Salicylic acid(SA)plays a pivotal role in plant response to biotic and abiotic stress.Several core SA signaling regulators and key proteins in SA biosynthesis have been well characterized.However,much remains unknown ...Salicylic acid(SA)plays a pivotal role in plant response to biotic and abiotic stress.Several core SA signaling regulators and key proteins in SA biosynthesis have been well characterized.However,much remains unknown about the origin,evolution,and early diversification of core elements in plant SA signaling and biosynthesis.In this study,we identified 10 core protein families in SA signaling and biosynthesis across green plant lineages.We found that the key SA signaling receptors,the nonexpresser of pathogenesis-related(NPR)proteins,originated in the most recent common ancestor(MRCA)of land plants and formed divergent groups in the ancestor of seed plants.However,key transcription factors for SA signaling,TGACG motif-binding proteins(TGAs),originated in the MRCA of streptophytes,arguing for the stepwise evolution of core SA signaling in plants.Different from the assembly of the core SA signaling pathway in the ancestor of seed plants,SA exists extensively in green plants,including chlorophytes and streptophyte algae.However,the full isochorismate synthase(ICS)-based SA synthesis pathway was first assembled in the MRCA of land plants.We further revealed that the ancient abnormal inflorescence meristem 1(AIM1)-basedβ-oxidation pathway is crucial for the biosynthesis of SA in chlorophyte algae,and this biosynthesis pathway may have facilitated the adaptation of early-diverging green algae to the high-light-intensity environment on land.Taken together,our findings provide significant insights into the early evolution and diversification of plant SA signaling and biosynthesis pathways,highlighting a crucial role of SA in stress tolerance during plant terrestrialization.展开更多
Mitogen-activated protein kinase （MAPK） pathways regulate signal transduction from different cellular com- partments and from the extracellular environment to the nucleus in all eukaryotes. One of the best-character...Mitogen-activated protein kinase （MAPK） pathways regulate signal transduction from different cellular com- partments and from the extracellular environment to the nucleus in all eukaryotes. One of the best-characterized MAPKs in Arabidopsis thaliana is MPK4, which was shown to be a negative regulator of systemic-acquired resistance. The mpk4 mutant accumulates salicylic acid （SA）, possesses constitutive expression of pathogenesis-related （PR） genes, and has an extremely dwarf phenotype. We show that suppression of SA and phylloquinone synthesis in chloroplasts by knocking down the IC51 gene （by crossing it with the icsl mutant） in the mpk4 mutant background did not revert mpk4-impaired growth. However, it did cause changes in the photosynthetic apparatus and severely impaired the quantum yield of pho- tosystem Ih Transmission microscopy analysis revealed that the chloroplasts＇ structure was strongly altered in the mpk4 and mpk4/icsl double mutant. Analysis of reactive oxygen species （ROS）-scavenging enzymes expression showed that suppression of SA and phylloquinone synthesis in the chloroplasts of the mpk4 mutant caused imbalances in ROS homeo- stasis which were more pronounced in mpk4/icsl than in mpk4. Taken together, the presented results strongly suggest that MPK4 is an ROS/hormonal rheostat hub that negatively, in an SA-dependent manner, regulates immune defenses, but at the same time positively regulates photosynthesis, ROS metabolism, and growth. Therefore, we concluded that MPK4 is a complex regulator of chloroplastic retrograde signaling for photosynthesis, growth, and immune defenses in Arabidopsis.展开更多
基金National Key Research and Development Program of China(2021 YFF1000404)National Natural Science Foun-dation of China(32130096)+1 种基金Central Public-interest Scientific Insti-tution Basal Research Fund(Y2022QC14)K.Y.was supported by the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences.
文摘Salicylic acid(SA)plays a pivotal role in plant response to biotic and abiotic stress.Several core SA signaling regulators and key proteins in SA biosynthesis have been well characterized.However,much remains unknown about the origin,evolution,and early diversification of core elements in plant SA signaling and biosynthesis.In this study,we identified 10 core protein families in SA signaling and biosynthesis across green plant lineages.We found that the key SA signaling receptors,the nonexpresser of pathogenesis-related(NPR)proteins,originated in the most recent common ancestor(MRCA)of land plants and formed divergent groups in the ancestor of seed plants.However,key transcription factors for SA signaling,TGACG motif-binding proteins(TGAs),originated in the MRCA of streptophytes,arguing for the stepwise evolution of core SA signaling in plants.Different from the assembly of the core SA signaling pathway in the ancestor of seed plants,SA exists extensively in green plants,including chlorophytes and streptophyte algae.However,the full isochorismate synthase(ICS)-based SA synthesis pathway was first assembled in the MRCA of land plants.We further revealed that the ancient abnormal inflorescence meristem 1(AIM1)-basedβ-oxidation pathway is crucial for the biosynthesis of SA in chlorophyte algae,and this biosynthesis pathway may have facilitated the adaptation of early-diverging green algae to the high-light-intensity environment on land.Taken together,our findings provide significant insights into the early evolution and diversification of plant SA signaling and biosynthesis pathways,highlighting a crucial role of SA in stress tolerance during plant terrestrialization.
文摘Mitogen-activated protein kinase （MAPK） pathways regulate signal transduction from different cellular com- partments and from the extracellular environment to the nucleus in all eukaryotes. One of the best-characterized MAPKs in Arabidopsis thaliana is MPK4, which was shown to be a negative regulator of systemic-acquired resistance. The mpk4 mutant accumulates salicylic acid （SA）, possesses constitutive expression of pathogenesis-related （PR） genes, and has an extremely dwarf phenotype. We show that suppression of SA and phylloquinone synthesis in chloroplasts by knocking down the IC51 gene （by crossing it with the icsl mutant） in the mpk4 mutant background did not revert mpk4-impaired growth. However, it did cause changes in the photosynthetic apparatus and severely impaired the quantum yield of pho- tosystem Ih Transmission microscopy analysis revealed that the chloroplasts＇ structure was strongly altered in the mpk4 and mpk4/icsl double mutant. Analysis of reactive oxygen species （ROS）-scavenging enzymes expression showed that suppression of SA and phylloquinone synthesis in the chloroplasts of the mpk4 mutant caused imbalances in ROS homeo- stasis which were more pronounced in mpk4/icsl than in mpk4. Taken together, the presented results strongly suggest that MPK4 is an ROS/hormonal rheostat hub that negatively, in an SA-dependent manner, regulates immune defenses, but at the same time positively regulates photosynthesis, ROS metabolism, and growth. Therefore, we concluded that MPK4 is a complex regulator of chloroplastic retrograde signaling for photosynthesis, growth, and immune defenses in Arabidopsis.
