CEP receptor signalling controls root system architecture in Arabidopsis and Medicago

Abstract

Root system architecture (RSA) influences the effectiveness of resources acquisition from soils but the genetic networks that control RSA remain largely unclear.We used rhizoboxes, X-ray computed tomography, grafting, auxin transport measurements and hormone quantification to demonstrate that Arabidopsis and Medicago CEP (C-TERMINALLY ENCODED PEPTIDE)-CEP RECEPTOR signalling controls RSA, the gravitropic set-point angle (GSA) of lateral roots (LRs), auxin levels and auxin transport.We showed that soil-grown Arabidopsis and Medicago CEP receptor mutants have a narrower RSA, which results from a steeper LR GSA. Grafting showed that CEPR1 in the shoot controls GSA. CEP receptor mutants exhibited an increase in rootward auxin transport and elevated shoot auxin levels. Consistently, the application of auxin to wild-type shoots induced a steeper GSA and auxin transport inhibitors counteracted the CEP receptor mutant's steep GSA phenotype. Concordantly, CEP peptides increased GSA and inhibited rootward auxin transport in wild-type but not in CEP receptor mutants.The results indicated that CEP-CEP receptor-dependent signalling outputs in Arabidopsis and Medicago control overall RSA, LR GSA, shoot auxin levels and rootward auxin transport. We propose that manipulating CEP signalling strength or CEP receptor downstream targets may provide means to alter RSA.

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

“…Our data highlights the importance of CEPR1 activity in the reproductive bolt for the delivery of nutrients for yield formation. The apparent perturbation of nitrogen status in cepr1 bolts suggests that CEPR1 plays a broader role in controlling nitrogen homeostasis at the whole-plant level, beyond roles previously identified in root nitrogen acquisition, root system architecture and nodulation (Huault et al, 2014;Tabata et al, 2014;Mohd-Radzman et al, 2016;Ohkubo et al, 2017;Chapman et al, 2020).…”

“…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).…”

A CEP Peptide Receptor-Like Kinase Regulates Auxin Biosynthesis and Ethylene Signaling to Coordinate Root Growth and Symbiotic Nodulation in Medicago truncatula

“…The increased acropetal polar auxin transport might, however, be related to the MtYUC2 upregulation observed in cra2. Recently, acropetal polar auxin transport and shoot auxin levels were shown to modulate RSA systemically from shoots depending on MtCRA2 by regulating the angle of lateral root emergence relative to the gravity vector (Chapman et al, 2020).…”

The CEP5 Peptide Promotes Abiotic Stress Tolerance, As Revealed by Quantitative Proteomics, and Attenuates the AUX/IAA Equilibrium in Arabidopsis

“…In addition, CEP family peptides impact the expression of nitrate transporters in the root, signal via XYLEM INTERMIXED WITH PHLOEM 1 (XIP1)/CEP RECEPTOR 1 (CEPR1) and CEPR2 and induce phloem-specific polypeptides in leaves that act as long-distance mobile signals trans-located to the root [7,8]. Recently, it was suggested that CEP-CEPRdependent signalling controls Arabidopsis and Medicago root system architecture, gravitropic set-point angle of lateral roots, shoot auxin levels and rootward auxin transport [9]. However, based on the diverse expression patterns of CEP family peptides [10] and a recently described role in sucrose-dependent enhancement of lateral root growth [11], these peptides likely play important roles beyond nitrogen acquisition.…”