Bilin-dependent regulation of chlorophyll biosynthesis by GUN4.

Abstract

Biosyntheses of chlorophyll and heme in oxygenic phototrophs share a common trunk pathway that diverges with insertion of magnesium or iron into the last common intermediate, protoporphyrin IX. Since both tetrapyrroles are pro-oxidants, it is essential that their metabolism is tightly regulated. Here, we establish that heme-derived linear tetrapyrroles (bilins) function to stimulate the enzymatic activity of magnesium chelatase (MgCh) via their interaction with GENOMES UNCOUPLED 4 (GUN4) in the model green alga <i>Chlamydomonas reinhardtii</i> A key tetrapyrrole-binding component of MgCh found in all oxygenic photosynthetic species, <i>Cr</i>GUN4, also stabilizes the bilin-dependent accumulation of protoporphyrin IX-binding <i>Cr</i>CHLH1 subunit of MgCh in light-grown <i>C. reinhardtii</i> cells by preventing its photooxidative inactivation. Exogenous application of biliverdin IXα reverses the loss of <i>Cr</i>CHLH1 in the bilin-deficient heme oxygenase (<i>hmox1</i>) mutant, but not in the <i>gun4</i> mutant. We propose that these dual regulatory roles of GUN4:bilin complexes are responsible for the retention of bilin biosynthesis in all photosynthetic eukaryotes, which sustains chlorophyll biosynthesis in an illuminated oxic environment.