Non-cellulosic polysaccharide distribution during G-layer formation in poplar tension wood fibers: abundance of rhamnogalacturonan I and arabinogalactan proteins but no evidence of xyloglucan
Abstract:RG-I and AGP, but not XG, are associated to the building of the peculiar mechanical properties of tension wood. Hardwood trees produce tension wood (TW) with specific mechanical properties to cope with environmental cues. Poplar TW fibers have an additional cell wall layer, the G-layer responsible for TW mechanical properties. We investigated, in two poplar hybrid species, the molecules potentially involved in the building of TW mechanical properties. First, we evaluated the distribution of the different class… Show more
“…In some plant species, lignifications of the G‐layer may occur at later stages of fiber development (Ghislain & Clair, ). The cell wall polymer that occurs specifically in fibers at the stage of tertiary cell wall deposition is rhamnogalacturonan‐I (RG‐I) with long β‐(1→4)‐galactan side chains (Gorshkova et al ., , ; Guedes et al ., ). The galactose content in cell wall polymers has even been suggested to be an indicator of the degree of G‐layer development in fibers of tension wood (Ruel & Barnoud, ).…”
Section: Tertiary Cell Walls Have Unique Biochemical and Architecturamentioning
confidence: 97%
“…Other cell wall components present in the G‐layers are glucomannan, the only hemicellulosic polymer found in both secondary and tertiary cell walls (Gorshkova et al ., ), and the arabinogalactan proteins (Morvan et al ., ; Gorshkova et al ., ). Xyloglucan, known to be involved in restoring the vertical position of inclined poplar trees (Mellerowicz et al ., ), is located at the external boundary of the G‐layer, where it becomes stapled to the previously deposited secondary cell wall (Baba et al ., ); xyloglucan was recently reported to be absent in the G‐layer itself (Guedes et al ., ). The biochemical differences between secondary and tertiary cell walls are reflected in corresponding gene expression, as revealed by comparison of the transcriptomes in flax fibers isolated at the stage of tertiary cell wall deposition and in tissues forming secondary cell walls (Gorshkov et al ., ).…”
Section: Tertiary Cell Walls Have Unique Biochemical and Architecturamentioning
confidence: 97%
“…The presence of RG‐I with side chains of β‐(1→4)‐galactan was detected in the tertiary cell walls of nonflax plants by biochemical characterization (Gorshkova et al ., ; Guedes et al ., ) and by immunocytochemistry (Bowling & Vaughn, ; Gritsch et al ., ; Guedes et al ., ). Immunolabeling with an antibody recognizing β‐1,4‐galactans is not always successful in the tertiary cell wall, as reported for phloem fibers of hemp (Blake et al ., ; Behr et al ., ).…”
Section: Peculiarities Of Tertiary Cell Wall‐specific Rg‐i and Relevamentioning
confidence: 99%
“…However, antibodies specific for the backbone of RG‐I and for β‐(1→4)‐galactosidase heavily bind tertiary cell walls of primary and secondary hemp fibers (Chernova et al ., ). In addition, galactosidase activity in the G‐layers of tension wood fibers was recently detected (Gorshkova et al ., ) and decreased labeling by β‐(1→4)‐galactan‐specific antibody with G‐layer maturation (Guedes et al ., ), which may be due to the in muro action of galactosidase. Together with the reports on the axial orientation of cellulose microfibrils in G‐fibers of many plant species (e.g.…”
Section: Peculiarities Of Tertiary Cell Wall‐specific Rg‐i and Relevamentioning
Plants, although sessile organisms, are nonetheless able to move their body parts; for example, during root contraction of geophytes or in the gravitropic reaction by woody stems. One of the major mechanisms enabling these movements is the development of specialized structures that possess contractile properties. Quite unlike animal muscles, for which the action is driven by protein-protein interactions in the protoplasma, the action of plant 'muscles' is polysaccharide-based and located in the uniquely designed, highly cellulosic cell wall that is deposited specifically in fibers. This review describes the development of such cell walls as a widespread phenomenon in the plant kingdom, gives reasons why it should be considered as a tertiary cell wall, and discusses the mechanism of action of the 'muscles'. The origin of the contractile properties lies in the tension of the axially oriented cellulose microfibrils due to entrapment of rhamnogalacturonan-I aggregates that limits the lateral interaction of microfibrils. Long side chains of the nascent rhamnogalacturonan-I are trimmed off during cell wall maturation leading to tension development. Similarities in the tertiary cell wall design in fibers of different plant origin indicate that the basic principles of tension creation may be universal in various ecophysiological situations.
“…In some plant species, lignifications of the G‐layer may occur at later stages of fiber development (Ghislain & Clair, ). The cell wall polymer that occurs specifically in fibers at the stage of tertiary cell wall deposition is rhamnogalacturonan‐I (RG‐I) with long β‐(1→4)‐galactan side chains (Gorshkova et al ., , ; Guedes et al ., ). The galactose content in cell wall polymers has even been suggested to be an indicator of the degree of G‐layer development in fibers of tension wood (Ruel & Barnoud, ).…”
Section: Tertiary Cell Walls Have Unique Biochemical and Architecturamentioning
confidence: 97%
“…Other cell wall components present in the G‐layers are glucomannan, the only hemicellulosic polymer found in both secondary and tertiary cell walls (Gorshkova et al ., ), and the arabinogalactan proteins (Morvan et al ., ; Gorshkova et al ., ). Xyloglucan, known to be involved in restoring the vertical position of inclined poplar trees (Mellerowicz et al ., ), is located at the external boundary of the G‐layer, where it becomes stapled to the previously deposited secondary cell wall (Baba et al ., ); xyloglucan was recently reported to be absent in the G‐layer itself (Guedes et al ., ). The biochemical differences between secondary and tertiary cell walls are reflected in corresponding gene expression, as revealed by comparison of the transcriptomes in flax fibers isolated at the stage of tertiary cell wall deposition and in tissues forming secondary cell walls (Gorshkov et al ., ).…”
Section: Tertiary Cell Walls Have Unique Biochemical and Architecturamentioning
confidence: 97%
“…The presence of RG‐I with side chains of β‐(1→4)‐galactan was detected in the tertiary cell walls of nonflax plants by biochemical characterization (Gorshkova et al ., ; Guedes et al ., ) and by immunocytochemistry (Bowling & Vaughn, ; Gritsch et al ., ; Guedes et al ., ). Immunolabeling with an antibody recognizing β‐1,4‐galactans is not always successful in the tertiary cell wall, as reported for phloem fibers of hemp (Blake et al ., ; Behr et al ., ).…”
Section: Peculiarities Of Tertiary Cell Wall‐specific Rg‐i and Relevamentioning
confidence: 99%
“…However, antibodies specific for the backbone of RG‐I and for β‐(1→4)‐galactosidase heavily bind tertiary cell walls of primary and secondary hemp fibers (Chernova et al ., ). In addition, galactosidase activity in the G‐layers of tension wood fibers was recently detected (Gorshkova et al ., ) and decreased labeling by β‐(1→4)‐galactan‐specific antibody with G‐layer maturation (Guedes et al ., ), which may be due to the in muro action of galactosidase. Together with the reports on the axial orientation of cellulose microfibrils in G‐fibers of many plant species (e.g.…”
Section: Peculiarities Of Tertiary Cell Wall‐specific Rg‐i and Relevamentioning
Plants, although sessile organisms, are nonetheless able to move their body parts; for example, during root contraction of geophytes or in the gravitropic reaction by woody stems. One of the major mechanisms enabling these movements is the development of specialized structures that possess contractile properties. Quite unlike animal muscles, for which the action is driven by protein-protein interactions in the protoplasma, the action of plant 'muscles' is polysaccharide-based and located in the uniquely designed, highly cellulosic cell wall that is deposited specifically in fibers. This review describes the development of such cell walls as a widespread phenomenon in the plant kingdom, gives reasons why it should be considered as a tertiary cell wall, and discusses the mechanism of action of the 'muscles'. The origin of the contractile properties lies in the tension of the axially oriented cellulose microfibrils due to entrapment of rhamnogalacturonan-I aggregates that limits the lateral interaction of microfibrils. Long side chains of the nascent rhamnogalacturonan-I are trimmed off during cell wall maturation leading to tension development. Similarities in the tertiary cell wall design in fibers of different plant origin indicate that the basic principles of tension creation may be universal in various ecophysiological situations.
“…Thus, based on RGL expression data, the presence of functionally distinct RGLs could be assumed: the RGLs that use RG‐I of the primary cell walls (Yapo ) as potential substrate, and the RGLs that modify RG‐I present in the gelatinous (tertiary) cell walls of plant fibers (Gorshkova et al , , Guedes et al ). The subfunctionalization of RGL genes probably occurred on the basis of RGL genes from group II of eudicots (Fig.…”
Rhamnogalacturonan lyases (RGLs; EC 4.2.2.23) degrade the rhamnogalacturonan I (RG‐I) backbone of pectins present in the plant cell wall. These enzymes belong to polysaccharide lyase family 4, members of which are mainly from plants and plant pathogens. RGLs are investigated, as a rule, as pathogen ‘weapons’ for plant cell wall degradation and subsequent infection. Despite the presence of genes annotated as RGLs in plant genomes and the presence of substrates for enzyme activity in plant cells, evidence supporting the involvement of this enzyme in certain processes is limited. The differential expression of some RGL genes in flax (Linum usitatissimum L.) tissues, revealed in our previous work, prompted us to carry out a total revision (phylogenetic analysis, analysis of expression and protein structure modeling) of all the sequences of flax predicted as coding for RGLs. Comparison of the expressions of LusRGL in various tissues of flax stem revealed that LusRGLs belong to distinct phylogenetic clades, which correspond to two co‐expression groups. One of these groups comprised LusRGL6‐A and LusRGL6‐B genes and was specifically upregulated in flax fibers during deposition of the tertiary cell wall, which has complex RG‐I as a key noncellulosic component. The results of homology modeling and docking demonstrated that the topology of the LusRGL6‐A catalytic site allowed binding to the RG‐I ligand. These findings lead us to suggest the presence of RGL activity in planta and the involvement of special isoforms of RGLs in the modification of RG‐I of the tertiary cell wall in plant fibers.
This review is the tenth update of the original article published in 1999 on the application of matrix‐assisted laser desorption/ionization mass spectrometry (MALDI) mass spectrometry to the analysis of carbohydrates and glycoconjugates and brings coverage of the literature to the end of 2018. Also included are papers that describe methods appropriate to glycan and glycoprotein analysis by MALDI, such as sample preparation techniques, even though the ionization method is not MALDI. Topics covered in the first part of the review include general aspects such as theory of the MALDI process, new methods, matrices, derivatization, MALDI imaging, fragmentation and the use of arrays. The second part of the review is devoted to applications to various structural types such as oligo‐ and poly‐saccharides, glycoproteins, glycolipids, glycosides, and biopharmaceuticals. Most of the applications are presented in tabular form. The third part of the review covers medical and industrial applications of the technique, studies of enzyme reactions, and applications to chemical synthesis. The reported work shows increasing use of combined new techniques such as ion mobility and highlights the impact that MALDI imaging is having across a range of diciplines. MALDI is still an ideal technique for carbohydrate analysis and advancements in the technique and the range of applications continue steady progress.
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