• Drought-induced xylem embolism is a primary cause of plant mortality. Although ~70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked.
• We quantified the vulnerability to drought-induced embolism, pressure-volume curves, in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads.
• Compared to other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than non-cycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads.
• Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits–particularly vessels–may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.
more »
« less
This content will become publicly available on June 19, 2025
Limited effects of xylem anatomy on embolism resistance in cycad leaves
Drought‐induced xylem embolism is a primary cause of plant mortality. Although We quantified the vulnerability to drought‐induced embolism, pressure–volume curves, Compared with other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than noncycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads. Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits – particularly vessels – may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.
- PAR ID:
- 10516221
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- ISSN:
- 0028-646X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Abstract Drought events may increase the likelihood that the plant water transport system becomes interrupted by embolism. Yet our knowledge about the temporal frequency of xylem embolism in the field is frequently lacking, as it requires detailed, long‐term measurements.
We measured xylem embolism resistance and midday xylem water potentials during the consecutive summers of 2019 and 2020 to estimate maximum levels of embolism in leaf and stem xylem of ten temperate angiosperm tree species. We also studied vessel and pit membrane characteristics based on light and electron microscopy to corroborate potential differences in embolism resistance between leaves and stems.
Apart from
A .pseudoplatanus andQ .petraea , eight species experienced minimum xylem water potentials that were close to or below those required to initiate embolism. Water potentials corresponding to ca. 12% loss of hydraulic conductivity (PLC) could occur in six species, while considerable levels of embolism around 50% PLC were limited toB .pendula andC .avellana . There was a general agreement in embolism resistance between stems and leaves, with leaves being equally or more resistant than stems. Also, xylem embolism resistance was significantly correlated to intervessel pit membrane thickness (T PM) for stems, but not to vessel diameter and total intervessel pit membrane surface area of a vessel.Our data indicate that low amounts of embolism occur in most species during moderate summer drought, and that considerable levels of embolism are uncommon. Moreover, our experimental and
T PMdata show that leaf xylem is generally no more vulnerable than stem xylem. -
more » « less
Summary Embolism spreading in angiosperm xylem occurs via mesoporous pit membranes between vessels. Here, we investigate how the size of pore constrictions in pit membranes is related to pit membrane thickness and embolism resistance.
Pit membranes were modelled as multiple layers to investigate how pit membrane thickness and the number of intervessel pits per vessel determine pore constriction sizes, the probability of encountering large pores, and embolism resistance. These estimations were complemented by measurements of pit membrane thickness, embolism resistance, and number of intervessel pits per vessel in stem xylem (
n = 31, 31 and 20 species, respectively).The modelled constriction sizes in pit membranes decreased with increasing membrane thickness, explaining the measured relationship between pit membrane thickness and embolism resistance. The number of pits per vessel affected constriction size and embolism resistance much less than pit membrane thickness. Moreover, a strong relationship between modelled and measured embolism resistance was observed.
Pore constrictions provide a mechanistic explanation for why pit membrane thickness determines embolism resistance, which suggests that hydraulic safety can be uncoupled from hydraulic efficiency. Although embolism spreading remains puzzling and encompasses more than pore constriction sizes, angiosperms are unlikely to have leaky pit membranes, which enables tensile transport of water.
-
more » « less
Summary Wood anatomical traits shape a xylem segment’s hydraulic efficiency and resistance to embolism spread due to declining water potential. It has been known for decades that variations in conduit connectivity play a role in altering xylem hydraulics. However, evaluating the precise effect of conduit connectivity has been elusive. The objective here is to establish an analytical linkage between conduit connectivity and grouping and tissue‐scale hydraulics.
It is hypothesized that an increase in conduit connectivity brings improved resistance to embolism spread due to increased hydraulic pathway redundancy. However, an increase in conduit connectivity could also reduce resistance due to increased speed of embolism spread with respect to pressure. We elaborate on this trade‐off using graph theory, percolation theory and computational modeling of xylem. The results are validated using anatomical measurements of
Acer branch xylem.Considering only species with vessels, increases in connectivity improve resistance to embolism spread without negatively affecting hydraulic conductivity. The often measured grouping index fails to capture the totality of the effect of conduit connectivity on xylem hydraulics.
Variations in xylem network characteristics, such as conduit connectivity, might explain why hypothesized trends among woody species, such as the ‘safety‐efficiency’ trade‐off hypothesis, are weaker than expected.
-
more » « less
Abstract Recent findings suggest that tree mortality and post‐drought recovery of gas exchange can be predicted from loss of function within the water transport system. Understanding the susceptibility of plants to hydraulic damage requires knowledge about the vulnerability of different plant organs to stress‐induced hydraulic dysfunction. This is particularly important in the context of vulnerability segmentation between plant tissues which is believed to protect more energetically ‘costly’ tissues, such as woody stems, by sacrificing ‘cheaper’ leaves early under drought conditions.
Differences in vulnerability segmentation between co‐occurring plant species could explain divergent behaviours during drought, yet there are few studies considering how this characteristic may vary within a plant community. Here we investigated community‐wide vulnerability segmentation by comparing leaf/shoot and stem vulnerability in all coexistent dominant canopy and understory woody species in a diverse dry sclerophyll woodland community, including multiple angiosperms and one gymnosperm.
Previously published terminal leaf/shoot vulnerability to loss of water transport capacity was compared with stem xylem vulnerability to embolism measured on the same species at the same site. We calculated hydraulic safety margins for stems to determine variation in the risk of hydraulic failure during drought among species.
The xylem of all species was found to be highly resistant to hydraulic dysfunction, with only two of the eight species exhibiting significantly different vulnerability to the overall mean. No evidence of vulnerability segmentation between shoots/leaves and stems was found in seven of the eight species.
Phylogenetically diverse canopy and understory species in this evergreen sclerophyll woodland appear to have evolved similar strategies of drought resistance, including low xylem vulnerability to embolism and general lack of vulnerability segmentation. This convergence in hydraulic safety indicates a lack of hydraulic niche partitioning in this woodland community.
A free
plain language summary can be found within the Supporting Information of this article.
