BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana

Hindt, Maria N.; Akmakjian, Garo Z.; Pivarski, Kara; Punshon, Tracy; Baxter, Ivan; Salt, David E.; Guerinot, Mary Lou

doi:10.1039/c7mt00152e

Cited by 146 publications

(180 citation statements)

References 59 publications

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“…However, a complementation analysis using an Arabidopsis bts mutant indicated that deleting the hemerythrin domains did not dramatically affect the physiological function of BTS, in contrast to the essential function of the RING Zn‐finger domain (Selote et al , Matthiadis and Long ), which suggests the limited importance of the hemerythrin domains in BTS function. Moreover, another study identified a bts mutant that disrupted expression of Fe‐related genes more predominantly under Fe‐sufficient than under Fe‐deficient conditions (Hindt et al ), similarly to our HRZ ‐knockdown rice (Kobayashi et al ). These results suggest that HRZs/BTS function better under Fe‐sufficient conditions than under Fe‐deficient conditions, regardless of the Fe deficiency‐induced expression of HRZs / BTS themselves.…”

Section: Introductionsupporting

confidence: 73%

Rice HRZ ubiquitin ligases are crucial for the response to excess iron

Aung

Kobayashi

Masuda

et al. 2018

Physiologia Plantarum

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Iron is essential for virtually all organisms but is toxic when present in excess. To acquire the proper amount of iron, plants induce expression of various genes involved in iron uptake and translocation in response to low iron availability. Two iron-binding ubiquitin ligases, OsHRZ1 and OsHRZ2, negatively regulate such iron deficiency responses in rice (Oryza sativa). Transgenic rice plants with repressed expression of OsHRZ1 and OsHRZ2 (HRZ knockdown lines) are tolerant to low iron availability and accumulate iron in shoots and seeds under both iron-sufficient and -deficient conditions without a growth penalty. Although the expression of OsHRZ1 and OsHRZ2 is transcriptionally upregulated under iron-deficient conditions, the physiological relevance of this induction is not known. In the present study, we analyzed the response of HRZ knockdown lines to excess iron. In the presence of severe excess iron, the HRZ knockdown lines grew worse than non-transformants. The HRZ knockdown lines showed stunted shoot and root growth and more severe leaf bronzing compared to non-transformants. Moreover, these lines accumulated more iron in shoots and exhibited severely elevated expression of various genes involved in iron uptake and translocation as well as jasmonate signaling compared to non-transformants. These results indicate that HRZ ubiquitin ligases are crucial for repressing iron deficiency responses and protecting cells from iron toxicity in the presence of excess iron. These results support the possibility that HRZs are intracellular Fe sensors and provide clues for developing plants tolerant of either iron deficiency or excess with higher iron contents in edible parts.

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Section: Introductionsupporting

confidence: 73%

Rice HRZ ubiquitin ligases are crucial for the response to excess iron

Aung

Kobayashi

Masuda

et al. 2018

Physiologia Plantarum

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“…Few Fe‐sensing proteins have been identified in plants (Kobayashi and Nishizawa, ). The HRZ [hemerythrin motif‐containing really interesting new gene (RING)‐and zinc‐finger] proteins BRUTUS (BTS), BTS‐like, OsHRZ1 and OsHRZ2 are E3 ligases involved in the low‐Fe response (Long et al ., ; Kobayashi et al ., ; Hindt et al ., ). They target to proteasomal degradation several basic helix–loop–helix transcription factors such as POPEYE (PYE) and PYE‐like factors such as bHLH104 and bHLH105, which are positive regulators of the low‐Fe response.…”

Section: Discussionmentioning

confidence: 97%

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

et al. 2019

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Summary Low‐phosphate (Pi) conditions are known to repress primary root growth of Arabidopsis at low pH and in an Fe‐dependent manner. This growth arrest requires accumulation of the transcription factor STOP1 in the nucleus, where it activates the transcription of the malate transporter gene ALMT1; exuded malate is suspected to interact with extracellular Fe to inhibit root growth. In addition, ALS3 – an ABC‐like transporter identified for its role in tolerance to toxic Al – represses nuclear accumulation of STOP1 and the expression of ALMT1. Until now it was unclear whether Pi deficiency itself or Fe activates the accumulation of STOP1 in the nucleus. Here, by using different growth media to dissociate the effects of Fe from Pi deficiency itself, we demonstrate that Fe is sufficient to trigger the accumulation of STOP1 in the nucleus, which, in turn, activates the expression of ALMT1. We also show that a low pH is necessary to stimulate the Fe‐dependent accumulation of nuclear STOP1. Furthermore, pharmacological experiments indicate that Fe inhibits proteasomal degradation of STOP1. We also show that Al acts like Fe for nuclear accumulation of STOP1 and ALMT1 expression, and that the overaccumulation of STOP1 in the nucleus of the als3 mutant grown in low‐Pi conditions could be abolished by Fe deficiency. Altogether, our results indicate that, under low‐Pi conditions, Fe2/3+ and Al3+ act similarly to increase the stability of STOP1 and its accumulation in the nucleus where it activates the expression of ALMT1.

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“…Bnams4 b triggers translocation of BTS to reshape a novel interaction network BTS is a nuclear localised E3 ligase. It binds to and degrades relative transcription factors in the iron-deficiency and drought responses Kobayashi et al, 2013;Selote et al, 2015Selote et al, , 2018Hindt et al, 2017). However, Bnams4 b is a chloroplast-localised protein .…”

Section: Researchmentioning

confidence: 99%

Two young genes reshape a novel interaction network in Brassica napus

et al. 2019

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Summary New genes often drive the evolution of gene interaction networks. In Brassica napus, the widely used genic male sterile breeding system 7365ABC is controlled by two young genes, Bnams4b and BnaMs3. However, the interaction mechanism of these two young genes remains unclear. Here, we confirmed that Bnams4b interacts with the nuclear localised E3 ligase BRUTUS (BTS). Ectopic expression of AtBRUTUS (AtBTS) and comparison between Bnams4b‐transgenic Arabidopsis and bts mutants suggested that Bnams4b may drive translocation of BTS to cause various toxic defects. BnaMs3 gained an exclusive interaction with the plastid outer‐membrane translocon Toc33 compared with Bnams3 and AtTic40, and specifically compensated for the toxic effects of Bnams4b. Heat shock treatment also rescued the sterile phenotype, and high temperature suppressed the interaction between Bnams4b and BTS in yeast. Furthermore, the ubiquitin system and TOC (translocon at the outer envelope membrane of chloroplasts) component accumulation were affected in Bnams4b‐transgenic Arabidopsis plants. Taken together, these results indicate that new chimeric Bnams4b carries BTS from nucleus to chloroplast, which may disrupt the normal ubiquitin–proteasome system to cause toxic effects, and these defects can be compensated by BnaMs3−Toc33 interaction or environmental heat shock. It reveals a scenario in which two population‐specific coevolved young genes reshape a novel interaction network in plants.

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BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana

Cited by 146 publications

References 59 publications

Rice HRZ ubiquitin ligases are crucial for the response to excess iron

Rice HRZ ubiquitin ligases are crucial for the response to excess iron

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

Two young genes reshape a novel interaction network in Brassica napus

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