scholarly journals From morphogenesis to pathogenesis: A cellulose loosening protein is one of the most widely distributed tools in nature

2019 ◽  
Author(s):  
William R. Chase ◽  
Olga Zhaxybayeva ◽  
Jorge Rocha ◽  
Daniel J. Cosgrove ◽  
Lori R. Shapiro

AbstractPlants must rearrange the network of complex carbohydrates in their cell walls during normal growth and development. To accomplish this, all plants depend on proteins called expansins that non-enzymatically loosen hydrogen bonds between cellulose microfibrils. Because of their key role in cell wall extension during growth, expansin genes are ubiquitous, diverse, and abundant throughout all land plants. Surprisingly, expansin genes have more recently been found in some bacteria and microbial eukaryotes, where their biological functions are largely unknown. Here, we reconstruct the phylogeny of microbial expansin genes. We find these genes in all eukaryotic microorganisms that have structural cellulose in their cell walls, suggesting expansins evolved in ancient marine microorganisms long before the evolution of land plants. We also find expansins in an unexpectedly high phylogenetic diversity of bacteria and fungi that do not have cellulosic cell walls. These bacteria and fungi with expansin genes inhabit varied ecological contexts mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell walls are present. The microbial expansin phylogeny shows evidence of multiple horizontal gene transfer events within and between bacterial and eukaryotic microbial lineages, which may in part underlie their unusually broad phylogenetic distribution. Taken together, we find expansins to be unexpectedly widespread in both bacterial and eukaryotic genetic backgrounds, and that the contribution of these genes to bacterial and fungal ecological interactions with plants and algae has likely been underappreciated.ImportanceCellulose is the most abundant biopolymer on earth. In plant cell walls, where most global cellulose biomass is found, cellulose microfibrils occur intertwined with hemicelluloses and pectins. The rigidity of this polysaccharide matrix provides plant cell walls with structural support, but this rigidity also restricts cellular growth and development. Irreversible, non-enzymatic loosening of structural carbohydrates by expansin proteins is key to successful cell wall growth in plants and green algae. Here, we find that expansin genes are distributed far more broadly throughout diverse bacterial and fungal lineages lacking cellulosic cell walls than previously known. Multiple horizontal gene transfer events are in part responsible for their unusually wide phylogenetic distribution. Together, these results suggest that in addition to being the key evolutionary innovation by which eukaryotes remodel structural cellulose in their cell walls, expansins likely have remarkably broad and under-recognized utility for microbial species that interact with plant and algal structural cellulose in diverse ecological contexts.

2021 ◽  
Vol 118 (51) ◽  
pp. e2111723118
Author(s):  
Yin Chang ◽  
Rox Middleton ◽  
Yu Ogawa ◽  
Tom Gregory ◽  
Lisa M. Steiner ◽  
...  

Chiral asymmetry is important in a wide variety of disciplines and occurs across length scales. While several natural chiral biomolecules exist only with single handedness, they can produce complex hierarchical structures with opposite chiralities. Understanding how the handedness is transferred from molecular to the macroscopic scales is far from trivial. An intriguing example is the transfer of the handedness of helicoidal organizations of cellulose microfibrils in plant cell walls. These cellulose helicoids produce structural colors if their dimension is comparable to the wavelength of visible light. All previously reported examples of a helicoidal structure in plants are left-handed except, remarkably, in the Pollia condensata fruit; both left- and right-handed helicoidal cell walls are found in neighboring cells of the same tissue. By simultaneously studying optical and mechanical responses of cells with different handednesses, we propose that the chirality of helicoids results from differences in cell wall composition. In detail, here we showed statistical substantiation of three different observations: 1) light reflected from right-handed cells is red shifted compared to light reflected from left-handed cells, 2) right-handed cells occur more rarely than left-handed ones, and 3) right-handed cells are located mainly in regions corresponding to interlocular divisions. Finally, 4) right-handed cells have an average lower elastic modulus compared to left-handed cells of the same color. Our findings, combined with mechanical simulation, suggest that the different chiralities of helicoids in the cell wall may result from different chemical composition, which strengthens previous hypotheses that hemicellulose might mediate the rotations of cellulose microfibrils.


Plants ◽  
2021 ◽  
Vol 10 (7) ◽  
pp. 1263
Author(s):  
David Stuart Thompson ◽  
Azharul Islam

The extensibility of synthetic polymers is routinely modulated by the addition of lower molecular weight spacing molecules known as plasticizers, and there is some evidence that water may have similar effects on plant cell walls. Furthermore, it appears that changes in wall hydration could affect wall behavior to a degree that seems likely to have physiological consequences at water potentials that many plants would experience under field conditions. Osmotica large enough to be excluded from plant cell walls and bacterial cellulose composites with other cell wall polysaccharides were used to alter their water content and to demonstrate that the relationship between water potential and degree of hydration of these materials is affected by their composition. Additionally, it was found that expansins facilitate rehydration of bacterial cellulose and cellulose composites and cause swelling of plant cell wall fragments in suspension and that these responses are also affected by polysaccharide composition. Given these observations, it seems probable that plant environmental responses include measures to regulate cell wall water content or mitigate the consequences of changes in wall hydration and that it may be possible to exploit such mechanisms to improve crop resilience.


1974 ◽  
Vol 52 (9) ◽  
pp. 2033-2036 ◽  
Author(s):  
N. C. Lyon ◽  
W. C. Mueller

Leaf tissue of Phaseolus vulgaris L. and Plantago major L. was prepared by the freeze-etch technique and examined in the electron microscope for the presence of ectodesmata. No structures analagous to ectodesmata observed with light microscopy could be found in freeze-etched preparations of chemically unfixed material or in material fixed only in glutaraldehyde. Objects appearing as broad, shallow, granular areas in the epidermal cell wall beneath the cuticle were observed in leaf replicas after fixation in complete sublimate fixative, the acid components of the sublimate fixative, or mercuric chloride alone. Because of their distribution and location, these objects can be considered analagous to ectodesmata observed by light microscopists. Because these areas occur only in chemically fixed walls and are localized within the walls in discrete areas, their presence supports the contention that ectodesmata are sites in the outer cell wall with defined physicochemical characteristics.


2020 ◽  
Author(s):  
Huimin Xu ◽  
Yuanyuan Zhao ◽  
Yuanzhen Suo ◽  
Yayu Guo ◽  
Yi Man ◽  
...  

Abstract Background: Cell wall imaging can considerably permit direct visualization of the molecular architecture of cell walls and provide the detailed chemical information on wall polymers, which is imperative to better exploit and use the biomass polymers; however, detailed imaging and quantifying of the native composition and architecture in the cell wall remains challenging.Results: Here, we describe a label-free imaging technology, coherent Raman scattering microscopy (CRS), including coherent anti-Stokes Raman scattering (CARS) microscopy and stimulated Raman scattering (SRS) microscopy, which images the major structures and chemical composition of plant cell walls. The major steps of the procedure are demonstrated, including sample preparation, setting the mapping parameters, analysis of spectral data, and image generation. Applying this rapid approach, which will help researchers understand the highly heterogeneous structures and organization of plant cell walls.Conclusions: This method can potentially be incorporated into label-free microanalyses of plant cell wall chemical composition based on the in situ vibrations of molecules.


mBio ◽  
2014 ◽  
Vol 5 (2) ◽  
Author(s):  
Volker Winstel ◽  
Patricia Sanchez-Carballo ◽  
Otto Holst ◽  
Guoqing Xia ◽  
Andreas Peschel

ABSTRACT The major clonal lineages of the human pathogen Staphylococcus aureus produce cell wall-anchored anionic poly-ribitol-phosphate (RboP) wall teichoic acids (WTA) substituted with d-Alanine and N-acetyl-d-glucosamine. The phylogenetically isolated S. aureus ST395 lineage has recently been found to produce a unique poly-glycerol-phosphate (GroP) WTA glycosylated with N-acetyl-d-galactosamine (GalNAc). ST395 clones bear putative WTA biosynthesis genes on a novel genetic element probably acquired from coagulase-negative staphylococci (CoNS). We elucidated the ST395 WTA biosynthesis pathway and identified three novel WTA biosynthetic genes, including those encoding an α-O-GalNAc transferase TagN, a nucleotide sugar epimerase TagV probably required for generation of the activated sugar donor substrate for TagN, and an unusually short GroP WTA polymerase TagF. By using a panel of mutants derived from ST395, the GalNAc residues carried by GroP WTA were found to be required for infection by the ST395-specific bacteriophage Φ187 and to play a crucial role in horizontal gene transfer of S. aureus pathogenicity islands (SaPIs). Notably, ectopic expression of ST395 WTA biosynthesis genes rendered normal S. aureus susceptible to Φ187 and enabled Φ187-mediated SaPI transfer from ST395 to regular S. aureus. We provide evidence that exchange of WTA genes and their combination in variable, mosaic-like gene clusters have shaped the evolution of staphylococci and their capacities to undergo horizontal gene transfer events. IMPORTANCE The structural highly diverse wall teichoic acids (WTA) are cell wall-anchored glycopolymers produced by most Gram-positive bacteria. While most of the dominant Staphylococcus aureus lineages produce poly-ribitol-phosphate WTA, the recently described ST395 lineage produces a distinct poly-glycerol-phosphate WTA type resembling the WTA backbone of coagulase-negative staphylococci (CoNS). Here, we analyzed the ST395 WTA biosynthesis pathway and found new types of WTA biosynthesis genes along with an evolutionary link between ST395 and CoNS, from which the ST395 WTA genes probably originate. The elucidation of ST395 WTA biosynthesis will help to understand how Gram-positive bacteria produce highly variable WTA types and elucidate functional consequences of WTA variation.


Author(s):  
WILLIAM S. YORK ◽  
ALAN G. DARVILL ◽  
MICHAEL MCNEIL ◽  
THOMAS T. STEVENSON ◽  
PETER ALBERSHEIM

Author(s):  
William S. York ◽  
Alan G. Darvill ◽  
Michael McNeil ◽  
Thomas T. Stevenson ◽  
Peter Albersheim

2019 ◽  
Vol 20 (12) ◽  
pp. 2946 ◽  
Author(s):  
Xiao Han ◽  
Li-Jun Huang ◽  
Dan Feng ◽  
Wenhan Jiang ◽  
Wenzhuo Miu ◽  
...  

Plant cells are separated by cellulose cell walls that impede direct cell-to-cell contact. In order to facilitate intercellular communication, plant cells develop unique cell-wall-spanning structures termed plasmodesmata (PD). PD are membranous channels that link the cytoplasm, plasma membranes, and endoplasmic reticulum of adjacent cells to provide cytoplasmic and membrane continuity for molecular trafficking. PD play important roles for the development and physiology of all plants. The structure and function of PD in the plant cell walls are highly dynamic and tightly regulated. Despite their importance, plasmodesmata are among the few plant cell organelles that remain poorly understood. The molecular properties of PD seem largely elusive or speculative. In this review, we firstly describe the general PD structure and its protein composition. We then discuss the recent progress in identification and characterization of PD-associated plant cell-wall proteins that regulate PD function, with particular emphasis on callose metabolizing and binding proteins, and protein kinases targeted to and around PD.


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