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Inferring the role of pit membranes in solute transport from solute exclusion studies in living conifer stems.

ABSTRACT: The functional role of pits between living and dead cells has been inferred from anatomical studies but amassing physiological evidence has been challenging. Centrifugation methods were used to strip water from xylem conduits, permitting a more quantitative gravimetric determination of the water and solid contents of cell walls than is possible by more traditional methods. Quantitative anatomical evidence was used to evaluate the water volume in xylem conduits and the water content of living cells. Quantitative perfusion of stems with polyethylene glycol of different molecular weight was used to determine the solute-free space. We measured the portioning of water and solute-free space among anatomical components in stems and demonstrated that lignin impeded the free movement of solutes with molecular weight >300. Hence, movement of large solutes from living cells to xylem conduits is necessarily confined to pit structures that permit transmembrane solute transport via primary walls without lignin. The functional role of pits was additionally indicated by combining data in this paper with previous studies of unusual osmotic relationships in woody species that lack pits between dead wood fibers and vessels. The absence of pits, combined with the evidence of exclusion of solutes of molecular weight >300, explains the unexpected osmotic properties.

SUBMITTER: Yang D

PROVIDER: S-EPMC7210765 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Inferring the role of pit membranes in solute transport from solute exclusion studies in living conifer stems.

Yang Dongmei D Wei Kailu K Li Junhui J Peng Guoquan G Tyree Melvin T MT

Journal of experimental botany 20200501 9

The functional role of pits between living and dead cells has been inferred from anatomical studies but amassing physiological evidence has been challenging. Centrifugation methods were used to strip water from xylem conduits, permitting a more quantitative gravimetric determination of the water and solid contents of cell walls than is possible by more traditional methods. Quantitative anatomical evidence was used to evaluate the water volume in xylem conduits and the water content of living cel ...[more]

PMID: 32020191

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Project description:Background and aimsThe ability to avoid drought-induced embolisms in the xylem is one of the essential traits for plants to survive periods of water shortage. Over the past three decades, hydraulic studies have been focusing on trees, which limits our ability to understand how herbs tolerate drought. Here we investigate the embolism resistance in inflorescence stems of four Arabidopsis thaliana accessions that differ in growth form and drought response. We assess functional traits underlying the variation in embolism resistance amongst the accessions studied using detailed anatomical observations.MethodsVulnerability to xylem embolism was evaluated via vulnerability curves using the centrifuge technique and linked with detailed anatomical observations in stems using light microscopy and transmission electron microscopy.Key resultsThe data show significant differences in stem P50, varying 2-fold from -1.58 MPa in the Cape Verde Island accession to -3.07 MPa in the woody soc1 ful double mutant. Out of all the anatomical traits measured, intervessel pit membrane thickness (TPM) best explains the differences in P50, as well as P12 and P88. The association between embolism resistance and TPM can be functionally explained by the air-seeding hypothesis. There is no evidence that the correlation between increased woodiness and increased embolism resistance is directly related to functional aspects. However, we found that increased woodiness is strongly linked to other lignification characters, explaining why mechanical stem reinforcement is indirectly related to increased embolism resistance.ConclusionsThe woodier or more lignified accessions are more resistant to embolism than the herbaceous accessions, confirming the link between increased stem lignification and increased embolism resistance, as also observed in other lineages. Intervessel pit membrane thickness and, to a lesser extent, theoretical vessel implosion resistance and vessel wall thickness are the missing functional links between stem lignification and embolism resistance.

Project description:Osteocytes, the most abundant cells in bone, are essential in maintaining tissue homeostasis and orchestrating bone's mechanical adaptation. Osteocytes depend upon load-induced convection within the lacunar-canalicular system (LCS) to maintain viability and to sense their mechanical environment. Using the fluorescence recovery after photobleaching (FRAP) imaging approach, we previously quantified the convection of a small tracer (sodium fluorescein, 376 Da) in the murine tibial LCS under intermittent cyclic loading. In the present study, we first expanded the investigation of solute transport using a larger tracer (parvalbumin, 12.3 kDa), which is comparable in size to some signaling proteins secreted by osteocytes. Murine tibiae were subjected to sequential FRAP tests under rest-inserted cyclic loading while the loading magnitude (0, 2.8, or 4.8 N) and frequency (0.5, 1, or 2 Hz) were varied. The characteristic transport rate k and the transport enhancement relative to diffusion (k/k0) were measured under each loading condition, from which the peak solute velocity in the LCS was derived using our LCS transport model. Both the transport enhancement and solute velocity increased with loading magnitude and decreased with loading frequency. Furthermore, the solute-matrix interaction, quantified in terms of the reflection coefficient through the osteocytic pericellular matrix (PCM), was measured and theoretically modeled. The reflection coefficient of parvalbumin (? = 0.084) was derived from the differential fluid and solute velocities within loaded bone. Using a newly developed PCM sieving model, the PCM's fiber configurations accounting for the measured interactions were obtained for the first time. The present study provided not only new data on the micro-fluidic environment experienced by osteocytes in situ but also a powerful quantitative tool for future study of the PCM, the critical interface that controls both outside-in and inside-out signaling in osteocytes during normal bone adaptation and in pathological conditions.

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Inferring the role of pit membranes in solute transport from solute exclusion studies in living conifer stems.

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Inferring the role of pit membranes in solute transport from solute exclusion studies in living conifer stems.

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