Inorganic phosphate(Pi)homeostasis in plants is regulated by inositol pyrophosphates(PP-InsPs),which mediate phosphate starvation responses.While beneficial microorganisms,such as arbuscular mycorrhizal fungi,contribu...Inorganic phosphate(Pi)homeostasis in plants is regulated by inositol pyrophosphates(PP-InsPs),which mediate phosphate starvation responses.While beneficial microorganisms,such as arbuscular mycorrhizal fungi,contribute to phosphate uptake,pathogenic fungi often exploit phosphate metabolism to enhance virulence.However,the exact mechanisms by which pathogens manipulate plant phosphate signaling remain largely unknown.Here,we highlight a recent study by Ulrich Schaffrath and colleagues(Science,2025)revealing that plant pathogenic fungi deploy conserved Nudix hydrolase effectors to hydrolyze PP-InsPs,thereby mimicking phosphate starvation and suppressing host immunity.These findings not only expand our understanding of plantpathogen interactions,but also open new avenues for crop protection and resistance breeding.展开更多
Inositol pyrophosphates(PP-InsPs)are important signaling molecules that regulate diverse cellular processes in eukaryotes,including energy homeostasis,phosphate(Pi)signaling,and phytohormone perception.Yet,in plants,t...Inositol pyrophosphates(PP-InsPs)are important signaling molecules that regulate diverse cellular processes in eukaryotes,including energy homeostasis,phosphate(Pi)signaling,and phytohormone perception.Yet,in plants,the enzymes responsible for their turnover remain largely unknown.Using a non-hydrolysable PP-InsP analog in a pull-down approach,we identified a family of Arabidopsis NUDIX-type hydrolases(NUDTs)that group into two closely related subclades.Through in vitro assays,heterologous expression systems,and higher order gene-edited mutants,we explored the substrate specificities and physiological roles of these hydrolases.Using a combination of strong anion exchange high-performance liquid chromatography(SAX-HPLC),polyacrylamide gel electrophoresis(PAGE),and capillary electrophoresis electrospray ionization mass spectrometry(CE-ESI-MS),we found that their PP-InsP pyrophosphatase activity is enantiomer selective and Mg^(2+)dependent.Specifically,SubcladeⅠNUDTs preferentially hydrolyze 4-InsP_(7),while SubcladeⅡNUDTs target 3-InsP_(7),with minor activity against other PP-InsPs,including5-InsP_(7).In higher order mutants of SubcladeⅡNUDTs,we observed defects in both Piand iron homeostasis,accompanied by increased levels of 1/3-InsP_(7)and 5-InsP_(7),with a markedly larger increase in 1/3-InsP_(7).Ectopic expression of NUDTs from both subclades induced local Pi starvation responses(PSRs),while RNA-seq analysis comparing wild-type(WT)and SubcladeⅡnudt12/13/16 loss-of-function plants indicates additional PSR-independent roles,potentially involving 1/3-InsP_(7) in the regulation of plant defense.Consistently,nudt12/13/16 mutants displayed enhanced resistance to Pseudomonas syringae infection,indicating a role in bacterial pathogen susceptibility.Expanding beyond SubcladeⅡNUDTs,we demonstrated susceptibility of the 3PP-position of PP-InsPs to enzymatic activities unrelated to NUDTs,and found that such activities are conserved across plants and humans.Additionally,we observed that NUDT effectors from pathogenic ascomycete fungi exhibit a substrate specificity similar to SubcladeⅠNUDTs.Collectively,our findings reveal new roles for NUDTs in PP-InsP signaling,plant nutrient and immune responses,and highlight a cross-kingdom conservation of PP-InsP-metabolizing enzymes.展开更多
基金the financial support from China Youth Science Foundation(22207037).
文摘Inorganic phosphate(Pi)homeostasis in plants is regulated by inositol pyrophosphates(PP-InsPs),which mediate phosphate starvation responses.While beneficial microorganisms,such as arbuscular mycorrhizal fungi,contribute to phosphate uptake,pathogenic fungi often exploit phosphate metabolism to enhance virulence.However,the exact mechanisms by which pathogens manipulate plant phosphate signaling remain largely unknown.Here,we highlight a recent study by Ulrich Schaffrath and colleagues(Science,2025)revealing that plant pathogenic fungi deploy conserved Nudix hydrolase effectors to hydrolyze PP-InsPs,thereby mimicking phosphate starvation and suppressing host immunity.These findings not only expand our understanding of plantpathogen interactions,but also open new avenues for crop protection and resistance breeding.
基金funded by grants from the Deutsche Forschungsgemeinschaft(SCHA 1274/4-1,SCHA 1274/5-1,and under Germany's Excellence Strategy,EXC2070–390732324,Pheno Rob to G.S.,JE 572/4-1 and under Germany's Excellence Strategy,CIBSS–EXC-2189–Project ID 390939984 to H.J.J.,LA 1338/18-1 to T.L.,and TRR356/I(491090170),TP-B08 and Project No.451218338 to M.K.R.-L.)by the Marie Sklodowska-Curie Action(Grant Agreement ID 101108767)to S.W.by the Department of Biotechnology,Government of India(Grant No.BT/PR45561/AGIII/103/1386/2023)to S.B.Open Access funding enabled and organized by Projekt DEAL
文摘Inositol pyrophosphates(PP-InsPs)are important signaling molecules that regulate diverse cellular processes in eukaryotes,including energy homeostasis,phosphate(Pi)signaling,and phytohormone perception.Yet,in plants,the enzymes responsible for their turnover remain largely unknown.Using a non-hydrolysable PP-InsP analog in a pull-down approach,we identified a family of Arabidopsis NUDIX-type hydrolases(NUDTs)that group into two closely related subclades.Through in vitro assays,heterologous expression systems,and higher order gene-edited mutants,we explored the substrate specificities and physiological roles of these hydrolases.Using a combination of strong anion exchange high-performance liquid chromatography(SAX-HPLC),polyacrylamide gel electrophoresis(PAGE),and capillary electrophoresis electrospray ionization mass spectrometry(CE-ESI-MS),we found that their PP-InsP pyrophosphatase activity is enantiomer selective and Mg^(2+)dependent.Specifically,SubcladeⅠNUDTs preferentially hydrolyze 4-InsP_(7),while SubcladeⅡNUDTs target 3-InsP_(7),with minor activity against other PP-InsPs,including5-InsP_(7).In higher order mutants of SubcladeⅡNUDTs,we observed defects in both Piand iron homeostasis,accompanied by increased levels of 1/3-InsP_(7)and 5-InsP_(7),with a markedly larger increase in 1/3-InsP_(7).Ectopic expression of NUDTs from both subclades induced local Pi starvation responses(PSRs),while RNA-seq analysis comparing wild-type(WT)and SubcladeⅡnudt12/13/16 loss-of-function plants indicates additional PSR-independent roles,potentially involving 1/3-InsP_(7) in the regulation of plant defense.Consistently,nudt12/13/16 mutants displayed enhanced resistance to Pseudomonas syringae infection,indicating a role in bacterial pathogen susceptibility.Expanding beyond SubcladeⅡNUDTs,we demonstrated susceptibility of the 3PP-position of PP-InsPs to enzymatic activities unrelated to NUDTs,and found that such activities are conserved across plants and humans.Additionally,we observed that NUDT effectors from pathogenic ascomycete fungi exhibit a substrate specificity similar to SubcladeⅠNUDTs.Collectively,our findings reveal new roles for NUDTs in PP-InsP signaling,plant nutrient and immune responses,and highlight a cross-kingdom conservation of PP-InsP-metabolizing enzymes.
