Nanodomain-localized formin gates symbiotic microbial entry in legume and solanaceous plants.
Saved in:
| Title: | Nanodomain-localized formin gates symbiotic microbial entry in legume and solanaceous plants. |
|---|---|
| Authors: | Qiao, Lijin (AUTHOR), Sun, Heng (AUTHOR), Tang, Jiping (AUTHOR), Hernández-Reyes, Casandra (AUTHOR), Lace, Beatrice (AUTHOR), Knerr, Julian (AUTHOR), Schulze, Eija (AUTHOR), Lee, Tak (AUTHOR), Keller, Jean (AUTHOR), Libourel, Cyril (AUTHOR), Yao, Jilin (AUTHOR), Zhao, Feiyang (AUTHOR), Ni, Ying (AUTHOR), Jia, Yutian (AUTHOR), Xu, Xia (AUTHOR), Yang, Guanghui (AUTHOR), Zhang, Lin (AUTHOR), Zhang, Yanli (AUTHOR), Grosse, Robert (AUTHOR), Tian, Changfu (AUTHOR) |
| Source: | Science. 3/5/2026, Vol. 391 Issue 6789, p1036-1045. 10p. |
| Subjects: | Formins, Medicago truncatula, Root-tubercles, Cytoskeleton, Microbial invasiveness, Mycorrhizal fungi |
| Abstract: | Colonization of plant roots by symbionts requires substantial morphodynamic reorganization. Examples are actin-scaffolded microcompartments called infection pockets formed during root nodule symbiosis (RNS) by legumes. We demonstrate that the actin-binding formin SYFO2 is indispensable for rhizobial infection in Medicago truncatula, where it drives actin polymerization in phase-separated and symbiosis-specific nanodomains. SYFO2 also regulates symbiotically active arbuscules formed during mycorrhizal symbiosis in plants outside the nodulating clade, indicating that it was additionally recruited to promote rhizobial infections in legumes. As part of our aim to enable nitrogen fixation in nonlegumes, we activated endogenous SYFO2 by stably introducing the RNS master regulator NODULE INCEPTION (NIN) into the natural nonhost tomato. This demonstrates the possibility of recruiting arbuscular mycorrhizae–related genes into an engineered nodulation-specific pathway. Editor's summary: Plant-fungal symbioses are widespread, but bacterial rhizobia only form nodulating relationships with legume plants. Qiao et al. found an actin-nucleating protein, SYFO2, which is part of the formin protein family and is involved in both types of symbiotic relationships. SYFO2 is required for entry of symbionts into root hairs in both the legume Medicago and the nonlegume tomato. By interacting with remorin proteins in membrane nanodomains, SYFO2 forms condensates to organize the cytoskeleton in preparation for microbe colonization. The legume symbiosis regulator NIN upregulates SYFO2 in both species despite tomato being unable to form nodulating rhizobial symbioses. This discovery may aid in the engineering of bacterial symbiosis in non-nodulating species. —Madeleine Seale INTRODUCTION: Plants form beneficial partnerships with soil microbes such as nitrogen-fixing bacteria (rhizobia) and nutrient-delivering fungi (mycorrhizae). For rhizobia to infect plant roots and deliver nitrogen, specialized structures called infection threads must form within root cells. This requires precise reorganization of the plant's internal actin cytoskeleton and cell membrane. However, the molecular mechanisms initiating this membrane remodeling for microbial entry remain poorly understood. RATIONALE: Previous studies have suggested that forces generated by the actin cytoskeleton might shape the membrane during microbial infection. We hypothesized that specific actin-regulating proteins are recruited to infection sites to drive this process. We focused on formin proteins, which are known to build actin filaments. We investigated a previously uncharacterized formin gene, SYFO2 (symbiotic formin 2), in the model legume Medicago truncatula, to determine whether it plays a role in symbiotic infection. RESULTS: We discovered that SYFO2 is critically required for rhizobia to enter Medicago root hairs and form infection threads. When rhizobia are present, SYFO2 proteins gather into specific foci (nanodomains) on the host cell membrane. At these sites, SYFO2 physically interacts with a membrane scaffold protein called SYMREM1. Our in vitro data suggest that this interaction drives the formation of concentrated protein droplets (by phase separation) at the membrane. Within these droplets, SYFO2 promotes the assembly of actin filaments from fragmented pieces. This localized actin assembly is essential for initiating the membrane invaginations that allow rhizobial entry. SYFO2 also plays a vital role in the older, more widespread mycorrhizal symbiosis in both Medicago and the nonlegume crop tomato. Although tomato does not form nodules with rhizobia and has lost the key nodulation regulator gene NIN, the promoter region of its SYFO2 gene retains a conserved DNA element that normally responds to NIN in legumes. Reintroducing the legume NIN protein into tomato plants successfully activated the expression of the tomato SYFO2 gene. CONCLUSION: Our work identifies SYFO2 as a key factor controlling the polarity switch from a tip-growing root hair to membrane invagination and infection thread outgrowth, enabling intracellular accommodation of beneficial microbes. SYFO2 functions by phase-separating with SYMREM1 nanodomains to locally concentrate and activate the actin assembly machinery at infection sites. The discovery that the tomato SYFO2 promoter retains a functional NIN-responsive element, despite the evolutionary loss of nodulation capability together with the NIN gene itself millions of years ago, reveals an unexpectedly deep retention of genetic components responsive to rhizobia signals within nonlegume plants. This shared SYFO2-dependent mechanism for accommodating diverse beneficial microbes provides a fundamental framework for understanding intracellular plant-microbe symbioses and offers strategies for engineering beneficial microbial associations in crops, such as by reactivating conserved genetic circuits. A conserved molecular framework for intracellular accommodation of cross-kingdom beneficial microbes.: The formin protein SYFO2 serves as a key molecular bridge linking symbiotic signals to actin-driven membrane invagination, facilitating intracellular accommodation of beneficial microbes. In the model legume M. truncatula, SYFO2 is indispensable not only for rhizobial entry into root hairs (controlled by the master symbiosis regulator NIN, which is absent in most non-nodulating species) but also for colonization by evolutionarily older arbuscular mycorrhizal fungi (AMF) in root cortical cells. SYFO2 is also required for AMF infection in the nonlegume crop tomato (Solanum lycopersicum). Tomato retains a functional SYFO2 transcriptional regulatory module that can be activated by heterologous NIN expression. This demonstrates cross-species regulatory conservation and positions the AMF infection machinery as an evolvable toolkit for nitrogen fixation engineering. [ABSTRACT FROM AUTHOR] |
| Copyright of Science is the property of American Association for the Advancement of Science and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.) | |
| Database: | Psychology and Behavioral Sciences Collection |
|
Full text is not displayed to guests.
Login for full access.
|
|
| Abstract: | Colonization of plant roots by symbionts requires substantial morphodynamic reorganization. Examples are actin-scaffolded microcompartments called infection pockets formed during root nodule symbiosis (RNS) by legumes. We demonstrate that the actin-binding formin SYFO2 is indispensable for rhizobial infection in Medicago truncatula, where it drives actin polymerization in phase-separated and symbiosis-specific nanodomains. SYFO2 also regulates symbiotically active arbuscules formed during mycorrhizal symbiosis in plants outside the nodulating clade, indicating that it was additionally recruited to promote rhizobial infections in legumes. As part of our aim to enable nitrogen fixation in nonlegumes, we activated endogenous SYFO2 by stably introducing the RNS master regulator NODULE INCEPTION (NIN) into the natural nonhost tomato. This demonstrates the possibility of recruiting arbuscular mycorrhizae–related genes into an engineered nodulation-specific pathway. Editor's summary: Plant-fungal symbioses are widespread, but bacterial rhizobia only form nodulating relationships with legume plants. Qiao et al. found an actin-nucleating protein, SYFO2, which is part of the formin protein family and is involved in both types of symbiotic relationships. SYFO2 is required for entry of symbionts into root hairs in both the legume Medicago and the nonlegume tomato. By interacting with remorin proteins in membrane nanodomains, SYFO2 forms condensates to organize the cytoskeleton in preparation for microbe colonization. The legume symbiosis regulator NIN upregulates SYFO2 in both species despite tomato being unable to form nodulating rhizobial symbioses. This discovery may aid in the engineering of bacterial symbiosis in non-nodulating species. —Madeleine Seale INTRODUCTION: Plants form beneficial partnerships with soil microbes such as nitrogen-fixing bacteria (rhizobia) and nutrient-delivering fungi (mycorrhizae). For rhizobia to infect plant roots and deliver nitrogen, specialized structures called infection threads must form within root cells. This requires precise reorganization of the plant's internal actin cytoskeleton and cell membrane. However, the molecular mechanisms initiating this membrane remodeling for microbial entry remain poorly understood. RATIONALE: Previous studies have suggested that forces generated by the actin cytoskeleton might shape the membrane during microbial infection. We hypothesized that specific actin-regulating proteins are recruited to infection sites to drive this process. We focused on formin proteins, which are known to build actin filaments. We investigated a previously uncharacterized formin gene, SYFO2 (symbiotic formin 2), in the model legume Medicago truncatula, to determine whether it plays a role in symbiotic infection. RESULTS: We discovered that SYFO2 is critically required for rhizobia to enter Medicago root hairs and form infection threads. When rhizobia are present, SYFO2 proteins gather into specific foci (nanodomains) on the host cell membrane. At these sites, SYFO2 physically interacts with a membrane scaffold protein called SYMREM1. Our in vitro data suggest that this interaction drives the formation of concentrated protein droplets (by phase separation) at the membrane. Within these droplets, SYFO2 promotes the assembly of actin filaments from fragmented pieces. This localized actin assembly is essential for initiating the membrane invaginations that allow rhizobial entry. SYFO2 also plays a vital role in the older, more widespread mycorrhizal symbiosis in both Medicago and the nonlegume crop tomato. Although tomato does not form nodules with rhizobia and has lost the key nodulation regulator gene NIN, the promoter region of its SYFO2 gene retains a conserved DNA element that normally responds to NIN in legumes. Reintroducing the legume NIN protein into tomato plants successfully activated the expression of the tomato SYFO2 gene. CONCLUSION: Our work identifies SYFO2 as a key factor controlling the polarity switch from a tip-growing root hair to membrane invagination and infection thread outgrowth, enabling intracellular accommodation of beneficial microbes. SYFO2 functions by phase-separating with SYMREM1 nanodomains to locally concentrate and activate the actin assembly machinery at infection sites. The discovery that the tomato SYFO2 promoter retains a functional NIN-responsive element, despite the evolutionary loss of nodulation capability together with the NIN gene itself millions of years ago, reveals an unexpectedly deep retention of genetic components responsive to rhizobia signals within nonlegume plants. This shared SYFO2-dependent mechanism for accommodating diverse beneficial microbes provides a fundamental framework for understanding intracellular plant-microbe symbioses and offers strategies for engineering beneficial microbial associations in crops, such as by reactivating conserved genetic circuits. A conserved molecular framework for intracellular accommodation of cross-kingdom beneficial microbes.: The formin protein SYFO2 serves as a key molecular bridge linking symbiotic signals to actin-driven membrane invagination, facilitating intracellular accommodation of beneficial microbes. In the model legume M. truncatula, SYFO2 is indispensable not only for rhizobial entry into root hairs (controlled by the master symbiosis regulator NIN, which is absent in most non-nodulating species) but also for colonization by evolutionarily older arbuscular mycorrhizal fungi (AMF) in root cortical cells. SYFO2 is also required for AMF infection in the nonlegume crop tomato (Solanum lycopersicum). Tomato retains a functional SYFO2 transcriptional regulatory module that can be activated by heterologous NIN expression. This demonstrates cross-species regulatory conservation and positions the AMF infection machinery as an evolvable toolkit for nitrogen fixation engineering. [ABSTRACT FROM AUTHOR] |
|---|---|
| ISSN: | 00368075 |
| DOI: | 10.1126/science.adx8542 |
