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  • Polysaccharide compositions of Collenchyma cell walls from celery (Apium graveolens L.) petioles
    2020
    Co-Authors: Da Chen, Ian Sims, Zoran Zujovic, Pj Harris, Ld Melton
    Abstract:

    © The Author(s). 2017. Background: Collenchyma serves as a mechanical support tissue for many herbaceous plants. Previous work based on solid-state NMR and immunomicroscopy suggested Collenchyma cell walls (CWs) may have similar polysaccharide compositions to those commonly found in eudicotyledon parenchyma walls, but no detailed chemical analysis was available. In this study, compositions and structures of cell wall polysaccharides of peripheral Collenchyma from celery petioles were investigated. Results: This is the first detailed investigation of the cell wall composition of Collenchyma from any plant. Celery petioles were found to elongate throughout their length during early growth, but as they matured elongation was increasingly confined to the upper region, until elongation ceased. Mature, fully elongated, petioles were divided into three equal segments, upper, middle and lower, and peripheral Collenchyma strands isolated from each. Cell walls (CWs) were prepared from the strands, which also yielded a HEPES buffer soluble fraction. The CWs were sequentially extracted with CDTA, Na2CO3, 1 M KOH and 4 M KOH. Monosaccharide compositions of the CWs showed that pectin was the most abundant polysaccharide [with homogalacturonan (HG) more abundant than rhamnogalacturonan I (RG-I) and rhamnogalacturonan II (RG-II)], followed by cellulose, and other polysaccharides, mainly xyloglucans, with smaller amounts of heteroxylans and heteromannans. CWs from different segments had similar compositions, but those from the upper segments had slightly more pectin than those from the lower two segments. Further, the pectin in the CWs of the upper segment had a higher degree of methyl esterification than the other segments. In addition to the anticipated water-soluble pectins, the HEPES-soluble fractions surprisingly contained large amounts of heteroxylans. The CDTA and Na2CO3 fractions were rich in HG and RG-I, the 1 M KOH fraction had abundant heteroxylans, the 4 M KOH fraction was rich in xyloglucan and heteromannans, and cellulose was predominant in the final residue. The structures of the xyloglucans, heteroxylans and heteromannans were deduced from the linkage analysis and were similar to those present in most eudicotyledon parenchyma CWs. Cross polarization with magic angle spinning (CP/MAS) NMR spectroscopy showed no apparent difference in the rigid and semi-rigid polysaccharides in the CWs of the three segments. Single-pulse excitation with magic-angle spinning (SPE/MAS) NMR spectroscopy, which detects highly mobile polysaccharides, showed the presence of arabinan, the detailed structure of which varied among the cell walls from the three segments. Conclusions: Celery Collenchyma CWs have similar polysaccharide compositions to most eudicotyledon parenchyma CWs. However, celery Collenchyma CWs have much higher XG content than celery parenchyma CWs. The degree of methyl esterification of pectin and the structures of the arabinan side chains of RG-I show some variation in the Collenchyma CWs from the different segments. Unexpectedly, the HEPES-soluble fraction contained a large amount of heteroxylans.

  • Changes in the orientations of cellulose microfibrils during the development of Collenchyma cell walls of celery (Apium graveolens L.)
    Planta, 2019
    Co-Authors: Da Chen, Laurence D. Melton, Duncan J. Mcgillivray, Timothy M. Ryan, Philip J. Harris
    Abstract:

    Main conclusion During development, cellulose microfibrils in Collenchyma walls become increasingly longitudinal, as determined by small-angle X-ray scattering, despite the walls maintaining a fine structure indicative of a crossed-polylamellate structure. Abstract Collenchyma cells have thickened primary cell walls and provide mechanical support during plant growth. During their development, these cells elongate and their walls thicken considerably. We used microscopy and synchrotron small-angle X-ray scattering to study changes in the orientations of cellulose microfibrils that occur during development in the walls of Collenchyma cells present in peripheral strands in celery ( Apium graveolens ) petioles. Transmission electron microscopy showed that the walls consisted of many lamellae (polylamellate), with lamellae containing longitudinally oriented cellulose microfibrils alternating with microfibrils oriented at higher angles. The lamellae containing longitudinally oriented microfibrils predominated at later stages of development. Nevertheless, transmission electron microscopy of specially stained, oblique sections provided evidence that the cellulose microfibrils were ordered throughout development as crossed-polylamellate structures. These results are consistent with our synchrotron small-angle X-ray scattering results that showed the cellulose microfibrils become oriented increasingly longitudinally during development. Some passive reorientation of cellulose microfibrils may occur during development, but extensive reorientation throughout the wall would destroy ordered structures. Atomic force microscopy and field emission scanning electron microscopy were used to determine the orientations of newly deposited cellulose microfibrils. These were found to vary widely among different cells, which could be consistent with the formation of crossed-polylamellate structures. These newly deposited cellulose microfibrils are deposited in a layer of pectic polysaccharides that lies immediately outside the plasma membrane. Overall, our results show that during development of Collenchyma walls, the cellulose microfibrils become increasingly longitudinal in orientation, yet organized, crossed-polylamellate structures are maintained.

  • Developmental changes in Collenchyma cell-wall polysaccharides in celery (Apium graveolens L.) petioles.
    BMC Plant Biology, 2019
    Co-Authors: Da Chen, Zoran D. Zujovic, Laurence D. Melton, Philip J. Harris
    Abstract:

    Collenchyma cells occur widely in eudicotyledons and provide mechanical support for growing organs. At maturity, the cells are elongated and have thick, non-lignified walls, which in celery contain cellulose and pectic polysaccharides, together with xyloglucans and heteroxylans and heteromannans. A previous study suggested that at least some of the Collenchyma cell wall in celery is laid down after expansion has stopped and is thus secondary. In the present study, we re-examined this. We used chemical analysis and immunomicroscopy to determine changes in the polysaccharide compositions of these walls during development. Additionally, solid-state NMR spectroscopy was used to examine changes in polysaccharide mobilities during development. We showed the Collenchyma walls are deposited only during cell expansion, i.e. they are primary walls. During cell-wall development, analytical and immunomicroscopy studies showed that within the pectic polysaccharides there were no overall changes in the proportions of homogalacturonans, but there was a decrease in their methyl esterification. There was also a decrease in the proportions of the (1 → 5)-α-l-arabinan and (1 → 4)-β-d-galactan side chains of rhamnogalacturonan I. The proportions of cellulose increased, and to a lesser extent those of xyloglucans and heteroxylans. Immunomicroscopy showed the homogalacturonans occurred throughout the walls and were most abundant in the middle lamellae and middle lamella junctions. Although the (1 → 4)-β-d-galactans occurred only in the rest of the walls, some of the (1 → 5)-α-l-arabinans also occurred in the middle lamellae and middle lamella junctions. During development, the location of the xyloglucans changed, being confined to the middle lamellae and middle lamella junctions early on, but later occurred throughout the walls. The location of the heteroxylans also changed, occurring mostly in the outer walls in young cells, but were more widely distributed in mature cells. Solid-state NMR spectroscopy showed that particularly cellulose, but also homogalacturonans, decreased in mobility during development. Our studies showed that celery Collenchyma cell walls are primary and that during their development the polysaccharides undergo dynamic changes. Changes in the mobilities of cellulose and homogalacturonans were consistent with the cell walls becoming stiffer as expansion ceases.

  • Additional file 7: of Developmental changes in Collenchyma cell-wall polysaccharides in celery (Apium graveolens L.) petioles
    2019
    Co-Authors: Da Chen, Zoran Zujovic, Laurence Melton, Philip Harris
    Abstract:

    Figure S7. CP/MAS NMR relaxation spectra of celery Collenchyma cell walls at developmental stage 4 obtained using various delay times. (DOCX 58 kb

  • Additional file 4: of Developmental changes in Collenchyma cell-wall polysaccharides in celery (Apium graveolens L.) petioles
    2019
    Co-Authors: Da Chen, Zoran Zujovic, Laurence Melton, Philip Harris
    Abstract:

    Figure S4. Immunogold labelling patterns of thin regions of celery Collenchyma cell walls at four developmental stages with LM19, LM20, LM5, LM6 and LM15. (DOCX 1130 kb

Laurence Melton - One of the best experts on this subject based on the ideXlab platform.

Michael C. Jarvis - One of the best experts on this subject based on the ideXlab platform.

  • structure of cellulose microfibrils in primary cell walls from Collenchyma
    Plant Physiology, 2013
    Co-Authors: Lynne H. Thomas, Craig J. Kennedy, Trevor V Forsyth, Adriana Sturcova, Clemens M Altaner, David C. Apperley, Timothy J. Wess, Michael C. Jarvis
    Abstract:

    In the primary walls of growing plant cells, the glucose polymer cellulose is assembled into long microfibrils a few nanometers in diameter. The rigidity and orientation of these microfibrils control cell expansion; therefore, cellulose synthesis is a key factor in the growth and morphogenesis of plants. Celery (Apium graveolens) Collenchyma is a useful model system for the study of primary wall microfibril structure because its microfibrils are oriented with unusual uniformity, facilitating spectroscopic and diffraction experiments. Using a combination of x-ray and neutron scattering methods with vibrational and nuclear magnetic resonance spectroscopy, we show that celery Collenchyma microfibrils were 2.9 to 3.0 nm in mean diameter, with a most probable structure containing 24 chains in cross section, arranged in eight hydrogen-bonded sheets of three chains, with extensive disorder in lateral packing, conformation, and hydrogen bonding. A similar 18-chain structure, and 24-chain structures of different shape, fitted the data less well. Conformational disorder was largely restricted to the surface chains, but disorder in chain packing was not. That is, in position and orientation, the surface chains conformed to the disordered lattice constituting the core of each microfibril. There was evidence that adjacent microfibrils were noncovalently aggregated together over part of their length, suggesting that the need to disrupt these aggregates might be a constraining factor in growth and in the hydrolysis of cellulose for biofuel production.

  • Control of thickness of Collenchyma cell walls by pectins
    Planta, 1992
    Co-Authors: Michael C. Jarvis
    Abstract:

    Near-isotropic stresses were generated within Collenchyma cell walls of celery (Apium graveolens L.) by exchanging K+ for Ca2+ ions, varying the ionic strength and de-esterifying the pectic carboxyl groups, treatments that changed the free-charge density of the pectic polysaccharides. The Collenchyma strands swelled radially with increasing free-charge density but there was very little longitudinal swelling. Depolymerising the pectins by β-elimination also induced much more radial than longitudinal swelling. Supported by earlier work on Nitella, these results indicate that pectins control the interlamellar spacing in cell walls and hold them together across their thickness, particularly against turgor stresses tending to delaminate the walls at the cell corners.

  • Direct Observation of Cell Wall Structure in Living Plant Tissues by Solid-State 13C NMR Spectroscopy
    Plant Physiology, 1990
    Co-Authors: Michael C. Jarvis, David C. Apperley
    Abstract:

    Solid-state 13C nuclear magnetic resonance (NMR) spectra of the following intact plant tissues were recorded by the crosspolarization magic-angle spinning technique: celery (Apium graveolens L.) Collenchyma; carob bean (Ceratonia siliqua L.), fenugreek (Trigonella foenum-graecum L.), and nasturtium (Tropaeolum majus L.) endosperm; and lupin (Lupinus polyphyllus Lindl.) seed cotyledons. All these tissues had thickened cell walls which allowed them to withstand the centrifugal forces of magic angle spinning and which, except in the case of lupin seeds, dominated the NMR spectra. The celery Collenchyma cell walls gave spectra typical of dicot primary cell walls. The carob bean and fenugreek seed spectra were dominated by resonances from galactomannans, which showed little sign of crystalline order. Resonances from β(1,4′)-d galactan were visible in the lupin seed spectrum, but there was much interference from protein. The nasturtium seed spectrum was largely derived from a xyloglucan, in which the conformation of the glucan core chain appeared to be intermediate between the solution form and solid forms of cellulose.

Philip J. Harris - One of the best experts on this subject based on the ideXlab platform.

  • Changes in the orientations of cellulose microfibrils during the development of Collenchyma cell walls of celery (Apium graveolens L.)
    Planta, 2019
    Co-Authors: Da Chen, Laurence D. Melton, Duncan J. Mcgillivray, Timothy M. Ryan, Philip J. Harris
    Abstract:

    Main conclusion During development, cellulose microfibrils in Collenchyma walls become increasingly longitudinal, as determined by small-angle X-ray scattering, despite the walls maintaining a fine structure indicative of a crossed-polylamellate structure. Abstract Collenchyma cells have thickened primary cell walls and provide mechanical support during plant growth. During their development, these cells elongate and their walls thicken considerably. We used microscopy and synchrotron small-angle X-ray scattering to study changes in the orientations of cellulose microfibrils that occur during development in the walls of Collenchyma cells present in peripheral strands in celery ( Apium graveolens ) petioles. Transmission electron microscopy showed that the walls consisted of many lamellae (polylamellate), with lamellae containing longitudinally oriented cellulose microfibrils alternating with microfibrils oriented at higher angles. The lamellae containing longitudinally oriented microfibrils predominated at later stages of development. Nevertheless, transmission electron microscopy of specially stained, oblique sections provided evidence that the cellulose microfibrils were ordered throughout development as crossed-polylamellate structures. These results are consistent with our synchrotron small-angle X-ray scattering results that showed the cellulose microfibrils become oriented increasingly longitudinally during development. Some passive reorientation of cellulose microfibrils may occur during development, but extensive reorientation throughout the wall would destroy ordered structures. Atomic force microscopy and field emission scanning electron microscopy were used to determine the orientations of newly deposited cellulose microfibrils. These were found to vary widely among different cells, which could be consistent with the formation of crossed-polylamellate structures. These newly deposited cellulose microfibrils are deposited in a layer of pectic polysaccharides that lies immediately outside the plasma membrane. Overall, our results show that during development of Collenchyma walls, the cellulose microfibrils become increasingly longitudinal in orientation, yet organized, crossed-polylamellate structures are maintained.

  • Developmental changes in Collenchyma cell-wall polysaccharides in celery (Apium graveolens L.) petioles.
    BMC Plant Biology, 2019
    Co-Authors: Da Chen, Zoran D. Zujovic, Laurence D. Melton, Philip J. Harris
    Abstract:

    Collenchyma cells occur widely in eudicotyledons and provide mechanical support for growing organs. At maturity, the cells are elongated and have thick, non-lignified walls, which in celery contain cellulose and pectic polysaccharides, together with xyloglucans and heteroxylans and heteromannans. A previous study suggested that at least some of the Collenchyma cell wall in celery is laid down after expansion has stopped and is thus secondary. In the present study, we re-examined this. We used chemical analysis and immunomicroscopy to determine changes in the polysaccharide compositions of these walls during development. Additionally, solid-state NMR spectroscopy was used to examine changes in polysaccharide mobilities during development. We showed the Collenchyma walls are deposited only during cell expansion, i.e. they are primary walls. During cell-wall development, analytical and immunomicroscopy studies showed that within the pectic polysaccharides there were no overall changes in the proportions of homogalacturonans, but there was a decrease in their methyl esterification. There was also a decrease in the proportions of the (1 → 5)-α-l-arabinan and (1 → 4)-β-d-galactan side chains of rhamnogalacturonan I. The proportions of cellulose increased, and to a lesser extent those of xyloglucans and heteroxylans. Immunomicroscopy showed the homogalacturonans occurred throughout the walls and were most abundant in the middle lamellae and middle lamella junctions. Although the (1 → 4)-β-d-galactans occurred only in the rest of the walls, some of the (1 → 5)-α-l-arabinans also occurred in the middle lamellae and middle lamella junctions. During development, the location of the xyloglucans changed, being confined to the middle lamellae and middle lamella junctions early on, but later occurred throughout the walls. The location of the heteroxylans also changed, occurring mostly in the outer walls in young cells, but were more widely distributed in mature cells. Solid-state NMR spectroscopy showed that particularly cellulose, but also homogalacturonans, decreased in mobility during development. Our studies showed that celery Collenchyma cell walls are primary and that during their development the polysaccharides undergo dynamic changes. Changes in the mobilities of cellulose and homogalacturonans were consistent with the cell walls becoming stiffer as expansion ceases.

  • Developmental changes in Collenchyma cell-wall polysaccharides in celery (Apium graveolens L.) petioles
    BMC, 2019
    Co-Authors: Da Chen, Zoran Zujovic, Laurence D. Melton, Philip J. Harris
    Abstract:

    Abstract Background Collenchyma cells occur widely in eudicotyledons and provide mechanical support for growing organs. At maturity, the cells are elongated and have thick, non-lignified walls, which in celery contain cellulose and pectic polysaccharides, together with xyloglucans and heteroxylans and heteromannans. A previous study suggested that at least some of the Collenchyma cell wall in celery is laid down after expansion has stopped and is thus secondary. In the present study, we re-examined this. We used chemical analysis and immunomicroscopy to determine changes in the polysaccharide compositions of these walls during development. Additionally, solid-state NMR spectroscopy was used to examine changes in polysaccharide mobilities during development. Results We showed the Collenchyma walls are deposited only during cell expansion, i.e. they are primary walls. During cell-wall development, analytical and immunomicroscopy studies showed that within the pectic polysaccharides there were no overall changes in the proportions of homogalacturonans, but there was a decrease in their methyl esterification. There was also a decrease in the proportions of the (1 → 5)-α-l-arabinan and (1 → 4)-β-d-galactan side chains of rhamnogalacturonan I. The proportions of cellulose increased, and to a lesser extent those of xyloglucans and heteroxylans. Immunomicroscopy showed the homogalacturonans occurred throughout the walls and were most abundant in the middle lamellae and middle lamella junctions. Although the (1 → 4)-β-d-galactans occurred only in the rest of the walls, some of the (1 → 5)-α-l-arabinans also occurred in the middle lamellae and middle lamella junctions. During development, the location of the xyloglucans changed, being confined to the middle lamellae and middle lamella junctions early on, but later occurred throughout the walls. The location of the heteroxylans also changed, occurring mostly in the outer walls in young cells, but were more widely distributed in mature cells. Solid-state NMR spectroscopy showed that particularly cellulose, but also homogalacturonans, decreased in mobility during development. Conclusions Our studies showed that celery Collenchyma cell walls are primary and that during their development the polysaccharides undergo dynamic changes. Changes in the mobilities of cellulose and homogalacturonans were consistent with the cell walls becoming stiffer as expansion ceases

  • Polysaccharide compositions of Collenchyma cell walls from celery (Apium graveolens L.) petioles
    BMC Plant Biology, 2017
    Co-Authors: Da Chen, Zoran D. Zujovic, Philip J. Harris, Ian M. Sims, Laurence D. Melton
    Abstract:

    Collenchyma serves as a mechanical support tissue for many herbaceous plants. Previous work based on solid-state NMR and immunomicroscopy suggested Collenchyma cell walls (CWs) may have similar polysaccharide compositions to those commonly found in eudicotyledon parenchyma walls, but no detailed chemical analysis was available. In this study, compositions and structures of cell wall polysaccharides of peripheral Collenchyma from celery petioles were investigated. This is the first detailed investigation of the cell wall composition of Collenchyma from any plant. Celery petioles were found to elongate throughout their length during early growth, but as they matured elongation was increasingly confined to the upper region, until elongation ceased. Mature, fully elongated, petioles were divided into three equal segments, upper, middle and lower, and peripheral Collenchyma strands isolated from each. Cell walls (CWs) were prepared from the strands, which also yielded a HEPES buffer soluble fraction. The CWs were sequentially extracted with CDTA, Na2CO3, 1 M KOH and 4 M KOH. Monosaccharide compositions of the CWs showed that pectin was the most abundant polysaccharide [with homogalacturonan (HG) more abundant than rhamnogalacturonan I (RG-I) and rhamnogalacturonan II (RG-II)], followed by cellulose, and other polysaccharides, mainly xyloglucans, with smaller amounts of heteroxylans and heteromannans. CWs from different segments had similar compositions, but those from the upper segments had slightly more pectin than those from the lower two segments. Further, the pectin in the CWs of the upper segment had a higher degree of methyl esterification than the other segments. In addition to the anticipated water-soluble pectins, the HEPES-soluble fractions surprisingly contained large amounts of heteroxylans. The CDTA and Na2CO3 fractions were rich in HG and RG-I, the 1 M KOH fraction had abundant heteroxylans, the 4 M KOH fraction was rich in xyloglucan and heteromannans, and cellulose was predominant in the final residue. The structures of the xyloglucans, heteroxylans and heteromannans were deduced from the linkage analysis and were similar to those present in most eudicotyledon parenchyma CWs. Cross polarization with magic angle spinning (CP/MAS) NMR spectroscopy showed no apparent difference in the rigid and semi-rigid polysaccharides in the CWs of the three segments. Single-pulse excitation with magic-angle spinning (SPE/MAS) NMR spectroscopy, which detects highly mobile polysaccharides, showed the presence of arabinan, the detailed structure of which varied among the cell walls from the three segments. Celery Collenchyma CWs have similar polysaccharide compositions to most eudicotyledon parenchyma CWs. However, celery Collenchyma CWs have much higher XG content than celery parenchyma CWs. The degree of methyl esterification of pectin and the structures of the arabinan side chains of RG-I show some variation in the Collenchyma CWs from the different segments. Unexpectedly, the HEPES-soluble fraction contained a large amount of heteroxylans.

  • Polysaccharide compositions of Collenchyma cell walls from celery (Apium graveolens L.) petioles
    BMC, 2017
    Co-Authors: Da Chen, Zoran Zujovic, Philip J. Harris, Ian M. Sims, Laurence D. Melton
    Abstract:

    Abstract Background Collenchyma serves as a mechanical support tissue for many herbaceous plants. Previous work based on solid-state NMR and immunomicroscopy suggested Collenchyma cell walls (CWs) may have similar polysaccharide compositions to those commonly found in eudicotyledon parenchyma walls, but no detailed chemical analysis was available. In this study, compositions and structures of cell wall polysaccharides of peripheral Collenchyma from celery petioles were investigated. Results This is the first detailed investigation of the cell wall composition of Collenchyma from any plant. Celery petioles were found to elongate throughout their length during early growth, but as they matured elongation was increasingly confined to the upper region, until elongation ceased. Mature, fully elongated, petioles were divided into three equal segments, upper, middle and lower, and peripheral Collenchyma strands isolated from each. Cell walls (CWs) were prepared from the strands, which also yielded a HEPES buffer soluble fraction. The CWs were sequentially extracted with CDTA, Na2CO3, 1 M KOH and 4 M KOH. Monosaccharide compositions of the CWs showed that pectin was the most abundant polysaccharide [with homogalacturonan (HG) more abundant than rhamnogalacturonan I (RG-I) and rhamnogalacturonan II (RG-II)], followed by cellulose, and other polysaccharides, mainly xyloglucans, with smaller amounts of heteroxylans and heteromannans. CWs from different segments had similar compositions, but those from the upper segments had slightly more pectin than those from the lower two segments. Further, the pectin in the CWs of the upper segment had a higher degree of methyl esterification than the other segments. In addition to the anticipated water-soluble pectins, the HEPES-soluble fractions surprisingly contained large amounts of heteroxylans. The CDTA and Na2CO3 fractions were rich in HG and RG-I, the 1 M KOH fraction had abundant heteroxylans, the 4 M KOH fraction was rich in xyloglucan and heteromannans, and cellulose was predominant in the final residue. The structures of the xyloglucans, heteroxylans and heteromannans were deduced from the linkage analysis and were similar to those present in most eudicotyledon parenchyma CWs. Cross polarization with magic angle spinning (CP/MAS) NMR spectroscopy showed no apparent difference in the rigid and semi-rigid polysaccharides in the CWs of the three segments. Single-pulse excitation with magic-angle spinning (SPE/MAS) NMR spectroscopy, which detects highly mobile polysaccharides, showed the presence of arabinan, the detailed structure of which varied among the cell walls from the three segments. Conclusions Celery Collenchyma CWs have similar polysaccharide compositions to most eudicotyledon parenchyma CWs. However, celery Collenchyma CWs have much higher XG content than celery parenchyma CWs. The degree of methyl esterification of pectin and the structures of the arabinan side chains of RG-I show some variation in the Collenchyma CWs from the different segments. Unexpectedly, the HEPES-soluble fraction contained a large amount of heteroxylans

Philip Harris - One of the best experts on this subject based on the ideXlab platform.