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...
Main Authors: | , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2023-10-01
|
Series: | Life |
Subjects: | |
Online Access: | https://www.mdpi.com/2075-1729/13/10/2020 |
_version_ | 1797573256609267712 |
---|---|
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. |
first_indexed | 2024-03-10T21:07:16Z |
format | Article |
id | doaj.art-caddb82fa07f4faca71cccff41adbe63 |
institution | Directory Open Access Journal |
issn | 2075-1729 |
language | English |
last_indexed | 2024-03-10T21:07:16Z |
publishDate | 2023-10-01 |
publisher | MDPI AG |
record_format | Article |
series | Life |
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 |