The 5-formyl-tetrahydrofolate proteome links folates with C/N metabolism and reveals feedback regulation of folate biosynthesis

Folates are indispensable for plant development, but their molecular mode of action remains elusive. We synthesized a probe, “5-F-THF-Dayne,” comprising 5-formyl-tetrahydrofolate (THF) coupled to a photoaffinity tag. Exploiting this probe in an affinity proteomics study in Arabidopsis thaliana, we r...

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Detalles Bibliográficos
Autores: Li, Weichao, Liang, Qiuju, Mishra, Ratnesh, Sánchez Muñoz, Raúl|||0000-0003-0235-2985, Wang, Huan, Chen, Xin, Van Der Straeten, Dominique, Zhang, Chunyi, Xiao, Youli
Tipo de recurso: artículo
Fecha de publicación:2021
País:España
Institución:Universitat Politècnica de Catalunya (UPC)
Repositorio:UPCommons. Portal del coneixement obert de la UPC
Idioma:inglés
OAI Identifier:oai:upcommons.upc.edu:2117/446414
Acceso en línea:https://hdl.handle.net/2117/446414
https://dx.doi.org/10.1093/plcell/koab198
Access Level:acceso abierto
Palabra clave:Folates
Folate biosynthesis
Àrees temàtiques de la UPC::Enginyeria agroalimentària::Agricultura::Biotecnologia i millora genètica vegetal
Descripción
Sumario:Folates are indispensable for plant development, but their molecular mode of action remains elusive. We synthesized a probe, “5-F-THF-Dayne,” comprising 5-formyl-tetrahydrofolate (THF) coupled to a photoaffinity tag. Exploiting this probe in an affinity proteomics study in Arabidopsis thaliana, we retrieved 51 hits. Thirty interactions were independently validated with in vitro expressed proteins to bind 5-F-THF with high or low affinity. Interestingly, the interactors reveal associations beyond one-carbon metabolism, covering also connections to nitrogen (N) metabolism, carbohydrate metabolism/photosynthesis, and proteostasis. Two of the interactions, one with the folate biosynthetic enzyme DIHYDROFOLATE REDUCTASE-THYMIDYLATE SYNTHASE 1 (AtDHFR-TS1) and another with N metabolism-associated glutamine synthetase 1;4 (AtGLN1;4), were further characterized. In silico and experimental analyses revealed G35/K36 and E330 as key residues for the binding of 5-F-THF in AtDHFR-TS1 and AtGLN1;4, respectively. Site-directed mutagenesis of AtGLN1;4 E330, which co-localizes with the ATP-binding pocket, abolished 5-F-THF binding as well as AtGLN1;4 activity. Furthermore, 5-F-THF was noted to competitively inhibit the activities of AtDHFR-TS1 and AtGLN1;4. In summary, we demonstrated a regulatory role for 5-F-THF in N metabolism, revealed 5-F-THF-mediated feedback regulation of folate biosynthesis, and identified a total of 14 previously unknown high-affinity binding cellular targets of 5-F-THF. Together, this sets a landmark toward understanding the role of folates in plant development.