Abstract
Plant genomes encode numerous small secretory peptides (SSPs) whose functions have yet to be explored. Based on structural features that characterize SSP families known to take part in postembryonic development, this comparative genome analysis resulted in the identification of genes coding for oligopeptides potentially involved in cell-to-cell communication. Because genome annotation based on short sequence homology is difficult, the criteria for the de novo identification and aggregation of conserved SSP sequences were first benchmarked across five reference plant species. The resulting gene families were then extended to 32 genome sequences, including major crops. The global phylogenetic pattern common to the functionally characterized SSP families suggests that their apparition and expansion coincide with that of the land plants. The SSP families can be searched online for members, sequences and consensus (http://bioinformatics.psb.ugent.be/webtools/PlantSSP/). Looking for putative regulators of root development, Arabidopsis thaliana SSP genes were further selected through transcriptome meta-analysis based on their expression at specific stages and in specific cell types in the course of the lateral root formation. As an additional indication that formerly uncharacterized SSPs may control development, this study showed that root growth and branching were altered by the application of synthetic peptides matching conserved SSP motifs, sometimes in very specific ways. The strategy used in the study, combining comparative genomics, transcriptome meta-analysis and peptide functional assays in planta, pinpoints factors potentially involved in non-cell-autonomous regulatory mechanisms. A similar approach can be implemented in different species for the study of a wide range of developmental programmes.
Highlights
Plants are complex organisms that consist of distinct cell types organized in tissues
Because the accuracy of gene models is crucial in this context, only species for which reliable genome annotations were available at the time this analysis was conducted were included: Arabidopsis, rice (Oryza sativa), poplar (Populus trichocarpa), grapevine (Vitis vinifera), and maize (Zea mays)
Most of these short preproproteins contain an amino (N)-terminal signal peptide and a conserved carboxyl (C)-terminal end that is cleaved off to yield the mature signal. This latter sequence corresponds to the secreted bioactive portion of the peptide hormones shown in multiple cases to act as a ligand of leucine-rich repeat-receptor-like kinase (LRR-RLK) membrane proteins (Benková and Hejátko, 2009; Butenko et al, 2009; Murphy et al, 2012)
Summary
Plants are complex organisms that consist of distinct cell types organized in tissues. Separate plant organs as well as neighbouring cells exchange a wide range of signals to coordinate development and respond to environmental stimuli. Peptides secreted into the apoplast by plant cells have been identified as extracellular signals involved in various biological processes, including development (Grienenberger and Fletcher, 2015; Murphy et al, 2012). These bioactive molecules are referred to hereafter as small secretory peptides (SSPs). Subclasses of cysteine-poor SSPs undergo additional post-translational modifications, among which proline hydroxylation, hydroxyproline arabinosylation, and tyrosine sulfation have been documented (Matsubayashi, 2014)
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