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 charactered. However, much remains unknown about the origin, evolution, and early diversification of core elements in plant SA signaling and biosynthesis. Here, we identified ten core protein families in SA signaling and biosynthesis across green plant lineages. We found that key SA signaling receptors, the nonexpresser of pathogenesis-related proteins (NPRs), 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 assembling of core SA signaling in the ancestor of seed plants, SA extensively exists 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 uncovered that the ancient abnormal inflorescence meristem 1 (AIM1)-based β-oxidation is crucial for the biosynthesis of SA in Chlorophyte algae, and this biosynthesis pathway may have facilitated the adaptation of early-diverging green algae for 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, and highlight the role of SA in stress tolerance during plant terrestrialization.
Proposed trajectories of origin and evolution of SA signaling and biosynthesis
The core receptors of SA signaling, NPR proteins, originated in the most recent common ancestor (MRCA) of land plants, while their partners, TGAs, originated in the MRCA of streptophytes. The NPR-TGA interaction occurred when this module was first assembled in the land plants. The differentiation of NPR functions occurred during the divergence of spermatophytes, which helped to build intricate stress response networks. However, SA extensively exists in green plants, including chlorophytes and streptophyte algae, although the ICS-based SA biosynthesis was first present in the MRCA of land plants. The core process of the β-oxidation-dependent SA biosynthesis pathway, AIM1-based β-oxidation, originated in the MRCA of green plants. Furthermore, we showed that the extensive presence of SA in green plant lineages is crucial for plant adaptation to high-irradiance environments after plant terrestrialization. Other possible unidentified elements are marked by question marks with grey backgrounds, and the absence of elements is indicated by blank backgrounds.
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