Dual localization of PDI5 couples endoplasmic reticulum proteostasis to meristem organization and meiotic fidelity in Arabidopsis.

Abstract

Plant growth and reproduction require coordinated control of hormone-dependent tissue patterning and faithful meiotic chromosome segregation, yet whether upstream proteostasis contributes to both processes remains unclear. Here, we show that Arabidopsis PROTEIN DISULFIDE ISOMERASE 5 (PDI5) contributes to auxin-associated developmental patterning and meiotic fidelity. Native-promoter reporter constructs corresponding to two annotated PDI5 transcript isoforms show distinct subcellular enrichment, with one displaying an endoplasmic reticulum (ER)-associated distribution and the other showing nuclear enrichment. Disruption of PDI5 alters bulk glycoprotein staining and glycoside and trafficking-associated transcriptional programs, reduces the abundance of PIN-FORMED 2-green fluorescent protein (PIN2-GFP), alters its brefeldin A-sensitive intracellular accumulation, and is associated with perturbed auxin-response patterning and disorganized root meristems. In reproductive tissues, the pdi5 mutant shows abnormal germline-associated cell-fate restriction, impaired meiotic chromosome behavior, reduced chiasma formation and decreased fertility. Proteomic and interaction analyses identify the cohesin subunit SISTER-CHROMATID COHESION PROTEIN 3 (SCC3) as a PDI5-associated protein, and disruption of a conserved SCC3 N809-centered motif reduces its detectable association with PDI5. In a PDI5 promoter-driven conditional complementation assay, SCC3^N809E fails to support fertility rescue. These findings support a model in which PDI5-dependent proteostasis contributes to auxin-associated developmental patterning and meiotic chromosome fidelity, potentially through compartmentally distributed PDI5 functions.