A molecular switch in sulfur metabolism to reduce arsenic and enrich selenium in rice grain

Sheng-Kai Sun,Xin-Yuan Huang,Xuejie Xu,Rüdiger Hell,Zhong Tang,Zhu Tang,Fang-Jie Zhao,Markus Wirtz

doi:10.1038/s41467-021-21282-5

Sheng-Kai Sun, Xin-Yuan Huang + Show 6 more

Open Access

https://doi.org/10.1038/s41467-021-21282-5

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Abstract

Rice grains typically contain high levels of toxic arsenic but low levels of the essential micronutrient selenium. Anthropogenic arsenic contamination of paddy soils exacerbates arsenic toxicity in rice crops resulting in substantial yield losses. Here, we report the identification of the gain-of-function arsenite tolerant 1 (astol1) mutant of rice that benefits from enhanced sulfur and selenium assimilation, arsenic tolerance, and decreased arsenic accumulation in grains. The astol1 mutation promotes the physical interaction of the chloroplast-localized O-acetylserine (thiol) lyase protein with its interaction partner serine-acetyltransferase in the cysteine synthase complex. Activation of the serine-acetyltransferase in this complex promotes the uptake of sulfate and selenium and enhances the production of cysteine, glutathione, and phytochelatins, resulting in increased tolerance and decreased translocation of arsenic to grains. Our findings uncover the pivotal sensing-function of the cysteine synthase complex in plastids for optimizing stress resilience and grain quality by regulating a fundamental macronutrient assimilation pathway.

Highlights

Rice grains typically contain high levels of toxic arsenic but low levels of the essential micronutrient selenium
Cys is synthesized in all subcellular compartments with own protein biogenesis by a two-step pathway: the formation of O-acetylserine (OAS) from serine and acetyl CoA catalyzed by serine acetyltransferase (SAT) and the condensation of OAS and sulfide to Cys catalyzed by Oacetylserine(thiol)lyase (OAS-TL)[21,22]
When grown hydroponically in a growth chamber, astol[1] segregated into two phenotypes, one with decreased growth compared with wild type (WT) and the other dying of leaves from tips inwards leading to eventual plant death (Fig. 1c, d, and Supplementary Fig. 1c–f)

Summary

Introduction

Rice grains typically contain high levels of toxic arsenic but low levels of the essential micronutrient selenium. Activation of the serineacetyltransferase in this complex promotes the uptake of sulfate and selenium and enhances the production of cysteine, glutathione, and phytochelatins, resulting in increased tolerance and decreased translocation of arsenic to grains. A key mechanism of As detoxification in plants is via the complexation of arsenite [As(III)] by thiol compounds, such as glutathione (GSH) and phytochelatins (PCs), and subsequent sequestration into the vacuoles[10,11,12,13,14] This mechanism reduces As translocation to rice grain[12,15,16,17]. Uncoupling of the OAS-sensing function of the plastidic CSC from its regulatory impact on SAT resulted in (1) enhanced S uptake and assimilation, (2) increased tolerance to As and (3) decreased As accumulation in rice grain. Besides the potential biotechnological applications, our findings uncover the pivotal sensing-function of the plastid CSC in the regulation of S and Se metabolism and tolerance to metalloid toxicity

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