Stomatal response to VPD is not triggered by changes in soil-leaf hydraulic conductance in Arabidopsis or Callitris.

Stomatal closure under high VPDL (leaf to air vapour pressure deficit) is a primary means by which plants prevent large excursions in transpiration rate and leaf water potential (Ψleaf) that could lead to tissue damage. Yet, the drivers of this response remain controversial. Changes in Ψleaf appear to drive stomatal VPDL response, but many argue that dynamic changes in soil-to-leaf hydraulic conductance (Ks-l) make an important contribution to this response pathway, even in well-hydrated soils. Here, we examined whether the regulation of whole plant stomatal conductance (gc) in response to typical changes in daytime VPDL is influenced by dynamic changes in Ks-l. We use well-watered plants of two species with contrasting ecological and physiological features: the herbaceous Arabidopsis thaliana (ecotype Columbia-0) and the dry forest conifer Callitris rhomboidea. The dynamics of Ks-l and gc were continuously monitored by combining concurrent in situ measurements of Ψleaf using an open optical dendrometer and whole plant transpiration using a balance. Large changes in VPDL were imposed to induce stomatal closure and observe the impact on Ks-l. In both species, gc was observed to decline substantially as VPDL increased, while Ks-l remained stable. Our finding suggests that stomatal regulation of transpiration is not contingent on a decrease in Ks-l. Static Ks-l provides a much simpler explanation for transpiration control in hydrated plants and enables simplified modelling and new methods for monitoring plant water use in the field.

Variation in xylem vulnerability to cavitation shapes the photosynthetic legacy of drought.

Increased drought conditions impact tree health, negatively disrupting plant water transport which, in turn, affects plant growth and survival. Persistent drought legacy effects have been documented in many diverse ecosystems, yet we still lack a mechanistic understanding of the physiological processes limiting tree recovery after drought. Tackling this question, we exposed saplings of a common Australian evergreen tree (Eucalyptus viminalis) to a cycle of drought and rewatering, seeking evidence for a link between the spread of xylem cavitation within the crown and the degree of photosynthetic recovery postdrought. Individual leaves experiencing >35% vein cavitation quickly died but this did not translate to a rapid overall canopy damage. Rather, whole canopies showed a gradual decline in mean postdrought gas exchange rates as water stress increased. This gradual loss of canopy function postdrought was due to a significant variation in cavitation vulnerability of leaves within canopies leading to diversity in the capacity of leaves within a single crown to recover function after drought. These results from the evergreen E. viminalis emphasise the importance of within-crown variation in xylem vulnerability as a central character regulating the dynamics of canopy death and the severity of drought legacy through time.

In situ characterisation of whole-plant stomatal responses to VPD using leaf optical dendrometry.

Vapour pressure deficit (VPD) plays a crucial role in regulating plant carbon and water fluxes due to its influence on stomatal behaviour and transpiration. Yet, characterising stomatal responses of the whole plant to VPD remains challenging due to methodological limitations. Here, we develop a novel method for in situ assessment of whole-plant stomatal responses (gc ) to VPD in the herbaceous plant Tanacetum cinerariifolium. To do this, we examine the relationship between daytime VPD and the corresponding soil-stem water potential gradient (ΔΨ) monitored using the optical dendrometry in well-hydrated plants under nonlimiting light in both glasshouse and field conditions. In glasshouse plants, ΔΨ increased proportionally with the VPD up to a threshold of 1.53 kPa, beyond which the slope decreased, suggesting a two-phase response in gc . This pattern aligned with corresponding gravimetrically measured gc behaviour, which also showed a decline when VPD exceeded a similar threshold. This response was then compared with that of field plants monitored using the optical dendrometry technique over a growing season under naturally variable VPD conditions and nonlimiting light and water supply. Field plants exhibited a similar threshold-type response to VPD but were more sensitive than glasshouse individuals with a VPD threshold of 0.74 kPa. The results showed that whole-plant gc responses to VPD can be characterised optically in T. cinerariifolium, introducing a new tool for the monitoring and characterisation of stomatal behaviour in situ.

The root of the problem: diverse vulnerability to xylem cavitation found within the root system of wheat plants.

The propagation of xylem embolism throughout the root systems of drought-affected plants remains largely unknown, despite this process being comparatively well characterized in aboveground tissues. We used optical and X-ray imaging to capture xylem embolism propagation across the intact root systems of bread wheat (Triticum aestivum L. 'Krichauff') plants subjected to drying. Patterns in vulnerability to xylem cavitation were examined to investigate whether vulnerability may vary based on root size and placement across the entire root system. Individual plants exhibited similar mean whole root system vulnerabilities to xylem cavitation but showed enormous 6 MPa variation within their component roots (c. 50 roots per plant). Xylem cavitation typically initiated in the smallest, peripheral parts of the root system and moved inwards and upwards towards the root collar last, although this trend was highly variable. This pattern of xylem embolism spread likely results in the sacrifice of replaceable small roots while preserving function in larger, more costly central roots. A distinct pattern of embolism-spread belowground has implications for how we understand the impact of drought in the root system as a critical interface between plant and soil.

Constant hydraulic supply enables optical monitoring of transpiration in a grass, a herb, and a conifer.

Plant transpiration is an inevitable consequence of photosynthesis and has a huge impact on the terrestrial carbon and water cycle, yet accurate and continuous monitoring of its dynamics is still challenging. Under well-watered conditions, canopy transpiration (Ec) could potentially be continuously calculated from stem water potential (Ψstem), but only if the root to stem hydraulic conductance (Kr-s) remains constant and plant capacitance is relatively small. We tested whether such an approach is viable by investigating whether Kr-s remains constant under a wide range of daytime transpiration rates in non-water-stressed plants. Optical dendrometers were used to continuously monitor tissue shrinkage, an accurate proxy of Ψstem, while Ec was manipulated in three species with contrasting morphological, anatomical, and phylogenetic identities: Tanacetum cinerariifolium, Zea mays, and Callitris rhomboidea. In all species, we found Kr-s to remain constant across a wide range of Ec, meaning that the dynamics of Ψstem could be used to monitor Ec. This was evidenced by the close agreement between measured Ec and that predicted from optically measured Ψstem. These results suggest that optical dendrometers enable both plant hydration and Ec to be monitored non-invasively and continuously in a range of woody and herbaceous species. This technique presents new opportunities to monitor transpiration under laboratory and field conditions in a diversity of woody, herbaceous, and grassy species.

Conduit position and connectivity affect the likelihood of xylem embolism during natural drought in evergreen woodland species.

BACKGROUND AND AIMS: Hydraulic failure is considered a main cause of drought-induced forest mortality. Yet, we have a limited understanding of how the varying intensities and long time scales of natural droughts induce and propagate embolism within the xylem. METHODS: X-ray computed tomography (microCT) images were obtained from different aged branch xylem to study the number, size and spatial distribution of in situ embolized conduits among three dominant tree species growing in a woodland community. KEY RESULTS: Among the three studied tree species, those with a higher xylem vulnerability to embolism (higher water potential at 50 % loss of hydraulic conductance; P50) were more embolized than species with lower P50. Within individual stems, the probability of embolism was independent of conduit diameter but associated with conduit position. Rather than the occurrence of random or radial embolism, we observed circumferential clustering of high and low embolism density, suggesting that embolism spreads preferentially among conduits of the same age. Older xylem also appeared more likely to accumulate embolisms than young xylem, but there was no pattern suggesting that branch tips were more vulnerable to cavitation than basal regions. CONCLUSIONS: The spatial analysis of embolism occurrence in field-grown trees suggests that embolism under natural drought probably propagates by air spreading from embolized into neighbouring conduits in a circumferential pattern. This pattern offers the possibility to understand the temporal aspects of embolism occurrence by examining stem cross-sections.

Herb and conifer roots show similar high sensitivity to water deficit.

Root systems play a major role in supplying the canopy with water, enabling photosynthesis and growth. Yet, much of the dynamic response of root hydraulics and its influence on gas exchange during soil drying and recovery remains uncertain. We examined the decline and recovery of the whole root hydraulic conductance (Kr) and canopy diffusive conductance (gc) during exposure to moderate water stress in two species with contrasting root systems: Tanacetum cinerariifolium (herbaceous Asteraceae) and Callitris rhomboidea (woody conifer). Optical dendrometers were used to record stem water potential at high temporal resolution and enabled non-invasive measurements of Kr calculated from the rapid relaxation kinetics of water potential in hydrating roots. We observed parallel declines in Kr and gc to <20% of unstressed levels during the early stages of water stress in both species. The recovery of Kr after rewatering differed between species. T. cinerariifolium recovered quickly, with 60% of Kr recovered within 2 h, while C. rhomboidea was much slower to return to its original Kr. Recovery of gc followed a similar trend to Kr in both species, with C. rhomboidea slower to recover. Our findings suggest that the pronounced sensitivity of Kr to drought is a common feature among different plant species, but recovery may vary depending on root type and water stress severity. Kr dynamics are proposed to modulate gc response during and following drought.

Xylem cavitation isolates leaky flowers during water stress in pyrethrum.

Flowers underpin plant evolution, genetic legacy and global food supply. They are exposed to similar evaporative conditions as leaves, yet floral physiology is a product of different selective forces. We used Tanacetum cinerariifolium, a perennial daisy, to examine the response of flowers to whole-plant water stress, determining if flowers constitute a liability during drought, and how this species has adapted to minimize risk associated with reproduction. We determined the relative transpiration cost of flowers and leaves and confirmed that flowers in this species are xylem-hydrated. The relative water stress tolerance of leaves and flowers then was compared using xylem vulnerability measurements linked with observed tissue damage during an acute drought treatment. Flowers were a major source of water loss during drought but the xylem supplying them was much more vulnerable to cavitation than leaves. This xylem vulnerability segmentation was confirmed by observations that most flowers died whereas leaves were minimally affected during drought. Early cavitation and hydraulic isolation of flowers during drought benefits the plant by slowing the dehydration of perennial vegetative organs and delaying systemic xylem damage. Our results highlight the need to understand flower xylem vulnerability as a means of predicting plant reproductive failure under future drought.