Plant-specific cochaperone SSR1 affects root elongation by modulating the mitochondrial iron-sulfur cluster assembly machinery

To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 ( SSR1 ), we screened for su ppressors of the s sr1-2 ( sus ) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2 , resulted...

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Published inPLoS genetics Vol. 21; no. 2; p. e1011597
Main Authors Feng, Xuanjun, Hu, Yue, Xie, Tao, Han, Huiling, Bonea, Diana, Zeng, Lijuan, Liu, Jie, Ying, Wenhan, Mu, Bona, Cai, Yuanyuan, Zhang, Min, Lu, Yanli, Zhao, Rongmin, Hua, Xuejun
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Published United States Public Library of Science 05.02.2025
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Abstract To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 ( SSR1 ), we screened for su ppressors of the s sr1-2 ( sus ) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2 , resulted from G87D and T55M single amino acid substitutions in HSCA2 (At5g09590) and ISU1 (At4g22220), both crucial components of the mitochondrial iron-sulfur (Fe-S) cluster assembly machinery. SSR1 displayed a robust cochaperone-like activity and interacted with HSCA2 and ISU1, facilitating the binding of HSCA2 to ISU1. In comparison to the wild-type plants, ssr1-2 mutants displayed increased iron accumulation in root tips and altered expression of genes responsive to iron deficiency. Additionally, the enzymatic activities of several iron-sulfur proteins and the mitochondrial membrane potential were reduced in ssr1-2 mutants. Interestingly, SSR1 appears to be exclusive to plant lineages and is induced by environmental stresses. Although HSCA2 G87D and ISU1 T55M can effectively compensate for the phenotypes associated with SSR1 deficiency under favorable conditions, their compensatory effects are significantly diminished under stress. Collectively, SSR1 represents a new and significant component of the mitochondrial Fe-S cluster assembly (ISC) machinery. It may also confer adaptive advantages on plant ISC machinery in response to environmental stress.
AbstractList To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 (SSR1), we screened for suppressors of the ssr1-2 (sus) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2, resulted from G87D and T55M single amino acid substitutions in HSCA2 (At5g09590) and ISU1 (At4g22220), both crucial components of the mitochondrial iron-sulfur (Fe-S) cluster assembly machinery. SSR1 displayed a robust cochaperone-like activity and interacted with HSCA2 and ISU1, facilitating the binding of HSCA2 to ISU1. In comparison to the wild-type plants, ssr1-2 mutants displayed increased iron accumulation in root tips and altered expression of genes responsive to iron deficiency. Additionally, the enzymatic activities of several iron-sulfur proteins and the mitochondrial membrane potential were reduced in ssr1-2 mutants. Interestingly, SSR1 appears to be exclusive to plant lineages and is induced by environmental stresses. Although HSCA2.sup.G87D and ISU1.sup.T55M can effectively compensate for the phenotypes associated with SSR1 deficiency under favorable conditions, their compensatory effects are significantly diminished under stress. Collectively, SSR1 represents a new and significant component of the mitochondrial Fe-S cluster assembly (ISC) machinery. It may also confer adaptive advantages on plant ISC machinery in response to environmental stress.
To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 ( SSR1 ), we screened for su ppressors of the s sr1-2 ( sus ) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2 , resulted from G87D and T55M single amino acid substitutions in HSCA2 (At5g09590) and ISU1 (At4g22220), both crucial components of the mitochondrial iron-sulfur (Fe-S) cluster assembly machinery. SSR1 displayed a robust cochaperone-like activity and interacted with HSCA2 and ISU1, facilitating the binding of HSCA2 to ISU1. In comparison to the wild-type plants, ssr1-2 mutants displayed increased iron accumulation in root tips and altered expression of genes responsive to iron deficiency. Additionally, the enzymatic activities of several iron-sulfur proteins and the mitochondrial membrane potential were reduced in ssr1-2 mutants. Interestingly, SSR1 appears to be exclusive to plant lineages and is induced by environmental stresses. Although HSCA2 G87D and ISU1 T55M can effectively compensate for the phenotypes associated with SSR1 deficiency under favorable conditions, their compensatory effects are significantly diminished under stress. Collectively, SSR1 represents a new and significant component of the mitochondrial Fe-S cluster assembly (ISC) machinery. It may also confer adaptive advantages on plant ISC machinery in response to environmental stress.
To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 ( SSR1 ), we screened for su ppressors of the s sr1-2 ( sus ) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2 , resulted from G87D and T55M single amino acid substitutions in HSCA2 (At5g09590) and ISU1 (At4g22220), both crucial components of the mitochondrial iron-sulfur (Fe-S) cluster assembly machinery. SSR1 displayed a robust cochaperone-like activity and interacted with HSCA2 and ISU1, facilitating the binding of HSCA2 to ISU1. In comparison to the wild-type plants, ssr1-2 mutants displayed increased iron accumulation in root tips and altered expression of genes responsive to iron deficiency. Additionally, the enzymatic activities of several iron-sulfur proteins and the mitochondrial membrane potential were reduced in ssr1-2 mutants. Interestingly, SSR1 appears to be exclusive to plant lineages and is induced by environmental stresses. Although HSCA2 G87D and ISU1 T55M can effectively compensate for the phenotypes associated with SSR1 deficiency under favorable conditions, their compensatory effects are significantly diminished under stress. Collectively, SSR1 represents a new and significant component of the mitochondrial Fe-S cluster assembly (ISC) machinery. It may also confer adaptive advantages on plant ISC machinery in response to environmental stress. Iron-sulfur (Fe-S) clusters are crucial components found in many proteins that play essential roles in various biological processes. The machinery responsible for making these clusters in mitochondria, known as ISC biosynthesis, has its origins in bacteria and remained largely unchanged through evolution. However, understanding of specific regulators that control Fe-S cluster production in plants is still limited. In this study, we identified a unique protein in plants, SSR1, which acts as a cochaperone. SSR1 facilitates the interaction between the two critical proteins, HSCA2 and ISU1, a necessary process for the release of Fe-S clusters from their scaffold. We also showed that SSR1 has evolved alongside the ISC biosynthetic machinery and that mutations in HSCA2 and ISU1 can compensate for its absence. This highlights the synergistic relationship between SSR1 and other components of the ISC machinery. Overall, this research uncovers a novel component of the ISC biosynthetic system and shows how it varies between plants, animals, and microorganisms.
To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 (SSR1), we screened for suppressors of the ssr1-2 (sus) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2, resulted from G87D and T55M single amino acid substitutions in HSCA2 (At5g09590) and ISU1 (At4g22220), both crucial components of the mitochondrial iron-sulfur (Fe-S) cluster assembly machinery. SSR1 displayed a robust cochaperone-like activity and interacted with HSCA2 and ISU1, facilitating the binding of HSCA2 to ISU1. In comparison to the wild-type plants, ssr1-2 mutants displayed increased iron accumulation in root tips and altered expression of genes responsive to iron deficiency. Additionally, the enzymatic activities of several iron-sulfur proteins and the mitochondrial membrane potential were reduced in ssr1-2 mutants. Interestingly, SSR1 appears to be exclusive to plant lineages and is induced by environmental stresses. Although HSCA2G87D and ISU1T55M can effectively compensate for the phenotypes associated with SSR1 deficiency under favorable conditions, their compensatory effects are significantly diminished under stress. Collectively, SSR1 represents a new and significant component of the mitochondrial Fe-S cluster assembly (ISC) machinery. It may also confer adaptive advantages on plant ISC machinery in response to environmental stress.To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 (SSR1), we screened for suppressors of the ssr1-2 (sus) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2, resulted from G87D and T55M single amino acid substitutions in HSCA2 (At5g09590) and ISU1 (At4g22220), both crucial components of the mitochondrial iron-sulfur (Fe-S) cluster assembly machinery. SSR1 displayed a robust cochaperone-like activity and interacted with HSCA2 and ISU1, facilitating the binding of HSCA2 to ISU1. In comparison to the wild-type plants, ssr1-2 mutants displayed increased iron accumulation in root tips and altered expression of genes responsive to iron deficiency. Additionally, the enzymatic activities of several iron-sulfur proteins and the mitochondrial membrane potential were reduced in ssr1-2 mutants. Interestingly, SSR1 appears to be exclusive to plant lineages and is induced by environmental stresses. Although HSCA2G87D and ISU1T55M can effectively compensate for the phenotypes associated with SSR1 deficiency under favorable conditions, their compensatory effects are significantly diminished under stress. Collectively, SSR1 represents a new and significant component of the mitochondrial Fe-S cluster assembly (ISC) machinery. It may also confer adaptive advantages on plant ISC machinery in response to environmental stress.
To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 (SSR1), we screened for suppressors of the ssr1-2 (sus) was performed and identified over a dozen candidates with varying degrees of root growth restoration. Among these, the two most effective suppressors, sus1 and sus2, resulted from G87D and T55M single amino acid substitutions in HSCA2 (At5g09590) and ISU1 (At4g22220), both crucial components of the mitochondrial iron-sulfur (Fe-S) cluster assembly machinery. SSR1 displayed a robust cochaperone-like activity and interacted with HSCA2 and ISU1, facilitating the binding of HSCA2 to ISU1. In comparison to the wild-type plants, ssr1-2 mutants displayed increased iron accumulation in root tips and altered expression of genes responsive to iron deficiency. Additionally, the enzymatic activities of several iron-sulfur proteins and the mitochondrial membrane potential were reduced in ssr1-2 mutants. Interestingly, SSR1 appears to be exclusive to plant lineages and is induced by environmental stresses. Although HSCA2G87D and ISU1T55M can effectively compensate for the phenotypes associated with SSR1 deficiency under favorable conditions, their compensatory effects are significantly diminished under stress. Collectively, SSR1 represents a new and significant component of the mitochondrial Fe-S cluster assembly (ISC) machinery. It may also confer adaptive advantages on plant ISC machinery in response to environmental stress.
Audience Academic
Author Zeng, Lijuan
Zhao, Rongmin
Ying, Wenhan
Hu, Yue
Bonea, Diana
Zhang, Min
Liu, Jie
Xie, Tao
Cai, Yuanyuan
Feng, Xuanjun
Hua, Xuejun
Mu, Bona
Lu, Yanli
Han, Huiling
AuthorAffiliation 6 Sichuan Keyuan Testing Center of Engineering Technology Co., Ltd; Chengdu, Sichuan, PR China
Université de Lorraine, FRANCE
2 Maize Research Institute of Sichuan Agricultural University, Wenjiang, Sichuan, China
3 Key Laboratory of Plant Secondary Metabolism and Regulation of Zhejiang Province, College of Life Sciences and Medicine, Zhejiang Sci-Tech University, Hangzhou, Zhejiang, China
7 Institute of Genetics and Developmental Biology, Beijing, China
1 State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Wenjiang, Sichuan, China
5 Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada
4 Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing, China
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Snippet To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 ( SSR1 ), we screened for su ppressors of the s sr1-2 ( sus ) was performed and identified over...
To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 (SSR1), we screened for suppressors of the ssr1-2 (sus) was performed and identified over a...
To elucidate the molecular function of SHORT AND SWOLLEN ROOT1 ( SSR1 ), we screened for su ppressors of the s sr1-2 ( sus ) was performed and identified over...
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StartPage e1011597
SubjectTerms Amino acids
Arabidopsis - genetics
Arabidopsis - growth & development
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Biology and Life Sciences
Gene Expression Regulation, Plant
Genetic aspects
Iron - metabolism
Iron in the body
Iron proteins
Iron-Sulfur Proteins - genetics
Iron-Sulfur Proteins - metabolism
Medicine and Health Sciences
Mitochondria
Mitochondria - genetics
Mitochondria - metabolism
Mitochondrial Proteins - genetics
Mitochondrial Proteins - metabolism
Molecular chaperones
Molecular Chaperones - genetics
Molecular Chaperones - metabolism
Mutation
Physiological aspects
Plant Roots - genetics
Plant Roots - growth & development
Plant Roots - metabolism
Research and Analysis Methods
Roots (Botany)
Sulfur
Sulfur - metabolism
Sulfur compounds
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Title Plant-specific cochaperone SSR1 affects root elongation by modulating the mitochondrial iron-sulfur cluster assembly machinery
URI https://www.ncbi.nlm.nih.gov/pubmed/39908322
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https://pubmed.ncbi.nlm.nih.gov/PMC11835332
https://doaj.org/article/e1d23e6e52c84502a8c85d119e300227
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