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 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.
The resistance of xylem conduits to embolism is a major factor defining drought tolerance and can set the distributional limits of species across rainfall gradients. Recent work suggests that the proximity of vessels to neighbors increases the vulnerability of a conduit. We therefore investigated whether the relative vessel area of xylem correlates with intra- and inter-generic variation in xylem embolism resistance in species pairs or triplets from the genera Acer, Cinnamomum, Ilex, Quercus and Persea, adapted to environments differing in aridity. We used the optical vulnerability method to assess embolism resistance in stems and conducted anatomical measurements on the xylem in which embolism resistance was quantified. Vessel lumen fraction (VLF) correlated with xylem embolism resistance across and within genera. A low VLF likely increases the resistance to gas movement between conduits, by diffusion or advection, whereas a high VLF enhances gas transport thorough increased conduit-to-conduit connectivity and reduced distances between conduits and therefore the likelihood of embolism propagation. We suggest that the rate of gas movement due to local pressure differences and xylem network connectivity is a central driver of embolism propagation in angiosperm vessels.
more » « less- Award ID(s):
- 2140119
- PAR ID:
- 10474389
- Editor(s):
- Martinez-Vilalta, Jordi
- Publisher / Repository:
- Oxford Academic
- Date Published:
- Journal Name:
- Tree Physiology
- Volume:
- 43
- Issue:
- 1
- ISSN:
- 1758-4469
- Page Range / eLocation ID:
- 75 to 87
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Acer branch xylem. -
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Summary Drought‐induced xylem embolism is a primary cause of plant mortality. Although
c . 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 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.
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Summary The hydraulic system of vascular plants and its integrity is essential for plant survival. To transport water under tension, the walls of xylem conduits must approximate rigid pipes. Against this expectation, conduit deformation has been reported in the leaves of a few species and hypothesized to function as a ‘circuit breaker’ against embolism. Experimental evidence is lacking, and its generality is unknown.
We demonstrated the role of conduit deformation in protecting the upstream xylem from embolism through experiments on three species and surveyed a diverse selection of vascular plants for conduit deformation in leaves.
Conduit deformation in minor veins occurred before embolism during slow dehydration. When leaves were exposed to transient increases in transpiration, conduit deformation was accompanied by large water potential differences from leaf to stem and minimal embolism in the upstream xylem. In the three species tested, collapsible vein endings provided clear protection of upstream xylem from embolism during transient increases in transpiration.
We found conduit deformation in diverse vascular plants, including 11 eudicots, ginkgo, a cycad, a fern, a bamboo, and a grass species, but not in two bamboo and a palm species, demonstrating that the potential for ‘circuit breaker’ functionality may be widespread across vascular plants.
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Shabala, Sergey (Ed.)Maintaining water transport in the xylem is critical for vascular plants to grow and survive. The drought-induced accumulation of embolism, when gas enters xylem conduits, causes declines in hydraulic conductance (K) and is ultimately lethal. Several methods can be used to estimate the degree of embolism in xylem, from measuring K in tissues to directly visualising embolism in conduits. One method allowing a direct quantification of embolised xylem area is the optical vulnerability (OV) technique. This method has been used across different organs and has a high spatial and temporal resolution. Here, we review studies using the OV technique, discuss the main advantages and disadvantages of this method, and summarise key advances arising from its use. Vulnerability curves generated by the OV method are regularly comparable to other methods, including the centrifuge and X-ray microtomography. A major advantage of the OV technique over other methods is that it can be simultaneously used to determine in situ embolism formation in leaves, stems and roots, in species spanning the phylogeny of land plants. The OV method has been used to experimentally investigate the spreading of embolism through xylem networks, associate embolism with downstream tissue death, and observe embolism formation in the field.more » « less