The expansin superfamily
© BioMed Central Ltd 2005
Published: 28 November 2005
The expansin superfamily of plant proteins is made up of four families, designated α-expansin, β-expansin, expansin-like A and expansin-like B. α-Expansin and β-expansin proteins are known to have cell-wall loosening activity and to be involved in cell expansion and other developmental events during which cell-wall modification occurs. Proteins in these two families bind tightly to the cell wall and their activity is typically assayed by their stimulation of cell-wall extension and stress relaxation; no bona fide enzymatic activity has been detected for these proteins. α-Expansin proteins and some, but not all, β-expansin proteins are implicated as catalysts of 'acid growth', the enlargement of plant cells stimulated by low extracellular pH. A divergent group of β-expansin genes are expressed at high levels in the pollen of grasses but not of other plant groups. They probably function to loosen maternal cell walls during growth of the pollen tube towards the ovary. All expansins consist of two domains; domain 1 is homologous to the catalytic domain of proteins in the glycoside hydrolase family 45 (GH45); expansin domain 2 is homologous to group-2 grass pollen allergens, which are of unknown biological function. Experimental evidence suggests that expansins loosen cell walls via a nonenzymatic mechanism that induces slippage of cellulose microfibrils in the plant cell wall.
Gene organization and evolutionary history
Sizes of the four expansin families in different plants
Last common ancestor
Curiously, grasses (but only grasses) also have an additional group of secreted proteins homologous only to expansin domain 2; these are known in the immunological literature as grass group-2 pollen allergens (G2As). They seem to have evolved from a truncated copy of a β-expansin gene and they share about 35-45% protein identity with their closest β-expansin relatives; their native biological function is uncertain. Although G2As evolved from a β-expansin ancestor, because of the loss of domain 1 they are considered a separate family and not part of the expansin superfamily.
Two other families of plant proteins show distant homology to expansin domain 1, but as they lack domain 2 they are not considered part of the superfamily. The closest (approximately 25-35% identity) has been variously called p12 and plant natriuretic peptide (PNP). These proteins become abundant in the xylem of blighted citrus trees , and they have been ascribed a signaling function [9, 10]. No wall-loosening activity has been found in extracts containing p12 (D.J.C. and T. Ceccardi, unpublished observations). More distantly related (about 20-30% identity) is the barwin-like domain that defines the PR4 family of antifungal proteins . Both these protein families were already present in the last ancestor of mosses and vascular plants.
Turning to non-plant organisms, various proteins with distant homology to full-length expansins or exclusively to domain 1 are found from bacteria to nematodes and mollusks [12–15]. Many of these are probably involved in the digestion of plant cell-wall material. A family of expansin-like proteins has been found in the slime mold Dictyostelium discoideum, where they could help to maintain the fluidity of the cellulosic cell walls in the stalk structure . Recent nomenclature rules  recommend that only proteins with homology to both expansin domains should be designated expansins. The polyphyletic group of non-plant expansins, such as those in Dictyostelium, can be referred to as expansin-like family X (EXLX). The relationship of the various groups of expansin-like X proteins with the plant expansins is unclear at the moment. Their divergence could predate the origin of land plants, or they could have been acquired later through horizontal transfer of a gene from one of the plant expansin families. The same applies to proteins with homology only to domain 1, both in plants and other organisms, in that it is possible that some of them originally evolved from an expansin protein with both domains.
Characteristic structural features
α-Expansin proteins can be distinguished from other expansins by the presence of a large insertion and a nearby deletion in domain 1; these are at either side of a conserved motif that is part of the conserved GH45 active site (HFD in the single-letter amino-acid code; Figure 4). Expansin-like A and expansin-like B proteins lack the HFD motif, which suggests that their action may differ from that of other expansins. Furthermore, expansin-like A proteins have a unique conserved motif (CDRC) at the amino terminus of domain 1, and their domain 2 has an extension of approximately 17 amino acids that is not found in other expansin families (Figure 4). The functional implications of these differences among families are currently unknown.
No proteins homologous to expansin domain 2 have yet been identified except for the G2A family. The structure of a G2A protein consists of two stacked β sheets with an immunoglobulin-like fold (Figure 5b) . On the basis of this structure, some highly conserved aromatic residues present in expansin domain 2 have been hypothesized to form a binding strip for cell-wall polysaccharides [1, 21], but this speculative idea has yet to be tested experimentally.
Localization and function
Expansins were first identified as wall-loosening proteins in studies of 'acid-induced growth' [3, 22–24]. It was known for years that low extracellular pH (< 5.5) causes cell-wall loosening in land plants as well as in a subset of green algae that have walls of similar structure . The process is mediated in large part by wall-bound expansins with an acidic pH optimum . Wall pH is normally determined by the activity of the plasma membrane H+ ATPase, which pumps protons to the cell wall; the pH of the wall is typically about 5.5 but may go below 4.5 in some circumstances [25, 26]. Acid-induced growth and expansin action are implicated in the growth responses of plants to hormones and to external stimuli such as light, drought, salt stress and submergence (anoxia) and in morphogenetic processes such as root-hair formation [27–31].
Expansin activity is most often associated with cell-wall loosening in growing cells ; this connection has been confirmed and extended by experiments in which expansin gene expression is manipulated in transgenic plants [35–38]. In most cases, silencing of expansin genes leads to inhibition of growth, whereas excessive ectopic expression leads to faster or abnormal growth. Localized expression of expansins is associated with the meristems and growth zones of the root and stem, as well as the formation of leaf primordia on shoot apical meristems  and the outgrowth of the epidermal cell walls during root-hair formation . Additionally, expansins are implicated in other developmental processes during which wall loosening occurs, such as fruit softening [41–46], xylem formation , abscission (leaf shedding) , seed germination , penetration of pollen tubes through the stigma and style [4, 50], formation of mycorrhizal associations with symbiotic fungi in root tissues , development of nitrogen-fixing nodules in legumes , development of parasitic plants [53, 54], and rehydration of 'resurrection' plants, which curl up tightly when dry and expand when wet . Some plants that are adapted to an aquatic environment respond to submergence with a pronounced elongation. This depends on wall acidification  and is correlated with activation of expansin gene expression [57–59].
In cell-fractionation studies, expansins are found bound to the cell wall, as expected from their activity [23, 60, 61]. With immunolocalization by light and electron microscopy, expansin proteins were localized to the cell wall [51, 61, 62], where they were found to be distributed throughout the thickness of the walls rather than concentrated in specific strata. There is at least one report that expansin mRNA can be found specifically at the polar ends of developing xylem cells ; transcript localization may be a means for ensuring that protein production and secretion is directed to the ends of these cells. It is not clear whether this mRNA targeting is unique to expansins in xylem or whether it is a more general phenomenon. Finally, grass pollen produces and secretes specialized β-expansin proteins in copious amounts (they are known as grass pollen group-1 allergens) [4, 64], but this is an unusual situation: expansins in other tissues have been found only at low concentrations.
Mechanism and regulation
All the α-expansin proteins that have been characterized so far have a pH optimum for cell-wall extension of about 4 [3, 23, 60]. This situation permits the cell to regulate α-expansin activity rapidly by modulating wall pH. The pH optimum of only one class of β-expansin proteins has been characterized, namely the group-1 grass pollen allergens (such as EXPB1 from maize), and it has a broad pH optimum centered at about 5.5 . These pollen proteins are probably not involved in acid growth but rather in the wall loosening that is associated with invasion of maternal tissues by pollen tubes. It is expected that β-expansin proteins in somatic tissues have a pH dependence more similar to that of α-expansins, but so far β-expansin proteins in an active state have not been extracted from somatic tissues, so this expectation remains to be tested experimentally. Also, both α-expansin and β-expansin proteins are activated by reducing agents [3, 4, 65]; this could be biologically significant, as the cell-wall redox potential can be modulated by electron transport across the plasma membrane.
Expansins do not have hydrolytic activity or any of the other enzymatic activities yet assayed [64, 66, 67]. A report that they are proteases was later refuted . Expansins also act very quickly - they induce rapid extension within seconds of addition to wall specimens, but they do not affect the plasticity or elasticity of the cell wall . In contrast, cell-wall creep caused by an endoglucanase has a long lag time and is accompanied by large increases in wall plasticity and elasticity, indicative of major structural changes in the cell wall (cutting of cross-links) . Thus, expansin's effects on cell walls are distinct from those expected of hydrolytic enzymes.
A nonenzymatic mechanism has been proposed for expansin action, in which expansin disrupts noncovalent bonds that tether matrix polysaccharides to the surface of cellulose microfibrils or to each other [1, 66, 69]. In this model, the expansin is thought to act like a zipper that enables microfibrils to move apart from each other by ungluing the chains that stick them together. This idea is also supported by experiments in which an expansin is applied to artificial composites made of bacterial cellulose and xyloglucan . Whatever their biochemical mechanism of action, expansins act in catalytic amounts to stimulate wall polymer creep without causing major covalent alterations of the cell wall .
In the published literature on expansins, gene expression has drawn the greatest amount of attention, but given the large size of the superfamily, the expression and presumptive role of many expansin genes remains unexplored. Although expression of specific expansin genes has been shown to be induced by hormones, by submergence, by drought stress, or by other stimuli, the signaling pathway has not been worked out in detail in even a single case. Major biochemical questions also remain regarding the specific wall polysaccharides on which expansins act, the differences between the action of α-expansins and β-expansins, and the molecular mechanisms underlying wall loosening. Answering these questions will require a much deeper understanding of cell-wall structure and in particular of how the cell wall is able to expand in a controlled fashion. Finally, it remains to be established whether expansin-like A and expansin-like B proteins have cell-wall loosening activity or not.
Additional data files
This work has been supported by grants to D.J.C. from the US National Science Foundation, the Department of Energy, and the National Institutes of Health.
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