Expansins and cell growth

doi:10.1016/j.pbi.2003.09.003

Current Opinion in Plant Biology

Volume 6, Issue 6, December 2003, Pages 603-610

https://doi.org/10.1016/j.pbi.2003.09.003 Get rights and content

Abstract

Expansins are now generally accepted to be key regulators of wall extension during growth. Several alternative roles for expansins have emerged in which the emphasis of their action is on wall breakdown or softening in processes such as fruit ripening, pollination, germination and abscission. Expansins are commonly encoded by substantial gene families and have classically been divided into two subfamilies, referred to as α- and β-expansins. Two further subfamilies have now been identified: γ-expansins, which were first described in Arabidopsis, and δ-expansins, which were identified in rice and are absent from Arabidopsis. Both are truncated versions of α- and β-expansins, with γ-expansins representing the amino-terminal half of a mature expansin and δ-expansins the carboxy-terminal half of a β-expansin. Functional roles for γ- and δ-expansins have yet to be defined, although recent data indicate a signalling role for γ-expansins.

Introduction

Cell growth and cell walls are intimately connected in plants. Cell walls have to be extremely strong to bear the stresses imposed by the internal turgor pressure of plant cells, but must also maintain the ability to extend during cell growth. The cellulose–hemicellulose network plays a leading role in determining the extensibility of cell walls, and enzymes that act on this network control the process of cell growth. Throughout the 1970s and 80s, it was generally held that glucanases loosen the structure of the wall to allow growth to occur. In the early 1990s, two new groups of proteins, xyloglucan endotransglucosylases (now known as xyloglucan endotransglucosylase/hydrolases [XTHs]) 1., 2. and expansins [3], almost simultaneously entered the pantheon of potential wall-loosening enzymes. XTHs are attractive wall-loosening candidates because their action involves breaking linkages in the xyloglucan–cellulose network and then reforming the same linkage in a new position. This action allows the breakage of stress-bearing bonds in the wall (thus increasing extensibility) without impairing overall wall integrity. This review focuses on the role of expansins in cell growth and other wall-associated events, and also provides an update on expansin sequence diversity.

Section snippets

Expansins induce wall extension during growth

Expansins were identified because of their ability to restore long-term extension to cell walls that were isolated from growing plant tissues [3]. The mechanism of expansin action appears to involve the disruption of hydrogen bonds between cellulose microfibrils and cross-linking glycans in the wall 4., 5.. Expansins directly induce wall extension whereas XTHs and glycanases generally do not 6., 7., as such a model involving primary and secondary wall-loosening mechanisms has been proposed [8].

The expansin gene family

The elucidation of the first expansin sequences [9] led to the realisation that these proteins are encoded by a substantial multigene family. Indeed the Arabidopsis genome contains 38 open reading frames (ORFs) that encode expansin-like proteins, two of which appear to be pseudogenes [10^••]. Phylogenetic analysis showed that the 38 ORFs could be separated into three clear subgroups on the basis of protein sequence similarity. The largest subgroup in Arabidopsis, with 26 members, is the

Eighty expansin-like ORFs in the rice genome

Lee and Kende 15., 16.• recently examined the rice expansin gene family and found a total of 40 expansin-encoding genes in rice. Now that the complete genome sequence of rice is publicly available, we have been able to ascertain the full extent of the rice expansin gene family and to compare it with that of Arabidopsis. BLAST searches of the rice genome revealed a total of 80 ORFs that encode expansin-like proteins, compared to the 38 in Arabidopsis. Sequence alignment and phylogenetic analysis

A new subfamily of expansin sequences

Rice possesses a hitherto unrecognised group of expansin-like sequences that are not found in Arabidopsis. On the basis of sequence similarity (Figure 2) and phylogenetic analysis, this subfamily (named δ-expansins) appears to have arisen as a result of recent duplication events associated with a distinct clade of β1-expansins (Figure 1). We have designated this group as a distinct subfamily because they encode truncated expansins that are similar in size to those of the γ-subfamily. By

Expansin biochemistry

Studies of expansin activity have generally involved the use of fairly crude protein extracts, which reveal little about the molecular details of expansin action. Several factors have limited the research carried out in this area. Expansins are difficult to purify, they are not typically abundant and most tissues express more than one closely related isoform. This is compounded by expansin assays that require a dedicated apparatus, are time-consuming and require considerable amounts of protein.

Expansins and growth

Expansins were identified because of their ability to induce wall extension, and the role of expansins in growth has been generally accepted. Initial studies [3] showed that expansin activity in cucumber hypocotyls was only extractable from actively growing tissues. Subsequent studies have generally supported this observation, highlighting a positive correlation between the presence of expansin activity, epitopes or transcripts and growth rates 22., 23., 24., 25., 26., 27..

Some of the most

Expansin mutants

We have obtained mutants lines that have T-DNA insertions in several different Arabidopsis expansin genes and have yet to see a pronounced phenotype in any of these plants. Similar outcomes have been reported elsewhere [34^••]. Moreover, it has been reported that knockout mutations in several expansin genes in the moss Physcomitrella patens caused no clear phenotype [35^•]. One clear reason that may account for this apparent lack of phenotype is the possibility of functional redundancy within the

Growth without expansins?

A recent report has indicated that expansins may not be required for plant growth in the grass Festuca pratensis, in which transcript accumulation for neither α- nor β-expansins correlated with regions of leaf cell expansion [21^••]. Similarly, in F. pratensis, assays of α-expansin activity and Western analysis indicated low expansin concentrations in the most rapidly growing tissues, with levels actually increasing as growth rates decreased. In-situ RNA hybridisation studies of α- and

Wall softening and breakdown

Several roles of expansins that do not involve wall expansion have emerged. Cosgrove et al. [11] showed that a β-expansin from maize pollen has expansin activity on maize silks. This protein is released from hydrating pollen grains onto the surface of the stigma and is proposed to soften stigmatic tissues, thus facilitating penetration by the pollen tube. Interestingly, it was recently shown that a similar (but in this case pistil-specific) β-expansin is expressed at high concentrations at the

Conclusions and future directions

It is over a decade since expansins were first identified. These past years have seen a consolidation of the view that expansins play a major role in cell-wall extension during growth, although there are tantalising indications that they might not always be completely necessary for this process. It has also become increasingly apparent that expansins are involved in a range of other wall-related processes beyond cell expansion. Several serious challenges remain to be tackled in this area.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

•
of special interest
••
of outstanding interest

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A novel protein associated with citrus blight has sequence similarities to expansin

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Natriuretic peptides and immunoreactants modify osmoticum-dependent volume changes in Solanum tuberosum L. mesophyll cell protoplasts

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Expansins: ever-expanding numbers and functions

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Expression of alpha-expansin and expansin-like genes in deepwater rice

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Expression of a heterologous expansin in transgenic tomato plants

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Expression of six expansin genes in relation to extension activity in developing strawberry fruit

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Local expression of expansin induces the entire process of leaf development and modifies leaf shape

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Differential expression of alpha- and beta-expansin genes in the elongating leaf of Festuca pratensis

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Expression of beta-expansins is correlated with internodal elongation in deepwater rice

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Submergence induces expansin gene expression in flooding-tolerant Rumex palustris and not in flooding-intolerant R. acetosa

Planta

(2000)

Cited by (275)

A conserved brassinosteroid-mediated BES1-CERP-EXPA3 signaling cascade controls plant cell elongation
2023, Cell Reports
Continuous plant growth is achieved by cell division and cell elongation. Brassinosteroids control cell elongation and differentiation throughout plant life. However, signaling cascades underlying BR-mediated cell elongation are unknown. In this study, we introduce cotton fiber, one of the most representative single-celled tissues, to decipher cell-specific BR signaling. We find that gain of function of GhBES1, a key transcriptional activator in BR signaling, enhances fiber elongation. The chromatin immunoprecipitation sequencing analysis identifies a cell-elongation-related protein, GhCERP, whose transcription is directly activated by GhBES1. GhCERP, a downstream target of GhBES1, transmits the GhBES1-mediated BR signaling to its target gene, GhEXPA3-1. Ultimately, GhEXPA3-1 promotes fiber cell elongation. In addition, inter-species functional analysis of the BR-mediated BES1-CERP-EXPA3 signaling cascade also promotes Arabidopsis root and hypocotyl growth. We propose that the BES1-CERP-EXPA3 module may be a broad-spectrum pathway that is universally exploited by diverse plant species to regulate BR-promoted cell elongation.
SlGH9-15 regulates tomato fruit cracking with hormonal and abiotic stress responsiveness cis-elements
2023, Journal of Integrative Agriculture
Fruit cracking occurs easily during the late period of fruit development when plants encounter an unsuitable environment, dramatically affecting fruit production and marketing. This study conducted the bulked segregant RNA-Seq (BSR) to identify the key regulatory gene of fruit cracking in tomatoes. BSR-Seq analysis illustrated that two regions associated with irregularly cracking were located on chromosomes 9 and 11, containing 127 candidate genes. Further, through differentially expression analysis and qRT-PCR in cracking-susceptible and cracking-resistant genotypes, the candidate gene SlGH9-15 (Solyc09g010210) with significantly differential expression levels was screened. Bioinformatics analysis of the GH9 gene family revealed that 20 SlGH9 genes were divided into three groups. The phylogenetic analysis showed that SlGH9-15 was closely related to cell wall construction-associated genes AtGH9B1, AtGH9B6, OsGH9B1, and OsGH9B3. The cis-acting elements analysis revealed that SlGH9-15 was activated by various hormones (ethylene and ABA) and abiotic stresses. The expression pattern indicated that 13 SlGH9 genes, especially SlGH9-15, were highly expressed in the cracking-susceptible genotype. Its expression level gradually increased during fruit development and achieved maximum value at the red ripe stage. Additionally, the cracking-susceptible tomato showed higher cellulase activity and lower cellulose content than the cracking-resistant tomato, particularly at the red ripe stage. This study identified SlGH9-15 as a key gene associated with fruit cracking in tomatoes for the first time and gives new insights for understanding the molecular mechanism and complex regulatory network of fruit cracking.
Fruit quality parameters and volatile compounds from ‘Palmer’ mangoes with internal breakdown
2022, Food Chemistry
The internal breakdown (IB) is a premature and uneven mango pulp ripening physiological disorder that is noticed only when the fruit is sliced for consumption. Thus, there is a demand for analytical methods to detect IB in mangoes to avoid consumer dissatisfaction and reduce postharvest waste. In this work, physicochemical and volatile compounds were determined to evaluate the ability to predict pulp IB. Principal components analysis (PCA) and partial least squares discriminant analysis (PLS-DA) of the data show that color, firmness, and volatiles compounds are important to give some information about the physiological changes caused by IB. The volatile compounds methacrylic acid, ethyl ester, isopentyl ethanoate, limonene oxide, (E)-2-pentenal, tetradecane, and γ-elemene were identified as chemical markers of IB. Therefore, mango physical and chemical characteristics combined with PCA and PLS-DA were successfully employed for the identification of IB in mangoes, showing significant differences between healthy and IB fruits.
Boosting enzymatic degradation of cellulose using a fungal expansin: Structural insight into the pretreatment mechanism
2022, Bioresource Technology
The recalcitrance of cellulosic biomass greatly hinders its enzymatic degradation. Expansins induce cell wall loosening and promote efficient cellulose utilization; however, the molecular mechanism underlying their action is not well understood. In this study, TlEXLX1, a fungal expansin from Talaromyces leycettanus JCM12802, was characterized in terms of phylogeny, synergy, structure, and mechanism of action. TlEXLX1 displayed varying degrees of synergism with commercial cellulase in the pretreatment of corn straw and filter paper. TlEXLX1 binds to cellulose via domain 2, mediated by CH–π interactions with residues Tyr291, Trp292, and Tyr327. Residues Asp237, Glu238, and Asp248 in domain 1 form hydrogen bonds with glucose units and break the inherent hydrogen bonding within the cellulose matrix. This study identified the expansin amino acid residues crucial for cellulose binding, and elucidated the structure and function of expansins in cell wall networks; this has potential applications in biomass utilization.
Comparative transcriptome study of the elongating internode in elephant grass (Cenchrus purpureus) seedlings in response to exogenous gibberellin applications
2022, Industrial Crops and Products
Bioenergy grass provides an important biomass resource for biofuel production worldwide. The internode elongation of grass stems is central to biomass production for biofuels; however, this process is poorly understood in elephant grass because it is a complex trait regulated by many genes. In this study, we adopted phenotypic, histological, transcriptomic, and phytohormone methods to investigate the regulatory mechanisms of internode elongation mediated by gibberellin (GA) in a dwarf cultivar and a standard cultivar. Phenotypic analysis revealed that exogenous GA₃ increased plant height by inducing both internode length and internode number in two cultivars with contrasting internode lengths. Histological analysis revealed that the GA₃ application increased the internode elongation through inducing both cell division and cell elongation. Phytohormone analysis indicated that exogenous GA₃ treatment significantly increased endogenous indole-3-acetic acid (IAA), and zeatin (ZR) contents but decreased abscisic acid (ABA) contents, while the expression levels of genes related to hormone metabolism and signaling were substantially changed. Consistent with the expression pattern, a significant increase in lignin and cellulose content were also observed after GA₃ treatment. Genes and transcription factors related to hormone metabolism and signaling, cell division, cell wall biosynthesis, and plant growth were identified as hub genes in the core coexpression network of the response to GA₃ application. This study showed that active cell division, cell elongation, and cell wall biosynthesis contribute to internode elongation following exogenous GA₃ applications and identified hub genes for these complex regulatory networks. These data elucidate mechanisms governing internode elongation in elephant grass and help breeders to develop elite cultivars with high biomass.
Genome-wide identification of expansin in Fragaria vesca and expression profiling analysis of the FvEXPs in different fruit development
2022, Gene
Strawberry is a highly efficient and economical horticultural crop plant, and strawberry fruits are easy to soften after ripening and decay after harvest, which severely impacts the economic benefits. Expansins are plant cell-wall loosening proteins involved in the process of fruit softening, loosening cell walls and reducing fruit firmness. In this study, 35 FvEXPs genes were identified in the F. vesaca genome. These genes were divided into four subfamilies (27 FvEXPAs, 5 FvEXPBs, 1 FvEXLAs, and 2 FvEXLBs) and were unevenly distributed on 7 chromosomes. Gene structure and motif analysis showed the conserved structure and motif in same subgroup, however, the different motifs and structures may reveal functional divergence of multigene family members of FvEXPs in different developmental stages of fruits. The expression profiling by RNA-seq and qRT-PCR analysis revealed that the FvEXP genes have distinct expression patterns among different stages of strawberry development and ripening. Among them, 3 genes (FvEXPA9, FvEXPA12, and FvEXPA27) were highly expressed in the ripening stage, FvEXPA9 and FvEXPA12 were especially highly expressed in turning stage, whereas FvEXPA27 was especially highly expressed in red stage. Our study provides a better understanding of the FvEXP genes, which may benefit strawberry biotechnological breeding and genetic modification for improving fruit quality and delaying fruit softening.

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^☆: Supplementary material associated with this article can be found at doi: 10.1016/j.pbi.2003.09.003

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Expansins and cell growth☆

Abstract

Introduction

Section snippets

Expansins induce wall extension during growth

The expansin gene family

Eighty expansin-like ORFs in the rice genome

A new subfamily of expansin sequences

Expansin biochemistry

Expansins and growth

Expansin mutants

Growth without expansins?

Wall softening and breakdown

Conclusions and future directions

References and recommended reading

J. Biol. Chem.

Plant Physiol. Biochem.

J. Mol. Evol.

Plant J.

Plant Cell Physiol.

Xyloglucan endotransglycosylase, a new wall-loosening enzyme-activity from plants

Biochem. J.

Two endogenous proteins that induce cell-wall extension in plants

Plant Cell

Disruption of hydrogen-bonding between plant-cell wall polymers by proteins that induce wall extension

Proc. Natl. Acad. Sci. U.S.A.

Expansin mode of action on cell walls: analysis of wall hydrolysis, stress-relaxation, and binding

Plant Physiol.

The relationship between xyloglucan endotrans-glycosylase and in vitro cell wall extension in cucumber hypocotyls

Planta

Autolysis and extension of isolated walls from growing cucumber hypocotyls

J. Exp. Bot.

Molecular-cloning and sequence-analysis of expansins — a highly conserved, multigene family of proteins that mediate cell-wall extension in plants

Proc. Natl. Acad. Sci. U.S.A.

Plant expansins are a complex multigene family with an ancient evolutionary origin

Plant Physiol.

Group I allergens of grass pollen as cell wall-loosening agents

Proc. Natl. Acad. Sci. U.S.A.

A novel protein associated with citrus blight has sequence similarities to expansin

Plant Mol. Biol.

Natriuretic peptides and immunoreactants modify osmoticum-dependent volume changes in Solanum tuberosum L. mesophyll cell protoplasts

Plant Sci.

Expansins: ever-expanding numbers and functions

Curr. Opin. Plant Biol.

Expression of alpha-expansin and expansin-like genes in deepwater rice

Plant Physiol.

Expression of a heterologous expansin in transgenic tomato plants

Planta

Expression of six expansin genes in relation to extension activity in developing strawberry fruit

J. Exp. Bot

Local expression of expansin induces the entire process of leaf development and modifies leaf shape

Proc. Natl. Acad. Sci. U.S.A.

Differential expression of alpha- and beta-expansin genes in the elongating leaf of Festuca pratensis

Plant Mol. Biol.

Expression of beta-expansins is correlated with internodal elongation in deepwater rice

Plant Physiol.

Submergence induces expansin gene expression in flooding-tolerant Rumex palustris and not in flooding-intolerant R. acetosa

Planta