Root-knot nematodes(RKNs)cause huge agricultural losses every year.They secrete a repertoire of effectors to facilitate parasitism through the induction of plant-derived giant feeding cells,which serve as their sole s...Root-knot nematodes(RKNs)cause huge agricultural losses every year.They secrete a repertoire of effectors to facilitate parasitism through the induction of plant-derived giant feeding cells,which serve as their sole source of nutrients.However,the mode of action of these effectors and their targeted host pro-teins remain largely unknown.In this study,we investigated the role of the effector Mi2G02 in Meloidogyne incognita parasitism.Host-derived Mi2G02 RNA interference in Arabidopsis thaliana affected giant cell development,whereas ectopic expression of Mi2G02 promoted root growth and increased plant sus-ceptibility to M.incognita.We used various combinations of approaches to study the specific interactions between Mi2G02 and A.thaliana GT-3a,a trihelix transcription factor.GT-3a knockout in A.thaliana affected feeding-site development,resulting in production of fewer egg masses,whereas GT-3a overex-pression in A.thaliana increased susceptibility to M.incognita and also root growth.Moreover,we demon-strated that Mi2G02 plays a role in maintaining GT-3a protein stabilization by inhibiting the 26S proteasome-dependent pathway,leading to suppression of TOZ and RAD23C expression and thus promoting nematode parasitism.This work enhances our understanding of how a pathogen effector manipulates the role and regulation of a transcription factor by interfering with a proteolysis pathway to reprogram gene expression for development of nematode feeding cells.展开更多
Root-knot nematodes(RKNs;genus Meloidogyne)are a class of plant parasites that infect the roots of many plant species.It is believed that RKNs target certain signaling molecules derived from plants to locate their hos...Root-knot nematodes(RKNs;genus Meloidogyne)are a class of plant parasites that infect the roots of many plant species.It is believed that RKNs target certain signaling molecules derived from plants to locate their hosts;however,currently,no plant compound has been unambiguously identified as a universal RKN attractant.To address this question,we screened a chemical library of synthetic compounds for Meloidogyne incognita attractants.The breakdown product of aminopropylam ino-anthraquinone,1,3-diam inopropane,as well as its related compounds,putrescine and cadaverine,were found to attract M.incognita.After exam ining various polyamines,M.incognita were found to be attracted specifically by natural com pounds that possess three to five methylene groups between two terminal amino groups.Using cryo-TO F-SIM S/SEM,cadaverine was indeed detected in soybean root cortex cells and the surrounding rhizosphere,establishing a chemical gradient.In addition to cadaverine,putrescine and 1,3-diam inopropane were also detected in root exudate by HPLC-MS/MS.Furtherm ore,exogenously applied cadaverine is sufficient to enhance M.incognita infection of Arabidopsis seedlings.These results suggest that M.incognita is likely attracted by polyam ines to locate the appropriate host plants,and the naturally occurring polyamines have potential applications in agriculture in developing protection strategies for crops from RKN infection.展开更多
Seed exudates influence the behavior of soil organisms,but howthis occurs remains unclear,particularly for multicellular animals.Here we show that compounds associated with Arabidopsis seed-coat mucilage regulate the ...Seed exudates influence the behavior of soil organisms,but howthis occurs remains unclear,particularly for multicellular animals.Here we show that compounds associated with Arabidopsis seed-coat mucilage regulate the behavior of soil-borne animals,specifically root-knot nematodes (RKNs).Infective RKN J2 larvae actively travel toward Arabidopsis seeds through chemotaxis.Analysis of Arabidopsis mucilage mutants demonstrated that the attraction of RKNs toArabidopsis seeds requires the synthesis and extrusion of.seed-coat mucilage.Extracted mucilage alone is not sufficient to attract RKNs,but seed-surface carbohydrates and proteins are required for this process.These findings suggest that the RKN chemoattractant is synthesized de novo upon mucilage extrusion but may be highly unstable.RKNs attracted by thismucilage-dependent mechanism can infect the emerging seedling.However,the attraction signal from seedling roots likely acts independently of the seed-coat signal and may mask the attraction to seed-coat mucilage after germination.Multiple RKN species are attracted byArabidopsis seeds,suggesting that this mechanism is conserved in RKNs.These findings indicate that seed exudate can regulate the behavior of multicellular animals and highlight the potential roles of seed-coat mucilage in biotic interactions with soil microorganisms.展开更多
基金supported by the Youth Innovation Program of the Chinese Academy of Agricultural Sciences (grant no.Y2022QC06)the National Natural Science Foundation of China (grant nos.32001878,32172366)+2 种基金the Natural Science Foundation of Beijing (grant no.6222054)the China Agricultural Research System (CARS-23)the French Government (National Research Agency,ANR)through"Investments for the Future"LabEx SIGNALIFE (#ANR-11-LABX-0028-01),IDEX UCAJedi (#ANR-15-IDEX-0).
文摘Root-knot nematodes(RKNs)cause huge agricultural losses every year.They secrete a repertoire of effectors to facilitate parasitism through the induction of plant-derived giant feeding cells,which serve as their sole source of nutrients.However,the mode of action of these effectors and their targeted host pro-teins remain largely unknown.In this study,we investigated the role of the effector Mi2G02 in Meloidogyne incognita parasitism.Host-derived Mi2G02 RNA interference in Arabidopsis thaliana affected giant cell development,whereas ectopic expression of Mi2G02 promoted root growth and increased plant sus-ceptibility to M.incognita.We used various combinations of approaches to study the specific interactions between Mi2G02 and A.thaliana GT-3a,a trihelix transcription factor.GT-3a knockout in A.thaliana affected feeding-site development,resulting in production of fewer egg masses,whereas GT-3a overex-pression in A.thaliana increased susceptibility to M.incognita and also root growth.Moreover,we demon-strated that Mi2G02 plays a role in maintaining GT-3a protein stabilization by inhibiting the 26S proteasome-dependent pathway,leading to suppression of TOZ and RAD23C expression and thus promoting nematode parasitism.This work enhances our understanding of how a pathogen effector manipulates the role and regulation of a transcription factor by interfering with a proteolysis pathway to reprogram gene expression for development of nematode feeding cells.
基金This work was supported by JSPS KAKENHI grants(25252032 and 15H01230 to K.F.,16H04168 to K.T.,24114009,24370024,16K14757,17H03967,and 18H05487 to S.S.)L.P.-B.and B.F.are supported by INRA and the French Government(National Research Agency,ANR)through the"Investments for the Future"LABEX SIGNALIFE program,reference no.ANR-11-LABX-0028-01.
文摘Root-knot nematodes(RKNs;genus Meloidogyne)are a class of plant parasites that infect the roots of many plant species.It is believed that RKNs target certain signaling molecules derived from plants to locate their hosts;however,currently,no plant compound has been unambiguously identified as a universal RKN attractant.To address this question,we screened a chemical library of synthetic compounds for Meloidogyne incognita attractants.The breakdown product of aminopropylam ino-anthraquinone,1,3-diam inopropane,as well as its related compounds,putrescine and cadaverine,were found to attract M.incognita.After exam ining various polyamines,M.incognita were found to be attracted specifically by natural com pounds that possess three to five methylene groups between two terminal amino groups.Using cryo-TO F-SIM S/SEM,cadaverine was indeed detected in soybean root cortex cells and the surrounding rhizosphere,establishing a chemical gradient.In addition to cadaverine,putrescine and 1,3-diam inopropane were also detected in root exudate by HPLC-MS/MS.Furtherm ore,exogenously applied cadaverine is sufficient to enhance M.incognita infection of Arabidopsis seedlings.These results suggest that M.incognita is likely attracted by polyam ines to locate the appropriate host plants,and the naturally occurring polyamines have potential applications in agriculture in developing protection strategies for crops from RKN infection.
文摘Seed exudates influence the behavior of soil organisms,but howthis occurs remains unclear,particularly for multicellular animals.Here we show that compounds associated with Arabidopsis seed-coat mucilage regulate the behavior of soil-borne animals,specifically root-knot nematodes (RKNs).Infective RKN J2 larvae actively travel toward Arabidopsis seeds through chemotaxis.Analysis of Arabidopsis mucilage mutants demonstrated that the attraction of RKNs toArabidopsis seeds requires the synthesis and extrusion of.seed-coat mucilage.Extracted mucilage alone is not sufficient to attract RKNs,but seed-surface carbohydrates and proteins are required for this process.These findings suggest that the RKN chemoattractant is synthesized de novo upon mucilage extrusion but may be highly unstable.RKNs attracted by thismucilage-dependent mechanism can infect the emerging seedling.However,the attraction signal from seedling roots likely acts independently of the seed-coat signal and may mask the attraction to seed-coat mucilage after germination.Multiple RKN species are attracted byArabidopsis seeds,suggesting that this mechanism is conserved in RKNs.These findings indicate that seed exudate can regulate the behavior of multicellular animals and highlight the potential roles of seed-coat mucilage in biotic interactions with soil microorganisms.
