Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation

C-terminally encoded peptides (CEPs) are plant developmental signals that regulate growth and adaptive responses to nitrogen stress conditions. These small signal peptides are common to all vascular plants, and intriguingly have been characterized in some plant parasitic nematodes. Here, we sought t...

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Main Authors: Shova Mishra, Weiming Hu, Peter DiGennaro
Format: Article
Language:English
Published: MDPI AG 2023-10-01
Series:Life
Subjects:
Online Access:https://www.mdpi.com/2075-1729/13/10/2020
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author Shova Mishra
Weiming Hu
Peter DiGennaro
author_facet Shova Mishra
Weiming Hu
Peter DiGennaro
author_sort Shova Mishra
collection DOAJ
description C-terminally encoded peptides (CEPs) are plant developmental signals that regulate growth and adaptive responses to nitrogen stress conditions. These small signal peptides are common to all vascular plants, and intriguingly have been characterized in some plant parasitic nematodes. Here, we sought to discover the breadth of root-knot nematode (RKN)-encoded CEP-like peptides and define the potential roles of these signals in the plant–nematode interaction, focusing on peptide activity altering plant root phenotypes and nitrogen uptake and assimilation. A comprehensive bioinformatic screen identified 61 CEP-like sequences encoded within the genomes of six root-knot nematode (RKN; <i>Meloidogyne</i> spp.) species. Exogenous application of an RKN CEP-like peptide altered <i>A. thaliana</i> and <i>M. truncatula</i> root phenotypes including reduced lateral root number in <i>M. truncatula</i> and inhibited primary root length in <i>A. thaliana</i>. To define the role of RKN CEP-like peptides, we applied exogenous RKN CEP and demonstrated increases in plant nitrogen uptake through the upregulation of nitrate transporter gene expression in roots and increased 15N/14N in nematode-formed root galls. Further, we also identified enhanced nematode metabolic processes following CEP application. These results support a model of parasite-induced changes in host metabolism and inform endogenous pathways to regulate plant nitrogen assimilation.
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spelling doaj.art-caddb82fa07f4faca71cccff41adbe632023-11-19T17:06:15ZengMDPI AGLife2075-17292023-10-011310202010.3390/life13102020Root-Knot-Nematode-Encoded CEPs Increase Nitrogen AssimilationShova Mishra0Weiming Hu1Peter DiGennaro2Entomology and Nematology Department, University of Florida, Gainesville, FL 32611, USAEntomology and Nematology Department, University of Florida, Gainesville, FL 32611, USAEntomology and Nematology Department, University of Florida, Gainesville, FL 32611, USAC-terminally encoded peptides (CEPs) are plant developmental signals that regulate growth and adaptive responses to nitrogen stress conditions. These small signal peptides are common to all vascular plants, and intriguingly have been characterized in some plant parasitic nematodes. Here, we sought to discover the breadth of root-knot nematode (RKN)-encoded CEP-like peptides and define the potential roles of these signals in the plant–nematode interaction, focusing on peptide activity altering plant root phenotypes and nitrogen uptake and assimilation. A comprehensive bioinformatic screen identified 61 CEP-like sequences encoded within the genomes of six root-knot nematode (RKN; <i>Meloidogyne</i> spp.) species. Exogenous application of an RKN CEP-like peptide altered <i>A. thaliana</i> and <i>M. truncatula</i> root phenotypes including reduced lateral root number in <i>M. truncatula</i> and inhibited primary root length in <i>A. thaliana</i>. To define the role of RKN CEP-like peptides, we applied exogenous RKN CEP and demonstrated increases in plant nitrogen uptake through the upregulation of nitrate transporter gene expression in roots and increased 15N/14N in nematode-formed root galls. Further, we also identified enhanced nematode metabolic processes following CEP application. These results support a model of parasite-induced changes in host metabolism and inform endogenous pathways to regulate plant nitrogen assimilation.https://www.mdpi.com/2075-1729/13/10/2020CEPplant-peptideroot-knot nematodenitrogen uptakeisotope labeling
spellingShingle Shova Mishra
Weiming Hu
Peter DiGennaro
Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation
Life
CEP
plant-peptide
root-knot nematode
nitrogen uptake
isotope labeling
title Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation
title_full Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation
title_fullStr Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation
title_full_unstemmed Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation
title_short Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation
title_sort root knot nematode encoded ceps increase nitrogen assimilation
topic CEP
plant-peptide
root-knot nematode
nitrogen uptake
isotope labeling
url https://www.mdpi.com/2075-1729/13/10/2020
work_keys_str_mv AT shovamishra rootknotnematodeencodedcepsincreasenitrogenassimilation
AT weiminghu rootknotnematodeencodedcepsincreasenitrogenassimilation
AT peterdigennaro rootknotnematodeencodedcepsincreasenitrogenassimilation