An official website of the United States government
ABSTRACT Freezing air temperatures kill most leaves, yet the leaves of some species can survive these events. Tracking the temporal and spatial dynamics of freezing remains an impediment to characterizing frost tolerance. Here we deploye time‐lapse imaging and image subtraction analysis, coupled with fine wire thermocouples, to discern the in situ spatial dynamics of freezing and thawing. Our method of analysis of pixel brightness reveals that ice formation in leaves exposed to natural frosts initiates in mesophyll before spreading to veins, and that while ex situ xylem sap freezes near 0°C, in situ xylem sap has a freezing point of −2°C in our model freezing‐resistant species ofLonicera. Photosynthetic rates in leaves that have been exposed to a rapid freeze or thaw do not recover, but leaves exposed to a slow, natural freezing and thawing to −10°C do recover. Using this method, we are able to quantify the spatial formation and timing of freezing events in leaves, and suggest that in situ and ex situ freezing points for xylem sap can differ by more than 4°C depending on the rate of temperature decline.
more »
« less
Droplet superpropulsion in an energetically constrained insect
Abstract Food consumption and waste elimination are vital functions for living systems. Although how feeding impacts animal form and function has been studied for more than a century since Darwin, how its obligate partner, excretion, controls and constrains animal behavior, size, and energetics remains largely unexplored. Here we study millimeter-scale sharpshooter insects (Cicadellidae) that feed exclusively on a plant’s xylem sap, a nutrient-deficit source (95% water). To eliminate their high-volume excreta, these insects exploit droplet superpropulsion, a phenomenon in which an elastic projectile can achieve higher velocity than the underlying actuator through temporal tuning. We combine coupled-oscillator models, computational fluid dynamics, and biophysical experiments to show that these insects temporally tune the frequency of their anal stylus to the Rayleigh frequency of their surface tension-dominated elastic drops as a single-shot resonance mechanism. Our model predicts that for these tiny insects, the superpropulsion of droplets is energetically cheaper than forming jets, enabling them to survive on an extreme energy-constrained xylem-sap diet. The principles and limits of superpropulsion outlined here can inform designs of energy-efficient self-cleaning structures and soft engines to generate ballistic motions.
more »
« less
- PAR ID:
- 10399434
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 14
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
SUMMARY Lipids have been observed attached to lumen‐facing surfaces of mature xylem conduits of several plant species, but there has been little research on their functions or effects on water transport, and only one lipidomic study of the xylem apoplast. Therefore, we conducted lipidomic analyses of xylem sap from woody stems of seven plants representing six major angiosperm clades, including basal magnoliids, monocots and eudicots, to characterize and quantify phospholipids, galactolipids and sulfolipids in sap using mass spectrometry. Locations of lipids in vessels ofLaurus nobiliswere imaged using transmission electron microscopy and confocal microscopy. Xylem sap contained the galactolipids di‐ and monogalactosyldiacylglycerol, as well as all common plant phospholipids, but only traces of sulfolipids, with total lipid concentrations in extracted sap ranging from 0.18 to 0.63 nmol ml−1across all seven species. Contamination of extracted sap from lipids in cut living cells was found to be negligible. Lipid composition of sap was compared with wood in two species and was largely similar, suggesting that sap lipids, including galactolipids, originate from cell content of living vessels. Seasonal changes in lipid composition of sap were observed for one species. Lipid layers coated all lumen‐facing vessel surfaces ofL. nobilis, and lipids were highly concentrated in inter‐vessel pits. The findings suggest that apoplastic, amphiphilic xylem lipids are a universal feature of angiosperms. The findings require a reinterpretation of the cohesion‐tension theory of water transport to account for the effects of apoplastic lipids on dynamic surface tension and hydraulic conductance in xylem.more » « less
-
Insects feeding on the nutrient-poor diet of xylem plant sap generally bear two microbial symbionts that are localized to different organs (bacteriomes) and provide complementary sets of essential amino acids (EAAs). Here, we investigate the metabolic basis for the apparent paradox that xylem-feeding insects are under intense selection for metabolic efficiency but incur the cost of maintaining two symbionts for functions mediated by one symbiont in other associations. Using stable isotope analysis of central carbon metabolism and metabolic modeling, we provide evidence that the bacteriomes of the spittlebug Clastoptera proteus display high rates of aerobic glycolysis, with syntrophic splitting of glucose oxidation. Specifically, our data suggest that one bacteriome (containing the bacterium Sulcia, which synthesizes seven EAAs) predominantly processes glucose glycolytically, producing pyruvate and lactate, and the exported pyruvate and lactate is assimilated by the second bacteriome (containing the bacterium Zinderia, which synthesizes three energetically costly EAAs) and channeled through the TCA cycle for energy generation by oxidative phosphorylation. We, furthermore, calculate that this metabolic arrangement supports the high ATP demand in Zinderia bacteriomes for Zinderia-mediated synthesis of energy-intensive EAAs. We predict that metabolite cross-feeding among host cells may be widespread in animal–microbe symbioses utilizing low-nutrient diets.more » « less
-
Abstract Host-microbe interactions are intimately linked to eukaryotic evolution, particularly in sap-sucking insects that often rely on obligate microbial symbionts for nutrient provisioning. Cicadas (Cicadidae: Auchenorrhyncha) specialize on xylem fluid and derive many essential amino acids and vitamins from intracellular bacteria or fungi (Hodgkinia,Sulcia, andOphiocordyceps) that are propagated via transmission from mothers to offspring. Despite the beneficial role of these non-gut symbionts in nutrient provisioning, the role of beneficial microbiota within the gut remains unclear. Here, we investigate the relative abundance and impact of host phylogeny and ecology on gut microbial diversity in cicadas using 16S ribosomal RNA gene amplicon sequencing data from 197 wild-collected cicadas and new mitochondrial genomes across 38 New Zealand cicada species, including natural hybrids between one pair of two species. We find low abundance and a lack of phylogenetic structure and hybrid effects but a significant role of elevation in explaining variation in gut microbiota.more » « less
-
Abstract Terrestrial photosynthesis requires the evaporation of water (transpiration) in exchange for CO2needed to form sugars. The water for transpiration is drawn up through plant roots, stem, and branches via a water potential gradient. However, this flow of water—or sap ascent—requires energy to lift the water to the canopy and to overcome the resistance of the plant’s water transporting xylem. Here, we use a combination of field measurements of plant physiology (hydraulic conductivity) and state‐of‐the‐science global estimates of transpiration to calculate how much energy is passively harvested by plants to power the sap ascent pump across the world’s terrestrial vegetation. Globally, we find that 0.06 W/m2is consumed in sap ascent over forest dominated ecosystems or 9.4 PWh/yr (equal to global hydropower energy production). Though small in comparison to other components of the Earth’s surface energy budget, sap ascent work in forests represents 14.2% of the energy compared to the energy consumed to create sugars through photosynthesis, with values up to 18% in temperate rainforests. The power needed for sap ascent generally increases with photosynthesis, but is moderated by both climate and plant physiology, as the most work is consumed in regions with large transpiration fluxes (such as the moist tropics) and in areas where vegetation has low conductivity (such as temperate rainforests dominated by conifer trees). Here, we present a bottom‐up analysis of sap ascent work that demonstrates its significant role in plant function across the globe.more » « less
