Combined impacts of irradiance and dehydration on leaf hydraulic conductance: insights into vulnerability and stomatal control

Guyot, Gaëlle; Scoffoni, Christine; Sack, Lawren

doi:10.1111/j.1365-3040.2011.02458.x

Cited by 116 publications

(141 citation statements)

References 87 publications

(227 reference statements)

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“…In that study, leaves were acclimated under low irradiance (less than 100 mmol quanta m 22 s 21 ). For many species, K leaf in hydrated leaves can be enhanced by many fold under high irradiance likely due to aquaporin expression (Cochard et al, 2007;Scoffoni et al, 2008;Maurel et al, 2015) and such high-light-acclimated leaves show stronger vulnerability before the turgor loss point (Guyot et al, 2012;Sack et al, 2016b). Similarly, a recent study partitioning the vulnerabilities of K x and K ox found that K ox was the strongest determinant of K leaf decline in two of four species (Trifiló et al, 2016), and, for the other two species, both xylem and outsidexylem pathways appeared to be strong drivers of K leaf decline.…”

Section: Resultsmentioning

confidence: 99%

“…The day before any of the measurements described below, shoots with a minimum of three nodes of stem below the leaves to be studied were excised in air from at least three individuals and transported in dark plastic bags filled with wet paper towels, where the shoot was recut underwater by a minimum of two nodes from the base and left to rehydrate overnight. We note that, although obtained in different years, both leaf and xylem hydraulic vulnerability curves were obtained from the same individuals, and no differences were found in K leaf values across years (Scoffoni et al, 2011;Guyot et al, 2012).…”

Section: Plant Materialsmentioning

confidence: 88%

“…Recent work has proposed that outside-xylem hydraulic decline may play a role in K leaf decline (Sade et al, 2014;Scoffoni et al, 2014;HernandezSantana et al, 2016;Trifiló et al, 2016). A study that partitioned the vulnerability of K leaf into that of K x and K ox (Trifiló et al, 2016) found that both contributed, depending on species, but measurements were made under low irradiance, which would minimize the response of K ox before the turgor loss point (Guyot et al, 2012;Sack et al, 2016b). A strong test of the relative roles of K x and K ox depends on their determination for illuminated leaves coupled with direct observations of the formation of emboli in the xylem.…”

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confidence: 99%

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Outside-Xylem Vulnerability, Not Xylem Embolism, Controls Leaf Hydraulic Decline during Dehydration

et al. 2017

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Leaf hydraulic supply is crucial to maintaining open stomata for CO 2 capture and plant growth. During drought-induced dehydration, the leaf hydraulic conductance (K leaf ) declines, which contributes to stomatal closure and, eventually, to leaf death. Previous studies have tended to attribute the decline of K leaf to embolism in the leaf vein xylem. We visualized at high resolution and quantified experimentally the hydraulic vulnerability of xylem and outside-xylem pathways and modeled their respective influences on plant water transport. Evidence from all approaches indicated that the decline of K leaf during dehydration arose first and foremost due to the vulnerability of outside-xylem tissues. In vivo x-ray microcomputed tomography of dehydrating leaves of four diverse angiosperm species showed that, at the turgor loss point, only small fractions of leaf vein xylem conduits were embolized, and substantial xylem embolism arose only under severe dehydration. Experiments on an expanded set of eight angiosperm species showed that outside-xylem hydraulic vulnerability explained 75% to 100% of K leaf decline across the range of dehydration from mild water stress to beyond turgor loss point. Spatially explicit modeling of leaf water transport pointed to a role for reduced membrane conductivity consistent with published data for cells and tissues. Plant-scale modeling suggested that outside-xylem hydraulic vulnerability can protect the xylem from tensions that would induce embolism and disruption of water transport under mild to moderate soil and atmospheric droughts. These findings pinpoint outside-xylem tissues as a central locus for the control of leaf and plant water transport during progressive drought.

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Section: Resultsmentioning

confidence: 99%

Section: Plant Materialsmentioning

confidence: 88%

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confidence: 99%

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Outside-Xylem Vulnerability, Not Xylem Embolism, Controls Leaf Hydraulic Decline during Dehydration

et al. 2017

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“…Although some of these species also had very vulnerable leaves at P k50 of 21 MPa or greater (Hao et al, 2008;Chen et al, 2009;Blackman et al, 2012;Guyot et al, 2012), the majority of previously studied species exhibited P k50 of 21.5 MPa or less and down to 24.3 MPa (Sack and Holbrook, 2006;Blackman et al, 2010;Johnson et al, 2012;Nardini et al, 2012;Bucci et al, 2013). Accordingly, stems were typically also more vulnerable to drought-induced hydraulic failure in herbs (21 to 23.8 MPa; Kocacinar and Sage, 2003;Rosenthal et al, 2010;Tixier et al, 2013;Nolf et al, 2014) Leaf hydraulic analysis in our study showed that all three Ranunculus spp.…”

Section: Discussionmentioning

confidence: 99%

Herb Hydraulics: Inter- and Intraspecific Variation in Three Ranunculus Species

et al. 2016

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(S.M.).The requirements of the water transport system of small herbaceous species differ considerably from those of woody species. Despite their ecological importance for many biomes, knowledge regarding herb hydraulics remains very limited. We compared key hydraulic features (vulnerability to drought-induced hydraulic decline, pressure-volume relations, onset of cellular damage, in situ variation of water potential, and stomatal conductance) of three Ranunculus species differing in their soil humidity preferences and ecological amplitude. All species were very vulnerable to water stress (50% reduction in whole-leaf hydraulic conductance [k leaf ] at 20.2 to 20.8 MPa). In species with narrow ecological amplitude, the drought-exposed Ranunculus bulbosus was less vulnerable to desiccation (analyzed via loss of k leaf and turgor loss point) than the humidhabitat Ranunculus lanuginosus. Accordingly, water stress-exposed plants from the broad-amplitude Ranunculus acris revealed tendencies toward lower vulnerability to water stress (e.g. osmotic potential at full turgor, cell damage, and stomatal closure) than conspecific plants from the humid site. We show that small herbs can adjust to their habitat conditions on interspecific and intraspecific levels in various hydraulic parameters. The coordination of hydraulic thresholds (50% and 88% loss of k leaf , turgor loss point, and minimum in situ water potential) enabled the study species to avoid hydraulic failure and damage to living cells. Reversible recovery of hydraulic conductance, desiccation-tolerant seeds, or rhizomes may allow them to prioritize toward a more efficient but vulnerable water transport system while avoiding the severe effects that water stress poses on woody species.

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“…In particular, the evaporative flux method requires steady-state transpiration and stable leaf water potential to enable the determination of K leaf . We followed the procedure tested and established for a wide range of species in previous work (Scoffoni et al, 2008Pasquet-Kok et al, 2010;Guyot et al, 2012). In measuring K leaf , 30 min was chosen as a minimum to ensure that leaves had acclimated to high irradiance and stomatal conductance had stabilized.…”

Section: Empirical Measurements Of K Oxmentioning

confidence: 99%

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

et al. 2015

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Leaves are arguably the most complex and important physicobiological systems in the ecosphere. Yet, water transport outside the leaf xylem remains poorly understood, despite its impacts on stomatal function and photosynthesis. We applied anatomical measurements from 14 diverse species to a novel model of water flow in an areole (the smallest region bounded by minor veins) to predict the impact of anatomical variation across species on outside-xylem hydraulic conductance (K ox ). Several predictions verified previous correlational studies: (1) vein length per unit area is the strongest anatomical determinant of K ox , due to effects on hydraulic pathlength and bundle sheath (BS) surface area; (2) palisade mesophyll remains well hydrated in hypostomatous species, which may benefit photosynthesis, (3) BS extensions enhance K ox ; and (4) the upper and lower epidermis are hydraulically sequestered from one another despite their proximity. Our findings also provided novel insights: (5) the BS contributes a minority of outside-xylem resistance; (6) vapor transport contributes up to two-thirds of K ox ; (7) K ox is strongly enhanced by the proximity of veins to lower epidermis; and (8) K ox is strongly influenced by spongy mesophyll anatomy, decreasing with protoplast size and increasing with airspace fraction and cell wall thickness. Correlations between anatomy and K ox across species sometimes diverged from predicted causal effects, demonstrating the need for integrative models to resolve causation. For example, (9) K ox was enhanced far more in heterobaric species than predicted by their having BS extensions. Our approach provides detailed insights into the role of anatomical variation in leaf function.

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Combined impacts of irradiance and dehydration on leaf hydraulic conductance: insights into vulnerability and stomatal control

Cited by 116 publications

References 87 publications

Outside-Xylem Vulnerability, Not Xylem Embolism, Controls Leaf Hydraulic Decline during Dehydration

Outside-Xylem Vulnerability, Not Xylem Embolism, Controls Leaf Hydraulic Decline during Dehydration

Herb Hydraulics: Inter- and Intraspecific Variation in Three Ranunculus Species

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

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