Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis

Abstract

Plants modulate the efficiency of root nitrogen (N) acquisition in response to shoot N demand. However, molecular components directly involved in this shoot-to-root communication remain to be identified. Here, we show that phloem-mobile CEPD-like 2 (CEPDL2) polypeptide is upregulated in the leaf vasculature in response to decreased shoot N status and, after translocation to the roots, promotes high-affinity uptake and root-to-shoot transport of nitrate. Loss of CEPDL2 leads to a reduction in shoot nitrate content and plant biomass. CEPDL2 contributes to N acquisition cooperatively with CEPD1 and CEPD2 which mediate root N status, and the complete loss of all three proteins severely impairs N homeostasis in plants. Reciprocal grafting analysis provides conclusive evidence that the shoot CEPDL2/CEPD1/2 genotype defines the high-affinity nitrate uptake activity in root. Our results indicate that plants integrate shoot N status and root N status in leaves and systemically regulate the efficiency of root N acquisition.

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

“…Grafting experiments indicated that nodule initiation is controlled by MtCRA2 systemically from shoots and lateral root formation locally within roots (Huault et al, 2014). The MtCRA2 receptor-like kinase is most closely related to XYLEM INTERMIXED WITH PHLOEM1/CEP RECEPTOR1 (XIP1/CEPR1) in Arabidopsis (Arabidopsis thaliana), which was shown to bind AtCEP1 peptides and systemically regulate nitrate uptake through the systemic effectors CEP DOWNSTREAM1/2 (CEPD1/2) and CEPD-LIKE2 (Huault et al, 2014;Tabata et al, 2014;Ohkubo et al, 2017;Ota et al, 2020). As root and nodule number phenotypes of MtCEP1-expressing roots and of cra2 mutants are opposite (Imin et al, 2013;Huault et al, 2014), this strongly suggests that CEP peptides could act depending on the MtCRA2 receptor, as recently demonstrated by Mohd-Radzman et al (2016).…”

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

“…However, in contrast to AtCEPD1 and AtCEPD2, AtCEPDL2 expression in the shoot was activated upon nitrogen deficiency irrespective of AtCEPR1 receptor activity, and was detected even in the shoots detached from the roots at low nitrogen concentrations. This suggests that AtCEPDL2 expression is regulated by nitrogen content in the shoot [80].…”

“…Moreover, Ota et al [80] recently detected two more genes with a high similarity to AtCEPD1 called AtCEPD-like 1 (CEPDL1) and CEPDL2. Their overexpression also caused activation of NRT2.1 expression in the roots even in nitrogen-reach medium (10 mM and 10 mM ).…”

“…Their overexpression also caused activation of NRT2.1 expression in the roots even in nitrogen-reach medium (10 mM and 10 mM ). Transcriptome study of plants overexpressing AtCEPDL2 found that AtCEPDL2 stimulates expression of the genes encoding transporters with high-affinity nitrate uptake, such as NRT2.1, NRT2.2, NRT2.4, and NRT3.1 as well as NRT1.5 that loads nitrate into xylem for its translocation from the root to shoot [80]. As its homologs AtCEPD1 and AtCEPD2, AtCEPDL2 protein is transported from the shoot to the root through the phloem, which was revealed by the analysis of promoter activity and fluorescence of GFP-AtCEPDL2 hybrid protein.…”

The interplay of phloem-mobile signals in plant development and stress response

“…In this case, both CKs and CEP appear to regulate gene expression. CEPDL2 then translocates to the root, where it affects both nitrate-uptake and transport through the regulation of the expression of several high-affinity nitrate transporters [120]. CEPD1/2 and CEPDL2 appear to be part of a dual N-sensing and response system, with CEPD1/2 responding to the root N status and CEPDL2 responding to the shoot status (Figure 3, blue).…”