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.

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.

Deadly acceleration in dehydration of Eucalyptus viminalis leaves coincides with high-order vein cavitation.

Xylem cavitation during drought is proposed as a major driver of canopy collapse, but the mechanistic link between hydraulic failure and leaf damage in trees is still uncertain. Here, we used the tree species manna gum (Eucalyptus viminalis) to explore the connection between xylem dysfunction and lethal desiccation in leaves. Cavitation damage to leaf xylem could theoretically trigger lethal desiccation of tissues by severing water supply under scenarios such as runaway xylem cavitation, or the local failure of terminal parts of the leaf vein network. To investigate the role of xylem failure in leaf death, we compared the timing of damage to the photosynthetic machinery (Fv/Fm decline) with changes in plant hydration and xylem cavitation during imposed water stress. The water potential at which Fv/Fm was observed to decline corresponded to the water potential marking a transition from slow to very rapid tissue dehydration. Both events also occurred simultaneously with the initiation of cavitation in leaf high-order veins (HOV, veins from the third order above) and the analytically derived point of leaf runaway hydraulic failure. The close synchrony between xylem dysfunction and the photosynthetic damage strongly points to water supply disruption as the trigger for desiccation of leaves in this hardy evergreen tree. These results indicate that runaway cavitation, possibly triggered by HOV network failure, is the tipping agent determining the vulnerability of E. viminalis leaves to damage during drought and suggest that HOV cavitation and runaway hydraulic failure may play a general role in determining canopy damage in plants.

Linking xylem network failure with leaf tissue death.

Global warming is expected to dramatically accelerate forest mortality as temperature and drought intensity increase. Predicting the magnitude of this impact urgently requires an understanding of the process connecting atmospheric drying to plant tissue damage. Recent episodes of forest mortality worldwide have been widely attributed to dry conditions causing acute damage to plant vascular systems. Under this scenario vascular embolisms produced by water stress are thought to cause plant death, yet this hypothetical trajectory has never been empirically demonstrated. Here we provide foundational evidence connecting failure in the vascular network of leaves with tissue damage caused during water stress. We observe a catastrophic sequence initiated by water column breakage under tension in leaf veins which severs local leaf tissue water supply, immediately causing acute cellular dehydration and irreversible damage. By highlighting the primacy of vascular network failure in the death of leaves exposed to drought or evaporative stress our results provide a strong mechanistic foundation upon which models of plant damage in response to dehydration can be confidently structured.

Less safety for more efficiency: water relations and hydraulics of the invasive tree Ailanthus altissima (Mill.) Swingle compared with native Fraxinus ornus L.

Invasion of natural habitats by alien trees is a threat to forest conservation. Our understanding of fundamental ecophysiological mechanisms promoting plant invasions is still limited, and hydraulic and water relation traits have been only seldom included in studies comparing native and invasive trees. We compared several leaf and wood functional and mechanistic traits in co-occurring Ailanthus altissima (Mill.) Swingle (Aa) and Fraxinus ornus L. (Fo). Aa is one of the most invasive woody species in Europe and North America, currently outcompeting several native trees including Fo. We aimed at quantifying inter-specific differences in terms of: (i) performance in resource use and acquisition; (ii) hydraulic efficiency and safety; (iii) carbon costs associated to leaf and wood construction; and (iv) plasticity of functional and mechanistic traits in response to light availability. Traits related to leaf and wood construction and drought resistance significantly differed between the two species. Fo sustained higher structural costs than Aa, but was more resistant to drought. The lower resistance to drought stress of Aa was counterbalanced by higher water transport efficiency, but possibly required mechanisms of resilience to drought-induced hydraulic damage. Larger phenotypic plasticity of Aa in response to light availability could also promote the invasive potential of the species.