Vessel‐associated cells in angiosperm xylem: Highly specialized living cells at the symplast–apoplast boundary

Morris, Hugh; Plavcová, Lenka; Gorai, Mustapha; Klepsch, Matthias; Kotowska, Martyna M.; Schenk, H. Jochen; Jansen, Steven

doi:10.1002/ajb2.1030

Cited by 60 publications

(53 citation statements)

References 120 publications

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“…Complete understanding of the underlying processes is especially challenging in woody plants owing to their large stature and presence of rigid, highly lignified cell walls that hinder methodological approaches. Despite attempts to elucidate the mechanisms of rapid transport via xylem and phloem elements (Meinzer et al ., ; Thompson & Holbrook, ; Holbrook & Zwieniecki, ; Pfautsch et al ., ), little is known regarding exchange of various molecules in trees, especially in a radial direction, at the boundary between dead and living cells (Barnett, ; Morris et al ., ). In this study, we provide first insights into the uptake of molecules at the apoplasm/symplast interface in woody tissues.…”

Section: Discussionmentioning

confidence: 97%

Endocytosis acts as transport pathway in wood

et al. 2019

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Summary In trees, dead and living cells of secondary xylem (wood) function collectively, rendering cell‐to‐cell communication challenging. Water and solutes are transported over long distances from the roots to the above‐ground organs via vessels, the main component of wood, and then radially over short distances to the neighboring cells. This enables proper functioning of trees and integrates whole‐plant activity. In this study, tracer loading, immunolocalization experiments and inhibitor assays were used to decipher the mechanisms enabling transport in wood of Acer pseudoplatanus (maple), Fraxinus excelsior (ash) and Populus tremula × tremuloides (poplar) trees. We show that tracer uptake from dead water‐conducting vessels, elements of the apoplasm, to living vessel‐associated cells (VACs) of the xylem parenchyma of the symplasm system proceeds via the endocytic pathway, including clathrin‐mediated and clathrin‐independent processes. These findings enhance our understanding of the transport pathways in complex wood tissue, providing experimental evidence of the involvement of VACs and endocytosis in radial uptake from vessels.

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Section: Discussionmentioning

confidence: 97%

Endocytosis acts as transport pathway in wood

et al. 2019

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“…4; Schenk et al, 2018), so the amounts extracted in sap may only be a small fraction of all apoplastic xylem lipids. Quantification of all apoplastic lipids in xylem would require either complete extraction from individual conduits with organic solvents and/or detergents, which could cause artifacts if these substances penetrated into living vessel-associated cells (Morris et al, 2018b), or quantification of lipids in vessel images via mass spectrometry imaging (Ellis et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…This was followed by reports of phospholipids in xylem sap and on conduit surfaces of five woody angiosperm species from diverse phylogenetic backgrounds (Schenk et al, 2017, Schenk et al, 2018). These findings raise questions about the origins of these lipids, which could be remains from previous living cell content (Scott et al, 1960; Esau, 1965; Esau et al, 1966b) or potentially be transported into vessels from conduit-associated parenchyma cells (Morris et al, 2018b). Even more important are questions about their functions in xylem (Schenk et al, 2015, Schenk et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Lipids in xylem sap of woody plants across the angiosperm phylogeny

Schenk

Michaud

Mocko

et al. 2019

Preprint

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Lipids have been observed attached to lumen-facing surfaces of mature xylem conduits of 2 several plant species, but there has been no research on their functions or effects on water 3 transport, and only one lipidomic study of the xylem apoplast. Therefore, we conducted 4 lipidomic analyses of xylem sap from seven plants representing six major angiosperm clades, 5 including basal angiosperms, monocots, and eudicots, to characterize and quantify 6 phospholipids, galactolipids, and sulfolipids in sap. We also imaged locations of lipids in vessels 7 of Laurus nobilis using confocal and transmission electron microscopy (TEM). Xylem sap was 8 extracted from cut woody stems, partially freeze-dried to concentrate the sap, extracted, and 9 analyzed via mass spectrometry. Lipids were imaged in xylem using TEM and confocal 10 microscopy. Lipids in xylem sap included the galactolipids di-and mono-11 galactosyldiacylglycerol (DGDG and MGDG), as well as all common plant phospholipids, but 12 only traces of sulfolipids, with total lipid concentrations ranging from 0.18 to 0.63 µmol / L 13 across all seven species. Lipid layers coated all lumen-facing vessel surfaces of Laurus nobilis, 14 and lipids were highly concentrated in inter-vessel pits. The findings suggest that apoplastic, 15 amphiphilic xylem lipids are a universal feature of angiosperms. They are concentrated in inter-16 vessel pits, where their low surface tension is likely to affect bubble entry via air seeding from 17gas-filled conduits. The findings force a reinterpretation of the cohesion-tension theory of water 18 transport to account for the effects of apoplastic lipids on the dynamic surface tension in the 19 xylem and on hydraulic conductance through inter-vessel pits.

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“…Dead xylem conduits are the products of programmed cell death, and the chemistry and ultrastructure of walls and pit membranes are products of the processes involved (Esau et al, 1966a, b;Bollhöner et al, 2012). Lipids and proteins observed in vessels are also likely to be products of living xylem cells, the living precursors of dead conduit cells (Esau, 1965;Esau et al, 1966b), and most likely vessel-associated cells (Morris et al, 2018). Even the dead part of xylem is very close to many living cells, and it would be a mistake to assume that sap flow through this system is governed exclusively by physical forces.…”

Section: Possible Functional Implications Of the Findingsmentioning

confidence: 99%

From the sap's perspective: The nature of vessel surfaces in angiosperm xylem

Schenk

Espino

Rich‐Cavazos

et al. 2018

American J of Botany

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Plant xylem is a unique evolutionary invention: It functions as a negative pressure hydraulic system that can move vast quantities of water and solutes over distances longer than 100 m. No other kind of organism transports liquids under negative pressure, and the most successful attempts to build an artificial negative pressure hydraulic system succeeded only to move a small amount of water over a few centimeters in a single microchannel (Wheeler and Stroock, 2008). That experiment proved that it is possible to move water under negative pressure, but it left the question unanswered how plants can do this so effectively and over such long distances. Somehow plants manage to move large volumes of water in heterogeneous channels that range in diameter from nanometers to a few hundred micrometers, that is, in nanofluidic and microfluidic systems where water moves very close to surfaces of other phases, both solid and gas (Eijkel and van den Berg, 2005;Squires and Quake, 2005). Plants move all this water efficiently along these phase surfaces without constantly creating gas bubbles in the system . What do we actually know about these surfaces in xylem conduits (i.e., vessels and tracheids)? INVITED SPECIAL ARTICLE PREMISE OF THE STUDY:Xylem sap in angiosperms moves under negative pressure in conduits and cell wall pores that are nanometers to micrometers in diameter, so sap is always very close to surfaces. Surfaces matter for water transport because hydrophobic ones favor nucleation of bubbles, and surface chemistry can have strong effects on flow. Vessel walls contain cellulose, hemicellulose, lignin, pectins, proteins, and possibly lipids, but what is the nature of the inner, lumen-facing surface that is in contact with sap?METHODS: Vessel lumen surfaces of five angiosperms from different lineages were examined via transmission electron microscopy and confocal and fluorescence microscopy, using fluorophores and autofluorescence to detect cell wall components. Elemental composition was studied by energy-dispersive X-ray spectroscopy, and treatments with phospholipase C (PLC) were used to test for phospholipids.KEY RESULTS: Vessel surfaces consisted mainly of lignin, with strong cellulose signals confined to pit membranes. Proteins were found mainly in inter-vessel pits and pectins only on outer rims of pit membranes and in vessel-parenchyma pits. Continuous layers of lipids were detected on most vessel surfaces and on most pit membranes and were shown by PLC treatment to consist at least partly of phospholipids. CONCLUSIONS:Vessel surfaces appear to be wettable because lignin is not strongly hydrophobic and a coating with amphiphilic lipids would render any surface hydrophilic. New questions arise about these lipids and their possible origins from living xylem cells, especially about their effects on surface tension, surface bubble nucleation, and pit membrane function.

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Vessel‐associated cells in angiosperm xylem: Highly specialized living cells at the symplast–apoplast boundary

Cited by 60 publications

References 120 publications

Endocytosis acts as transport pathway in wood

Endocytosis acts as transport pathway in wood

Lipids in xylem sap of woody plants across the angiosperm phylogeny

From the sap's perspective: The nature of vessel surfaces in angiosperm xylem

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