Matrix solubilization and cell wall weakening by β‐expansin (group‐1 allergen) from maize pollen

Abstract

SUMMARYBeta-expansins accumulate to high levels in grass pollen, a feature apparently unique to grasses. These proteins, which are major human allergens, facilitate pollen tube penetration of the maize stigma and style (the silk). Here we report that treatment of maize silk cell walls with purified b-expansin from maize pollen led to solubilization of wall matrix polysaccharides, dominated by feruloyated highly substituted glucuronoarabinoxylan (60%) and homogalacturonan (35%). Such action was selective for cell walls of grasses, and indicated a target preferentially found in grass cell walls, probably the highly substituted glucuronoarabinoxylan. Several tests for lytic activities by b-expansin were negative and polysaccharide solubilization had weak temperature dependence, which indicated a non-enzymatic process. Concomitant with matrix solubilization, b-expansin treatment induced creep, reduced the breaking force and increased the plastic compliance of wall specimens. From comparisons of the pH dependencies of these processes, we conclude that matrix solubilization was linked closely to changes in wall plasticity and breaking force, but not so closely coupled to cell wall creep. Because matrix solubilization and increased wall plasticity have not been found with other expansins, we infer that these novel activities are linked to the specialized role of grass pollen b-expansins in promotion of penetration of the pollen tube through the stigma and style, most likely by weakening the middle lamella.

The Target of β-Expansin EXPB1 in Maize Cell Walls from Binding and Solid-State NMR Studies

“…This new information complements previous data showing that EXPB1 specifically loosens grass CWs and solubilizes hsGAX from maize CWs Tabuchi et al, 2011). Previous biochemical data indicate that hsGAX displays only weak binding to cellulose (Carpita, 1983), thus it is unlikely to serve as a load-bearing linker directly interconnecting cellulose microfibrils but may act as space-filling interstitial material between cellulose microfibrils (Carpita et al, 2001).…”

“…Consistent with this idea, Tabuchi et al (2011) found that treatment of maize CWs with EXPB1 induces release (solubilization) of a form of GAX with a high degree of arabinose substitution (hsGAX) as well as smaller amounts of homogalacturonan (HG). Extensive testing of EXPB1 did not detect any enzymatic activities, just as tests for enzymatic activities with a-expansins and bacterial expansins proved to be negative (McQueen-Mason and Cosgrove, 1995;Kerff et al, 2008;Georgelis et al, 2011Georgelis et al, , 2015.…”

“…780-0021) chromatography and further fractionated on a Discover C5 reverse-phase HPLC column (Sigma-Aldrich no. 568422) Tabuchi et al, 2011).…”

“…Moreover, EXPB1 caused marked mechanical weakening of grass CWs, as measured in tensile force/extension assays. These actions were likewise specific to grass CWs, as polysaccharide release and wall weakening were not seen when EXPB1 was applied to CWs from a variety of nongrass species, nor have they been found with a-expansins (McQueen-Mason and Cosgrove, 1995;Yuan et al, 2001;Tabuchi et al, 2011) or bacterial expansins (Georgelis et al, 2014). Thus, while EXPB1 action has commonalities with a-expansin action, namely induction of CW creep and stress relaxation, it also has unique features.…”

GmEXPB2, a Cell Wall β-Expansin Gene, Affects Soybean Nodulation through Modifying Root Architecture and Promoting Nodule Formation and Development

“…One of the hypothesized actions of expansin is the weakening of noncovalent binding between cellulose fibers, and it is supported by the finding of expansin weakening the hydrogen bonding of pure cellulose paper (McQueen-Mason and Cosgrove, 1994). Meanwhile, many studies have reported that expansins have no hydrolytic or other enzymatic activities (McQueen-Mason et al, 1993;Li and Cosgrove, 2001;Tabuchi et al, 2011). In addition to that, Cosgrove et al (1998) also mentioned that although expansin lacks hydrolytic activity itself, it does enhance the hydrolysis of crystalline cellulose by cellulases.…”