Retrograde sulfur flow from glucosinolates to cysteine in Arabidopsis thaliana
Sugiyama, Ryosuke Li, Rui Kuwahara, Ayuko Nakabayashi, Ryo Sotta, Naoyuki Mori, Tetsuya Ito, Takehiro Ohkama-Ohtsu, Naoko Fujiwara, Toru Saito, Kazuki
Li, Rui
Kuwahara, Ayuko
Nakabayashi, Ryo
Sotta, Naoyuki
Mori, Tetsuya
Ito, Takehiro
Ohkama-Ohtsu, Naoko
Fujiwara, Toru
Saito, Kazuki
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Alternative Title
Abstract
Specialized (secondary) metabolic pathways in plants have long been considered one-way routes of leading primary metabolite precursors to bioactive end products. Conversely, endogenous degradation of such “end” products in plant tissues has been observed following environmental stimuli, including nutrition stress. Therefore, it is of general interest whether specialized metabolites can be reintegrated into primary metabolism to recover the invested resources, especially in the case of nitrogen- or sulfur-rich compounds. Here, we demonstrate that endogenous glucosinolates (GLs), a class of sulfur-rich plant metabolites, are exploited as a sulfur source by the reallocation of sulfur atoms to primary metabolites such as cysteine in Arabidopsis thaliana. Tracer experiments using 34S- or deuterium-labeled GLs depicted the catabolic processing of GL breakdown products in which sulfur is mobilized from the thioglucoside group in GL molecules, potentially accompanied by the release of the sulfate group. Moreover, we reveal that beta-glucosidases BGLU28 and BGLU30 are the major myrosinases that initiate sulfur reallocation by hydrolyzing particular GL species, conferring sulfur deficiency tolerance in A. thaliana, especially during early development. The results delineate the physiological function of GL as a sulfur reservoir, in addition to their well-known functions as defense chemicals. Overall, our findings demonstrate the bidirectional interaction between primary and specialized metabolism, which enhances our understanding of the underlying metabolic mechanisms via which plants adapt to their environments. © 2021 National Academy of Sciences. All rights reserved.
Keywords
Glucosinolate, Specialized metabolism, Stress response, Sulfur
Source Title
Proceedings of the National Academy of Sciences of the United States of America
Publisher
National Academy of Sciences
Series/Report No.
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Rights
Attribution 4.0 International
Date
2021-05-25
DOI
10.1073/pnas.2017890118
Type
Article