The cell wall-localized atypical β-1,3 glucanase ZERZAUST controls tissue morphogenesis in <i>Arabidopsis thaliana</i>

Approximately 1% of plant proteins are predicted to be post-translationally modified with a glycosylphosphatidylinositol (GPI) anchor that tethers the polypeptide to the outer leaflet of the plasma membrane. Whereas the synthesis and structure of GPI anchors is largely conserved across eukaryotes, the repertoire of functional domains present in the GPI-anchored proteome has diverged substantially. In plants, this includes a large fraction of the GPI-anchored proteome being further modified with plant-specific arabinogalactan (AG) O-glycans. The importance of the GPI-anchored proteome to plant development is underscored by the fact that GPI biosynthetic null mutants exhibit embryo lethality. Mutations in genes encoding specific GPI-anchored proteins (GAPs) further supports their contribution to diverse biological processes, occurring at the interface of the plasma membrane and cell wall, including signaling, cell wall metabolism, cell wall polymer cross-linking, and plasmodesmatal transport. Here, we review the literature concerning plant GPI-anchored proteins, in the context of their potential to act as molecular hubs that mediate interactions between the plasma membrane and the cell wall, and their potential to transduce the signal into the protoplast and, thereby, activate signal transduction pathways.

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“…BC1 was also shown to be PI-PLD sensitive. Similarly, the GAP ZERZAUST (ZET) localized not to PM but to the cell wall (Vaddepalli et al 2017).…”

Section: Cell Wall Versus Pm Localizationmentioning

confidence: 99%

Plant glycosylphosphatidylinositol anchored proteins at the plasma membrane‐cell wall nexus

Yeats

Bacic

Johnson

2018

JIPB

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“…For example, whole-genome transcriptomics analysis revealed that many genes responsive to SUB -mediated signal transduction relate to cell wall remodeling [45]. Moreover, Fourier-transform infrared spectroscopy (FTIR)-analysis indicated that flowers of sub and qky mutants share overlapping defects in cell wall biochemistry [46]. Thus, apart from functionally connecting RK-mediated signal transduction and PD-dependent cell-cell communication SUB signaling also relates to cell wall biology.…”

Section: Introductionmentioning

confidence: 99%

The Arabidopsis receptor kinase STRUBBELIG regulates the response to cellulose deficiency

Chaudhary

Chen

Gao

et al. 2019

Preprint

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23 24 Short title: SUB mediates cell wall stress signaling 25 26 Abstract 29 Plant cells are encased in a semi-rigid cell wall of complex build. As a consequence, 30 cell wall remodeling is essential for the control of growth and development as well as 31 the regulation of abiotic and biotic stress responses. Plant cells actively sense physico-32 chemical changes in the cell wall and initiate corresponding cellular responses. 33 However, the underlying cell wall monitoring mechanisms remain poorly understood.34 In Arabidopsis the atypical receptor kinase STRUBBELIG (SUB) mediates tissue 35 morphogenesis. Here, we show that SUB-mediated signal transduction also regulates 36 the cellular response to a reduction in the biosynthesis of cellulose, a central 37 carbohydrate component of the cell wall. SUB signaling affects early increase of 38 intracellular reactive oxygen species, stress gene induction as well as ectopic lignin 39 and callose accumulation upon exogenous application of the cellulose biosynthesis 40 inhibitor isoxaben. Moreover, our data reveal that SUB signaling is required for 41 maintaining cell size and shape of root epidermal cells and the recovery of root 42 growth after transient exposure to isoxaben. SUB is also required for root growth 43 arrest in mutants with defective cellulose biosynthesis. Genetic data further indicate 44 that SUB controls the isoxaben-induced cell wall stress response independently from 45 other known receptor kinase genes mediating this response, such as THESEUS1 or 46 MIK2. We propose that SUB functions in a least two distinct biological processes: the 47 control of tissue morphogenesis and the response to cell wall damage. Taken together, 48 our results reveal a novel signal transduction pathway that contributes to the 49 molecular framework underlying cell wall integrity signaling. 50 51 52 3 53 Author Summary54 Plant cells are encapsulated by a semi-rigid and biochemically complex cell wall. This 55 particular feature has consequences for multiple biologically important processes, 56 such as cell and organ growth or various stress responses. For a plant cell to grow the 57 cell wall has to be modified to allow cell expansion, which is driven by outward-58 directed turgor pressure generated inside the cell. In return, changes in cell wall 59 architecture need to be monitored by individual cells, and to be coordinated across 60 cells in a growing tissue, for an organ to attain its regular size and shape. Cell wall 61 surveillance also comes also into play in the reaction against certain stresses, 62 including for example infection by plant pathogens, many of which break through the 63 cell wall during infection, thereby generating wall-derived factors that can induce 64 defense responses. There is only limited knowledge regarding the molecular system 65 that monitors the composition and status of the cell wall. Here we provide further 66 insight into the mechanism. We show that the cell surface receptor STRUBBELIG, 67 previously known to control organ development in Ar...

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“…In Ler background, zet-1 carrying a loss-of-function mutation in ZET locus (At1g64760) (Fig. 1A,B), shows a strong slm mutant phenotype (Vaddepalli et al . 2017) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…1J). This construct was used in a previous study to complement zet-1 mutants in L er background (Vaddepalli et al . 2017).…”

Section: Resultsmentioning

confidence: 99%

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Asymmetric redundancy of ZERZAUST and ZERZAUST HOMOLOG in different accessions of Arabidopsis thaliana

Vaddepalli

Fulton

Schneitz

2018

Preprint

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35Divergence among duplicate genes is one of the important sources of evolutionary 36 innovation. But, the contribution of duplicate divergence to variation in Arabidopsis 37 accessions is sparsely known. Recently, we studied the role of a cell wall localized protein, 38 ZERZAUST (ZET), in Landsberg erecta (Ler) accession. Here, we present the study of ZET 39 in Columbia (Col) accession, which not only showed differential expression patterns in 40 comparison to Ler, but also revealed its close homolog, ZERZAUST HOMOLOG (ZETH). 41 Although, genetic analysis implied redundancy, expression analysis revealed divergence, 42 with ZETH showing minimal expression in both Col and Ler. In addition, ZETH shows 43 relatively higher expression levels in Col compared to Ler. Our data also reveal 44 compensatory up-regulation of ZETH in Col, but not in Ler, implying it is perhaps 45 dispensable in Ler. However, a novel CRISPR/Cas9-induced zeth allele confirmed that ZETH 46 has residual activity in Ler. The results provide genetic evidence for accession-specific 47 differences in compensation mechanism and asymmetric gene contribution. Thus, our work 48 reveals a novel example for how weakly expressed homologs contribute to diversity among 49 accessions. 50 51 52 How genetic variation translates into phenotypic variation is of immense scientific interest 53 (Weigel 2012). Among others, gene duplication followed by functional divergence is an 54 important source of evolutionary complexity and innovation in multicellular organisms 55 (Ohno 1970; Lynch and Conery 2000; Lynch and Katju 2004). Many gene pairs after 56 duplication revert to single gene state but the ones that sustained undergo functionalization. 57 The Arabidopsis genome underwent several duplication events which resulted in large 58 number of homologous genes and regions across the genome (Blanc and Wolfe 2004; 59 Ambrosino et al. 2016; Panchy et al. 2016). The functional importance of homologs has been 60 demonstrated in various aspects of plant signaling and metabolism (Briggs et al. 2006). But, 61 whether and how the differentiation in duplicate gene expression contributes to accession 62 variation in Arabidopsis is not known. 63 64 Studies have shown that divergence of many duplicate genes occurs by expression divergence 65 among and within species (Gu et al. 2004; Li et al. 2005). This phenomenon expands gene 66 regulatory networks and contributes to physiological and morphological diversity (Carroll 67 2000; Lynch and Conery 2000; Gu et al. 2004; Rensing 2014). In Arabidopsis, about two-68 thirds of duplicates were shown to exhibit expression divergence (Haberer et al. 2004). An 69 evolutionary study on gene duplication revealed that duplicate genes show a high degree of 70 variance in expression within species and suggested that this variation partly depends upon 71 the biological function of the gene involved (Kliebenstein 2008). Another study also found 72 high variance of duplicated gene expression between closely related A. thaliana and A. 73 arenosa...

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The cell wall-localized atypical β-1,3 glucanase ZERZAUST controls tissue morphogenesis in Arabidopsis thaliana

Cited by 47 publications

References 66 publications

Plant glycosylphosphatidylinositol anchored proteins at the plasma membrane‐cell wall nexus

Plant glycosylphosphatidylinositol anchored proteins at the plasma membrane‐cell wall nexus

The Arabidopsis receptor kinase STRUBBELIG regulates the response to cellulose deficiency

Asymmetric redundancy of ZERZAUST and ZERZAUST HOMOLOG in different accessions of Arabidopsis thaliana

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