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Revealing catastrophic failure of leaf networks under stress.

ABSTRACT: The intricate patterns of veins that adorn the leaves of land plants are among the most important networks in biology. Water flows in these leaf irrigation networks under tension and is vulnerable to embolism-forming cavitations, which cut off water supply, ultimately causing leaf death. Understanding the ways in which plants structure their vein supply network to protect against embolism-induced failure has enormous ecological and evolutionary implications, but until now there has been no way of observing dynamic failure in natural leaf networks. Here we use a new optical method that allows the initiation and spread of embolism bubbles in the leaf network to be visualized. Examining embolism-induced failure of architecturally diverse leaf networks, we found that conservative rules described the progression of hydraulic failure within veins. The most fundamental rule was that within an individual venation network, susceptibility to embolism always increased proportionally with the size of veins, and initial nucleation always occurred in the largest vein. Beyond this general framework, considerable diversity in the pattern of network failure was found between species, related to differences in vein network topology. The highest-risk network was found in a fern species, where single events caused massive disruption to leaf water supply, whereas safer networks in angiosperm leaves contained veins with composite properties, allowing a staged failure of water supply. These results reveal how the size structure of leaf venation is a critical determinant of the spread of embolism damage to leaves during drought.

SUBMITTER: Brodribb TJ

PROVIDER: S-EPMC4855591 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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Revealing catastrophic failure of leaf networks under stress.

Brodribb Timothy J TJ Bienaimé Diane D Marmottant Philippe P

Proceedings of the National Academy of Sciences of the United States of America 20160411 17

The intricate patterns of veins that adorn the leaves of land plants are among the most important networks in biology. Water flows in these leaf irrigation networks under tension and is vulnerable to embolism-forming cavitations, which cut off water supply, ultimately causing leaf death. Understanding the ways in which plants structure their vein supply network to protect against embolism-induced failure has enormous ecological and evolutionary implications, but until now there has been no way o ...[more]

PMID: 27071104

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Project description:BackgroundBrassica carinata (A) Braun has recently gained increased attention across the world as a sustainable biofuel crop. B. carinata is grown as a summer crop in many regions where high temperature is a significant stress during the growing season. However, little research has been conducted to understand the mechanisms through which this crop responds to high temperatures. Understanding traits that improve the high-temperature adaption of this crop is essential for developing heat-tolerant varieties. This study investigated lipid remodeling in B. carinata in response to high-temperature stress. A commercial cultivar, Avanza 641, was grown under sunlit-controlled environmental conditions in Soil-Plant-Atmosphere-Research (SPAR) chambers under optimal temperature (OT; 23/15°C) conditions. At eight days after sowing, plants were exposed to one of the three temperature treatments [OT, high-temperature treatment-1 (HT-1; 33/25°C), and high-temperature treatment-2 (HT-2; 38/30°C)]. The temperature treatment period lasted until the final harvest at 84 days after sowing. Leaf samples were collected at 74 days after sowing to profile lipids using electrospray-ionization triple quadrupole mass spectrometry.ResultsTemperature treatment significantly affected the growth and development of Avanza 641. Both high-temperature treatments caused alterations in the leaf lipidome. The alterations were primarily manifested in terms of decreases in unsaturation levels of membrane lipids, which was a cumulative effect of lipid remodeling. The decline in unsaturation index was driven by (a) decreases in lipids that contain the highly unsaturated linolenic (18:3) acid and (b) increases in lipids containing less unsaturated fatty acids such as oleic (18:1) and linoleic (18:2) acids and/or saturated fatty acids such as palmitic (16:0) acid. A third mechanism that likely contributed to lowering unsaturation levels, particularly for chloroplast membrane lipids, is a shift toward lipids made by the eukaryotic pathway and the channeling of eukaryotic pathway-derived glycerolipids that are composed of less unsaturated fatty acids into chloroplasts.ConclusionsThe lipid alterations appear to be acclimation mechanisms to maintain optimal membrane fluidity under high-temperature conditions. The lipid-related mechanisms contributing to heat stress response as identified in this study could be utilized to develop biomarkers for heat tolerance and ultimately heat-tolerant varieties.

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Revealing catastrophic failure of leaf networks under stress.

Publications

Revealing catastrophic failure of leaf networks under stress.

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