CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants

Abstract

The manifestation of repetitive developmental programmes during plant growth can be adjusted in response to various environmental cues. During root development, this means being able to precisely control root growth and lateral root development. Small signalling peptides have been found to play roles in many aspects of root development. One member of the CEP (C-TERMINALLY ENCODED PEPTIDE) gene family has been shown to arrest root growth. Here we report that CEP genes are widespread among seed plants but are not present in land plants that lack true branching roots or root vasculature. We have identified 10 additional CEP genes in Arabidopsis. Expression analysis revealed that CEP genes are regulated by environmental cues such as nitrogen limitation, increased salt levels, increased osmotic strength, and increased CO2 levels in both roots and shoots. Analysis of synthetic CEP variants showed that both peptide sequence and modifications of key amino acids affect CEP biological activity. Analysis of several CEP over-expression lines revealed distinct roles for CEP genes in root and shoot development. A cep3 knockout mutant showed increased root and shoot growth under a range of abiotic stress, nutrient, and light conditions. We demonstrate that CEPs are negative regulators of root development, slowing primary root growth and reducing lateral root formation. We propose that CEPs are negative regulators that mediate environmental influences on plant development.

Different Pathways Act Downstream of the CEP Peptide Receptor CRA2 to Regulate Lateral Root and Nodule Development

“…It remains to be determined how the same peptide-receptor module can activate different downstream pathways depending on the root lateral organ considered. Because CEP gene expression is primarily regulated by environmental cues, and notably by N-availability (Delay et al, 2013;Imin et al, 2013), the MtCEP-CRA2 regulatory pathway is likely an important route for plants to control root system architecture in response to environmental influences such as N-availability. The widespread distribution of CEP genes in seed plants and their absence in early plant lineages (Delay et al, 2013;Ogilvie et al, 2014) suggests that CEP-dependent regulatory pathways are likely to operate widely.…”

“…For instance, cepr1 phenotypes in Arabidopsis are somewhat different compared to cra2 phenotypes in M. truncatula (Tabata et al, 2014, Huault et al, 2014. In addition, the phenotypic effects of CEP peptides on lateral root and main root growth are different in Arabidopsis and Medicago (Delay et al, 2013;Imin et al, 2013;Tabata et al, 2014). Therefore, modulating CEP pathways may be a way to generate different root system architectures in various plants depending on their environments.…”

“…Therefore, understanding signaling molecules, receptors, and downstream pathways that regulate both nodule and LR development in legumes under different environmental conditions is essential to improve nutrient acquisition by the root system. C-TERMINALLY ENCODED PEPTIDEs (CEPs) have recently been implicated in controlling major aspects of root development (Ohyama et al, 2008;Delay et al, 2013;Imin et al, 2013;Tabata et al, 2014;Djordjevic et al, 2015;Mohd-Radzman et al, 2015). CEP peptides are signaling molecules that positively regulate nodulation and negatively regulate LR emergence in several legumes Mohd-Radzman et al, 2015).…”

Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

“…M. truncatula CLE genes were initially annotated by Mortier et al (2010) using Mt2.0, and this was expanded recently to a total of 52 CLE genes by Hastwell et al (2017) using Mt4.0 in their identification pipeline. Studies by Imin et al (2013), Delay et al (2013b), and Ogilvie et al (2014) collectively identified 14 M. truncatula CEP (MtCEP) family members. Noteworthy, seven of the 14 MtCEPs identified in Mt3.5 are missing from Mt4.0, and conversely, a single MtCEP is present solely in Mt4.0.…”

The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions

“…In silico analysis showed that CEP-containing genes occur only in seed plants and are absent in mosses and algae (Ohyama et al, 2008;Delay et al, 2013;Imin et al, 2013;Roberts et al, 2013;Li et al, 2014;Ogilvie et al, 2014). Overexpression of CEP1 in Arabidopsis results in the arrest of root growth (Ohyama et al, 2008), and, in Medicago truncatula, overexpression of CEP1 or application of synthetic CEP1 results in inhibition of lateral root formation, enhancement of nodulation, and the induction of periodic circumferential root swellings Mohd-Radzman et al, 2015).…”