Pyrenoid Starch Sheath Is Required for LCIB Localization and the CO2-Concentrating Mechanism in Green Algae.

Chihana Toyokawa,Hideya Fukuzawa,Takashi Yamano

doi:10.1104/pp.19.01587

Abstract

Aquatic photosynthetic organisms induce a CO2-concentrating mechanism (CCM) to overcome the difficulty of acquiring inorganic carbon under CO2-limiting conditions. As part of the CCM, the CO2-fixing enzyme Rubisco is enriched in the pyrenoid located in the chloroplast, and, in many green algae, several thick starch plates surround the pyrenoid to form a starch sheath. In Chlamydomonas reinhardtii, low-CO2-inducible protein B (LCIB), which is an essential factor for the CCM, displays altered cellular localization in response to a decrease in environmental CO2 concentration, moving from dispersed throughout the chloroplast stroma to around the pyrenoid. However, the mechanism behind LCIB migration remains poorly understood. Here, we report the characteristics of an Isoamylase1-less mutant (4-D1), which shows aberrant LCIB localization and starch sheath formation. Under very-low-CO2 conditions, 4-D1 showed retarded growth, lower photosynthetic affinities against inorganic carbon, and a decreased accumulation level of the HCO3 - transporter HLA3. The aberrant localization of LCIB was also observed in another starch-sheathless mutant sta11-1, but not in sta2-1, which possesses a thinned starch sheath. These results suggest that the starch sheath around the pyrenoid is required for the correct localization of LCIB and for the operation of CCM.

Highlights

Aquatic photosynthetic organisms induce a CO2-concentrating mechanism (CCM) to overcome the difficulty of acquiring inorganic carbon under CO2-limiting conditions
We elucidated the contribution of the starch sheath to the CCM by characterizing mutants with aberrant low-CO2–inducible protein B (LCIB) localization
A previous study proposed that starch sheath formation itself is not involved in the CCM, because the isa1 allelic mutant BAFJ-6, in which no starch sheath formed, did not show a significant decrease in Ci affinity compared with cw-15 cells (Villarejo et al, 1996)

Summary

Introduction

Aquatic photosynthetic organisms induce a CO2-concentrating mechanism (CCM) to overcome the difficulty of acquiring inorganic carbon under CO2-limiting conditions. In Chlamydomonas reinhardtii, low-CO2–inducible protein B (LCIB), which is an essential factor for the CCM, displays altered cellular localization in response to a decrease in environmental CO2 concentration, moving from dispersed throughout the chloroplast stroma to around the pyrenoid. To maintain photosynthetic activity in such a CO2-deficient environment, most aquatic algae induce a CO2-concentrating mechanism (CCM) for the active uptake of inorganic carbon (Ci; CO2 and HCO32) into cells and to concentrate CO2 into the pyrenoid, where Rubisco is enriched in the chloroplast (Badger et al, 1980). Other studies have suggested that absence of the starch sheath does not affect the photosynthetic ability of the cells, indicating that the Another essential factor for the CCM is the active Ci transport system that concentrates extracellular Ci into the pyrenoid. It was reported that Chlamydomonas acclimates to two distinct limiting CO2 conditions, termed low-CO2 (LC; ;0.03% to 0.5% CO2 in growth-chamber culture or 7–70 mM CO2 in liquid culture) and verylow–CO2 (VLC; ,0.02% CO2 or ,7 mM CO2), and that there are at least two types of Ci transport systems dependent on external CO2 concentrations (Wang and Spalding, 2014a)

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