4.8 Article

Fungal phytochrome chromophore biosynthesis at mitochondria

Journal

EMBO JOURNAL
Volume 40, Issue 17, Pages -

Publisher

WILEY
DOI: 10.15252/embj.2021108083

Keywords

chromophore; heme; heme oxygenase; metabolon; phytochrome

Funding

  1. German Science Foundation [DFG Fi-459/19-1]
  2. Karlsruhe School of Optics and Photonics, DFG [GSC 21]

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This study reveals the involvement of mitochondria in light sensing in fungi, related to phytochrome dependence. Phytochrome photoreceptors in fungi contain a linear, heme-derived tetrapyrrole as chromophore, suggesting different approaches for chromophore biosynthesis and insertion into phytochrome in plants and fungi.
Mitochondria are essential organelles because of their function in energy conservation. Here, we show an involvement of mitochondria in phytochrome-dependent light sensing in fungi. Phytochrome photoreceptors are found in plants, bacteria, and fungi and contain a linear, heme-derived tetrapyrrole as chromophore. Linearization of heme requires heme oxygenases (HOs) which reside inside chloroplasts in planta. Despite the poor degree of conservation of HOs, we identified two candidates in the fungus Alternaria alternata. Deletion of either one phenocopied phytochrome deletion. The two enzymes had a cooperative effect and physically interacted with phytochrome, suggesting metabolon formation. The metabolon was attached to the surface of mitochondria with a C-terminal anchor (CTA) sequence in HoxA. The CTA was necessary and sufficient for mitochondrial targeting. The affinity of phytochrome apoprotein to HoxA was 57,000-fold higher than the affinity of the holoprotein, suggesting a kiss-and-go mechanism for chromophore loading and a function of mitochondria as assembly platforms for functional phytochrome. Hence, two alternative approaches for chromophore biosynthesis and insertion into phytochrome evolved in plants and fungi.

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