New insights into tomato CLE peptide repertoire and perception mechanisms

Abstract

Precision in sensing the environmental cues and adjusting the growth and the physiology of the root system is necessary for plant robustness. Plants achieve their phenotypic plasticity by tightly controlling and buffering developmental decisions. In addition to the classical plant hormones, the CLE peptides are exceptionally important in mediating development, and responses to environmental stresses. While the CLV3-CLV1 module appears to be highly conserved to control the proliferation of the shoot apical meristem stem cells, we do not know whether the function of root-specific CLEs that are implicated in vascular development, in mediating drought stress, sugar starvation, phosphate and nitrate deficit in Arabidopsis is also conserved in other plant species. Here we present a careful re-analysis of the CLE signaling components in the tomato genome and show that the mechanism of root-active CLE peptides is deeply conserved in Arabidopsis and tomato. Due to the small gene size and high sequence variability, it is extremely difficult to precisely annotate SlCLE genes in plant genomes. Our analysis of the SlCLE family, based on a combination of iterative tBLASTn and Hidden-Markov-Model (HMM), revealed thirty-seven new SlCLEs in addition to the fifteen reported previously. Analyzing publicly available RNAseq datasets, we found that the majority of SlCLE genes are preferentially expressed in root tissues. We could confirm the biological activities of selected SlCLE peptides which had a conserved potency like their Arabidopsis orthologs to suppress primary root growth. We show, that root responses are mediated by SlCLAVATA2, indicating the conservation of CLE perception mechanism.