Research Progress on the Iron-sulfur Cluster Synthesis System and Regulation in Plant Mitochondria

doi:10.11983/CBB24103

Abstract

Abstract: Iron-sulfur [Fe-S] clusters, which act as cofactors for iron-sulfur proteins, are ubiquitously implicated in a diverse array of biological processes, such as photosynthesis, respiration, electron transport, and the biosynthesis of essential vitamins and cofactors. Their intracellular biogenesis is modulated by a suite of proteins that catalyze and regulate the process, with compartmentalization occurring within discrete subcellular compartments. Mitochondria, as the central organelles for cellular energy metabolism, harbor numerous key metabolic enzymes that are iron-sulfur proteins, necessitating the provision of iron-sulfur clusters by the mitochondrial assembly machinery, the iron-sulfur cluster (ISC). Advancements in research, particularly from bacteria and yeast systems, have facilitated significant strides in the identification and functional characterization of pivotal catalytic and regulatory proteins within the plant mitochondrial ISC system. Additionally, considerable progress has been made in the research of the role in iron-sulfur clusters in the plant growth and development. The elucidation of plant-specific components within the iron-sulfur cluster synthesis machinery and the mechanisms by which this system responds to environmental stress are areas of growing interest. This manuscript provides a comprehensive review of the current state of research on the mechanism of iron-sulfur cluster synthesis in plants, with a particular focus on the mitochondrial ISC assembly system. It also provides a succinct synopsis of the role of key genes within the ISC system in plant growth and development, as well as their involvement in the response to abiotic stressors.

Key words: iron-sulfur clusters, mitochondria, ISC system, plants, stress response

Tao Xie, Yifan Zhang, Yunhui Liu, Huiyu You, Jibenben Xia, Rong Ma, Chunni Zhang, Xuejun Hua. Research Progress on the Iron-sulfur Cluster Synthesis System and Regulation in Plant Mitochondria[J]. Chinese Bulletin of Botany, 2025, 60(4): 499-514.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB24103

https://www.chinbullbotany.com/EN/Y2025/V60/I4/499

Figures/Tables 4

Figure 1 The basic structure of iron-sulfur clusters (adapted from Lu, 2018) (A) [2Fe-2S] type iron-sulfur clusters linked by 4 cysteines; (B) NEET [2Fe-2S] iron-sulfur clusters connected by three cysteines and one histidine; (C) Rieske [2Fe-2S] connected by two cysteines and two histidine; (D) [3Fe-4S] connected by three cysteine residues; (E) [4Fe-4S] linked by four cysteine residues; (F) [4Fe-4S] coordinated by four cysteine residues, can bind heme with mercaptan coordination bonds.

Figure 2 Hypothetical model of the mitochondrial ISC biosynthetic pathway in Arabidopsis thaliana (adapted from Lill, 2009) The schematic diagram refers to the yeast mitochondrial ISC synthesis pathway model, and the components in the red box have not yet been reported in Arabidopsis. In the first step, the AtNfs1-AtIsd11 complex desulfurates cysteine, and Frataxin may provide iron. The unidentified homologous iron transport proteins Mrs3 and Mrs4 can transport iron from the cytoplasm to the mitochondria where it binds with Frataxin, whereas AtMFDR and AtMFDX may assist in electron transfer by NADPH. Iron and sulfur are synthesized into iron-sulfur clusters on AtIsu1. In the second step, AtHscA2 and AtHscB bind to AtIsu1, promoting the release of iron-sulfur clusters from AtIsu1. The third step involves transporting the iron-sulfur clusters to various iron-sulfur proteins, such as GrxS15, mitochondrial iron-sulfur proteins, fumarase, biosynthetic enzymes, and electron transport chain complexes I, II, and III. The transport of some iron-sulfur proteins requires the participation of iron-sulfur cluster assembly factors 1 and 2 (AtIscA1 and AtIscA2), and the assembly factor AtIBA57.

Table 1 Phenotypes of mutant alleles involved in mitochondrial [Fe-S] cluster assembly genes in Arabidopsis thaliana

基因	突变类型	生长表型	参考文献
Frataxin	SALK_021263	生长迟缓、果实鲜重降低且种子数减少	Busi et al., 2006
	SALK_094203	部分种子不育	Busi et al., 2004
	SALK_122008	部分种子不育, 毛绒根	Martin et al., 2009
ISU1	过表达	提升铁的富集能力	Song et al., 2022
	RNAi	茎细, 植株矮小	Frazzon et al., 2007
	SALK_006332	植株矮小	Frazzon et al., 2007
NFS1	过表达	新叶扇形边缘、杂乱花序、莲座叶和尾状叶腋下的腋芽增多, 对病菌的抗性增强	Frazzon et al., 2007 Fonseca et al., 2020
HscB	SALK_099684	根的铁吸收水平降低, 铁在枝叶中积累	Leaden et al., 2016
HscB	SALK_085159	茎部显示出无蜡状表型, 具有光滑的外表	Xu et al., 2009
HscA1	SALK_081383、SALK_081385、 SALK_128982和SALK_140494	茎短, 莲座叶变小	Wei et al., 2019
HscA2	SAIL_354_E09、SAIL_302_G07和 HscA2m点突变	无明显表型, 对外源脯氨酸具有抗性	Wei et al., 2019; Zhang et al., 2025
GrxS15	SALK_112767、GrxS15^amiR、 SALK_112767C、GK-837C05 和SAIL_431_H03	根短, 莲座叶变小, 根尖呼吸速率降低, 对砷胁迫的抗性增强, 早期胚胎致死	Moseler et al., 2015; Ströher et al., 2016
SSR1	FLAG_356A08和FLAG_571A02	根生长受到抑制	Feng et al., 2025

Figure 3 Heatmap of gene expression related to the ISC synthesis pathway in Arabidopsis thaliana under various abiotic stresses Heatmap of mitochondrial iron-sulfur protein gene expression under various abiotic stresses, with data sourced from the Arabidopsis eFP Browser (https://bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi). The color markings indicate the fold change in gene expression relative to that in the control group. The time of stress treatment shown in the graph is 24 h for all the samples.

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