A Profusion of Molecular Scissors for Pectins: Classification, Expression, and Functions of Plant Polygalacturonases

Yang, Yang; Yu, Youjian; Liang, Ying; Anderson, Charles T.; Cao, Jiashu

doi:10.3389/fpls.2018.01208

Title: A Profusion of Molecular Scissors for Pectins: Classification, Expression, and Functions of Plant Polygalacturonases

Abstract

In plants, the construction, differentiation, maturation, and degradation of the cell wall are essential for development. Pectins, which are major constituents of primary cell walls in eudicots, function in multiple developmental processes through their synthesis, modification, and degradation. Several pectin modifying enzymes regulate pectin degradation via different modes of action. Polygalacturonases (PGs), which function in the last step of pectin degradation, are a crucial class of pectin-modifying enzymes. Based on differences in their hydrolyzing activities, PGs can be divided into three main types: exo-PGs, endo-PGs, and rhamno-PGs. Their functions were initially investigated based on the expression patterns of PG genes and measurements of total PG activity in organs. In most plant species, PGs are encoded by a large, multigene family. However, due to the lack of genome sequencing data in early studies, the number of identified PG genes was initially limited. Little was initially known about the evolution and expression patterns of PG family members in different species. Furthermore, the functions of PGs in cell dynamics and developmental processes, as well as the regulatory pathways that govern these functions, are far from fully understood. In this review, we focus on how recent studies have begun to fill in these blanks.more »« less

Authors:: Yang, Yang; Yu, Youjian; Liang, Ying; Anderson, Charles T.; Cao, Jiashu

Publication Date:: Tue Aug 14 00:00:00 EDT 2018

Research Org.:: Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF); Pennsylvania State Univ., University Park, PA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1464559

Alternate Identifier(s):: OSTI ID: 1510519

Grant/Contract Number:: DE–SC0001090; SC0001090

Resource Type:: Journal Article: Published Article

Journal Name:: Frontiers in Plant Science

Additional Journal Information:: Journal Name: Frontiers in Plant Science Journal Volume: 9; Journal ID: ISSN 1664-462X

Publisher:: Frontiers Research Foundation

Country of Publication:: Switzerland

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; polygalacturonase; pectin modification; cell wall; classification; expression pattern; function

Citation Formats


                    Yang, Yang, Yu, Youjian, Liang, Ying, Anderson, Charles T., and Cao, Jiashu. A Profusion of Molecular Scissors for Pectins: Classification, Expression, and Functions of Plant Polygalacturonases.  Switzerland: N. p., 2018. 
        Web.  doi:10.3389/fpls.2018.01208.

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                    Yang, Yang, Yu, Youjian, Liang, Ying, Anderson, Charles T., & Cao, Jiashu. A Profusion of Molecular Scissors for Pectins: Classification, Expression, and Functions of Plant Polygalacturonases.  Switzerland.  https://doi.org/10.3389/fpls.2018.01208

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                    Yang, Yang, Yu, Youjian, Liang, Ying, Anderson, Charles T., and Cao, Jiashu. 2018.  
        "A Profusion of Molecular Scissors for Pectins: Classification, Expression, and Functions of Plant Polygalacturonases".  Switzerland.  https://doi.org/10.3389/fpls.2018.01208.

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@article{osti_1464559,

  title        = {A Profusion of Molecular Scissors for Pectins: Classification, Expression, and Functions of Plant Polygalacturonases},

  author       = {Yang, Yang and Yu, Youjian and Liang, Ying and Anderson, Charles T. and Cao, Jiashu},

  abstractNote = {In plants, the construction, differentiation, maturation, and degradation of the cell wall are essential for development. Pectins, which are major constituents of primary cell walls in eudicots, function in multiple developmental processes through their synthesis, modification, and degradation. Several pectin modifying enzymes regulate pectin degradation via different modes of action. Polygalacturonases (PGs), which function in the last step of pectin degradation, are a crucial class of pectin-modifying enzymes. Based on differences in their hydrolyzing activities, PGs can be divided into three main types: exo-PGs, endo-PGs, and rhamno-PGs. Their functions were initially investigated based on the expression patterns of PG genes and measurements of total PG activity in organs. In most plant species, PGs are encoded by a large, multigene family. However, due to the lack of genome sequencing data in early studies, the number of identified PG genes was initially limited. Little was initially known about the evolution and expression patterns of PG family members in different species. Furthermore, the functions of PGs in cell dynamics and developmental processes, as well as the regulatory pathways that govern these functions, are far from fully understood. In this review, we focus on how recent studies have begun to fill in these blanks. On the basis of identified PG family members in multiple species, we review their structural characteristics, classification, and molecular evolution in terms of plant phylogenetics. We also highlight the diverse expression patterns and biological functions of PGs during various developmental processes, as well as their mechanisms of action in cell dynamic processes. How PG functions are potentially regulated by hormones, transcription factors, environmental factors, pH and Ca2+ is discussed, indicating directions for future research into PG function and regulation.},

  doi          = {10.3389/fpls.2018.01208},

  url          = {https://www.osti.gov/biblio/1464559},
  journal      = {Frontiers in Plant Science},

  issn         = {1664-462X},

  number       = ,

  volume       = 9,

  place        = {Switzerland},

  year         = {Tue Aug 14 00:00:00 EDT 2018},

  month        = {Tue Aug 14 00:00:00 EDT 2018}

}

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Summary Pectin is the most abundant component of primary cell walls in eudicot plants. The modification and degradation of pectin affects multiple processes during plant development, including cell expansion, organ initiation, and cell separation. However, the extent to which pectin degradation by polygalacturonases affects stem development and secondary wall formation remains unclear. Using an activation tag screen, we identified a transgenic Arabidopsis thaliana line with longer etiolated hypocotyls, which overexpresses a gene encoding a polygalacturonase. We designated this gene as POLYGALACTURONASE INVOLVED IN EXPANSION 2 ( PGX 2 ), and the corresponding activation tagged line as PGX 2 ^ATmore » . PGX 2 is widely expressed in young seedlings and in roots, stems, leaves, flowers, and siliques of adult plants. PGX 2‐ GFP localizes to the cell wall, and PGX 2 ^AT plants show higher total polygalacturonase activity and smaller pectin molecular masses than wild‐type controls, supporting a function for this protein in apoplastic pectin degradation. A heterologously expressed, truncated version of PGX 2 also displays polygalacturonase activity in vitro . Like previously identified PGX 1 ^AT plants, PGX 2 ^AT plants have longer hypocotyls and larger rosette leaves, but they also uniquely display early flowering, earlier stem lignification, and lodging stems with enhanced mechanical stiffness that is possibly due to decreased stem thickness. Together, these results indicate that PGX 2 both functions in cell expansion and influences secondary wall formation, providing a possible link between these two developmental processes.« less
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Abstract

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Cloning of cDNAs encoding cell-wall hydrolases from pear (Pyrus communis) fruit and their involvement in fruit softening and development of melting texture journal, February 2006

The Cleavable N-terminal Domain of Plant Endopolygalacturonases from Clade B May Be Involved in a Regulated Secretion Mechanism journal, July 2001

Pectin secretion and distribution in the anther during pollen development in Lilium journal, May 2001

Copy number variation of a gene cluster encoding endopolygalacturonase mediates flesh texture and stone adhesion in peach journal, February 2016

Characterization of a ubiquitous expressed gene family encoding polygalacturonase in Arabidopsis thaliana journal, January 2000

Expression patterns of cell wall-modifying genes from banana during fruit ripening and in relationship with finger drop journal, April 2009

The polygalacturonase gene BcMF2 from Brassica campestris is associated with intine development journal, November 2008

A Novel Approach to Dissect the Abscission Process in Arabidopsis journal, September 2012

Genome-wide identification and characterization of polygalacturonase genes in Cucumis sativus and Citrullus lanatus
journal, January 2014

Endopolygalacturonase and the Melting Flesh (M) Locus in Peach
journal, March 1996

Rhamnogalacturonan α-d-Galactopyranosyluronohydrolase: An Enzyme That Specifically Removes the Terminal Nonreducing Galacturonosyl Residue in Rhamnogalacturonan Regions of Pectin
journal, May 1998

The beta subunit of tomato fruit polygalacturonase isoenzyme 1: isolation, characterization, and identification of unique structural features.
journal, September 1992

Crystal Structure of Polygalacturonase from Erwinia carotovora ssp. carotovora
journal, September 1998

How to let go: pectin and plant cell adhesion
journal, July 2015

POLYGALACTURONASE INVOLVED IN EXPANSION3 Functions in Seedling Development, Rosette Growth, and Stomatal Dynamics in Arabidopsis thaliana
journal, October 2017

New Insights into the Role of T3 Loop in Determining Catalytic Efficiency of GH28 Endo-Polygalacturonases
journal, September 2015

Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species
journal, January 2014

Growth of the plant cell wall
journal, November 2005

POLYGALACTURONASE INVOLVED IN EXPANSION1 Functions in Cell Elongation and Flower Development in Arabidopsis
journal, March 2014

Suppression of 9 - cis - Epoxycarotenoid Dioxygenase, Which Encodes a Key Enzyme in Abscisic Acid Biosynthesis, Alters Fruit Texture in Transgenic Tomato
journal, November 2011

Polygalacturonase Gene Expression in Ripe Melon Fruit Supports a Role for Polygalacturonase in Ripening-Associated Pectin Disassembly
journal, June 1998

Activities of several membrane and cell-wall hydrolases, ethylene biosynthetic enzymes, and cell wall polyuronide degradation during low-temperature storage of intact and fresh-cut papaya (Carica papaya) fruit
journal, May 2003

Didehydrophenylalanine, an abundant modification in the beta subunit of plant polygalacturonases
journal, February 2017

Melatonin promotes ripening and improves quality of tomato fruit during postharvest life
journal, August 2014

Two crystal structures of pectin lyase A from Aspergillus reveal a pH driven conformational change and striking divergence in the substrate-binding clefts of pectin and pectate lyases
journal, May 1997

QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malusxdomestica Borkh.)
journal, May 2010

Overexpression of stress-inducible OsBURP16, the β subunit of polygalacturonase 1, decreases pectin content and cell adhesion and increases abiotic stress sensitivity in rice : OsBURP16 overexpression in rice
journal, November 2013

Gene structure dynamics and divergence of the polygalacturonase gene family of plants and fungus
journal, January 2008

Lateral Organ Boundaries Domain16 and 18 Act Downstream of the AUXIN1 and LIKE-AUXIN3 Auxin Influx Carriers to Control Lateral Root Development in Arabidopsis
journal, June 2015

Expression of Defense Genes in Strawberry Fruits Treated with Different Resistance Inducers
journal, March 2014

Pectin methylesterase and its proteinaceous inhibitor: a review
journal, December 2010

Polygalacturonase-Mediated Solubilization and Depolymerization of Pectic Polymers in Tomato Fruit Cell Walls: Regulation by pH and Ionic Conditions
journal, August 1998

Changes in Polygalacturonase Activity and Calcium Content during Ripening of Grape Berries
journal, January 2001

Shifting foundations: the mechanical cell wall and development
journal, February 2016

Papaya CpERF9 acts as a transcriptional repressor of cell-wall-modifying genes CpPME1/2 and CpPG5 involved in fruit ripening
journal, August 2016

The carbohydrate-binding module of Fragaria × ananassa expansin 2 (CBM-FaExp2) binds to cell wall polysaccharides and decreases cell wall enzyme activities “in vitro”
journal, July 2012

Enzyme-Less Growth in Chara and Terrestrial Plants
journal, June 2016

Annotation and comparative analysis of the glycoside hydrolase genes in Brachypodium distachyon
journal, January 2010

Toward a Systems Approach to Understanding Plant Cell Walls
journal, December 2004

Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution
journal, September 2001

BcMF9, a novel polygalacturonase gene, is required for both Brassica campestris intine and exine formation
journal, October 2009

AtC3H14, a plant-specific tandem CCCH zinc-finger protein, binds to its target mRNAs in a sequence-specific manner and affects cell elongation in Arabidopsis thaliana
journal, November 2014

The Role of Ethylene and Cold Temperature in the Regulation of the Apple POLYGALACTURONASE1 Gene and Fruit Softening
journal, March 2010

Polygalacturonases: Many Genes in Search of a Function
journal, June 1998

Characterization of a tobacco gene encoding a pollen-specific polygalacturonase
journal, May 1994

Expression of polygalacturonases and evidence to support their role during cell separation processes in Arabidopsis thaliana
journal, October 2007

Cobtorin target analysis reveals that pectin functions in the deposition of cellulose microfibrils in parallel with cortical microtubules: Function of pectin on cellulose deposition
journal, October 2010

Overexpression of AtDOF4.7, an Arabidopsis DOF Family Transcription Factor, Induces Floral Organ Abscission Deficiency in Arabidopsis
journal, May 2010

Pectin-Induced Changes in Cell Wall Mechanics Underlie Organ Initiation in Arabidopsis
journal, October 2011

Microspore Separation in the quartet 3 Mutants of Arabidopsis Is Impaired by a Defect in a Developmentally Regulated Polygalacturonase Required for Pollen Mother Cell Wall Degradation
journal, October 2003

Gibberellin-induced changes in the transcriptome of grapevine (Vitis labrusca × V. vinifera) cv. Kyoho flowers
journal, January 2015

Ethylene-Dependent and -Independent Processes Associated with Floral Organ Abscission in Arabidopsis
journal, December 2003

Control of root cap maturation and cell detachment by BEARSKIN transcription factors in Arabidopsis
journal, November 2016

A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: Confirmed actors and newcomers
journal, January 2008

Three Different Polygalacturonases Are Expressed in Tomato Leaf and Flower Abscission, Each with a Different Temporal Expression Pattern
journal, April 1997

An update on polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein that protects crop plants against pathogens
journal, March 2015

The role of pectin in plant morphogenesis
journal, September 2012

Oligogalacturonide-Auxin Antagonism Does Not Require Posttranscriptional Gene Silencing or Stabilization of Auxin Response Repressors in Arabidopsis
journal, August 2011

Intron loss mediated structural dynamics and functional differentiation of the polygalacturonase gene family in land plants
journal, December 2010

Patterns of expansion and expression divergence in the plant polygalacturonase gene family
journal, January 2006

Calcium deficiency in potato (Solanum tuberosum ssp. tuberosum) leaves and its effects on the pectic composition of the apoplastic fluid
journal, May 2000

Expression and sequence comparison of the Aspergillus niger and Aspergillus tubigensis genes encoding polygalacturonase II
journal, June 1991

Tracking developmentally regulated post-synthetic processing of homogalacturonan and chitin using reciprocal oligosaccharide probes
journal, November 2014

Thermal and High-Pressure Inactivation of Tomato Polygalacturonase: A Kinetic Study
journal, June 2002

Arabidopsis Phyllotaxis Is Controlled by the Methyl-Esterification Status of Cell-Wall Pectins
journal, December 2008

Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development
journal, January 2013

Biochemical characterization of a pollen-specific cDNA encoding polygalacturonase in Lilium longiflorum
journal, March 2006

ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 Are Polygalacturonases Required for Cell Separation during Reproductive Development in Arabidopsis
journal, January 2009

Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence
journal, March 2013

Report on the Current Inventory of the Toolbox for Plant Cell Wall Analysis: Proteinaceous and Small Molecular Probes
journal, May 2018

Expression Divergence and Functional Redundancy of Polygalacturonases in Floral Organ Abscission
journal, November 2006

Hypersensitive Ethylene Signaling and ZMdPG1 Expression Lead to Fruit Softening and Dehiscence
journal, March 2013

Biochemical and Immunocytological Characterizations of Arabidopsis Pollen Tube Cell Wall
journal, June 2010

An oligogalacturonide-derived molecular probe demonstrates the dynamics of calcium-mediated pectin complexation in cell walls of tip-growing structures
journal, May 2017

Activation tagging of Arabidopsis POLYGALACTURONASE INVOLVED IN EXPANSION2 promotes hypocotyl elongation, leaf expansion, stem lignification, mechanical stiffening, and lodging
journal, February 2017

Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling
journal, June 2006

Examination of the Abscission-Associated Transcriptomes for Soybean, Tomato, and Arabidopsis Highlights the Conserved Biosynthesis of an Extensible Extracellular Matrix and Boundary Layer
journal, December 2015

Cloning of cDNAs encoding cell-wall hydrolases from pear (Pyrus communis) fruit and their involvement in fruit softening and development of melting texture
journal, February 2006

The Cleavable N-terminal Domain of Plant Endopolygalacturonases from Clade B May Be Involved in a Regulated Secretion Mechanism
journal, July 2001

Pectin secretion and distribution in the anther during pollen development in Lilium
journal, May 2001

Copy number variation of a gene cluster encoding endopolygalacturonase mediates flesh texture and stone adhesion in peach
journal, February 2016

Characterization of a ubiquitous expressed gene family encoding polygalacturonase in Arabidopsis thaliana
journal, January 2000

Expression patterns of cell wall-modifying genes from banana during fruit ripening and in relationship with finger drop
journal, April 2009

The polygalacturonase gene BcMF2 from Brassica campestris is associated with intine development
journal, November 2008

A Novel Approach to Dissect the Abscission Process in Arabidopsis
journal, September 2012

Structure and Evolution of Parallel β-Helix Proteins
journal, January 1998

Postharvest UV-C irradiation inhibits the production of ethylene and the activity of cell wall-degrading enzymes during softening of tomato (Lycopersicon esculentum L.) fruit
journal, December 2013

A comparative analysis of the evolution, expression, and cis-regulatory element of polygalacturonase genes in grasses and dicots
journal, September 2016