Protein Disulfide Isomerase Like 1-1 Participates in the Maturation of Proglutelin Within the Endoplasmic Reticulum in Rice Endosperm

Abstract

The rice esp2 mutation was previously characterized by the abnormal accumulation of elevated levels of proglutelin and the absence of an endosperm-specific protein disulfide isomerase like (PDIL1-1). Here we show that Esp2 is the structural gene for PDIL1-1 and that this lumenal chaperone is asymmetrically distributed within the cortical endoplasmic reticulum (ER) and largely restricted to the cisternal ER. Temporal studies indicate that PDIL1-1 is essential for the maturation of proglutelin only when its rate of synthesis significantly exceeds its export from the ER, a condition resulting in its build up in the ER lumen and the induction of ER quality control processes which lower glutelin levels as well as those of the other storage proteins. As proglutelin is initially synthesized on the cisternal ER, its deposition within prolamine protein bodies in esp2 suggests that PDIL1-1 helps retain proglutelin in the cisternal ER lumen until it attains competence for ER export and, thereby, indirectly preventing heterotypic interactions with prolamine polypeptides.

Gene-gene interactions between mutants that accumulate abnormally high amounts of proglutelin in rice seed

“…Hence, the epistatic nature of esp2 to the other glup genes supports the view that PDI1-1 functions early in the maturation and trafficking of proglutelins and that disulfide-bond formation within the ER is one of the first events of proglutelin maturation (Satoh-Cruz et al 2010a). Moreover, the hypostatic relationship of the seven glup/ Glup mutant lines to esp2 suggests that these genes are involved in maturation steps subsequent to disulfide bond formation within the ER or downstream transport processes beginning with ER export.…”

“…The esp2 seeds lack the ER-localized PDI1-1 which results in the accumulation of mis-localized proglutelin with prolamins within the ER (Satoh-Cruz et al 2010a, Takemoto et al 2002. Hence, the epistatic nature of esp2 to the other glup genes supports the view that PDI1-1 functions early in the maturation and trafficking of proglutelins and that disulfide-bond formation within the ER is one of the first events of proglutelin maturation (Satoh-Cruz et al 2010a).…”

“…An antibody against BiP was raised against a 14 amino acid synthetic peptide of rice BiP as described in Satoh-Cruz et al (2010a).…”

“…The genes for three of these mutants esp2, glup3 and glup4 have been identified. The Esp2 gene encodes the protein disulfide isomerase 1-1 (PDI 1-1), which catalyzes the formation of intramolecular disulfide bonds and serves as a molecular chaperone within the endoplasmic reticulum (Satoh-Cruz et al 2010a, Takemoto et al 2002. The Glup3 gene encodes a vacuolar processing enzyme (VPE), an activity which proteolytically processes proglutelin into acidic and basic subunits within the PSV (Kumamaru et al 2010), while Glup4 gene encodes the small GTPase Rab5a, which participates in the trafficking of proglutelin from Golgi apparatus to the PSV (Satoh-Cruz et al 2010b).…”

Distinct Roles of Protein Disulfide Isomerase and P5 Sulfhydryl Oxidoreductases in Multiple Pathways for Oxidation of Structurally Diverse Storage Proteins in Rice

“…The rice endosperm provides an ideal system for studying specific functions of the PDI family oxidoreductases. A PDIL1;1 knockout mutant esp2 accumulates large protein aggregates containing proglutelins through intermolecular disulfide bonds in the ER (Takemoto et al, 2002;Onda et al, 2009;Satoh-Cruz et al, 2010). These studies leave little room for doubt that PDIL1;1 facilitates oxidative folding of proglutelins and that its activity is indispensable when the rate of proglutelin synthesis exceeds a critical rate.…”