The Plastid and Mitochondrial Peptidase Network in Arabidopsis thaliana: A Foundation for Testing Genetic Interactions and Functions in Organellar Proteostasis

Abstract

Plant plastids and mitochondria have dynamic proteomes. Protein homeostasis in these organelles is maintained by a proteostasis network containing protein chaperones, peptidases, and their substrate recognition factors. However, many peptidases, as well as their functional connections and substrates, are poorly characterized. This review provides a systematic insight into the organellar peptidase network in We present a compendium of known and putative Arabidopsis peptidases and inhibitors, and compare the distribution of plastid and mitochondrial peptidases to the total peptidase complement. This comparison shows striking biases, such as the (near) absence of cysteine and aspartic peptidases and peptidase inhibitors, whereas other peptidase families were exclusively organellar; reasons for such biases are discussed. A genome-wide mRNA-based coexpression data set was generated based on quality controlled and normalized public data, and used to infer additional plastid peptidases and to generate a coexpression network for 97 organellar peptidase baits (1742 genes, making 2544 edges). The graphical network includes 10 modules with specialized/enriched functions, such as mitochondrial protein maturation, thermotolerance, senescence, or enriched subcellular locations such as the thylakoid lumen or chloroplast envelope. The peptidase compendium, including the autophagy and proteosomal systems, and the annotation based on the MEROPS nomenclature of peptidase clans and families, is incorporated into the Plant Proteome Database.

Plastidial NAD-Dependent Malate Dehydrogenase: A Moonlighting Protein Involved in Early Chloroplast Development through Its Interaction with an FtsH12-FtsHi Protease Complex

“…The FtsH12-FtsHi complex contains several members of the FtsHi family (FtsHi1, FtsHi2, FtsHi4, and FtsHi5), which lack the zinc binding motif that is considered essential for its metalloprotease activity. In a coexpression network, all members of the FtsH12-FtsHi complex clustered together with genes involved in plastid translation, division, and positioning, as well as amino acid metabolism (Majsec et al, 2017). Nonproteolytic FtsHi proteins were reported to be absent from the cyanobacterium Synechocystis and are thought to have evolved at a later stage of evolution through gene duplication (Sokolenko et al, 2002).…”

CaaX-Like Protease of Cyanobacterial Origin Is Required for Complex Plastid Biogenesis in Malaria Parasites

“…It is possible that AMR4 and its secondary plastid homologs act in a similar pathway as At Sco4. However, many primary chloroplasts, including A. thaliana have an expanded repertoire of uncharacterized CPBP proteins ( 41 ), therefore limiting our ability to infer AMR4 function. Altogether, we consider it likely that AMR4 resides in one of the inner two apicoplast membranes and performs a conserved but unknown role in plastid maintenance.…”

Autocatalytic Processing and Substrate Specificity of Arabidopsis Chloroplast Glutamyl Peptidase

“…In our recent co-expression peptidase network (Majsec et al, 2017), CGEP forms a tight co-expression module (Module VI) with two other peptidases, namely dual-localized plastid/mitochondria OOP and stromal methionine aminopeptidase 1B (MAP1B). This module contains 70 non-redundant genes making 81 edges and a relative enrichment in starch metabolism (7% compared with 0.8% for the whole network).…”

“…The MS data have been deposited to the PRIDE Archive (http://www.ebi.ac.uk/pride/archive/) via the PRIDE partner repository and are available as PXD017189 in ProteomeExchange (http://www.proteomexchange.org/). expressed genes for each bait was based on the hypergeometric test (Majsec et al, 2017).…”

“…INTRODUCTION Organellar peptidases (proteases) play important roles in proteome homeostasis (proteostasis) (van Wijk, 2015). Arabidopsis chloroplasts house ~90-95 proteins directly involved with intra-chloroplast protein maturation and proteolysis (Majsec et al, 2017).…”