Xylem cavitation isolates leaky flowers during water stress in pyrethrum

Abstract

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.

Reproductive water supply is prioritised during drought in tomato

“…J. Brodribb, Powers, Cochard, & Choat, 2020;Choat et al, 2012). Despite the serious consequences of reproductive failure to agriculture and conservation, however, the effects of water stress on plant reproduction are not well resolved (Bourbia, Carins-Murphy, Gracie, & Brodribb, 2020;Roddy, 2019;Zhang, Zhang, Brodribb, & Hu, 2020). Hydraulic traits have been used to effectively model plant mortality in drought (W. R. Anderegg et al, 2015;Choat et al, 2018;Choat et al, 2012;Sperry & Love, 2015;Sperry & Tyree, 1988;Urli et al, 2013;Vilagrosa et al, 2012) yet such traits in reproductive and floral organs are not well integrated into whole plant hydraulic vulnerability models.…”

“…Xylem with greater resistance to cavitation maintains an intact water supply to tissues longer in water limiting conditions (Sperry & Tyree, 1988;Melvin T Tyree & Sperry, 1989). Relationships between xylem cavitation and plant damage have been widely characterized in woody tissues, but only recently have the implications of xylem cavitation been considered in the context of plant reproductive success (Bourbia et al, 2020;Roddy, Jiang, Cao, Simonin, & Brodersen, 2019;Zhang & Brodribb, 2017).…”

“…Flowers which transpire rapidly must rely on the xylem as the most efficient transporter of water, exposing them to the water stress experienced by the whole plant. Alternately, if flower water loss is negligible, then water may be supplied by the phloem, theoretically allowing the flower to be largely disconnected from the apoplastic water stress (Bourbia et al, 2020;Chapotin, Holbrook, Morse, & Gutiérrez, 2003;De La Barrera & Nobel, 2004). However, the estimated contribution of xylem supplied water to the water balance of fruit and flowers varies significantly.…”

“…Evidence suggests that reproductive tissues are exposed to xylem cavitation in drought conditions, and water loss from flowering structures also contributes to whole plant water stress (Bourbia et al, 2020;Lambrecht, 2013;Roddy, 2019;Zhang, Carins Murphy, Cardoso, Jordan, & Brodribb, 2018). These observations highlight the need to include reproductive organs in hydraulic models to understand the broader patterns in xylem vulnerability throughout the plant (Bourbia et al, 2020).…”

“…Evidence suggests that reproductive tissues are exposed to xylem cavitation in drought conditions, and water loss from flowering structures also contributes to whole plant water stress (Bourbia et al, 2020;Lambrecht, 2013;Roddy, 2019;Zhang, Carins Murphy, Cardoso, Jordan, & Brodribb, 2018). These observations highlight the need to include reproductive organs in hydraulic models to understand the broader patterns in xylem vulnerability throughout the plant (Bourbia et al, 2020). Based on the hydraulic vulnerability segmentation hypothesis, distal, short-lived organs requiring a low carbon investment should be more vulnerable to cavitation than non-redundant organs, helping to prologue plant survival in drought (Johnson et al, 2016;Melvin T. Tyree & Ewers, 1991;Zimmermann, 2013).…”