Performing the paradoxical: how plant peroxidases modify the cell wall

doi:10.1016/j.tplants.2004.09.002

Trends in Plant Science

Volume 9, Issue 11, November 2004, Pages 534-540

https://doi.org/10.1016/j.tplants.2004.09.002 Get rights and content

Since their appearance in the first land plants, genes encoding class III peroxidases have been duplicated many times during evolution and now compose a large multigene family. The reason for these many genes is elusive, and we are still searching for the specific function of every member of the family. Nevertheless, our current understanding implicates peroxidases as key players during the whole life cycle of a plant, and particularly in cell wall modifications, in roles that can be antagonistic depending on the developmental stage. This diversity of functions derives in part from two possible catalytic cycles of peroxidases involving the consumption or release of H₂O₂ and reactive oxygen species (e.g. O₂ radical dot ⁻, H₂O₂, OH).

Section snippets

Germination

Peroxidase activity can be detected in seeds and their mucilage before germination. By generating hydroxyl radicals ( radical dot OH), peroxidases could play a crucial role in seed protection as well as in the first days of germination by reducing pathogenic attack. Indeed, ROS are believed to play a role in defending seeds against pathogens. In this respect, two studies of tomato (Lycopersicon esculentum) and radish (Raphanus sativus) seeds confirm that peroxidase production begins as soon as the radicle

Cellular growth and cell wall loosening

Growth by cell elongation (as opposed to growth by cell division) leads to an irreversible increase in cell volume that occurs together with a relaxation of the cell wall. The biochemical processes involved in cell wall loosening during extension growth are only partially known. Several enzymatic mechanisms have been proposed, such as the cleavage and reassembly of xyloglucan polymers by xyloglucan endotransglycosylase or the suppression of hydrogen bonds between cellulose and xyloglucan by

Cell wall cross-linking

Peroxidases can control the availability of H₂O₂ in the cell wall (Figure 2), which is a prerequisite for the cross-linking of phenolic groups, to inhibit cell elongation (Figure 4). Peroxidases catalyze this process in response to various external factors such as wounding, pathogen interactions and environmental constraints or just as a part of normal cell wall development during growth, differentiation and senescence. Indeed, dehydration and pathogen invasion can be limited by the formation

Diferulic bonds

The formation of diferulic linkages occurs at various stages during cell wall formation. Elongation and cell wall extensibility are inversely correlated to the increase in the content of ferulic and diferulic acid in the primary cell wall 31, 32, 33. Indeed, during lignification, cell walls are further stiffened by the formation of diferulic linkages between polysaccharide-bound lignins or polysaccharides. Ferulate can also join a lignin moiety to a polysaccharide without forming a diferulic

Extensins

Extensins are hydroxyproline-rich proteins (HPRP) and are essential for primary cell wall structure and development in plants 40, 41, 42. There is strong evidence that peroxidases work closely with extensins during the process of cell wall stiffening. Peroxidases can create rigid extensin cross-links that block any further wall loosening and hence cell expansion [43]. The precise nature of these cross-links is still being debated: isodityrosine bonds or Tyr–Lys bonds have been implicated in

Lignification and suberization

Cross-linking of phenolic monomers in the formation of suberin and the oxidative coupling of lignin subunits as part of lignin biosynthesis are related to secondary cell wall formation [56] and have been associated with reduction of extensibility and growth. Peroxidases [57] and laccases [58] are both candidates for monolignol unit oxidation, which leads to the final step of lignin assembly. Using H₂O₂ as an oxidant, peroxidases can generate monolignol phenoxy radicals that couple spontaneously

Senescence

Senescence is the final stage before complete tissue death. It is dependent on various plant hormones, such as cytokinins, which prevent the onset of senescence, or ethylene and salicylic acid, which by contrast induce the senescent phenotype in vivo [69]. Several morphological and cellular changes are associated with this mechanism. For example, in some plants, leaves fall off the stem (abscission) before complete death. Moreover, changes in gene expression have been reported during

Conclusions

To date, studies of plant peroxidases have provided evidence that class III peroxidases are omnipresent enzymes, expressed throughout the plant life cycle from germination to senescence. They can induce cell wall loosening and growth by elongation as well as cross-linking of cell wall components. Indeed, the balance between cleavage and cross-linking is associated with ROS action and with H₂O₂ and ascorbate concentrations. These compounds can regulate enzyme activity as well as peroxidase gene

Acknowledgements

We thank William Deakin and Xavier Perret for their critical reading and constructive suggestions, and Olivier Lustenberger, Laurent Falquet and Vassilios Ioannidis for the realization of the peroxidase website. We thank the University of Geneva and the Swiss National Science Foundation (grant 31-068003.02) for research support to C.P. and C.D.

Glossary

Heme peroxidases:: oxidoreductases containing usually ferriprotoporphyrin IX as prosthetic group. Able to oxidize various substrates via the reduction of hydrogen peroxide.
Neofunctionalization:: acquisition of a novel function in a protein owing to mutations or duplications at the DNA level during evolution.
Paralog:: homologous genes produced by duplication within a genome.
Suberin:: wax-like lipid polymer resulting from the polymerization of fatty acids and phenolics. It is formed in the outer cell

References (76)

D.J. Schuller
The crystal structure of peanut peroxidase
Structure
(1996)
M. Tognolli
Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana
Gene
(2002)
F. Passardi
The plant peroxidase multigenic family in rice and its evolution in green plants
Phytochemistry
(2004)
J. Zhang
Evolution by gene duplication: an update
Trends Ecol. Evol.
(2003)
C. Dunand
Expression of a peroxidase gene in zucchini in relation with hypocotyl growth
Plant Physiol. Biochem.
(2003)
C. Schweikert
Scission of polysaccharides by peroxidase-generated hydroxyl radicals
Phytochemistry
(2000)
J.G. Miller et al.
Characteristics of xyloglucan after attack by hydroxyl radicals
Carbohydr. Res.
(2001)
Y. Kawamura
Stress-relaxation analysis of submerged and air-grown rice coleoptiles: correlation with cell wall biosynthesis and growth
J. Plant Physiol.
(2000)
N.C. Veitch
Horseradish peroxidase: a modern view of a classic enzyme
Phytochemistry
(2004)
N.J. Price
A biochemical and molecular characterization of LEP1, an extensin peroxidase from lupin
J. Biol. Chem.
(2003)

C. Dunand

Identification and characterisation of Ca²⁺–pectate binding peroxidases in Arabidopsis thaliana

J. Plant Physiol.

(2002)

K. Shah

Purification and identification of a Ca²⁺–pectate binding peroxidase from Arabidopsis leaves

Phytochemistry

(2004)

K.A. Blee

A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification

Phytochemistry

(2003)

M.C. Kiefer-Meyer

Cloning and sequence analysis of laccase-encoding cDNA clones from tobacco

Gene

(1996)

L. Valério

Expression analysis of the Arabidopsis peroxidase multigenic family

Phytochemistry

(2004)

K.G. Welinder

Plant peroxidases: structure–function relationships

L. Duroux et al.

The peroxidase gene family in plants: a phylogenetic overview

J. Mol. Evol.

(2003)

S. Hiraga

A large family of class III plant peroxidases

Plant Cell Physiol.

(2001)

C. Penel

Plant Peroxidases

(1992)

A. Liszkay

Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth

Planta

(2003)

G.I. Berglund

The catalytic pathway of horseradish peroxidase at high resolution

Nature

(2002)

B. Halliwell

Generation of hydrogen peroxide, superoxide and hydroxyl radicals during the oxidation of dihydroxyfumaric acid by peroxidase

Biochem. J.

(1977)

Y. Morohashi et al.

Development of beta-1,3-glucanase activity in germinated tomato seeds

J. Exp. Bot.

(2000)

C.T. Wu

Class I beta-1,3-glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence

Plant Physiol.

(2001)

L.M. Bellani

Differences in the activity and distribution of peroxidases from three different portions of germinating Brassica oleracea seeds

Physiol. Plant.

(2002)

M. Gijzen

Seed peroxidases

Plant Perox. Newslett.

(1997)

A. Scialabba

Effects of ageing on peroxidase activity and localization in radish (Raphanus sativus L.) seeds

Eur. J. Histochem.

(2002)

J. Cordewener

Tunicamycin-inhibited carrot somatic embryogenesis can be restored by secreted cationic peroxidase isoenzymes

Planta

(1991)

D.J. Cosgrove

Wall structure and wall loosening. A look backwards and forwards

Plant Physiol.

(2001)

P. Schopfer

Histochemical demonstration and localization of H₂O₂ in organs of higher plants by tissue printing on nitrocellulose paper

Plant Physiol.

(1994)

J.H. Joo

Role of auxin-induced reactive oxygen species in root gravitropism

Plant Physiol.

(2001)

M. Cordoba-Pedregosa

Zonal changes in ascorbate and hydrogen peroxide contents, peroxidase, and ascorbate-related enzyme activities in onion roots

Plant Physiol.

(2003)

M. Cordoba-Pedregosa

Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate

Plant Physiol.

(1996)

S.C. Fry

Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals

Biochem. J.

(1998)

S.X. Chen et al.

Hydroxyl-radical production in physiological reactions. A novel function of peroxidase

Eur. J. Biochem.

(1999)

A.A. Rodriguez

Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension

Plant Physiol.

(2002)

P. Schopfer

Evidence that hydroxyl radicals mediate auxin-induced extension growth

Planta

(2002)

P. Schopfer

Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth

Plant J.

(2001)

Cited by (720)

Overexpressing peach PpePAO1 gene improves the nutrient value of tomato and enhances resistance against Botrytis cinerea
2024, Postharvest Biology and Technology
Polyamine oxidase (PAO), which catalyzes the catabolism of spermidine and spermine, is involved in fruit ripening and pathogen response. However, the function of PAO in fruit quality and disease resistance against Botrytis cinerea (B. cinerea) is still unclear. The effect of polyamine oxidation on tomato fruit quality and disease resistance against B. cinerea was investigated. Overexpressing peach PAO gene PpePAO1 increased ethylene production and accelerated fruit ripening of transgenetic lines. The ascorbic acid (AsA) and lycopene contents were dramatically higher in transgenic lines. The transgenic lines exhibited a much lower disease incidence and smaller lesion area after incubation of B. cinerea. The contents of H₂O₂ and O₂^•− in transgenic fruits were much higher than control after infection, and an ROS burst and PCD were observed in the infection site of transgenic leaves. Furthermore, the activity of the antioxidases SOD, POD, CAT and APX were higher in transgenic lines after infection. The expression of AsA biosynthesis-related genes in transgenic lines was significantly higher than control. Taken together, our study highlights enhancing polyamine oxidation as a novel approach for improving the nutritional value of tomato and resistance against B. cinerea.
Genome-wide identification of class III peroxidases in colored calla lily and enhanced resistance to soft rot bacteria
2024, Physiological and Molecular Plant Pathology
Soft rot disease is one of the primary issues in the production of colored calla lilies, significantly limiting large-scale production. This research conducts an in-depth investigation of the class III peroxidase gene family in colored calla lily, identifying 80 ZePER genes, with their motifs and structural domains remaining conserved. Through phylogenetic tree analysis, these genes were classified into 9 distinct clades. Collinearity analysis and the distribution of ZePER genes suggest that the two main events of ZePER gene family evolution was whole-genome duplication (WGD) as well as tandem duplication. Cis-acting element analysis showed that the ZePER genes could be directly modulated by essential hormones like jasmonic acid (JA) and salicylic acid (SA), highlighting their role in biotic stress responses. Transcriptome profiling revealed tissue-specific gene expressions and their essential function in responding to soft rot bacteria. Upon inoculation with Pectobacterium carotovorum, the leaves manifested a significant upregulation of ZePER genes expression, and there was a concurrent surge in JA and SA content. Treatments with methyl jasmonate (MeJA) and benzothiadiazole (BTH) induced ZePER gene expression and augmented the plant's disease resistance. This indicates the crucial role of ZePER genes in regulating reactive oxygen species in leaves. In summary, these findings emphasize the importance of ZePER genes in the defense mechanisms of colored calla lily.
Roles and regulation of the RBOHD enzyme in initiating ROS-mediated systemic signaling during biotic and abiotic stress
2024, Plant Stress
Reactive oxygen species are, at high levels, harmful to plant cells, whereas, at a balanced and controlled level, they are involved in transduction of oxidative signaling. The apoplast, also known as the extracellular matrix plays a vital role in transferring the extracellular signals to internal organelles and the signal from cell to cell. Moreover, having a lower level of antioxidants renders it a favorable compartment for ROS production and maintenance. Multiple routes for H₂O₂ production exist in the apoplast; however, a prominent source is the NADPH oxidases, also named respiratory burst oxidase homologs (RBOHs). Many stimuli, such as pathogens, extracellular ATP, hormones, and abiotic stresses can trigger the RBOH-dependent ROS production in the apoplast. RBOHD and RBOHF are extensively studied and proposed typical roles in stomatal conductance and pathogen responses. In this review, we provide an update on RBOH enzymes and the regulatory mechanisms controlling the key enzyme of the family, RBOHD. Furthermore, we performed a phylogenetic analysis by including the RBOH protein family of Arabidopsis and some important crop species which have not been studied before, such as Brasssica rapa, Brassica oleracea, Oriza sativa, Glycine max, and Zea mays to characterize the evolutionary relationship of these isoforms in order to better classify them. We further describe how ROS are perceived and transduced inside the cell and how this interlinks with other systemic signals, including hormones, and abiotic stress responses such as those toward light and salt stress.
Shaping the life in karst: Antioxidative response of two Balkan endemic Scilla species
2024, Biochemical Systematics and Ecology
Scilla litardierei and S. lakusicii are closely related species endemic to the Dinarides. While S. litardierei is a characteristic species of wet meadows in karst fields, S. lakusicii inhabits open rocky habitats in the surroundings of karst fields. During their life cycle, plants in karst areas are subjected to the influence of drought, waterlogging, high temperature and high intensity of light. The goal of our investigation was a comparative analysis of the isoenzyme profiles and activities of superoxide dismutase (SOD) and Class III peroxidase (POX) in the roots, leaves and flowers of S. litardierei and S. lakusicii that grew in different karst localities within their native range in the Dinarides. Field research was performed on karst fields and neighboring karst areas in eastern Herzegovina (Bosnia and Herzegovina) during the vegetation season in 2017. SODs are key enzymes in plant antioxidant defense, while POXs, in addition to their antioxidant role, play an important role in plant growth and development. The highest protein concentration in roots was measured for S. litardierei from the Lastva locality (13.416 ± 4.213 mg/gFW), while the lowest was measured in S. lakusicii from Popovo Polje (2.516 ± 0.565 mg/gFW). The highest SOD activity was measured for all three plants' organs from Fatničko Polje. The highest POX activity in leaf samples was measured in S. litardierei from Dabarsko Polje (0.6012 ± 0.210 μmol/mg*min), in the flower samples also in S. litardierei from Dabarsko Polje (0.288 ± 0.005 μmol/mg*min), while in root samples the highest POX activity was measured in S. litardierei from Fatničko Polje. SOD and POX isoenzyme profiles vary depending on Scilla species, locality and plant organ. According to our results, SOD and POX could play an important role in the adaptive mechanisms of Scilla species in their natural karst habitats.
Genome-wide identification of the Pyrus R2R3-MYB gene family and PhMYB62 regulation analysis in Pyrus hopeiensis flowers at low temperature
2024, International Journal of Biological Macromolecules
The R2R3-MYB gene family play an important role in plant growth, development and stress responses. In this study, a total of 122 PcoR2R3-MYB genes were identified and grouped into 26 clades in pear. And these PcoMYBs were unevenly distributed among 17 chromosomes. The sequence characteristics, conversed motifs, exon/intron structures, classification, duplication events and cis-acting elements were also investigated. The gene duplication events showed that segmental duplication may play key roles in expansion of the PcoMYB gene family. Pyrus hopeiensis, which is a valuable wild resource, has strong cold resistance. An integrative analyses of miRNA and mRNA showed that PhMYB62 was involved in regulating low-temperature stress in P. hopeiensis flower organs. Subcellular localization analysis showed that PhMYB62 protein was specifically localized to the nucleus. The result of DAP-seq showed that PhMYB62 responded to low-temperature stress in P. hopeiensis by regulating TFs, which were associated with plant stress resistance, and POD, GAUT12, AUX28 and CHS genes. Subsequently, yeast one-hybrid verified that PhMYB62 could bind and activate the promoter of POD gene. The current study would provide a comprehensive information for further functional research on the stress-responsive R2R3-MYB gene candidates in pear, and may help to identify the genes associated with cold resistance for the cultivation of cold-resistant pear varieties.
Yarrowia lipolytica increased the activities of disease defense related enzymes and anti-fungal compounds in asparagus (Asparagus officinalis)
2024, Pesticide Biochemistry and Physiology
Fungal diseases pose significant threats to the production of asparagus, resulting in economic losses and decreased crop quality. The potential of the yeast Yarrowia lipolytica as a biocontrol agent against Fusarium proliferatum, a common pathogen of asparagus, was investigated in this study. The effects of Y. lipolytica treatment on decay incidence, disease index, and activities of major disease defense-related enzymes were investigated. In addition, we examined the levels of antifungal compounds such as total phenols, flavonoids, and lignin in asparagus plants exposed to Y. lipolytica. The results showed that Y. lipolytica treatment significantly reduced decay incidence and disease index caused by F. proliferatum when compared to the control group. Furthermore, Y. lipolytica-treated plants showed increased activity of disease defense-related enzymes, indicating that defense responses were activated. The activities of all evaluated enzymes were significantly higher in Y. lipolytica-treated asparagus, indicating an improved ability to combat fungal pathogens. Furthermore, Y. lipolytica treatment increased the content of antifungal compounds such as total phenols, flavonoids, and lignin, which are known to possess antimicrobial properties. These findings highlight the potential of Y. lipolytica as a biocontrol agent for fungal diseases in asparagus crops. The ability of Y. lipolytica to reduce disease incidence, boost disease defense-related enzymes, and increase antifungal compound content provides valuable insights into its efficacy as a natural and sustainable approach to disease management. However, further investigations are needed to optimize application methods and determine its efficacy under field conditions.

View all citing articles on Scopus

View full text

Trends in Plant Science

Performing the paradoxical: how plant peroxidases modify the cell wall

Section snippets

Germination

Cellular growth and cell wall loosening

Cell wall cross-linking

Diferulic bonds

Extensins

Lignification and suberization

Senescence

Conclusions

Acknowledgements

Glossary

Structure

Gene

Phytochemistry

Trends Ecol. Evol.

Plant Physiol. Biochem.

Phytochemistry

Carbohydr. Res.

J. Plant Physiol.

Phytochemistry

J. Biol. Chem.

J. Plant Physiol.

Phytochemistry

Phytochemistry

Gene

Phytochemistry

Plant peroxidases: structure–function relationships

The peroxidase gene family in plants: a phylogenetic overview

J. Mol. Evol.

A large family of class III plant peroxidases

Plant Cell Physiol.

Plant Peroxidases

Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth

Planta

The catalytic pathway of horseradish peroxidase at high resolution

Nature

Generation of hydrogen peroxide, superoxide and hydroxyl radicals during the oxidation of dihydroxyfumaric acid by peroxidase

Biochem. J.

Development of beta-1,3-glucanase activity in germinated tomato seeds

J. Exp. Bot.

Class I beta-1,3-glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence

Plant Physiol.

Differences in the activity and distribution of peroxidases from three different portions of germinating Brassica oleracea seeds

Physiol. Plant.

Seed peroxidases

Plant Perox. Newslett.

Effects of ageing on peroxidase activity and localization in radish (Raphanus sativus L.) seeds

Eur. J. Histochem.

Tunicamycin-inhibited carrot somatic embryogenesis can be restored by secreted cationic peroxidase isoenzymes

Planta

Wall structure and wall loosening. A look backwards and forwards

Plant Physiol.

Histochemical demonstration and localization of H2O2 in organs of higher plants by tissue printing on nitrocellulose paper

Plant Physiol.

Role of auxin-induced reactive oxygen species in root gravitropism

Plant Physiol.

Zonal changes in ascorbate and hydrogen peroxide contents, peroxidase, and ascorbate-related enzyme activities in onion roots

Plant Physiol.

Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate

Plant Physiol.

Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals

Biochem. J.

Hydroxyl-radical production in physiological reactions. A novel function of peroxidase

Eur. J. Biochem.

Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension

Plant Physiol.

Evidence that hydroxyl radicals mediate auxin-induced extension growth

Planta

Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth

Plant J.

Histochemical demonstration and localization of H₂O₂ in organs of higher plants by tissue printing on nitrocellulose paper