New insights into the post-translational modification of multiple phosphoenolpyruvate carboxylase isoenzymes by phosphorylation and monoubiquitination during sorghum seed development and germination

Ruíz-Ballesta, Isabel; Baena, Guillermo; Gandullo, Jacinto; Wang, Liqun; She, Yi‐Min; Plaxton, William C.; Echevarrı́a, Cristina

doi:10.1093/jxb/erw186

Cited by 33 publications

(26 citation statements)

References 33 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Indeed, degradation of both PEPC and PPCK by the polyubiquitin–proteasome pathway has been reported5960. Recently, monoubiquitination of PEPC during sorghum seed development and germination were also documented61. Additionally, the dephosphorylation of PEPC is catalyzed by PP2A1256.…”

Section: Discussionmentioning

confidence: 98%

Genome-wide Analysis of Phosphoenolpyruvate Carboxylase Gene Family and Their Response to Abiotic Stresses in Soybean

Wang

Zhong

Cong

et al. 2016

Sci Rep

View full text Add to dashboard Cite

Phosphoenolpyruvate carboxylase (PEPC) plays an important role in assimilating atmospheric CO2 during C4 and crassulacean acid metabolism photosynthesis, and also participates in various non-photosynthetic processes, including fruit ripening, stomatal opening, supporting carbon–nitrogen interactions, seed formation and germination, and regulation of plant tolerance to stresses. However, a comprehensive analysis of PEPC family in Glycine max has not been reported. Here, a total of ten PEPC genes were identified in soybean and denominated as GmPEPC1-GmPEPC10. Based on the phylogenetic analysis of the PEPC proteins from 13 higher plant species including soybean, PEPC family could be classified into two subfamilies, which was further supported by analyses of their conserved motifs and gene structures. Nineteen cis-regulatory elements related to phytohormones, abiotic and biotic stresses were identified in the promoter regions of GmPEPC genes, indicating their roles in soybean development and stress responses. GmPEPC genes were expressed in various soybean tissues and most of them responded to the exogenously applied phytohormones. GmPEPC6, GmPEPC8 and GmPEPC9 were significantly induced by aluminum toxicity, cold, osmotic and salt stresses. In addition, the enzyme activities of soybean PEPCs were also up-regulated by these treatments, suggesting their potential roles in soybean response to abiotic stresses.

show abstract

Section: Discussionmentioning

confidence: 98%

Genome-wide Analysis of Phosphoenolpyruvate Carboxylase Gene Family and Their Response to Abiotic Stresses in Soybean

Wang

Zhong

Cong

et al. 2016

Sci Rep

View full text Add to dashboard Cite

show abstract

“…All PTPCs are subject to a light-dependent phosphorylation process involving an N -terminal regulatory serine that interacts with metabolite effectors, such as the feedback inhibitor L-malate, and the allosteric activator Glucose-6-phosphate (Glc-6P; Echevarria and Vidal, 2003). In addition, C 3 -type plant PEPCs have also been shown to be regulated by monoubiquitination (Uhrig et al, 2008; Shane et al, 2013; Ruiz-Ballesta et al, 2014, 2016), though this has not been demonstrated for the photosynthetic C 4 -PEPC to date (unpublished results).…”

Section: Introductionmentioning

confidence: 98%

“…Due to the key role that this enzyme plays in the C 4 pathway, the biochemical and signaling mechanisms controlling PEPC activity in the cytosol of leaf mesophyll cells have received significant research attention (Chollet et al, 1996; Echevarria and Vidal, 2003; Izui et al, 2004). In sorghum, PEPC belongs to a multigene family encoding five closely related plant-type PEPCs (PTPC; SbPEPC1-5) and one distantly related bacterial-type PEPC (BTPC) (Ruiz-Ballesta et al, 2016). Of the PTPCs, one family member, SbPEPC1, is an example of a C 4 photosynthetic PEPC, playing a functional role in C 4 and Crassulacean acid metabolism (CAM)-type photosynthesis, while the remaining four homologs, SbPEPC2-5, are C 3 PEPCs, that perform alternative functions in plants (O’Leary et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Anionic Phospholipids Induce Conformational Changes in Phosphoenolpyruvate Carboxylase to Increase Sensitivity to Cathepsin Proteases

et al. 2019

Self Cite

View full text Add to dashboard Cite

Phosphoenolpyruvate carboxylase (PEPC) is a cytosolic, homotetrameric enzyme that serves a variety of functions in plants, acting as the primary form of CO 2 fixation in the C 4 photosynthesis pathway (C 4 -PEPC). In a previous work we have shown that C 4 -PEPC bind anionic phospholipids, resulting in PEPC inactivation. Also, we showed that PEPC can associate with membranes and to be partially proteolyzed. However, the mechanism controlling this remains unknown. Using semi purified-PEPC from sorghum leaf and a panel of PEPC-specific antibodies, we analyzed the conformational changes in PEPC induced by anionic phospholipids to cause the inactivation of the enzyme. Conformational changes observed involved the exposure of the C -terminus of PEPC from the native, active enzyme conformation. Investigation of the protease activity associated with PEPC demonstrated that cysteine proteases co-purify with the enzyme, with protease-specific substrates revealing cathepsin B and L as the major protease species present. The anionic phospholipid-induced C-terminal exposed conformation of PEPC appeared highly sensitive to the identified cathepsin protease activity and showed initial proteolysis of the enzyme beginning at the N -terminus. Taken together, these data provide the first evidence that anionic phospholipids promote not only the inactivation of the PEPC enzyme, but also its proteolysis.

show abstract

“…PEPC is subjected to different post-translational modifications (PTMs), such as phosphorylation, monoubiquitination, NO-related PTMs (S-nitrosylation, Tyr-nitration), and oxidative stress-associated PTMs (carbonylation) [ 9 , 10 , 11 , 12 , 13 ]. In addition, the acetylation of Arabidopsis PEPCs has recently been reported [ 14 ].…”

Section: Introductionmentioning

confidence: 99%

Genetic and Pharmacological Inhibition of Autophagy Increases the Monoubiquitination of Non-Photosynthetic Phosphoenolpyruvate Carboxylase

Baena

Feria

Hernández-Huertas

et al. 2020

Plants

Self Cite

View full text Add to dashboard Cite

Phosphoenolpyruvate carboxylase (PEPC) is an enzyme with key roles in carbon and nitrogen metabolisms. The mechanisms that control enzyme stability and turnover are not well known. This paper investigates the degradation of PEPC via selective autophagy, including the role of the monoubiquitination of the enzyme in this process. In Arabidopsis, the genetic inhibition of autophagy increases the amount of monoubiquitinated PEPC in the atg2, atg5, and atg18a lines. The same is observed in nbr1, which is deficient in a protein that recruits monoubiquitinated substrates for selective autophagy. In cultured tobacco cells, the chemical inhibition of the degradation of autophagic substrates increases the quantity of PEPC proteins. When the formation of the autophagosome is blocked with 3-methyladenine (3-MA), monoubiquitinated PEPC accumulates as a result. Finally, pull-down experiments with a truncated version of NBR1 demonstrate the recovery of intact and/or fragmented PEPC in Arabidopsis leaves and roots, as well as cultured tobacco cells. Taken together, the results show that a fraction of PEPC is cleaved via selective autophagy and that the monoubiquitination of the enzyme has a role in its recruitment towards this pathway. Although autophagy seems to be a minor pathway, the results presented here increase the knowledge about the role of monoubiquitination and the regulation of PEPC degradation.

show abstract

New insights into the post-translational modification of multiple phosphoenolpyruvate carboxylase isoenzymes by phosphorylation and monoubiquitination during sorghum seed development and germination

Abstract: HighlightThis work documents the remarkable versatility and complexity of in vivo post-translational modifications (monoubiquitination and phosphorylation) of different plant-type phosphoenolpyruvate carboxylase (PEPC) isoenzymes during the life cycle of sorghum seeds.

Cited by 33 publications

References 33 publications

Genome-wide Analysis of Phosphoenolpyruvate Carboxylase Gene Family and Their Response to Abiotic Stresses in Soybean

Genome-wide Analysis of Phosphoenolpyruvate Carboxylase Gene Family and Their Response to Abiotic Stresses in Soybean

Anionic Phospholipids Induce Conformational Changes in Phosphoenolpyruvate Carboxylase to Increase Sensitivity to Cathepsin Proteases

Genetic and Pharmacological Inhibition of Autophagy Increases the Monoubiquitination of Non-Photosynthetic Phosphoenolpyruvate Carboxylase

Contact Info

Product

Resources

About