Drought will not leave your glass empty: Low risk of hydraulic failure revealed by long-term drought observations in world’s top wine regions

Charrier, Guillaume; Delzon, Sylvain; Domec, Jean‐Christophe; Zhang, Li; Delmas, Chloé; Merlin, Isabelle; Corso, Déborah; King, Andrew; Ojeda, Hernán; Ollat, Nathalie; Prieto, Jorge; Scholach, Thibaut; Skinner, Paul; Leeuwen, Cornelis van; Gambetta, Grégory A.

doi:10.1126/sciadv.aao6969

Cited by 116 publications

(155 citation statements)

References 44 publications

(81 reference statements)

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“…Although this ecologically counterintuitive condition has only been observed in highly vulnerable Betula species (Klepsch et al, ; Sperry & Saliendra, ), it is not known in evergreen species (Brodribb et al, ; Lucani, Brodribb, Jordan, & Mitchell, ; Rodriguez‐Dominguez et al, ; Skelton et al, ). By contrast, several reports suggest leaves are more vulnerable to dysfunction than stems (Charrier et al, ; Choat et al, ; Cochard et al, ; Hochberg et al, ; Johnson et al, , ; Pivovaroff et al, ; Rodriguez‐Dominguez et al, ; Scoffoni & Sack, ; Skelton et al, ; Tyree et al, ; Zhu et al, ); however, here we find no evidence for this scenario in the majority of the studied species because leaf hydraulic conductance declined with a very similar kinetic to the accumulation of embolism in the stems. Another possible source of error is the fact that neither stems nor leaves were high pressure ‘flushed’ prior to measurement to remove possible resident embolisms.…”

Section: Discussioncontrasting

confidence: 92%

“…This hypothesis proposes that vulnerability segmentation between plant tissues could serve to protect more energetically 'costly' tissues, such as stems, from embolisms and sacrifice 'less costly' leaves (Johnson et al, 2016;Klepsch et al, 2018;Pivovaroff, Sack, & Santiago, 2014;Skelton et al, 2018;Tyree & Ewers, 1991;Wolfe, Sperry, & Kursar, 2016;Zhu, Liu, Xu, Cao, & Ye, 2016). Leaves have often been shown to be more vulnerable to water deficit than branches in both deciduous and evergreen woody tree species (Charrier et al, 2018;Choat, Ball, Luly, & Holtum, 2005;Cochard, Bréda, Granier, & Aussenac, 1992;Hochberg et al, 2017;Johnson et al, 2011Johnson et al, , 2016Pivovaroff et al, 2014;Rodriguez-Dominguez, Carins-Murphy, Lucani, & Brodribb, 2018;Skelton et al, 2018;Tyree, Cochard, Cruiziat, Sinclair, & Ameglio, 1993;Zhu et al, 2016). The degree of segmentation may vary across rainfall gradients, with species in more arid environments having greater levels of segmentation than those occurring in more mesic environments (Skelton et al, 2018;Zhu et al, 2016).…”

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confidence: 99%

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Lack of vulnerability segmentation among woody species in a diverse dry sclerophyll woodland community

et al. 2020

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Recent findings suggest that tree mortality and post‐drought recovery of gas exchange can be predicted from loss of function within the water transport system. Understanding the susceptibility of plants to hydraulic damage requires knowledge about the vulnerability of different plant organs to stress‐induced hydraulic dysfunction. This is particularly important in the context of vulnerability segmentation between plant tissues which is believed to protect more energetically ‘costly’ tissues, such as woody stems, by sacrificing ‘cheaper’ leaves early under drought conditions. Differences in vulnerability segmentation between co‐occurring plant species could explain divergent behaviours during drought, yet there are few studies considering how this characteristic may vary within a plant community. Here we investigated community‐wide vulnerability segmentation by comparing leaf/shoot and stem vulnerability in all coexistent dominant canopy and understory woody species in a diverse dry sclerophyll woodland community, including multiple angiosperms and one gymnosperm. Previously published terminal leaf/shoot vulnerability to loss of water transport capacity was compared with stem xylem vulnerability to embolism measured on the same species at the same site. We calculated hydraulic safety margins for stems to determine variation in the risk of hydraulic failure during drought among species. The xylem of all species was found to be highly resistant to hydraulic dysfunction, with only two of the eight species exhibiting significantly different vulnerability to the overall mean. No evidence of vulnerability segmentation between shoots/leaves and stems was found in seven of the eight species. Phylogenetically diverse canopy and understory species in this evergreen sclerophyll woodland appear to have evolved similar strategies of drought resistance, including low xylem vulnerability to embolism and general lack of vulnerability segmentation. This convergence in hydraulic safety indicates a lack of hydraulic niche partitioning in this woodland community. A free plain language summary can be found within the Supporting Information of this article.

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Section: Discussioncontrasting

confidence: 92%

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Lack of vulnerability segmentation among woody species in a diverse dry sclerophyll woodland community

et al. 2020

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“…First, in situ flow‐centrifuge measurements highlighted that the resistance to xylem embolism increased in both lines throughout plant development. Similar ontogenic changes in the resistance to xylem embolism have been observed in grapevine stems across the growing season (Charrier et al, ) as well as between juvenile and adult individuals of red oak (Cavender‐Bares & Bazzaz, ), laurel (Lamarque et al, ), and Tasmanian bluegum (Lucani, Brodribb, Jordan, & Mitchell, ). Although there is no clear explanation for these patterns, possible causes include increased lignification and changes in wood anatomical features through time (Lens et al, ; Li et al, ; Wheeler, Sperry, Hacke, & Hoang, ).…”

Section: Discussionsupporting

confidence: 56%

“…Preliminary tests using both standard (27‐cm large rotor) and large (42‐cm large) Cavitron (Cochard, ; Cochard et al, ) proved unsuccessful to determine maximum stem hydraulic conductivity ( k s , m 2 MPa −1 s −1 ) and construct vulnerability curves due to the open‐vessel artefact (Torres‐Ruiz et al, ). Measurements were consequently carried out using a Cavitron equipped with a 100‐cm diameter rotor (DG‐MECA, Gradignan, France), which permits proper embolism vulnerability determination in long‐vesseled species (Charrier et al, ; Lamarque et al, ). Two sets of plants differing in their development stage were compared, including five 90‐day‐old individuals per line and four and seven 170‐day‐old WT and sp12, respectively.…”

Section: Methodsmentioning

confidence: 99%

Over‐accumulation of abscisic acid in transgenic tomato plants increases the risk of hydraulic failure

Lamarque

Delzon

Toups

et al. 2020

Plant Cell & Environment

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Climate change threatens food security, and plant science researchers have investigated methods of sustaining crop yield under drought. One approach has been to overproduce abscisic acid (ABA) to enhance water use efficiency. However, the concomitant effects of ABA overproduction on plant vascular system functioning are critical as it influences vulnerability to xylem hydraulic failure. We investigated these effects by comparing physiological and hydraulic responses to water deficit between a tomato (Solanum lycopersicum) wild type control (WT) and a transgenic line overproducing ABA (sp12). Under well‐watered conditions, the sp12 line displayed similar growth rate and greater water use efficiency by operating at lower maximum stomatal conductance. X‐ray microtomography revealed that sp12 was significantly more vulnerable to xylem embolism, resulting in a reduced hydraulic safety margin. We also observed a significant ontogenic effect on vulnerability to xylem embolism for both WT and sp12. This study demonstrates that the greater water use efficiency in the tomato ABA overproducing line is associated with higher vulnerability of the vascular system to embolism and a higher risk of hydraulic failure. Integrating hydraulic traits into breeding programmes represents a critical step for effectively managing a crop's ability to maintain hydraulic conductivity and productivity under water deficit.

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“…Furthermore, our results are supported by a recent study on grapevine in which stomatal closure preceded embolism in leaves by days, and leaves were shed before a significant amount of embolism did accumulate in the stem (Hochberg et al, ; cf. Charrier et al, ). However, we acknowledge that when Ψ soil gets extremely negative, the trees will not be able to significantly uncouple their Ψ predawn / Ψ midday from the decrease in Ψ soil as long as they do not take effective means to uncouple themselves from the soil matrix (cf.…”

Section: Discussionmentioning

confidence: 99%

No role for xylem embolism or carbohydrate shortage in temperate trees during the severe 2015 drought

et al. 2018

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Temperate forests are predicted to experience an increased frequency and intensity of climate change‐induced summer droughts and heat waves in the near future. Yet, while previous studies clearly showed a high drought sensitivity of different temperate tree species, the vulnerability of the physiological integrity of these trees remains unclear. Here, we assessed the sensitivity of six temperate tree species to severe water limitation during three consecutive growing seasons, including the exceptional 2015 central European summer drought and heat wave. Specifically, we assessed stem increment growth, sap flow, water potentials, hydraulic vulnerability, and nonstructural carbohydrate contents in leaves and branches to determine how mature temperate trees responded to this exceptional weather event and how the observed responses relate to variation in xylem embolism and carbohydrate economy. We found that the trees' predawn water potentials reached their minimum values during the 2015 summer drought and most species reduced their sap flow by up to 80%. Also, increment growth was strongly impaired with the onset of the drought in all species. Despite the strong responses in the trees' growth and water relations, all species exhibited minimum midday shoot water potentials well away from values associated with severe embolism (P50). In addition, we detected no distinct decrease in nonstructural carbohydrate contents in leaves, bark, and stems throughout the drought event. Synthesis. This study shows that mature individuals of six common central European forest tree species strongly reacted to a severe summer drought by reducing their water consumption and stopping growth. We found, however, no indications for xylem embolism or carbohydrate depletion in these trees. This suggests, that xylem embolism formation and carbohydrate reserve depletion are not routine in temperate trees during seasonal strong drought and reveals a low vulnerability of the physiological integrity of temperate trees during drought events as we describe here.

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Drought will not leave your glass empty: Low risk of hydraulic failure revealed by long-term drought observations in world’s top wine regions

Abstract: Long-term observations in Napa Valley and Bordeaux reveal that grapevines never reach a lethal level of drought.

Cited by 116 publications

References 44 publications

Lack of vulnerability segmentation among woody species in a diverse dry sclerophyll woodland community

Lack of vulnerability segmentation among woody species in a diverse dry sclerophyll woodland community

Over‐accumulation of abscisic acid in transgenic tomato plants increases the risk of hydraulic failure

No role for xylem embolism or carbohydrate shortage in temperate trees during the severe 2015 drought

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