Investigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial Symbiosis
Rhizobia are rod-shaped bacteria that form nitrogen-fixing root nodules on leguminous plants; however, they don’t carry MreB, a key determinant of rod-like cell shape. Here, we introduced an actin-like mreB homolog from a pseudomonad into Mesorhizobium huakuii 7653R (a microsymbiont of Astragalus si...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2021-06-01
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| Series: | Molecular Plant-Microbe Interactions |
| Online Access: | https://doi.org/10.1094/MPMI-10-20-0299-FI |
| _version_ | 1818650475493326848 |
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| author | Wenlong Zhao Huixia Zhu Feng Wei Donglai Zhou Youguo Li Xue-Xian Zhang |
| author_facet | Wenlong Zhao Huixia Zhu Feng Wei Donglai Zhou Youguo Li Xue-Xian Zhang |
| author_sort | Wenlong Zhao |
| collection | DOAJ |
| description | Rhizobia are rod-shaped bacteria that form nitrogen-fixing root nodules on leguminous plants; however, they don’t carry MreB, a key determinant of rod-like cell shape. Here, we introduced an actin-like mreB homolog from a pseudomonad into Mesorhizobium huakuii 7653R (a microsymbiont of Astragalus sinicus L.) and examined the molecular, cellular, and symbiotic phenotypes of the resultant mutant. Exogenous mreB caused an enlarged cell size and slower growth in laboratory medium. However, the mutant formed small, ineffective nodules on A. sinicus (Nod+ Fix−), and rhizobial cells in the infection zone were unable to differentiate into bacteroids. RNA sequencing analysis also revealed minor effects of mreB on global gene expression in free-living cells but larger effects for cells grown in planta. Differentially expressed nodule-specific genes include cell cycle regulators such as the tubulin-like ftsZ1 and ftsZ2. Unlike the ubiquitous FtsZ1, an FtsZ2 homolog was commonly found in Rhizobium, Sinorhizobium, and Mesorhizobium spp. but not in closely related nonsymbiotic species. Bacterial two-hybrid analysis revealed that MreB interacts with FtsZ1 and FtsZ2, which are targeted by the host-derived nodule-specific cysteine-rich peptides. Significantly, MreB mutation D283A disrupted the protein–protein interactions and restored the aforementioned phenotypic defects caused by MreB in M. huakuii. Together, our data indicate that MreB is detrimental for modern rhizobia and its interaction with FtsZ1 and FtsZ2 causes the symbiotic process to cease at the late stage of bacteroid differentiation. These findings led to a hypothesis that loss of mreB in the common ancestor of members of Rhizobiales and subsequent acquisition of ftsZ2 are critical evolutionary steps leading to legume-rhizobial symbiosis. |
| first_indexed | 2024-12-17T01:50:48Z |
| format | Article |
| id | doaj.art-8fbd677baec44c39a5f8ecbef08a601c |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-12-17T01:50:48Z |
| publishDate | 2021-06-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-8fbd677baec44c39a5f8ecbef08a601c2022-12-21T22:08:05ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062021-06-0134554755910.1094/MPMI-10-20-0299-FIInvestigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial SymbiosisWenlong ZhaoHuixia ZhuFeng WeiDonglai ZhouYouguo LiXue-Xian ZhangRhizobia are rod-shaped bacteria that form nitrogen-fixing root nodules on leguminous plants; however, they don’t carry MreB, a key determinant of rod-like cell shape. Here, we introduced an actin-like mreB homolog from a pseudomonad into Mesorhizobium huakuii 7653R (a microsymbiont of Astragalus sinicus L.) and examined the molecular, cellular, and symbiotic phenotypes of the resultant mutant. Exogenous mreB caused an enlarged cell size and slower growth in laboratory medium. However, the mutant formed small, ineffective nodules on A. sinicus (Nod+ Fix−), and rhizobial cells in the infection zone were unable to differentiate into bacteroids. RNA sequencing analysis also revealed minor effects of mreB on global gene expression in free-living cells but larger effects for cells grown in planta. Differentially expressed nodule-specific genes include cell cycle regulators such as the tubulin-like ftsZ1 and ftsZ2. Unlike the ubiquitous FtsZ1, an FtsZ2 homolog was commonly found in Rhizobium, Sinorhizobium, and Mesorhizobium spp. but not in closely related nonsymbiotic species. Bacterial two-hybrid analysis revealed that MreB interacts with FtsZ1 and FtsZ2, which are targeted by the host-derived nodule-specific cysteine-rich peptides. Significantly, MreB mutation D283A disrupted the protein–protein interactions and restored the aforementioned phenotypic defects caused by MreB in M. huakuii. Together, our data indicate that MreB is detrimental for modern rhizobia and its interaction with FtsZ1 and FtsZ2 causes the symbiotic process to cease at the late stage of bacteroid differentiation. These findings led to a hypothesis that loss of mreB in the common ancestor of members of Rhizobiales and subsequent acquisition of ftsZ2 are critical evolutionary steps leading to legume-rhizobial symbiosis.https://doi.org/10.1094/MPMI-10-20-0299-FI |
| spellingShingle | Wenlong Zhao Huixia Zhu Feng Wei Donglai Zhou Youguo Li Xue-Xian Zhang Investigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial Symbiosis Molecular Plant-Microbe Interactions |
| title | Investigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial Symbiosis |
| title_full | Investigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial Symbiosis |
| title_fullStr | Investigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial Symbiosis |
| title_full_unstemmed | Investigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial Symbiosis |
| title_short | Investigating the Involvement of Cytoskeletal Proteins MreB and FtsZ in the Origin of Legume-Rhizobial Symbiosis |
| title_sort | investigating the involvement of cytoskeletal proteins mreb and ftsz in the origin of legume rhizobial symbiosis |
| url | https://doi.org/10.1094/MPMI-10-20-0299-FI |
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