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Dynamic Responses of Barley Root Succinyl-Proteome to Short-Term Phosphate Starvation and Recovery.

ABSTRACT: Barley (Hordeum vulgare L.)-a major cereal crop-has low Pi demand, which is a distinct advantage for studying the tolerance mechanisms of phosphorus deficiency. We surveyed dynamic protein succinylation events in barley roots in response to and recovery from Pi starvation by firstly evaluating the impact of Pi starvation in a Pi-tolerant (GN121) and Pi-sensitive (GN42) barley genotype exposed to long-term low Pi (40 d) followed by a high-Pi recovery for 10 d. An integrated proteomics approach involving label-free, immune-affinity enrichment, and high-resolution LC-MS/MS spectrometric analysis was then used to quantify succinylome and proteome in GN121 roots under short-term Pi starvation (6, 48 h) and Pi recovery (6, 48 h). We identified 2,840 succinylation sites (Ksuc) across 884 proteins; of which, 11 representative Ksuc motifs had the preferred amino acid residue (lysine). Furthermore, there were 81 differentially abundant succinylated proteins (DFASPs) from 119 succinylated sites, 83 DFASPs from 110 succinylated sites, 93 DFASPs from 139 succinylated sites, and 91 DFASPs from 123 succinylated sites during Pi starvation for 6 and 48 h and during Pi recovery for 6 and 48 h, respectively. Pi starvation enriched ribosome pathways, glycolysis, and RNA degradation. Pi recovery enriched the TCA cycle, glycolysis, and oxidative phosphorylation. Importantly, many of the DFASPs identified during Pi starvation were significantly overexpressed during Pi recovery. These results suggest that barley roots can regulate specific Ksuc site changes in response to Pi stress as well as specific metabolic processes. Resolving the metabolic pathways of succinylated protein regulation characteristics will improve phosphate acquisition and utilization efficiency in crops.

SUBMITTER: Wang J

PROVIDER: S-EPMC8045032 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Phosphate (Pi) stress is an important environmental factor that limits plant growth and development. Of various posttranslational modifications (PTMs), protein phosphorylation and succinylation are the two most important PTMs that regulate multiple biological processes in response to Pi stress. However, these PTMs have been investigated individually but their interactions with proteins in response to Pi stress remain poorly understood. In this study, to elucidate the underlying mechanisms of protein phosphorylation and succinylation in response to Pi stress, we performed a global analysis of the barley root phosphorylome and succinylome in Pi starvation and recovery stages, respectively. A total of 3,634 and 884 unique phosphorylated and succinylated proteins, respectively, corresponding to 11,538 and 2,840 phospho- and succinyl-sites, were identified; of these, 275 proteins were found to be simultaneously phosphorylated and succinylated. Gene Set Enrichment Analysis was performed with a Kyoto Encyclopedia of Genes and Genomes pathway database revealing pathways that significantly enriched in the phosphorylome and succinylome. Such pathways, were dynamically regulated by Pi starvation and recovery treatments, and could be partitioned into distinct metabolic processes. In particular, phosphorylated proteins related to purine, the mitogen-activated protein kinase (MAPK) signaling pathway, pyrimidine, and ATP-binding cassette (ABC) transporters were upregulated in both Pi deprivation and recovery stages. Succinylated proteins, significantly upregulated by both Pi starvation and recovery, were enriched in nitrogen metabolism and phenylpropanoid biosynthesis. Meanwhile, succinylated proteins that were significantly downregulated by both Pi starvation and recovery were enriched in lysine degradation and tryptophan metabolism. This highlighted the importance of these metabolic pathways in regulating Pi homeostasis. Furthermore, protein-protein interaction network analyses showed that the response of central metabolic pathways to Pi starvation and recovery was significantly modulated by phosphorylation or succinylation, both individually and together. In addition, we discovered relevant proteins involved in MAPK signaling and phenylpropanoid biosynthetic pathways existing in interactions between phosphorylated and succinylated proteins in response to Pi recovery. The current study not only provides a comprehensive analysis of phosphorylated and succinylated proteins in plant responses to Pi starvation and recovery, but also reveals detailed interactions between phosphorylated and succinylated proteins in barley roots.

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Dynamic Responses of Barley Root Succinyl-Proteome to Short-Term Phosphate Starvation and Recovery.

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