The origin and evolution of salicylic acid signaling and biosynthesis in plants

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.

Loss of two families of SPX domain-containing proteins required for vacuolar polyphosphate accumulation coincides with the transition to phosphate storage in green plants

Phosphorus is an essential nutrient for plants.It is stored as inorganic phosphate(Pi)in the vacuoles of land plants but as inorganic polyphosphate(polyP)in chlorophyte algae.Although it is recognized that the SPX-Major Facilitator Superfamily(MFS)and VPE proteins are responsible for Pi influx and efflux,respectively,across the tonoplast in land plants,the mechanisms that underlie polyP homeostasis and the transition of phosphorus storage forms during the evolution of green plants remain unclear.In this study,we showed that CrPTCI,encoding a protein with both SPX and SLC(permease solute carrier 13)domains for Pi transport,and CrVTC4,encoding a protein with both SPX and vacuolar transporter chaperone(VTC)domains for polyP synthesis,are required for vacuolar polyP accumulation in the chlorophyte Chlamydomonas rein-hardtii.Phylogenetic analysis showed that the SPX-SLC,SPX-VTC,and SPX-MFS proteins were present in the common ancestor of green plants(Viridiplantae).The SPX-SLC and SPX-VTC proteins are conserved among species that store phosphorus as vacuolar polyP and absent from genomes of plants that store phosphorus as vacuolar Pi.By contrast,SPX-MFS genes are present in the genomes of streptophytes that store phosphorus as Pi in the vacuoles.These results suggest that loss of SPX-SLC and SPX-VTC genes and functional conservation of SPX-MFS proteins during the evolution of streptophytes accompanied the change from ancestral polyP storage to Pi storage.