Special Issue: Plant Cell Wall   

April 2015, Volume 57 Issue 4, Pages 326每445.


Cover Caption: Plant Cell Wall
The cover shows a confocal microscope image of tobacco protoplasts transiently transformed with a gene cassette containing a signal sequence of a lignin polymerising peroxidase of Norway spruce fused with a GFP sequence, showing the ER- and apoplast-localized lignin polymerising peroxidase (green) that is involved in cell wall formation (see also Shigeto et al., pp. 349每356). Chloroplast auto-fluorescence is shown in red. Photo was taken by Mikko Lehtonen, University of Helsinki.

 

          Editorial
JIPB Board, supporting the plant science community through teamwork  
Author: Chun-Ming Liu
Journal of Integrative Plant Biology 2015 57(4): 326每327
Published Online: March 10, 2015
DOI: 10.1111/jipb.12352
Abstract (Browse 618)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
The plant cell wall  
Author: Kurt Fagerstedt and Anna Kärkönen
Journal of Integrative Plant Biology 2015 57(4): 328每329
Published Online: March 7, 2015
DOI: 10.1111/jipb.12351
Abstract (Browse 635)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
          Invited Expert Reviews
The connection of cytoskeletal network with plasma membrane and the cell wall  
Author: Zengyu Liu, Staffan Persson and Yi Zhang
Journal of Integrative Plant Biology 2015 57(4): 330每340
Published Online: February 18, 2015
DOI: 10.1111/jipb.12342
      
    

The cell wall provides external support of the plant cells, while the cytoskeletons including the microtubules and the actin filaments constitute an internal framework. The cytoskeletons contribute to the cell wall biosynthesis by spatially and temporarily regulating the transportation and deposition of cell wall components. This tight control is achieved by the dynamic behavior of the cytoskeletons, but also through the tethering of these structures to the plasma membrane. This tethering may also extend beyond the plasma membrane and impact on the cell wall, possibly in the form of a feedback loop. In this review, we discuss the linking components between the cytoskeletons and the plasma membrane, and/or the cell wall. We also discuss the prospective roles of these components in cell wall biosynthesis and modifications, and aim to provide a platform for further studies in this field.

 

Liu Z, Persson S, Zhang Y (2015) The connection of cytoskeletal network with plasma membrane and the cell wall. J Integr Plant Biol 57: 330–340 doi: 10.1111/jipb.12342

Abstract (Browse 700)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
In this review, we summarize the linking proteins involved in the association of the cytoskeletons and the plasma membrane, and/or the cell wall. The prospective roles of these proteins in cell wall biosynthesis and modifications are discussed, aiming to provide a platform for further studies in this field.
          Research Articles
Norway spruce (Picea abies) laccases: Characterization of a laccase in a lignin-forming tissue culture  
Author: Sanna Koutaniemi, Heli A. Malmberg, Liisa K. Simola, Teemu H. Teeri and Anna Kärkönen
Journal of Integrative Plant Biology 2015 57(4): 341每348
Published Online: January 27, 2015
DOI: 10.1111/jipb.12333
      
    

Secondarily thickened cell walls of water-conducting vessels and tracheids and support-giving sclerenchyma cells contain lignin that makes the cell walls water impermeable and strong. To what extent laccases and peroxidases contribute to lignin biosynthesis in muro is under active evaluation. We performed an in silico study of Norway spruce (Picea abies (L.) Karst.) laccases utilizing available genomic data. As many as 292 laccase encoding sequences (genes, gene fragments, and pseudogenes) were detected in the spruce genome. Out of the 112 genes annotated as laccases, 79 are expressed at some level. We isolated five full-length laccase cDNAs from developing xylem and an extracellular lignin-forming cell culture of spruce. In addition, we purified and biochemically characterized one culture medium laccase from the lignin-forming cell culture. This laccase has an acidic pH optimum (pH 3.8–4.2) for coniferyl alcohol oxidation. It has a high affinity to coniferyl alcohol with an apparent Km value of 3.5 μM; however, the laccase has a lower catalytic efficiency (Vmax/Km) for coniferyl alcohol oxidation compared with some purified culture medium peroxidases. The properties are discussed in the context of the information already known about laccases/coniferyl alcohol oxidases of coniferous plants.

 

Koutaniemi S, Malmberg HA, Simola LK, Teeri TH, Kärkönen A (2015) Norway spruce (Picea abies) laccases: Characterization of a laccase in a lignin-forming tissue culture. J Integr Plant Biol 57: 341–348 doi: 10.1111/jipb.12333

Abstract (Browse 771)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
In order to resolve how lignin, an important cell wall component is synthesized in Norway spruce, we have studied laccases with biochemical, molecular biological and bioinformatic means. Laccases are enzymes that participate in the final stages of lignin biosynthesis in many species. Spruce contains numerous laccase genes in the genome.
Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem  
Author: Jun Shigeto, Yoshitaka Itoh, Sakie Hirao, Kaori Ohira, Koki Fujita and Yuji Tsutsumi
Journal of Integrative Plant Biology 2015 57(4): 349每356
Published Online: January 27, 2015
DOI: 10.1111/jipb.12334
      
    
Shigeto J, Itoh Y, Hirao S, Ohira K, Fujita K, Tsutsumi Y (2015)
Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin
content and structure in Arabidopsis stem. J Integr Plant Biol 57: 349
356 doi: 10.1111/jipb.

Plant class III heme peroxidases catalyze lignin polymerization. Previous reports have shown that at least three Arabidopsis thaliana peroxidases, AtPrx2, AtPrx25 and AtPrx71, are involved in stem lignification using T-DNA insertion mutants, atprx2, atprx25, and atprx71. Here, we generated three double mutants, atprx2/atprx25, atprx2/atprx71, and atprx25/atprx71, and investigated the impact of the simultaneous deficiency of these peroxidases on lignins and plant growth. Stem tissue analysis using the acetyl bromide method and derivatization followed by reductive cleavage revealed improved lignin characteristics, such as lowered lignin content and increased arylglycerol-β-aryl (β-O-4) linkage type, especially β-O-4 linked syringyl units, in lignin, supporting the roles of these genes in lignin polymerization. In addition, none of the double mutants exhibited severe growth defects, such as shorter plant stature, dwarfing, or sterility, and their stems had improved cell wall degradability. This study will contribute to progress in lignin bioengineering to improve lignocellulosic biomass.

 

Shigeto J, Itoh Y, Hirao S, Ohira K, Fujita K, Tsutsumi Y (2015) Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. J Integr Plant Biol 57: 349–356 doi: 10.1111/jipb.12334

Abstract (Browse 770)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
This study showed that simultaneous deficiency of AtPrx2, AtPrx25, and AtPrx71 enhanced lignin decrease of each single mutant, suggesting that the effect on plants can be regulated stepwise by multiple knockouts of these peroxidases. Therefore, manipulation of peroxidase genes is an attractive strategy to improve lignin characteristics.
Ectopic lignification in primary cellulose-deficient cell walls of maize cell suspension cultures  
Author: Hugo Mélida, Asier Largo-Gosens, Esther Novo-Uzal, Rogelio Santiago, Federico Pomar, Pedro García, Penélope García-Angulo, José Luis Acebes, Jesús Álvarez and Antonio Encina
Journal of Integrative Plant Biology 2015 57(4): 357每372
Published Online: March 4, 2015
DOI: 10.1111/jipb.12346
      
    

Maize (Zea mays L.) suspension-cultured cells with up to 70% less cellulose were obtained by stepwise habituation to dichlobenil (DCB), a cellulose biosynthesis inhibitor. Cellulose deficiency was accompanied by marked changes in cell wall matrix polysaccharides and phenolics as revealed by Fourier transform infrared (FTIR) spectroscopy. Cell wall compositional analysis indicated that the cellulose-deficient cell walls showed an enhancement of highly branched and cross-linked arabinoxylans, as well as an increased content in ferulic acid, diferulates and p-coumaric acid, and the presence of a polymer that stained positive for phloroglucinol. In accordance with this, cellulose-deficient cell walls showed a fivefold increase in Klason-type lignin. Thioacidolysis/GC-MS analysis of cellulose-deficient cell walls indicated the presence of a lignin-like polymer with a Syringyl/Guaiacyl ratio of 1.45, which differed from the sensu stricto stress-related lignin that arose in response to short-term DCB-treatments. Gene expression analysis of these cells indicated an overexpression of genes specific for the biosynthesis of monolignol units of lignin. A study of stress signaling pathways revealed an overexpression of some of the jasmonate signaling pathway genes, which might trigger ectopic lignification in response to cell wall integrity disruptions. In summary, the structural plasticity of primary cell walls is proven, since a lignification process is possible in response to cellulose impoverishment.

 

Mélida H, Largo-Gosens A, Novo-Uzal E, Santiago R, Pomar F, García P, García-Angulo P, Acebes JL, Álvarez J, Encina A (2015) Ectopic lignification in primary cellulose-deficient cell walls of maize cell suspension cultures. J Integr Plant Biol 57: 357–372 doi: 10.1111/jipb.12346

Abstract (Browse 617)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Despite their compositional and structural complexity, primary plant cell walls have revealed as highly dynamic compartments able to sense and adapt to different conditions. In this article we report how primary cell walls response to a reduction in cellulose, their major load-bearing component, accumulating a non-expected component, lignin.
The biosynthesis and wall-binding of hemicelluloses in cellulose-deficient maize cells: An example of metabolic plasticity  
Author: María de Castro, Janice G. Miller, José Luis Acebes, Antonio Encina, Penélope García-Angulo and Stephen C. Fry
Journal of Integrative Plant Biology 2015 57(4): 373每387
Published Online: January 22, 2015
DOI: 10.1111/jipb.12331
      
    

Cell-suspension cultures (Zea mays L., Black Mexican sweet corn) habituated to 2,6-dichlorobenzonitrile (DCB) survive with reduced cellulose owing to hemicellulose network modification. We aimed to define the hemicellulose metabolism modifications in DCB-habituated maize cells showing a mild reduction in cellulose at different stages in the culture cycle. Using pulse-chase radiolabeling, we fed habituated and non-habituated cultures with [3H]arabinose, and traced the distribution of 3H-pentose residues between xylans, xyloglucans and other polymers in several cellular compartments for 5 h. Habituated cells were slower taking up exogenous [3H]arabinose. Tritium was incorporated into polysaccharide-bound arabinose and xylose residues, but habituated cells diverted a higher proportion of their new [3H]xylose residues into (hetero) xylans at the expense of xyloglucan synthesis. During logarithmic growth, habituated cells showed slower vesicular trafficking of polymers, especially xylans. Moreover, habituated cells showed a decrease in the strong wall-binding of all pentose-containing polysaccharides studied; correspondingly, especially in log-phase cultures, habituation increased the proportion of 3H-hemicelluloses ([3H]xylans and [3H]xyloglucan) sloughed into the medium. These findings could be related to the cell walls' cellulose-deficiency, and consequent reduction in binding sites for hemicelluloses; the data could also reflect the habituated cells' reduced capacity to integrate arabinoxylans by extra-protoplasmic phenolic cross-linking, as well as xyloglucans, during wall assembly.

 

de Castro M, Miller JG, Acebes JL, Encina A, García-Angulo P, Fry SC (2015) The biosynthesis and wall-binding of hemicelluloses in cellulose-deficient maize cells: An example of metabolic plasticity. J Integr Plant Biol 57: 373–387 doi: 10.1111/jipb.12331

Abstract (Browse 584)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
"2,6-Dichlorobenzonitrile is a herbicide that blocks cellulose synthesis. Maize cell-cultures can &habituate*, becoming tolerant of moderate 2,6-dichlorobenzonitrile concentrations. Although these cells produce cellulose-poor walls, they compensate by modifying how they integrate non-cellulosic polysaccharides (hemicelluloses) into the cell-wall architecture 〞 an excellent example of the tremendous plasticity of plant metabolism."
Cellulose structure and lignin distribution in normal and compression wood of the Maidenhair tree (Ginkgo biloba L.)  
Author: Seppo Andersson, Yurong Wang, Raili Pönni, Tuomas Hänninen, Marko Mononen, Haiqing Ren, Ritva Serimaa and Pekka Saranpää
Journal of Integrative Plant Biology 2015 57(4): 388每395
Published Online: March 4, 2015
DOI: 10.1111/jipb.12349
      
    

We studied in detail the mean microfibril angle and the width of cellulose crystals from the pith to the bark of a 15-year-old Maidenhair tree (Ginkgo biloba L.). The orientation of cellulose microfibrils with respect to the cell axis and the width and length of cellulose crystallites were determined using X-ray diffraction. Raman microscopy was used to compare the lignin distribution in the cell wall of normal/opposite and compression wood, which was found near the pith. Ginkgo biloba showed a relatively large mean microfibril angle, varying between 19° and 39° in the S2 layer, and the average width of cellulose crystallites was 3.1–3.2 nm. Mild compression wood without any intercellular spaces or helical cavities was observed near the pith. Slit-like bordered pit openings and a heavily lignified S2L layer confirmed the presence of compression wood. Ginkgo biloba showed typical features present in the juvenile wood of conifers. The microfibril angle remained large over the 14 annual rings. The entire stem disc, with a diameter of 18 cm, was considered to consist of juvenile wood. The properties of juvenile and compression wood as well as the cellulose orientation and crystalline width indicate that the wood formation of G. biloba is similar to that of modern conifers.

 

Andersson S, Wang Y, Pönni R, Hänninen T, Mononen M, Ren H, Serimaa R, Saranpää P (2015) Cellulose structure and lignin distribution in normal and compression wood of the Maidenhair tree (Ginkgo biloba L.). J Integr Plant Biol 57: 388–395 doi: 10.1111/jipb.12349

Abstract (Browse 734)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Maidenhair tree has been described as a living fossil. We studied its cellulose structure and lignin distribution in the cell wall of normal and reaction wood. The properties of juvenile and compression wood as well as the cellulose orientation and crystalline size are similar to modern conifers like Norway spruce.
Endo-汕-1,4-glucanases impact plant cell wall development by influencing cellulose crystallization  
Author: Magdalena Glass, Sarah Barkwill, Faride Unda and Shawn D. Mansfield
Journal of Integrative Plant Biology 2015 57(4): 396每410
Published Online: March 10, 2015
DOI: 10.1111/jipb.12353
      
    
Cell walls are vital to the normal growth and development of plants as they protect the protoplast and provide rigidity to the stem. Here, two poplar and Arabidopsis orthologous endoglucanases, which have been proposed to play a role in secondary cell wall development, were examined. The class B endoglucanases, PtGH9B5 and AtGH9B5, are secreted enzymes that have a predicted glycosylphosphatidylinositol anchor, while the class C endoglucanases, PtGH9C2 and AtGH9C2, are also predicted to be secreted but instead contain a carbohydrate-binding module. The poplar endoglucanases were expressed in Arabidopsis using both a 35S promoter and the Arabidopsis secondary cell wall-specific CesA8 promoter. Additionally, Arabidopsis t-DNA insertion lines and an RNAi construct was created to downregulate AtGH9C2 in Arabidopsis. All of the plant lines were examined for changes in cell morphology and patterning, growth and development, cell wall crystallinity, microfibril angle, and proportion of cell wall carbohydrates. Misregulation of PtGH9B5/AtGH9B5 resulted in changes in xylose content, while misregulation of PtGH9C2/AtGH9C2 resulted in changes in crystallinity, which was inversely correlated with changes in plant height and rosette diameter. Together, these results suggest that these endoglucanases affect secondary cell wall development by contributing to the cell wall crystallization process.

 

Glass M, Barkwill S, Unda F, Mansfield SD (2015) Endo-b-1,4-glucanases impact plant cell wall development by influencing cellulose crystallization. J Integr Plant Biol 57: 396–410 doi: 10.1111/jipb.12353

Abstract (Browse 576)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
The current architecture of proteins and cellular processes thought to be involved in, or influence cellulose biosynthesis are rapidly being elucidated. Among the gene families putatively involved are endoglucanases, and here we characterize two endoglucanase (among 25 in Arabidopsis) and demonstrate that they impact cellulose crystallization and plant development.
A general method for assaying homo- and hetero-transglycanase activities that act on plant cell-wall polysaccharides  
Author: Lenka Franková and Stephen C. Fry
Journal of Integrative Plant Biology 2015 57(4): 411每428
Published Online: January 31, 2015
DOI: 10.1111/jipb.12337
      
    

Transglycanases (endotransglycosylases) cleave a polysaccharide (donor-substrate) in mid-chain, and then transfer a portion onto another poly- or oligosaccharide (acceptor-substrate). Such enzymes contribute to plant cell-wall assembly and/or re-structuring. We sought a general method for revealing novel homo- and hetero-transglycanases, applicable to diverse polysaccharides and oligosaccharides, separating transglycanase-generated 3H-polysaccharides from unreacted 3H-oligosaccharides—the former immobilized (on filter-paper, silica-gel or glass-fiber), the latter eluted. On filter-paper, certain polysaccharides [e.g. (1[RIGHTWARDS ARROW]3, 1[RIGHTWARDS ARROW]4)-β-d-glucans] remained satisfactorily adsorbed when water-washed; others (e.g. pectins) were partially lost. Many oligosaccharides (e.g. arabinan-, galactan-, xyloglucan-based) were successfully eluted in appropriate solvents, but others (e.g. [3H]xylohexaitol, [3H]mannohexaitol [3H]cellohexaitol) remained immobile. On silica-gel, all 3H-oligosaccharides left an immobile ‘ghost’ spot (contaminating any 3H-polysaccharides), which was diminished but not prevented by additives e.g. sucrose or Triton X-100. The best stratum was glass-fiber (GF), onto which the reaction-mixture was dried then washed in 75% ethanol. Washing led to minimal loss or lateral migration of 3H-polysaccharides if conducted by slow percolation of acidified ethanol. The effectiveness of GF-blotting was well demonstrated for Chara vulgaris trans-β-mannanase. In conclusion, our novel GF-blotting technique efficiently frees transglycanase-generated 3H-polysaccharides from unreacted 3H-oligosaccharides, enabling high-throughput screening of multiple postulated transglycanase activities utilising chemically diverse donor- and acceptor-substrates.

 

Franková L, Fry SC (2015) A general method for assaying homo- and hetero-transglycanase activities that act on plant cell-wall polysaccharides. J Integr Plant Biol 57: 411–428 doi: 10.1111/jipb.12337

Abstract (Browse 609)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
We demonstrate a novel glass fiber blotting method for assaying transglycanases 每 enzymes that cut and paste polysaccharides. Compared with conventional methods, also discussed in this paper, it allows screening of non-desalted enzyme extracts for multiple proposed enzyme activities utilizing a wide range of qualitatively different polysaccharide and oligosaccharide substrates.
Distribution, structure and biosynthetic gene families of (1,3;1,4)-汕-glucan in Sorghum bicolor  
Author: Riksfardini A. Ermawar, Helen M. Collins, Caitlin S. Byrt, Natalie S. Betts, Marilyn Henderson, Neil J. Shirley, Julian Schwerdt, Jelle Lahnstein, Geoffrey B. Fincher and Rachel A. Burton
Journal of Integrative Plant Biology 2015 57(4): 429每445
Published Online: February 7, 2015
DOI: 10.1111/jipb.12338
      
    

In cereals, the presence of soluble polysaccharides including (1,3;1,4)-β-glucan has downstream implications for human health, animal feed and biofuel applications. Sorghum bicolor (L.) Moench is a versatile crop, but there are limited reports regarding the content of such soluble polysaccharides. Here, the amount of (1,3;1,4)-β-glucan present in sorghum tissues was measured using a Megazyme assay. Very low amounts were present in the grain, ranging from 0.16%–0.27% (w/w), while there was a greater quantity in vegetative tissues at 0.12–1.71% (w/w). The fine structure of (1,3;1,4)-β-glucan, as denoted by the ratio of cellotriosyl and cellotetraosyl residues, was assessed by high performance liquid chromatography (HPLC) and ranged from 2.6–3:1 in the grain, while ratios in vegetative tissues were lower at 2.1–2.6:1. The distribution of (1,3;1,4)-β-glucan was examined using a specific antibody and observed with fluorescence and transmission electron microscopy. Micrographs showed a variable distribution of (1,3;1,4)-β-glucan influenced by temporal and spatial factors. The sorghum orthologs of genes implicated in the synthesis of (1,3;1,4)-β-glucan in other cereals, such as the Cellulose synthase-like (Csl) F and H gene families were defined. Transcript profiling of these genes across sorghum tissues was carried out using real-time quantitative polymerase chain reaction, indicating that, as in other cereals, CslF6 transcripts dominated.

 

Ermawar RA, Collins HM, Byrt CS, Betts NS, Henderson M, Shirley NJ, Schwerdt J, Lahnstein J, Fincher GB, Burton RA (2015) Distribution, structure and biosynthetic gene families of (1,3;1,4)-b-glucan in Sorghum bicolor. J Integr Plant Biol 57: 429–445 doi: 10.1111/jipb.12338
Abstract (Browse 706)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Sorghum is an important emerging cereal that has been relatively neglected. Mixed-linkage glucan is a plant polysaccharide, valuable for human health and to biofuel industries, that has been well studied in barley and wheat. Here we characterise mixed-linkage glucan in parts of the sorghum plant, including the grain.
 

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