Revealing catastrophic failure of leaf networks under stress
Identifieur interne : 000495 ( Pmc/Corpus ); précédent : 000494; suivant : 000496Revealing catastrophic failure of leaf networks under stress
Auteurs : Timothy J. Brodribb ; Diane Bienaimé ; Philippe MarmottantSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2016.
Abstract
Water sustains photosynthesis and growth of land plants, but it must be transported from the soil to leaves under high tension. Drying soil leads to an increase in water tension, exposing plants to the problem of breakage of the water column, causing embolisms that cut off water supply, leading to tissue death during drought. The ability of leaves to resist embolism formation is a key adaptive axis in plant evolution, and yet the process itself has never been visualized in the leaf venation. We describe a new optical method that allows the evolution and spread of embolism in the entire leaf network to be mapped, thus revealing general rules in the sequence of leaf vein transport failure.
Url:
DOI: 10.1073/pnas.1522569113
PubMed: 27071104
PubMed Central: 4855591
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PMC:4855591Le document en format XML
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<author><name sortKey="Brodribb, Timothy J" sort="Brodribb, Timothy J" uniqKey="Brodribb T" first="Timothy J." last="Brodribb">Timothy J. Brodribb</name>
<affiliation><nlm:aff id="aff1">School of Biological Sciences,<institution>University of Tasmania</institution>
, Hobart, Tasmania 7001,<country>Australia</country>
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<author><name sortKey="Bienaime, Diane" sort="Bienaime, Diane" uniqKey="Bienaime D" first="Diane" last="Bienaimé">Diane Bienaimé</name>
<affiliation><nlm:aff id="aff2">CNRS/Université Grenoble-Alpes,<institution>Laboratoire Interdisciplinaire de Physique UMR 5588</institution>
, Grenoble, F-38401,<country>France</country>
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<author><name sortKey="Marmottant, Philippe" sort="Marmottant, Philippe" uniqKey="Marmottant P" first="Philippe" last="Marmottant">Philippe Marmottant</name>
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<affiliation><nlm:aff id="aff2">CNRS/Université Grenoble-Alpes,<institution>Laboratoire Interdisciplinaire de Physique UMR 5588</institution>
, Grenoble, F-38401,<country>France</country>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Revealing catastrophic failure of leaf networks under stress</title>
<author><name sortKey="Brodribb, Timothy J" sort="Brodribb, Timothy J" uniqKey="Brodribb T" first="Timothy J." last="Brodribb">Timothy J. Brodribb</name>
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<author><name sortKey="Bienaime, Diane" sort="Bienaime, Diane" uniqKey="Bienaime D" first="Diane" last="Bienaimé">Diane Bienaimé</name>
<affiliation><nlm:aff id="aff2">CNRS/Université Grenoble-Alpes,<institution>Laboratoire Interdisciplinaire de Physique UMR 5588</institution>
, Grenoble, F-38401,<country>France</country>
</nlm:aff>
</affiliation>
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<author><name sortKey="Marmottant, Philippe" sort="Marmottant, Philippe" uniqKey="Marmottant P" first="Philippe" last="Marmottant">Philippe Marmottant</name>
<affiliation><nlm:aff id="aff1">School of Biological Sciences,<institution>University of Tasmania</institution>
, Hobart, Tasmania 7001,<country>Australia</country>
;</nlm:aff>
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<affiliation><nlm:aff id="aff2">CNRS/Université Grenoble-Alpes,<institution>Laboratoire Interdisciplinaire de Physique UMR 5588</institution>
, Grenoble, F-38401,<country>France</country>
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<series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>Water sustains photosynthesis and growth of land plants, but it must be transported from the soil to leaves under high tension. Drying soil leads to an increase in water tension, exposing plants to the problem of breakage of the water column, causing embolisms that cut off water supply, leading to tissue death during drought. The ability of leaves to resist embolism formation is a key adaptive axis in plant evolution, and yet the process itself has never been visualized in the leaf venation. We describe a new optical method that allows the evolution and spread of embolism in the entire leaf network to be mapped, thus revealing general rules in the sequence of leaf vein transport failure.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher><publisher-name>National Academy of Sciences</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27071104</article-id>
<article-id pub-id-type="pmc">4855591</article-id>
<article-id pub-id-type="publisher-id">201522569</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1522569113</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Plant Biology</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="heading"><subject>Physical Sciences</subject>
<subj-group><subject>Environmental Sciences</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Revealing catastrophic failure of leaf networks under stress</article-title>
<alt-title alt-title-type="short">Moving embolisms visualized in droughted leaves</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Brodribb</surname>
<given-names>Timothy J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bienaimé</surname>
<given-names>Diane</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Marmottant</surname>
<given-names>Philippe</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
School of Biological Sciences,<institution>University of Tasmania</institution>
, Hobart, Tasmania 7001,<country>Australia</country>
;</aff>
<aff id="aff2"><sup>b</sup>
CNRS/Université Grenoble-Alpes,<institution>Laboratoire Interdisciplinaire de Physique UMR 5588</institution>
, Grenoble, F-38401,<country>France</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. Email: <email>timothyb@utas.edu.au</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Maarten J. Chrispeels, University of California, San Diego, La Jolla, CA, and approved March 9, 2016 (received for review November 15, 2015)</p>
</fn>
<fn fn-type="con"><p>Author contributions: T.J.B. and P.M. designed research; T.J.B., D.B., and P.M. performed research; T.J.B. and D.B. analyzed data; and T.J.B. and P.M. wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>26</day>
<month>4</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>11</day>
<month>4</month>
<year>2016</year>
</pub-date>
<volume>113</volume>
<issue>17</issue>
<fpage>4865</fpage>
<lpage>4869</lpage>
<self-uri xlink:title="pdf" xlink:href="pnas.201522569.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>Water sustains photosynthesis and growth of land plants, but it must be transported from the soil to leaves under high tension. Drying soil leads to an increase in water tension, exposing plants to the problem of breakage of the water column, causing embolisms that cut off water supply, leading to tissue death during drought. The ability of leaves to resist embolism formation is a key adaptive axis in plant evolution, and yet the process itself has never been visualized in the leaf venation. We describe a new optical method that allows the evolution and spread of embolism in the entire leaf network to be mapped, thus revealing general rules in the sequence of leaf vein transport failure.</p>
</abstract>
<abstract><p>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.</p>
</abstract>
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