these chemicals, we then performed quantitative trait locus (QTL) mapping to locate them on the genome, identified biosynthetic candidate genes in the QTL intervals, and examined expression patterns of candidate genes using RNA-seq. Male flowers emitted more total terpenoids than females, but females produced more benzenoids. Male tissue contained greater amounts of phenolic glycosides, but females had more chalcones and flavonoids. A flavonoid pigment and a spermidine derivative were found only in males. Male catkins were almost twice the mass of females. Forty-two QTL were mapped for 25 chemical traits and catkin mass across 16 of the 19 S. purpurea chromosomes. Several candidate genes were identified, including a chalcone isomerase associated with seven compounds. A better understanding of the genetic basis of the sexually dimorphic chemistry of a dioecious species may shed light on how chemically mediated ecological interactions may have helped in the evolution and maintenance of dioecy.
-
Plants are attacked by multiple insect pest species and insect herbivory can alter plant defense mechanisms. The plant defense responses to a specific herbivore may also contribute to the herbivore growth/survival on plants. Feeding by one insect species can modulate the plant defenses, which can either facilitate or hamper the colonization of subsequent incoming insects. However, little is known about the effect of sequential herbivory on sorghum plants. In this study, we demonstrate that a specialist aphid, sugarcane aphid (SCA; Melanaphis sacchari ) grows faster on sorghum than a generalist aphid species, greenbug (GB; Schizaphis graminum ). We also determined how the pre-infestation of SCA on sorghum affected the invasion of GB and vice-versa . Our sequential herbivory experiments revealed that SCA reproduction was lower on GB-primed sorghum plants, however, the reverse was not true. To assess the differences in plant defenses induced by specialist vs. generalist aphids, we monitored the expression of salicylic acid (SA) and jasmonic acid (JA) marker genes, and flavonoid biosynthetic pathway genes after 48 h of aphid infestation. The results indicated that GB infestation induced higher expression of SA and JA-related genes, and flavonoid pathway genes ( DFR , FNR , and FNSII ) compared to SCA infestation. Overall, our results suggested that GB-infested plants activate the plant defenses via phytohormones and flavonoids at early time points and hampers the colonization of incoming SCA, as well as explain the reproductive success of SCA compared to GB.more » « less
-
Glass, Jennifer B. (Ed.)ABSTRACT Microbe-mediated transformations of arsenic (As) often require As to be taken up into cells prior to enzymatic reaction. Despite the importance of these microbial reactions for As speciation and toxicity, understanding of how As bioavailability and uptake are regulated by aspects of extracellular water chemistry, notably dissolved organic matter (DOM), remains limited. Whole-cell biosensors utilizing fluorescent proteins are increasingly used for high-throughput quantification of the bioavailable fraction of As in water. Here, we present a mathematical framework for interpreting the time series of biosensor fluorescence as a measure of As uptake kinetics, which we used to evaluate the effects of different forms of DOM on uptake of trivalent arsenite. We found that thiol-containing organic compounds significantly inhibited uptake of arsenite into cells, possibly through the formation of aqueous complexes between arsenite and thiol ligands. While there was no evidence for competitive interactions between arsenite and low-molecular-weight neutral molecules (urea, glycine, and glyceraldehyde) for uptake through the aquaglyceroporin channel GlpF, which mediates transport of arsenite across cell membranes, there was evidence that labile DOM fractions may inhibit arsenite uptake through a catabolite repression-like mechanism. The observation of significant inhibition of arsenite uptake at DOM/As ratios commonly encountered in wetland pore waters suggests that DOM may be an important control on the microbial uptake of arsenite in the environment, with aspects of DOM quality playing an important role in the extent of inhibition. IMPORTANCE The speciation and toxicity of arsenic in environments like rice paddy soils and groundwater aquifers are controlled by microbe-mediated reactions. These reactions often require As to be taken up into cells prior to enzymatic reaction, but there is limited understanding of how microbial arsenic uptake is affected by variations in water chemistry. In this study, we explored the effect of dissolved organic matter (DOM) quantity and quality on microbial As uptake, with a focus on the role of thiol functional groups that are well known to form aqueous complexes with arsenic. We developed a quantitative framework for interpreting fluorescence time series from whole-cell biosensors and used this technique to evaluate effects of DOM on the rates of microbial arsenic uptake. We show that thiol-containing compounds significantly decrease rates of As uptake into microbial cells at environmentally relevant DOM/As ratios, revealing the importance of DOM quality in regulating arsenic uptake, and subsequent biotransformation, in the environment.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1126/sciadv.aax8254
