A Sap Peptide Conserved across Flowering Plants Positively Regulates Lignin Biosynthesis, Biomass and Immunity

Abstract

Signaling peptides act as hormones to deliver short- or long-distance intercellular signals to govern complex developmental processes. Identifying endogenous signaling peptides is challenging due to their low abundance and the unknown cleavage sites required for release from precursor proteins, not to mention the investigation of their evolutionary roles across species. Consequently, very few peptides were evolutionarily characterized in vivo, especially long-distance signaling peptides. Here we present current largest peptidomic datasets from six species (maize, camphor tree, tomato, rose gum, soybean and poplar), totaling 12,242 peptides, selected from all representative evolutionary clades of angiosperms, including monocots, magnoliids, rosid eudicots, and asterid eudicots. A sap peptide was found to be identical across all six species and named as ASAP (angiosperm sap peptide), emerging as the most conserved peptide family discovered thus far. ASAP rapidly induces a series of protein phosphorylation involved in a signaling cascade previously reported to regulate lignin biosynthesis, plant growth and plant immunity. Functional assays on ASAP activity demonstrated its capability on the induction of monolignol biosynthesis and lignin deposition. High-throughput phenomic analyses showed that ASAP significantly increased plant above- and below-ground biomass. In addition, ASAP treatment enhanced plant immunity and reduced the number of galls and egg masses against nematode invasion. This study provides insights into the conservation and functional significance of plant long-distance mobile signaling peptides, offering potential applications in crop improvement and disease management strategies.