The peptide SCOOP12 acts on reactive oxygen species homeostasis to modulate cell division and elongation in Arabidopsis primary root

Abstract

Small secreted peptides have been described as key contributors to complex signalling networks that control plant development and stress responses. The Brassicaceae-specific PROSCOOP family encodes precursors of Serine riCh endOgenOus Peptides named SCOOPs. In Arabidopsis thaliana, SCOOP12 has been shown to promote defence response against pathogens and to be involved in root development. Here, we explore its role as a moderator of the primary root development. We show that the PROSCOOP12 null mutation leads to longer primary roots through the development of longer differentiated cells while PROSCOOP12 overexpression induces dramatic plant growth impairments. In comparison, the exogenous application of the synthetic SCOOP12 peptide shortens root through meristem size and cell length reductions. Moreover, superoxide anion (O2.-) and hydrogen peroxide (H2O2) productions in root tips vary according to SCOOP12 abundance. Then, by using ROS scavengers that suppress the proscoop12 phenotype, SCOOP12-root growth regulation could be associated with ROS metabolism. Furthermore, our results suggest that peroxidases act as potential SCOOP12 downstream targets to regulate H2O2 production, which in turn triggers cell wall modifications in root. Finally, a massive transcriptional reprogramming, including the induction of genes from numerous other pathways for ethylene, salicylic acid and glucosinolates biosynthesis, was observed, emphasizing its dual role in defense and development.

The PROSCOOP10 Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis

“…Based on their identified native sequences, we tested the effects of the SCOOP10 synthetic peptides on seedling growth and ROS production in Col-0 and mik2-1 genotypes in comparison to the effects of the SCOOP12 and flg22 peptides as positive controls (Figure 4). The SCOOP12 amino acid sequence was the same as that already used by Gully et al [4] and Guillou et al [9] and based on the prediction without post-translational modifications.…”

“…This raises the question of the involvement of the SCOOP peptides in different biological functions; notably, in plant development. Indeed, PROSCOOP12 (AT5G44585) is constitutively expressed in roots and recent studies have shown that SCOOP12 moderates root elongation through the control of reactive oxygen species (ROS) homeostasis [9]. This study focuses on PROSCOOP10 (AT5G44580), which is highly expressed in aerial parts [10,11].…”

The PROSCOOP10 gene encodes two extracellular hydroxylated peptides and impacts flowering time in Arabidopsis

“…4). The SCOOP12 amino acid sequence was the same already used by Gully et al (2019) and Guillou et al (2022) and based on prediction without post-translational modifications.…”

“…This raises the question of the involvement of the SCOOP peptides in different biological functions, notably in plant development. Indeed, PROSCOOP12 ( AT5G44585 ) is constitutively expressed in roots and recent studies have shown that SCOOP12 is a moderator of root elongation through the control of reactive oxygen species (ROS) homeostasis (Guillou et al ., 2022). This study focuses on PROSCOOP10 ( AT5G44580 ) which is highly expressed in the aerial parts.…”

Halophyte Nitraria billardieri CIPK25 mitigates salinity-induced cell damage by alleviating H2O2 accumulation

“…ROS are important signaling molecules that have been revealed to affect plant response to environmental stresses, regulating programmed cell death (PCD) and hormone signaling ( Xie et al, 2014 ; You et al, 2014 ; Leng et al, 2017 ; Tognetti et al, 2017 ; Zhang et al, 2022 ). ROS signaling disruption causes defects during plant development ( Guillou et al, 2022 ; Zhang et al, 2022 ), activating detoxification pathways for remediation of salinity-induced damage ( Zhu, 2002 ). Therefore, for adaptive responses, plants have evolved specific mechanisms to regulate the production and scavenging of ROS through enzymatic and non-enzymatic antioxidative processes ( Nadarajah, 2020 ; Dias et al, 2022 ; Šoln and Koce, 2022 ).…”