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Impact of Acidic Ph on Plant Cell Wall Polysaccharide Structure and Dynamics: Insights Into the Mechanism of Acid Growth in Plants from Solid-State NMR

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Impact of Acidic Ph on Plant Cell Wall Polysaccharide Structure and Dynamics: Insights Into the Mechanism of Acid Growth in Plants from Solid-State NMR Cellulose (2019) 26:291–304 https://doi.org/10.1007/s10570-018-2094-7 (0123456789().,-volV)(0123456789().,-volV) ORIGINAL PAPER Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR Pyae Phyo . Ying Gu . Mei Hong Received: 1 September 2018 / Accepted: 19 October 2018 / Published online: 24 October 2018 Ó Springer Nature B.V. 2018 Abstract Acidification of plant primary cell walls spectra measured with long mixing times indicate that causes cell wall expansion and plant growth. To the acidic cell wall has weaker cellulose–pectin understand how acidic pH affects the molecular interactions, and water-polysaccharide 1H spin diffu- structure and dynamics of wall polysaccharides, we sion data show that cellulose microfibrils are better have now characterized and compared Arabidopsis hydrated at low pH. Taken together, these results thaliana primary cell walls in neutral (pH 6.8) and indicate a cascade of chemical and conformational acidic (pH 4.0) conditions using solid-state NMR changes of wall polysaccharides due to cell wall spectroscopy. Quantitative 13C solid-state NMR spec- acidification. These changes start with neutralization tra indicate that the pH 4.0 cell wall has neutral of the pectic polysaccharides, which disrupts calcium galacturonic acid residues in homogalacturonan (HG) crosslinking of HG, causes partial aggregation of the and rhamnogalacturonan (RG). 13C INEPT spectra, interfibrillar HG, weakens cellulose–pectin interac- which selectively detect highly dynamic polymers, tions, and increases the hydration of both cellulose indicate that some of the HG and RG chains in the microfibrils and matrix polysaccharides. These molec- interfibrillar region have become more dynamic in the ular-level structural and dynamical changes are acidic wall compared to the neutral cell wall, whereas expected to facilitate polysaccharide slippage, which other chains have become more rigid. Consistent with underlies cell wall loosening and expansion, and may this increased dynamic heterogeneity, C–H dipolar occur both independent of and as a consequence of couplings and 2D 13C–13C correlation spectra indicate protein-mediated wall loosening. that some of the HG backbones are partially aggre- gated in the acidic cell wall. Moreover, 2D correlation P. Phyo Á M. Hong (&) Department of Chemistry, Massachusetts Institute of Technology, 170 Albany Street, Cambridge, MA 02139, USA e-mail: [email protected] Y. Gu Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA 16802, USA 123 292 Cellulose (2019) 26:291–304 Graphical abstract Keywords Plant primary cell wall Á Solid-state Introduction NMR Á Acidic pH Á Acid growth Á Cellulose–pectin interaction The primary cell wall of growing plants possesses a complex and interconnected polysaccharide network to provide both mechanical strength and flexibility to Abbreviations the cell. The mechanical strength allows plant cell Ara, A Arabinose walls to withstand tensile and compressive forces CW Cell wall while the flexibility allows the cell wall to expand to CP Cross polarization permit plant tissue growth (Cosgrove 2018). In DP Direct polarization growing plants, the polysaccharide network is altered Gal Galactose by a number of environmental factors and wall- GalA, Galacturonic acid modifying agents to loosen the cell wall. Among these, GA the best-known trigger for wall loosening and exten- HG Homogalacturonan sion is auxin-induced acidification. The acid growth INEPT Insensitive nuclei enhanced by theory, introduced five decades ago (Arsuffi and polarization transfer Braybrook 2018; Hager et al. 1971; Majda and Robert i Interior crystalline cellulose 2018), states that the hormone auxin activates plasma- MAS Magic-angle spinning membrane H?-ATPase proton pumps to acidify the PDSD Proton-driven 13C–13C spin diffusion extracellular or apoplastic pH, which in turn activates RG-I Rhamnogalacturonan I wall-loosening enzymes as well as increasing the Rha R Rhamnose intracellular turgor pressure to allow cell elongation. SSNMR Solid-state nuclear magnetic resonance The apoplastic pH is normally about 6, but auxin s Surface amorphous cellulose treatment decreases it to 4.5–5.0. When neutral or XyG Xyloglucan basic buffer is introduced, cell expansion subsides Xyl, x Xylose (Hager et al. 1971; Tepfer and Cleland 1979). At the end of cell growth, calcium channels are activated to increase the calcium ion concentration in the cytosol, 123 Cellulose (2019) 26:291–304 293 which inhibits the H?-ATPase activity, which in turn primary cell walls of Arabidopsis (Dick-Perez et al. raises the apoplastic pH, halting wall expansion 2011), Brachypodium (Wang et al. 2014), and Zea (Majda and Robert 2018). Mays (Wang et al. 2016a) provided detailed and While acid growth of plants is triggered by auxin multifaceted evidence that pectin interaction with in vivo, research on many plant species in the last few cellulose and pectin dynamics in the interfibrillar decades have shown that acidic pH, in the absence of space are important for wall mechanics. For example, the hormone itself, already causes wall extension 13C spectra of the cell walls of a fast-growing (Hager 2003). When the primary cell wall is clamped Arabidopsis mutant (Phyo et al. 2017b) and rapidly to a constant-force extensometer, the wall is found to elongating Arabidopsis inflorescence stem (Phyo et al. extend readily in acidic buffer, in the absence of auxin, 2017a) show weaker pectin–cellulose through-space while almost no extension is found at neutral pH cross peaks and increased methyl esterification levels, (Cosgrove 2000; Durachko and Cosgrove 2009; Ezaki implying the reduced homogalacturonan (HG) et al. 2005). Interestingly, wall extension in tissues crosslinking, compared to their respective slower such as coleoptile or hypocotyl is inhibited by Cu2?, growing counterparts. The NMR spectra of inflores- Co2?, and Mn2?, which inhibit enzymatic processes, cence primary cell wall also show higher pectin indicating the involvement of proteins in acid growth concentrations, increased RG-I sidechain branching, (Hager 2003; Hager et al. 1971; Prat et al. 1984; Tepfer larger pectin mobility, and higher pectin hydration. and Cleland 1979). A number of proteins and enzymes For never-dried primary cell walls of two-week-old have been identified to be involved in acid growth Arabidopsis seedlings, pectin–cellulose cross peaks (Hager 2003; Laskowski et al. 2006). For example, the are observed in 2D 13C–13C correlation spectra (Wang wall-loosening protein, expansin, is activated by wall et al. 2015), and water accessibility of cellulose lags acidification and exhibits optimal activity at pH 4 behind the hydration of pectins (White et al. 2014), (Cosgrove et al. 1997, 2000, 2005; Durachko and indicating that the cellulose surface is covered by Cosgrove 2009). Exogenous auxin treatment induces pectins. Together, these solid-state NMR data point to the expression of various genes, including those pectin–cellulose interactions as an essential feature of encoding for pectin methylesterases (PMEs) and mature primary cell walls, which need to be weakened pectate lyases in Arabidopsis roots (Laskowski et al. in order to allow wall expansion, and indicate that 2006). PME activity cleaves methyl-esters from HG, reduced pectin crosslinking and higher esterification which were shown by AFM indentation data to cause may correlate with wall loosening. tissue softening prior to cell wall expansion (Bray- Given these observations of pectins’ role in primary brook and Peaucelle 2013). When de-methyl-esterifi- cell wall mechanics, here we investigate how acidic cation is inhibited, pectin lyases can no longer degrade pH changes the structure and dynamics of wall pectins, which correlates with reduced wall loosening. polysaccharides, in the absence of protein and enzyme These data suggest that acidic pH causes wall loos- actions. We treated the Arabidopsis primary cell wall ening by inducing protein and enzyme processes that to a pH 4 buffer, and compared its 13C NMR spectra eventually change the pectin structural network. with those of neutral-pH cell wall. The 13C solid-state However, this protein-centric view of acid growth NMR spectra give a wealth of information about pH- does not explain the fact that auxin-induced plant induced differences in polysaccharide chemical struc- growth starts rapidly, within minutes, well before ture, molecular mobility, hydration, and intermolecu- transcriptional changes that activate wall-loosening lar interactions. The NMR data indicate that wall proteins (Cosgrove 2000;Lu¨then et al. 1990; Mcqu- acidification to pH 4 quantitatively neutralizes all een-mason and Cosgrove 1995). To answer the galacturonic acid residues in HG and RG-I, which question of whether acid growth of plant cells has a profoundly changes the structure and dynamics of the protein-independent mechanism, it is instructive to polysaccharide network. The pectins become partially consider the recent increasing body of molecular-level separated from cellulose microfibrils, as manifested in structural and dynamical information about plant cell 2D 13C–13C correlation spectra. Pectins are partially wall polysaccharides obtained from solid-state NMR aggregated, as shown by measured 13C–1H dipolar (Dick-Perez et al. 2011; Wang and Hong 2016; Wang couplings, consistent with charge neutralization of et al. 2012, 2015). 13C NMR spectra of 13C-enriched GalA and the
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