Root-derived small peptides: Key regulators of plant development, stress resilience, and nutrient acquisition

Abstract

Small peptides (SPs), emerging as crucial signaling molecules in plants, regulate diverse processes such as plant development, stress tolerance, and nutrient acquisition. Consisting of fewer than 100 amino acids, SPs are classified into two main groups: precursor-derived SPs and small open reading frame (sORF)-encoded SPs, including miRNA-encoded SPs. SPs are secreted from various plant parts, with root-derived SPs playing particularly significant roles in stress tolerance and nutrient uptake. Even at low concentrations, root-derived SPs are highly effective signaling molecules that influence the distribution and effects of phytohormones, particularly auxin. For instance, under low phosphorus conditions, CLAVATA3/Embryo-Surrounding Region-Related (CLE/CLV), a root-derived SP, enhances root apical meristem differentiation and root architecture to improve phosphate acquisition. By interacting with CLV2 and PEPR2 receptors, it modulates auxin-related pathways, directing root morphology changes to optimize nutrient uptake. During nitrogen (N) starvation, root-derived SPs are transported to the shoot, where they interact with leucine-rich repeat receptor kinases (LRR-RKs) to alleviate nitrogen deficiency. Similarly, C-terminally Encoded Peptides (CEPs) are involved in primary root growth and N-acquisition responses. Despite the identification of many SPs, countless others remain to be discovered, and the functions of those identified so far remain elusive. This review focuses on the functions of root-derived SPs, such as CLE, CEP, RALF, RGF, PSK, PSY, and DVL, and discusses the receptor-mediated signaling pathways involved. Additionally, it explores the roles of SPs in root architecture, plant development, and their metabolic functions in nutrient signaling.