Post-translational coordination of chlorophyll biosynthesis and breakdown by BCMs maintains chlorophyll homeostasis during leaf development

Peng Wang,Andreas S Richter,Stefan Geimer,Julius R W Kleeberg,Bernhard Grimm

doi:10.1038/s41467-020-14992-9

Peng Wang, Andreas S Richter + Show 3 more

Open Access

https://doi.org/10.1038/s41467-020-14992-9

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Abstract

Chlorophyll is indispensable for life on Earth. Dynamic control of chlorophyll level, determined by the relative rates of chlorophyll anabolism and catabolism, ensures optimal photosynthesis and plant fitness. How plants post-translationally coordinate these two antagonistic pathways during their lifespan remains enigmatic. Here, we show that two Arabidopsis paralogs of BALANCE of CHLOROPHYLL METABOLISM (BCM) act as functionally conserved scaffold proteins to regulate the trade-off between chlorophyll synthesis and breakdown. During early leaf development, BCM1 interacts with GENOMES UNCOUPLED 4 to stimulate Mg-chelatase activity, thus optimizing chlorophyll synthesis. Meanwhile, BCM1’s interaction with Mg-dechelatase promotes degradation of the latter, thereby preventing chlorophyll degradation. At the onset of leaf senescence, BCM2 is up-regulated relative to BCM1, and plays a conserved role in attenuating chlorophyll degradation. These results support a model in which post-translational regulators promote chlorophyll homeostasis by adjusting the balance between chlorophyll biosynthesis and breakdown during leaf development.

Highlights

Chlorophyll is indispensable for life on Earth
To identify novel regulators of Chl biosynthesis and catabolism, we screened publicly available datasets for Arabidopsis genes of unknown function that exhibit the transcriptional signatures of Chl biosynthesis genes (CBGs) or catabolic genes (CCGs), and identified At2g35260, hereafter designated BCM1
Immunoblot analyses using a BCM1 antiserum raised against recombinant Arabidopsis His-BCM155 showed that BCM1 accumulates as an ~36 kDa protein in all Arabidopsis tissues except roots (Fig. 1b)

Summary

Introduction

Dynamic control of chlorophyll level, determined by the relative rates of chlorophyll anabolism and catabolism, ensures optimal photosynthesis and plant fitness. At the onset of leaf senescence, BCM2 is up-regulated relative to BCM1, and plays a conserved role in attenuating chlorophyll degradation. These results support a model in which post-translational regulators promote chlorophyll homeostasis by adjusting the balance between chlorophyll biosynthesis and breakdown during leaf development. During the life cycle of plants, leaf development and seed maturation are usually accompanied by a visible change in pigmentation from pale-yellow to green and from green to brown or yellow, which reflects the initial rise and subsequent fall in the content of chlorophyll (Chl)[1]. Six enzymatic steps convert eight molecules of ALA into protoporphyrin IX (Proto), which is the common precursor for both

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