ArabidopsisABERRANT PEROXISOME MORPHOLOGY9 Is a Peroxin That Recruits the PEX1-PEX6 Complex to Peroxisomes

Abstract

Peroxisomes have pivotal roles in several metabolic processes, such as the detoxification of H 2 O 2 and b-oxidation of fatty acids, and their functions are tightly regulated by multiple factors involved in peroxisome biogenesis, including protein transport. This study describes the isolation of an embryonic lethal Arabidopsis thaliana mutant, aberrant peroxisome morphology9 (apem9), which is compromised in protein transport into peroxisomes. The APEM9 gene was found to encode an unknown protein. Compared with apem9 having the nucleotide substitution, the knockdown mutants showed severe defects in peroxisomal functions and plant growth. We showed that expression of APEM9 altered PEROXIN6 (PEX6) subcellular localization from the cytosol to peroxisomes. In addition, we showed that PEX1 and PEX6 comprise a heterooligomer and that this complex was recruited to peroxisomal membranes via protein-protein interactions of APEM9 with PEX6. These findings show that APEM9 functions as an anchoring protein, similar to Pex26 in mammals and Pex15p in yeast. Interestingly, however, the identities of amino acids among these anchoring proteins are quite low. These results indicate that although the association of the PEX1-PEX6 complex with peroxisomal membranes is essential for peroxisomal functions, the protein that anchors this complex evolved uniquely in plants.

Peroxisome Function, Biogenesis, and Dynamics in Plants

“…Arabidopsis RNAi lines targeting PEX1, PEX6, or PEX26 display decreased b-oxidation and matrix protein import (Nito et al, 2007;Goto et al, 2011). Although PEX1 is the most commonly mutated gene in peroxisome biogenesis disorder patients (for review, see Braverman et al, 2016), Arabidopsis pex1 mutants were only recently reported (Rinaldi et al, 2017).…”

“…The viable aberrant peroxisome morphology9 missense allele shows wild-type b-oxidation but impaired matrix protein import in some cells (Goto et al, 2011). The pex26-1 splice-site mutation confers b-oxidation deficiency and low PEX5 levels like typical pex6 mutants .…”

“…The PEX1-PEX6 heterohexamer is tethered to the peroxisome by a tail-anchored protein known as PEX15 in yeast (Elgersma et al, 1997), PEX26 in mammals (Matsumoto et al, 2003), and APEM9/DAYU/PEX26 in plants (Goto et al, 2011;Li et al, 2014;Gonzalez et al, 2017). PEX26 binds PEX1-PEX6 via PEX6 (Birschmann et al, 2003;Matsumoto et al, 2003;Goto et al, 2011). Unlike PEX22 enhancement of PEX4 activity (El Magraoui et al, 2014), tether binding decreases PEX1-PEX6 ATPase activity in yeast (Gardner et al, 2015).…”

“…PEX1 and PEX6 are members of the ATPases associated with diverse cellular activities family and function in yeast as a trimer of PEX1-PEX6 dimers (Blok et al, 2015;Ciniawsky et al, 2015;Gardner et al, 2015). The PEX1-PEX6 heterohexamer is tethered to the peroxisome by a tail-anchored protein known as PEX15 in yeast (Elgersma et al, 1997), PEX26 in mammals (Matsumoto et al, 2003), and APEM9/DAYU/PEX26 in plants (Goto et al, 2011;Li et al, 2014;Gonzalez et al, 2017). PEX26 binds PEX1-PEX6 via PEX6 (Birschmann et al, 2003;Matsumoto et al, 2003;Goto et al, 2011).…”

“…Arabidopsis pex26 null mutants display embryo lethality (Goto et al, 2011) and pollen maturation defects (Li et al, 2014). The viable aberrant peroxisome morphology9 missense allele shows wild-type b-oxidation but impaired matrix protein import in some cells (Goto et al, 2011).…”