Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition

Abstract

Plants uptake nitrogen (N) from the soil mainly in the form of nitrate. However, nitrate is often distributed heterogeneously in natural soil. Plants, therefore, have a systemic long-distance signalling mechanism by which N starvation on one side of the root leads to a compensatory N uptake on the other N-rich side. This systemic N acquisition response is triggered by a root-to-shoot mobile peptide hormone, C-TERMINALLY ENCODED PEPTIDE (CEP), originating from the N-starved roots, but the molecular nature of the descending shoot-to-root signal remains elusive. Here, we show that phloem-specific polypeptides that are induced in leaves upon perception of root-derived CEP act as descending long-distance mobile signals translocated to each root. These shoot-derived polypeptides, which we named CEP DOWNSTREAM 1 (CEPD1) and CEPD2, upregulate the expression of the nitrate transporter gene NRT2.1 in roots specifically when nitrate is present in the rhizosphere. Arabidopsis plants deficient in this pathway show impaired systemic N acquisition response accompanied with N-deficiency symptoms. These fundamental mechanistic insights should provide a conceptual framework for understanding systemic nutrient acquisition responses in plants.

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

“…3). Previous studies connecting nutrient acquisition and SSP function in M. truncatula have focused largely on the roles of CLE and CEP genes in N status-dependent root development and nodulation (Mortier et al, 2010;Delay et al, 2013a;Imin et al, 2013;Okamoto et al, 2013;Araya et al, 2014;Huault et al, 2014;Tabata et al, 2014;Mohd-Radzman et al, 2016;Ohkubo et al, 2017). Demonstrating the validity of our data sets, we could confirm these previous reports of CLE and CEP regulation (Supplemental Table S7).…”

“…SSPs encompass many regulatory signaling molecules controlling a multitude of plant growth and development processes, including nodulation and acclimation to nutrient stress (Czyzewicz et al, 2013;Djordjevic et al, 2015;Ohkubo et al, 2017). The identification of such SSPs is of great interest for the improvement of agronomic traits and crop productivity (Bao et al, 2017), particularly in relation to nutrient acquisition.…”

“…A small number of Signaling-SSPs from various species have been shown to impact traits related to plant nutrient homeostasis and acquisition, such as lateral root development and symbiotic interactions Okamoto et al, 2016;de Bang et al, 2017;Ohkubo et al, 2017). However, the full extent of Signaling-SSPs involved in acclimation to fluctuations in nutrient availability has not been explored.…”

TGACG‐BINDING FACTORs (TGAs) and TGA‐interacting CC‐type glutaredoxins modulate hyponastic growth in Arabidopsis thaliana

“…This implies that TGA1/TGA4 should be present in the same cells as ROXY8 and ROXY9. Indeed, Promoter:β‐GLUCORONIDASE ( GUS ) reporter constructs have revealed that both ROXY9 (Ohkubo et al ., ) and TGA1 (Ruiz‐Medrano et al ., ) are expressed in the vascular tissue. Whether expression occurs specifically in the phloem or in the xylem has been determined only for the ROXY9 Prom :GUS construct, this construct has been used to unravel phloem‐specific expression.…”

Regulation of plant peptide hormones and growth factors by post‐translational modification

“…The signals that are sent from the shoot to the root are two phloem‐mobile polypeptides called CEP DOWNSTREAM (CEPD1) and CEPD2 that are responsible for CEPR1‐dependent induction of the nitrate transporter NRT2.1 (Ohkubo et al . ). In legumes, CEPs regulate nodulation and lateral root development (Taleski et al .…”