Peptide hormones in plants

Abstract

Peptide hormones are defined as small secreted polypeptide-based intercellular communication signal molecules. Such peptide hormones are encoded by nuclear genes, and often go through proteolytic processing of preproproteins and post-translational modifications. Most peptide hormones are secreted out of the cell to interact with membrane-associated receptors in neighboring cells, and subsequently activate signal transductions, leading to changes in gene expression and cellular responses. Since the discovery of the first plant peptide hormone, systemin, in tomato in 1991, putative peptide hormones have continuously been identified in different plant species, showing their importance in both short- and long-range signal transductions. The roles of peptide hormones are implicated in, but not limited to, processes such as self-incompatibility, pollination, fertilization, embryogenesis, endosperm development, stem cell regulation, plant architecture, tissue differentiation, organogenesis, dehiscence, senescence, plant-pathogen and plant-insect interactions, and stress responses. This article, collectively written by researchers in this field, aims to provide a general overview for the discoveries, functions, chemical natures, transcriptional regulations, and post-translational modifications of peptide hormones in plants. We also updated recent discoveries in receptor kinases underlying the peptide hormone sensing and down-stream signal pathways. Future prospective and challenges will also be discussed at the end of the article.

Keywords: Peptide hormones; Post-translational modifications; Proteolytic processing; Receptor-like kinase; Secretions; Signal transductions.

Fig. 1

Categorization of peptide hormone families in plants, based on their structures and biosynthetic pathways. Peptide families in plants can be categorized into four distinct groups based on their functions, structures, and biosynthetic pathways. Peptides that undergo post-translational modification (PTM) and exhibit cysteine-richness (Cys-rich) are secreted via the conventional protein secretion (CPS) pathway. In this pathway, preprotein precursors are initially processed in the endoplasmic reticulum (ER), subsequently transported to the Golgi apparatus, and finally secreted into the apoplast through the endomembrane system. In contrast to the CPS pathway, precursors derived from immunoreactive peptides (such as systemin and Pep) and small open reading frames (sORFs) or microRNAs are secreted via the unconventional protein secretion (UPS) pathway, which includes vacuoles, Exocyst-positive organelles (EXPOs), and multivesicular bodies (MVBs). Major references to classification schemes for these polypeptide families are presented, including ^aCPS and ^aUPS referenced from Wang X., 2018 (2018); ^bPTM and ^bCys-rich from Matsubayashi 2014 (2014); ^cImmunoreaction from Del Corpo D., 2024 (2024); ^dsORF/microRNA from Tavormina P., 2015 (2015); ^eCLE from Ohyama K., 2009 (2009); ^fRALF from Murphy E., 2014 (2014); ^gPEP from Huffaker A., 2006 (2006); ^hENOD40 from Campalans A., 2004 (2004)

Fig. 2

Functional roles and diversity of plant peptides Plant peptides play diverse biological roles across various tissues, contributing to growth, development, and responses to both abiotic and biotic stresses

Fig. 3

The CLE–BAM–CIK signaling pathway regulates protophloem differentiation. Perception of CLE 25/26/45 ligands by the extracellular domain of BAM1/3 receptors located on the plasma membrane triggers the interaction between BAM1/3 and CIKs. The BAM–CIK receptor complex then undergoes phosphorylation. The phosphorylated receptor complex subsequently leads to phosphorylation of PBL34/35/36, mediating downstream signaling events to regulate protophloem differentiation and maintain root meristem homeostasis

Fig. 4

Fine-tuning of plant development through antagonistic peptides. A model of pollen PCP-B peptides repression of stigma RALF23/33 peptide during pollen-stigma interaction. Before pollination, RALF23/33 induces ROS production in the stigmatic papillary cells through a FER/ANJ-controlled signaling pathway. Upon pollination, the competitive binding of pollen PCP-Bs to the stigma ANJ–FER receptor complex displaces stigmatic RALF23/33, repressing ROS production and thus stimulating pollen hydration. B Autocrine peptides RALF4/19 in the pollen tube activate the BUPS1/2–ANX1/2–LLG2/3 receptor complexes, ensuring the maintenance of cell wall integrity and promoting pollen tube growth within the transmitting tract. Upon reaching the micropyle, the ovule-secreted RALF34 competes with RALF4/19 for binding to BUPs/ANXs receptors, leading to pollen tube bursting and successful fertilization. C the competitive binding of STOMAGEN and EPF2 to the ER receptor kinase, along with its coreceptor TMM, finely tunes the initiation of stomatal development. The ER receptor kinase perceives the EPF2 peptide, leading to the inhibition of stomatal formation. Concurrently, STOMAGEN competes with EPF1/2 for the binding sites on the ER–TMM complex, positively regulating stomatal development. D the antagonistic regulation of leaf senescence by SCOOP10 and SCOOP12 peptides occurs via the MIK2 receptor-like kinase. MIK2 functions as a negative regulator of leaf senescence, with SCOOP10 promoting senescence by inhibiting MIK2 phosphorylation during the early stages. Conversely, SCOOP12 competes with SCOOP10 for binding to the MIK2 receptor, activating its phosphorylation during later stages of senescence, thereby suppressing senescence