Advances in proteome-wide analysis of plant lysine acetylation

Abstract

Lysine acetylation (LysAc) is a conserved and important post-translational modification (PTM) that plays a key role in plant physiological and metabolic processes. Based on advances in Lys-acetylated protein immunoenrichment and mass-spectrometric technology, LysAc proteomics studies have been performed in many species. Such studies have made substantial contributions to our understanding of plant LysAc, revealing that Lys-acetylated histones and nonhistones are involved in a broad spectrum of plant cellular processes. Here, we present an extensive overview of recent research on plant Lys-acetylproteomes. We provide in-depth insights into the characteristics of plant LysAc modifications and the mechanisms by which LysAc participates in cellular processes and regulates metabolism and physiology during plant growth and development. First, we summarize the characteristics of LysAc, including the properties of Lys-acetylated sites, the motifs that flank Lys-acetylated lysines, and the dynamic alterations in LysAc among different tissues and developmental stages. We also outline a map of Lys-acetylated proteins in the Calvin-Benson cycle and central carbon metabolism-related pathways. We then introduce some examples of the regulation of plant growth, development, and biotic and abiotic stress responses by LysAc. We discuss the interaction between LysAc and N^α-terminal acetylation and the crosstalk between LysAc and other PTMs, including phosphorylation and succinylation. Finally, we propose recommendations for future studies in the field. We conclude that LysAc of proteins plays an important role in the regulation of the plant life cycle.

Keywords: PTM crosstalk; lysine acetylproteomes; modified characteristics; plant growth and development; stress responses.

Figure 1

Distribution of Lys-acetylated sites in a single protein identified in plant Lys-acetylproteomes. Detailed information can be found in Supplemental Table 1.

Figure 2

Distribution of Lys-acetylated proteins across subcellular compartments. (A) Distribution of proteins with multiple Lys-acetylated sites across subcellular compartments. (B) Distribution of Lys-acetylated proteins identified in whole Lys-acetylproteomes across subcellular compartments. Leaves, seeds, buds, and cells indicate the materials analyzed to produce the plant Lys-acetylproteomes.

Figure 3

Distribution of protein secondary structures surrounding Lys-acetylated sites (α helix, β strand, and coil).

Figure 4

Lys-acetylated model of proteins involved in the Calvin–Benson cycle and central carbon metabolism. The Lys-acetylated enzymes relevant to the Calvin–Benson cycle and central carbon metabolism summarized from 20 Lys-acetylproteomes are noted with boxes of different colors to reflect their frequency of modification by LysAc. PRK, phosphoribulokinase; Rubisco, ribulose bisphosphate carboxylase/oxygenase; PGK, phosphoglycerate kinase; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; TPI, triosephosphate isomerase; FBA, fructose-bisphosphate aldolase; FBPase, fructose-1,6-bisphosphatase; SBPase, sedoheptulose-1,7-bisphosphatase; RPE, ribulose phosphate epimerase; RPI, ribose-5-phosphate isomerase; PGluM, phosphoglucomutase; HK, hexokinase; GPI, glucose-6-phosphate isomerase; FRK, fructokinase; PFK, phosphofructokinase; PGlyM, 2,3-bisphosphoglycerate-independent phosphoglycerate mutase; ENO, enolase; PK, pyruvate kinase; PDC, pyruvate decarboxylase; ALDH, acetaldehyde dehydrogenase; ADH, alcohol dehydrogenase; PDHE1, pyruvate dehydrogenase complex E1 subunit; DLD, dihydrolipoyl dehydrogenase; DLAT, dihydrolipoamide acetyltransferase; CS, citrate synthase; AH, aconitate hydratase; IDH, isocitrate dehydrogenase; ODH, oxoglutarate dehydrogenase; SCS, succinyl-CoA synthetase; SDH, succinate dehydrogenase; FH, fumarate hydratase; ME, malic enzyme; MDH, malate dehydrogenase; G6PD, glucose-6-phosphate 1-dehydrogenase; PGL, 6-phosphogluconolactonase; PGD, 6-phosphogluconate dehydrogenase; TK, transketolase; TAL, transaldolase; R5P, ribose-5-phosphate; Ru5P, ribulose-5-phosphate; RuBP, ribulose-1,5-bisphosphate; 3-PGA, 3-phosphoglycerate; DPGA, 1,3-disphosphoglycerate; PGALD, 3-phosphoglyceraldehyde; DHAP, dihydroxyacetone phosphate; FBP, fructose-1,6-bisphosphate; F6P, fructose-6-phosphate; E4P, erythrose-4-phosphate; SBP, sedoheptulose-1,7-bisphosphate; S7P, sedoheptulose-7-phosphate; Xu5P, xylulose-5-phosphate; G1P, glucose-1-phosphate; G6P, glucose-6-phosphate; 2-PGA, 2-phosphoglycerate; PEP, phosphoenolpyruvate; OAA, oxaloacetate; CA, cis-aconitate; ICA, isocitrate; α-KGA, 2-oxoglutarate; SA, succinate; FA, fumarate; MA, malate; 6-PGL, 6-phosphoglucono-1,5-lactone; 6-PG, 6-phosphogluconate.

Figure 5

Putative LysAc networks in the plant life cycle. (A) LysAc is involved in plant growth, development, and stress responses. (B) Crosstalk between LysAc and other PTMs.