CEP–CEPR1 signalling inhibits the sucrose-dependent enhancement of lateral root growth

Abstract

Lateral root (LR) proliferation is a major determinant of soil nutrient uptake. How resource allocation controls the extent of LR growth remains unresolved. We used genetic, physiological, transcriptomic, and grafting approaches to define a role for C-TERMINALLY ENCODED PEPTIDE RECEPTOR 1 (CEPR1) in controlling sucrose-dependent LR growth. CEPR1 inhibited LR growth in response to applied sucrose, other metabolizable sugars, and elevated light intensity. Pathways through CEPR1 restricted LR growth by reducing LR meristem size and the length of mature LR cells. RNA-sequencing of wild-type (WT) and cepr1-1 roots with or without sucrose treatment revealed an intersection of CEP–CEPR1 signalling with the sucrose transcriptional response. Sucrose up-regulated several CEP genes, supporting a specific role for CEP–CEPR1 in the response to sucrose. Moreover, genes with basally perturbed expression in cepr1-1 overlap with WT sucrose-responsive genes significantly. We found that exogenous CEP inhibited LR growth via CEPR1 by reducing LR meristem size and mature cell length. This result is consistent with CEP–CEPR1 acting to curtail the extent of sucrose-dependent LR growth. Reciprocal grafting indicates that LR growth inhibition requires CEPR1 in both the roots and shoots. Our results reveal a new role for CEP–CEPR1 signalling in controlling LR growth in response to sucrose.

The Peptide Hormone Receptor CEPR1 Functions in the Reproductive Tissue to Control Seed Size and Yield

“…CEPD1) of CEPR1 displayed altered expression in cepr1 bolts, consistent with a locally perturbed CEPR1-signalling status involving both feedforward and feedback loops. Similar transcriptional perturbations occur to CEP-CEPR1 pathway genes locally in cepr1 root tissues (Chapman et al, 2019). These transcriptional responses, together with CEPR1 expression in the vasculature of reproductive tissues and the dependence of seed size and yield on local CEPR1 activity, demonstrates that CEPR1 specifically acts in bolt tissues to control aspects of nitrogen mobilisation and delivery to reproductive sinks.…”

“…We explored whether CEPR1 plays a role in vegetative and reproductive development by examining two independent knockout mutant alleles in the No-0 and Col-0 backgrounds (cepr1-1 and cepr1-3, respectively) (Tabata et al, 2014;Chapman et al, 2019). Both cepr1 knockout mutants displayed a ~30% retardation in rosette growth (Fig.…”

“…The previously described Arabidopsis (Arabidopsis thaliana) No-0 cepr1-1 (RATM11-2459; RIKEN) (Bryan et al, 2012;Tabata et al, 2014) and Col-0 cepr1-3 (467C01; GABI-Kat) (Kleinboelting et al, 2012;Chapman et al, 2019) mutant lines were used. Sterilised seedlings were grown on solidified media (1% w/v Type M agar) containing ½ strength Murashige-Skoog (MS) basal salts (Sigma) at pH 5.7 for 7-10 days until seedlings were transferred to soil (seed raising mix; Debco, Bella Vista NSW) supplemented with Osmocote Exact fertiliser and grown in chambers at 22 °C.…”

“…The interaction of the root-derived CEPs with CEPR1 in the shoot vasculature triggers the upregulation of phloem-mobile shootto-root signals, namely the glutaredoxins CEP DOWNSTREAM 1 (CEPD1) and CEPD2, that upregulate the level of nitrate transporter expression in roots selectively exposed to high nitrate (Ohkubo et al, 2017). Recently, we demonstrated that local and systemic CEP-CEPR1 signalling curtails the expenditure of resources to control lateral root growth in response to elevated shoot-derived carbon (Chapman et al, 2019), and that systemic CEP-CEPR1 signalling controls aspects of root system architecture in soil (Chapman et al, 2020). CEP-CEPR1 signalling also controls main root growth in Arabidopsis (Delay et al, 2013b;Delay et al, 2019).…”

“…Since the identification of CEPR1 as a CEP receptor (Tabata et al, 2014), its developmental and physiological role has been defined primarily in the context of roots. For example, CEP-CEPR1/CRA2 signalling controls the extent of root growth and development, root nodule number in legumes, and nitrate uptake in roots (Tabata et al, 2014;Mohd-Radzman et al, 2016;Roberts et al, 2016;Taleski et al, 2016;Taleski et al, 2018;Chapman et al, 2019;Delay et al, 2019;Chapman et al, 2020). Grafting and split root studies show that CEPR1 influences nitrate uptake in Arabidopsis via a systemic mechanism, and that the rate of nitrate uptake is reduced in cepr1-1 (Tabata et al, 2014).…”