Craterostigma plantagineumcell wall composition is remodelled during desiccation and the glycine‐rich protein CpGRP1 interacts with pectins through clustered arginines

Abstract

Summary Craterostigma plantagineum belongs to the desiccation‐tolerant angiosperm plants. Upon dehydration, leaves fold and the cells shrink which is reversed during rehydration. To understand this process changes in cell wall pectin composition, and the role of the apoplastic glycine‐rich protein 1 (CpGRP1) were analysed. Cellular microstructural changes in hydrated, desiccated and rehydrated leaf sections were analysed using scanning electron microscopy. Pectin composition in different cell wall fractions was analysed with monoclonal antibodies against homogalacturonan, rhamnogalacturonan I, rhamnogalacturonan II and hemicellulose epitopes. Our data demonstrate changes in pectin composition during dehydration/rehydration which is suggested to affect cell wall properties. Homogalacturonan was less methylesterified upon desiccation and changes were also demonstrated in the detection of rhamnogalacturonan I, rhamnogalacturonan II and hemicelluloses. CpGRP1 seems to have a central role in cell adaptations to water deficit, as it interacts with pectin through a cluster of arginine residues and de‐methylesterified pectin presents more binding sites for the protein−pectin interaction than to pectin from hydrated leaves. CpGRP1 can also bind phosphatidic acid (PA) and cardiolipin. The binding of CpGRP1 to pectin appears to be dependent on the pectin methylesterification status and it has a higher affinity to pectin than its binding partner CpWAK1. It is hypothesised that changes in pectin composition are sensed by the CpGRP1−CpWAK1 complex therefore leading to the activation of dehydration‐related responses and leaf folding. PA might participate in the modulation of CpGRP1 activity.

LsGRP1, a class II glycine‐rich protein of Lilium, confers plant resistance via mediating innate immune activation and inducing fungal programmed cell death

“…The C-terminal region of LsGRP1 is the first case of class II GRPs found to function as a fungal apoptosis PCD-inducing domain to assist disease resistance Chen, 2014, 2017; this study). By contrast, AtGRP3 and CpGRP1 use the C-terminal regions to interact with cell wall-associated kinases (WAKs), and thereby affect disease resistance and probably dehydration-related responses, respectively (Park et al, 2001;Yang et al, 2003;Giarola et al, 2016;Gramegna et al, 2016;Jung et al, 2019). As the C-terminal regions of plant class II GRPs share higher sequence similarities with the others belonging to the same clades of either monocot or dicot ( Figure S3), the antimicrobial activity associated with most or certain C-terminal regions of class II GRPs is of interest to investigate.…”

“…Similarly, Nicotiana tabacum cdiGRP is up-regulated under cadmium stress, and its accumulation in cell walls blocks the systemic infection of tobamovirus via enhancing vascular callose deposition Citovsky,2002, 2005). In terms of abiotic stress, apoplast-accumulated CpGRP1 of Craterostigma plantagineum seems to play a central role in activating dehydration-related responses to water deficit through interacting with CpWAK1, an ortholog of Arabidopsis AtWAK2 (Giarola et al, 2016;Jung et al, 2019). Accordingly, the cell surface-localized plant class II GRPs, including LsGRP1 of lily, possibly mediate defence against diverse stresses while the corresponding defence activators appear.…”

The dehydration- and ABA-inducible germin-like protein CpGLP1 from Craterostigma plantagineum has SOD activity and may contribute to cell wall integrity during desiccation

“…Available data support the hypothesis that this phenomenon is required to reduce the mechanical and oxidative stress generated by the loss of water and thus protect cellular integrity from lethal damage. (Giarola et al 2016;Jones and McQueen-Mason 2004;Jung et al 2019;Vicré et al 1999Vicré et al , 2004. Cell wall folding is accomplished by a combination of constitutive and inducible mechanisms involving the controlled and coordinated rearrangement of molecular and physical linkage of cell wall structures (Jones and McQueen-Mason 2004;Jung et al 2019;Moore et al 2008).…”

“…Our understanding of cell wall folding mechanisms in resurrection plants is puzzling as species seem to have evolved species-specific strategies to cope with reversible shrinking and folding. Some species like Myrothamnus flabellifolia rely on high constitutive levels of pectic-arabinans, arabinogalactan–proteins and arabinoxylans, whereas others, such as Craterostigma spp., adjust cell wall plasticity via dehydration-induced biochemical reactions (Jung et al 2019 ; Moore et al 2008 , 2013 ). Among such mechanisms, the reduction of the hemicellulose xyloglucan content and modifications of pectin structures have been described (Jung et al 2019 ; Vicré et al 1999 , 2004 ).…”

Water status signaling in resurrection plants: a possible role for cell wall glycine‐rich proteins

“…For over two decades, Dorothea Bartels and her group at the University of Bonn (Bonn, Germany) have been working to uncover such mechanisms in the resurrection plant Craterostigma plantagineum . Their latest study, published in The Plant Journal (Jung et al , ), sheds light on how these plants sense water status in the apoplast and send the signal into the cell.…”