<i>In situ</i>microscopy reveals reversible cell wall swelling in kelp sieve tubes: one mechanism for turgor generation and flow control?

Knoblauch, Jan; Drobnitch, Sarah Tepler; Peters, Winfried S.; Knoblauch, Michael

doi:10.1111/pce.12736

Cited by 16 publications

(16 citation statements)

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“…Wounds can alter the translocation of materials (sugars, nutrients) within the frond or, if significant enough, cause the kelp to devote energy toward growing new fronds (i.e. a branching response) rather than continue growing the wounded frond (Sargent and Lantrip, 1952;Black, 1974;Fox, 2013;Knoblauch et al, 2016), but there was no evidence of altered growth in the individuals used in our study. Overall, wounded and healed tissues were able to resist both slow and fast strain rates, suggesting that the kelp's healing mechanism is sufficient to reduce the risk of the frond breaking from different loading regimes, such as the wave surge (slow rate of loading) and wave impingement (fast rate of loading) portions of a wave cycle (Gaylord, 1999;Gaylord et al, 2008;Jensen and Denny, 2015).…”

Section: Effects Of Wounds On Materials Propertiesmentioning

confidence: 76%

Mechanical properties of the wave-swept kelp, Egregia menziesii, change with season, growth rate, and herbivore wounds

Burnett

Koehl

2019

Journal of Experimental Biology

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The resistance of macroalgae to damage by hydrodynamic forces depends on the mechanical properties of their tissues. Although factors such as water-flow environment, algal growth rate and damage by herbivores have been shown to influence various material properties of macroalgal tissues, the interplay of these factors as they change seasonally and affect algal mechanical performance has not been worked out. We used the perennial kelp Egregia menziesii to study how the material properties of the rachis supporting a frond changed seasonally over a 2 year period, and how those changes correlated with seasonal patterns of the environment, growth rate and herbivore load. Rachis tissue became stiffer, stronger and less extensible with age (distance from the meristem). Thus, slowly growing rachises were stiffer, stronger and tougher than rapidly growing ones. Growth rates were highest in spring and summer when upwelling and long periods of daylight occurred. Therefore, rachis tissue was most resistant to damage in the winter, when waves were large as a result of seasonal storms. Herbivory was greatest during summer, when rachis growth rates were high. Unlike other macroalgae, E. menziesii did not respond to herbivore damage by increasing rachis tissue strength, but rather by growing in width so that the cross-sectional area of the wounded rachis was increased. The relative timing of environmental factors that affect growth rates (e.g. upwelling supply of nutrients, daylight duration) and of those that can damage macroalgae (e.g. winter storms, summer herbivore outbreaks) can influence the material properties and thus the mechanical performance of macroalgae.

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Section: Effects Of Wounds On Materials Propertiesmentioning

confidence: 76%

Mechanical properties of the wave-swept kelp, Egregia menziesii, change with season, growth rate, and herbivore wounds

Burnett

Koehl

2019

Journal of Experimental Biology

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“…6) is that the more elastic inner cell wall might facilitate the optimization of cytoplasmic diameter via dilation/contraction of the cell wall in response to altered turgor pressure. The radial distribution of elastic properties may buffer immediate changes in turgor such as diurnal rhythms of phloem and xylem pressure resulting in reversible swelling of sieve tube cell walls (Pfautsch et al, 2015;Knoblauch et al, 2016).…”

Section: Specific Modulation Of Galactan With Regard To Phloem Functionmentioning

confidence: 99%

Branched Pectic Galactan in Phloem-Sieve-Element Cell Walls: Implications for Cell Mechanics

et al. 2017

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A major question in plant biology concerns the specification and functional differentiation of cell types. This is in the context of constraints imposed by networks of cell walls that both adhere cells and contribute to the form and function of developing organs. Here, we report the identification of a glycan epitope that is specific to phloem sieve element cell walls in several systems. A monoclonal antibody, designated LM26, binds to the cell wall of phloem sieve elements in stems of Arabidopsis (Arabidopsis thaliana), Miscanthus x giganteus, and notably sugar beet (Beta vulgaris) roots where phloem identification is an important factor for the study of phloem unloading of Suc. Using microarrays of synthetic oligosaccharides, the LM26 epitope has been identified as a b-1,6-galactosyl substitution of b-1,4-galactan requiring more than three backbone residues for optimized recognition. This branched galactan structure has previously been identified in garlic (Allium sativum) bulbs in which the LM26 epitope is widespread throughout most cell walls including those of phloem cells. Garlic bulb cell wall material has been used to confirm the association of the LM26 epitope with cell wall pectic rhamnogalacturonan-I polysaccharides. In the phloem tissues of grass stems, the LM26 epitope has a complementary pattern to that of the LM5 linear b-1,4-galactan epitope, which is detected only in companion cell walls. Mechanical probing of transverse sections of M. x giganteus stems and leaves by atomic force microscopy indicates that phloem sieve element cell walls have a lower indentation modulus (indicative of higher elasticity) than companion cell walls.

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“…Conversely, the wall swelling effects Zimmermann () depicted seem markedly similar to those found in sieve tubes of brown algae of the order Laminariales (Figure ). In these kelps, sieve tube walls swell reversibly in response to changes in intracellular pressure (Knoblauch et al , ). For over a century, phycologists have documented various stages of wall swelling in kelp sieve tubes, apparently without ever noticing the underlying process (Knoblauch and Peters, ).…”

Section: Introductionmentioning

confidence: 99%

“…(a) Two adjacent sieve elements of Macrocystis pyrifera with thickened walls (Sykes, , plate XIX figure 31). (b) Light micrograph of two adjacent sieve elements in Nereocystis luetkeana , as described by Knoblauch et al (). The lateral wall of the upper sieve element has swollen in response to injury, while the lower one shows the normal thin‐walled habit.…”

Section: Introductionmentioning

confidence: 99%

“…Due to the extreme sensitivity of the symplasmic sieve tube network that functions as a whole, the activities of fully functional sieve tubes can only be monitored by advanced microscopy methods in whole plants (Truernit, ). In situ microscopy is technically demanding and has been successful in a limited number of species, including Arabidopsis thaliana (Oparka et al , ; Froelich et al , ), the legume Vicia faba (Knoblauch and van Bel, ), the squash Cucurbita maxima (Furch et al , ), the morning glory Ipomoea nil (Knoblauch et al , ), and the kelp Nereocystis luetkeana (Knoblauch et al , ). Vines like I. nil lend themselves comparatively well to in situ microscopy, as their flexible shoots can be mounted on microscope stages with minimal disturbance of the rest of the plant (Knoblauch et al , ).…”

Section: Introductionmentioning

confidence: 99%

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Sieve elements rapidly develop ‘nacreous walls’ following injury − a common wounding response?

Knoblauch

Vasina

et al. 2020

The Plant Journal

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Thick glistening cell walls occur in sieve tubes of all major land plant taxa. Historically, these 'nacreous walls' have been considered a diagnostic feature of sieve elements; they represent a conundrum, though, in the context of the widely accepted pressure-flow theory as they severely constrict sieve tubes. We employed the cucurbit Gerrardanthus macrorhizus as a model to study nacreous walls in sieve elements by standard and in situ confocal microscopy and electron microscopy, focusing on changes in functional sieve tubes that occur when prepared for microscopic observation. Over 90% of sieve elements in tissue sections processed for microscopy by standard methods exhibit nacreous walls. Sieve elements in whole, live plants that were actively transporting as shown by phloem-mobile tracers, lacked nacreous walls and exhibited open lumina of circular cross-sections instead, an appropriate structure for M€ unch-type mass flow of the cell contents. Puncturing of transporting sieve elements with micropipettes triggered the rapid (<1 min) development of nacreous walls that occluded the cell lumen almost completely. We conclude that nacreous walls are preparation artefacts rather than structural features of transporting sieve elements. Nacreous walls in land plants resemble the reversibly swellable walls found in various algae, suggesting that they may function in turgor buffering, the amelioration of osmotic stress, wounding-induced sieve tube occlusion, and possibly local defence responses of the phloem.

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In situmicroscopy reveals reversible cell wall swelling in kelp sieve tubes: one mechanism for turgor generation and flow control?

Cited by 16 publications

References 64 publications

Mechanical properties of the wave-swept kelp, Egregia menziesii, change with season, growth rate, and herbivore wounds

Mechanical properties of the wave-swept kelp, Egregia menziesii, change with season, growth rate, and herbivore wounds

Branched Pectic Galactan in Phloem-Sieve-Element Cell Walls: Implications for Cell Mechanics

Sieve elements rapidly develop ‘nacreous walls’ following injury − a common wounding response?

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