Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers

Abstract

Flowers are critical for angiosperm reproduction and the production of food, fibre and pharmaceuticals, yet for unknown reasons they appear particularly sensitive to combined heat and drought stress. A possible explanation for this may be the co-occurrence of leaky cuticles in flower petals and a vascular system that has a low capacity to supply water and is prone to failure under water stress. These characteristics may render reproductive structures more susceptible than leaves to run-away cavitation – an uncontrolled feedback cycle between rising water stress and declining water transport efficiency that can rapidly lead to lethal tissue desiccation. We provide modelling and empirical evidence to demonstrate that flower damage in the perennial crop pyrethrum (Tanacetum cinerariifolium), in the form of irreversible desiccation, corresponds with run-away cavitation in the flowering stem after a combination of heat and water stress. We show that tissue damage is linked to greater evaporative demand during high temperatures rather than direct thermal stress. High floral transpiration dramatically reduced the soil water deficit at which run-away cavitation was triggered in pyrethrum flowering stems. Identifying run-away cavitation as a mechanism leading to heat damage and reproductive losses in pyrethrum provides different avenues for process-based modelling to understand the impact of climate change on cultivated and natural plant systems. This framework allows future investigation of the relative susceptibility of diverse plant species to reproductive failure under hot and dry conditions.

Evidence of combined flower thermal and drought vulnerabilities portends reproductive failure under hotter‐drought conditions

“…Thus, given that the cuticle represents the major hydrophobic barrier against residual water loss (Duursma et al, 2019), and considering that the relative investment in cuticle is positively associated with TMA (John et al, 2017; Onoda et al, 2012), we expected that, due to their lower construction cost, flowers would be leakier to water vapor than leaves. Contrary to our hypothesis, and to the findings of other studies (Bourbia et al, 2020; Carins‐Murphy et al, 2023; Cheng et al, 2021; Roddy, 2023), a clear pattern in the variation of g flower and g leaf‐res within species was not observed (Figure ), which thus resulted in the lack of significant differences in g min between organs (Figure 2c). A possible explanation for these unexpected results may involve the different sources of water leaks integrated by the residual conductance (Duursma et al, 2019; Machado et al, 2020), and their differential contribution to g flower and g leaf‐res .…”

“…Despite floral capacitance effectively buffering Ψ flower , a combination of low TSM and LSM make floral organs more vulnerable to turgor loss during hotter‐drought. In line with our findings, a recent study showed that combined heat and drought stresses dramatically increased the likelihood of flower mortality in a perennial crop species (Carins‐Murphy et al, 2023). Importantly, in addition to impairments to reproductive success, increases in air temperature can also compromise overall plant survival under drought conditions, especially for those species with lower flower T p .…”

“…Although all the species we studied bloom throughout the rainy season, our results reinforce the evidence that projected increases in hotter‐drought events during coming decades could compromise reproductive success (Carins‐Murphy et al, 2023), especially for species with low LSM and TSM. Thus, considering the further increases in T max projected for the region (IPCC, 2023; PBMC, 2020), it is likely that species with larger LSMs in the present would exceed their T p , or operate close to this point in the coming decades.…”

“…Although heat‐induced changes in cuticular waxes were already demonstrated for leaves (Billon et al, 2020; Bueno et al, 2019; Slot et al, 2021), to the best of our knowledge, this is the first study to show that flowers are also prone to this type of damage. On the other hand, the lack of variation in g flower under high temperatures in two woody species (Figure 6), and one perennial crop (Carins‐Murphy et al, 2023), suggest that, like leaves (Slot et al, 2021), thermal damage to flower cuticle is species‐specific. Thus, given that high T p is thought to reflect adaptation to hot environments (e.g., deserts) (Bueno et al, 2019), it is possible that the low flower T p observed in most of the studied species may result from the lack of selective pressure exerted by the mild Cerrado climate during their anthesis; whereas leaves, which usually face higher temperatures throughout the year, are built with a more thermally resistant cuticle.…”

“…This threshold is called phase‐transition temperature ( T p ) and represents the temperature above which cuticular permeability increases as a result of changes in the structure of cuticular waxes (Bueno et al, 2019). However, although the T p values can provide important information regarding the ability of a given organ to avoid uncontrolled water loss under hotter‐droughts (Billon et al, 2020), little is known about the thermal dynamics of g flower in floral organs (Carins‐Murphy et al, 2023). Despite the lack of information, considering that T p values are associated with cuticle chemical properties (Bueno et al, 2019) and that the relative investment in this structure varies positively with the increase in TMA (John et al, 2017; Onoda et al, 2012), it is feasible to suggest that the lower carbon allocation to build flowers may result in the construction of organs with less effective hydrophobic barriers.…”