CEP3 levels affect starvation-related growth responses of the primary root

Abstract

CEPs (C-TERMINALLY ENCODED PEPTIDEs) inhibit Arabidopsis primary root growth by unknown mechanisms. We investigated how CEP3 levels control primary root growth. CEP3 peptide application decreased cell division, S-phase cell number, root meristematic cell number, and meristem zone (MZ) size in a dose- and CEP RECEPTOR1-dependent manner. Grafting showed that CEP3-dependent growth inhibition requires root and shoot CEPR1. CEP3 induced mitotic quiescence in MZ cells significantly faster than that induced by nutrient limitation alone. CEP3 also inhibited the restoration of S-phase to mitotically quiescence cells by nutrient resupply without quantitatively reducing TARGET OF RAPAMYCIN (TOR) kinase activity. In contrast, cep3-1 had an increased meristem size and S-phase cell number under nitrogen (N)-limited conditions, but not under N-sufficient conditions. Furthermore, cep3-1 meristematic cells remained in S-phase longer than wild-type cells during a sustained carbon (C) and N limitation. RNA sequencing showed that CEP3 peptide down-regulated genes involved in S-phase entry, cell wall and ribosome biogenesis, DNA replication, and meristem expansion, and up-regulated genes involved in catabolic processes and proteins and peptides that negatively control meristem expansion and root growth. Many of these genes were reciprocally regulated in cep3-1. The results suggest that raising CEP3 induces starvation-related responses that curtail primary root growth under severe nutrient limitation.

CEP receptor signalling controls root system architecture in Arabidopsis and Medicago

“…Prior publications reported that CEPR1 controls local (root) and systemic (shoot) LR growth in Arabidopsis whereas CRA2 controls LR number locally in Medicago (Huault et al , 2014; Tabata et al , 2014; Mohd‐Radzman et al , 2015; Roberts et al , 2016; Chapman et al , 2019; Delay et al , 2019; Laffont et al , 2019). Therefore, we grafted hypocotyls of Arabidopsis WT and cepr1 mutants and Medicago A17 and cra2‐11 to determine if the CEP receptor controls the GSA from the root and/or the shoot (Fig.…”

“…This is notable as some other CEP–CEP receptor‐mediated processes that control root growth (e.g. main root growth, LR growth and density) were not entirely congruent between Medicago and Arabidopsis (Delay et al , 2013, 2019; Imin et al , 2013; Huault et al , 2014; Tabata et al , 2014; Djordjevic et al , 2015; Mohd‐Radzman et al , 2015, 2016; Roberts et al , 2016; Chapman et al , 2019; Laffont et al , 2019).…”

“…Prior studies have revealed that CEP–CEP receptor signalling pathways play multiple roles in controlling main root and LR growth in Arabidopsis and LR and nodule number in Medicago (Delay et al , 2013, 2019; Imin et al , 2013; Huault et al , 2014; Tabata et al , 2014; Djordjevic et al , 2015; Mohd‐Radzman et al , 2015, 2016; Shabala et al , 2016; Taleski et al , 2016, 2018; Chapman et al , 2019; Laffont et al , 2019) in addition to the roles we describe here in RSA and GSA. There is evidence that some CEP–CEP receptor signalling responses are controlled by distinct mechanisms; for example CEP‐dependent lateral root density is controlled by local root responses in Medicago (Huault et al , 2014; Laffont et al , 2019), by contrast to the shoot‐controlled root responses described here.…”

Molecular Dialog between Root and Shoot via Regulatory Peptides and Its Role in Systemic Control of Plant Development

“…AtCEP3 was shown to be activated in the root upon nitrogen deficiency. Moreover, a mutant defective in the AtCEP3 gene exhibited more developed root system under different stress factors (for example, nitrogen deficiency or salination) as compared with wild-type plants; on a standard medium, it did not show differences comparing with wild-type plants [76]. These data suggest that CEP peptides (and especially AtСЕР3) act as negative regulators of root-system development under stress conditions.…”

SiCEP3, a C-terminally encoded peptides fromSetaria italica, promotes ABA import and signaling pathway

“…The identification of CEP receptors 1 and 2 (CEPR1 and CEPR2) in Arabidopsis suggested that sensing of root-derived CEP peptides by these shoot receptors mediates systemic nitrogen-demand signaling (Tabata et al, 2014). Application of CEP3 peptide decreases cell division, S-phase cell number, root meristematic cell number, and meristem zone (MZ) size in a dose- and CEPR1-dependent manner, especially under severe nutrient limitation (Delay et al, 2019). In Medicago , MtCEP1 is expressed in primary root tips, vascular tissue, and lateral organ primordia, particularly under nitrogen (N) limitations (Imin et al, 2013).…”