Plants are indispensable for life on earth and represent organisms of extreme biological diversity with unique molecular capabilities 1. Here, we present a quantitative atlas of the transcriptomes, proteomes and phosphoproteomes of 30 tissues of the model plant Arabidopsis thaliana. It provides initial answers to how many genes exist as proteins (>18,000), where they are expressed, in which approximate quantities (>6 orders of magnitude dynamic range) and to what extent they are phosphorylated (>43,000 sites). We present examples for how the data may be used, for instance, to discover proteins translated from short open reading frames, to uncover sequence motifs involved in protein expression regulation, to identify tissue-specific protein complexes or phosphorylation-mediated signaling events to name a few. Interactive access to this unique resource for the plant community is provided via ProteomicsDB and ATHENA which include powerful bioinformatics tools to explore and characterize Arabidopsis proteins, their modifications and interplay. Main The plant model organism Arabidopsis thaliana (AT) has revolutionized our understanding of plant biology and influenced many other areas of the life sciences 1. Knowledge derived from Arabidopsis has also provided mechanistic understanding of important agronomic traits in crop species 2. The Arabidopsis genome was sequenced 20 years ago and hundreds of natural variants have since been analyzed at the genome and epigenome level 3,4. In contrast, the Arabidopsis proteome as the main executer of most biological processes is far less comprehensively characterized. To address this gap, we used state-of-the-art mass spectrometry and RNA sequencing (RNA-seq) to provide the first integrated proteomic, phosphoproteomic and transcriptomic atlas of Arabidopsis. Illustrated by selected examples, we show how this rich molecular resource can be used to explore the function of single proteins or entire pathways across multiple omics levels. Multi-omics atlas of Arabidopsis We generated an expression atlas covering, on average, 17,603 ± 1,317 transcripts, 14,430 ± 911 proteins and 14,689 ± 2,509 phosphorylation sites (p-sites) per tissue, using a reproducible biochemical and analytical approach (Fig. 1a,b; Extended Data Fig. 1a-c; Supplementary Data 1,2). In total, the protein expression data covers 18,210 of the 27,655 protein-coding genes (66%) annotated in Araport11 5. This is a substantial increase compared to the percentage of genes with protein level evidence reported in UniProt (27%) 6 and more than double the number of proteins identified in an earlier tissue proteome analysis 7 (Fig. 1c, Extended Data Fig. 1d-f). In addition, we report tissue-resolved quantitative evidence for a total of 43,903 p-sites making this study the most comprehensive single Arabidopsis phosphoproteome published to date (Fig. 1c). 47% of the expressed proteome was found to be phosphorylated in at least one instance, confirming earlier analyses of individual
Signaling mediated by cell surface receptor kinases is central to the coordination of growth patterns during organogenesis. Receptor kinase signaling is in part controlled through endocytosis and subcellular distribution of the respective receptor kinase. For the majority of plant cell surface receptors, the underlying trafficking mechanisms are not characterized. In Arabidopsis, tissue morphogenesis requires the atypical receptor kinase STRUBBELIG (SUB). Here, we studied the endocytic mechanism of SUB. Our data revealed that a functional SUB–enhanced green fluorescent protein (EGFP) fusion is ubiquitinated in vivo. We further showed that plasma membrane-bound SUB:EGFP becomes internalized in a clathrin-dependent fashion. We also found that SUB:EGFP associates with the trans-Golgi network and accumulates in multivesicular bodies and the vacuole. Co-immunoprecipitation experiments revealed that SUB:EGFP and clathrin are present within the same protein complex. Our genetic analysis showed that SUB and CLATHRIN HEAVY CHAIN (CHC) 2 regulate root hair patterning. By contrast, genetic reduction of CHC activity ameliorates the floral defects of sub mutants. Taken together, the data indicate that SUB undergoes clathrin-mediated endocytosis, that this process does not rely on stimulation of SUB signaling by an exogenous agent, and that SUB genetically interacts with clathrin-dependent pathways in a tissue-specific manner.
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...
Plant cells are encased in a semi-rigid cell wall of complex build. As a consequence, cell wall remodeling is essential for the control of growth and development as well as the regulation of abiotic and biotic stress responses. Plant cells actively sense physico-chemical changes in the cell wall and initiate corresponding cellular responses. However, the underlying cell wall monitoring mechanisms remain poorly understood. In Arabidopsis the atypical receptor kinase STRUBBELIG (SUB) mediates tissue morphogenesis. Here, we show that SUBmediated signal transduction also regulates the cellular response to a reduction in the biosynthesis of cellulose, a central carbohydrate component of the cell wall. SUB signaling affects early increase of intracellular reactive oxygen species, stress gene induction as well as ectopic lignin and callose accumulation upon exogenous application of the cellulose biosynthesis inhibitor isoxaben. Moreover, our data reveal that SUB signaling is required for maintaining cell size and shape of root epidermal cells and the recovery of root growth after transient exposure to isoxaben. SUB is also required for root growth arrest in mutants with defective cellulose biosynthesis. Genetic data further indicate that SUB controls the isoxaben-induced cell wall stress response independently from other known receptor kinase genes mediating this response, such as THESEUS1 or MIK2. We propose that SUB functions in a least two distinct biological processes: the control of tissue morphogenesis and the response to cell wall damage. Taken together, our results reveal a novel signal transduction pathway that contributes to the molecular framework underlying cell wall integrity signaling.
Cell wall remodeling is essential for the control of growth and development as well as the regulation of stress responses. However, the underlying cell wall monitoring mechanisms remain poorly understood. Regulation of root hair fate and flower development in Arabidopsis thaliana requires signaling mediated by the atypical receptor kinase STRUBBELIG (SUB). Furthermore, SUB is involved in cell wall integrity signaling and regulates the cellular response to reduced levels of cellulose, a central component of the cell wall. Here, we show that continuous exposure to sub-lethal doses of the cellulose biosynthesis inhibitor isoxaben results in altered root hair patterning and floral morphogenesis. Genetically impairing cellulose biosynthesis also results in root hair patterning defects. We further show that isoxaben exerts its developmental effects through the attenuation of SUB signaling. Our evidence indicates that downregulation of SUB is a multi-step process and involves changes in SUB complex architecture at the plasma membrane, enhanced removal of SUB from the cell surface, and downregulation of SUB transcript levels. The results provide molecular insight into how the cell wall regulates cell fate and tissue morphogenesis.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.