Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea

Polygalacturonase-inhibiting proteins (PGIPs) are cell wall proteins that inhibit pathogen polygalacturonases (PGs). PGIPs, like other defense-related proteins, contain extracellular leucine-rich repeats (eLRRs), which are required for pathogen PG recognition. The importance of these PGIPs in plant...

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Main Authors: Vishnutej Ellur, Wei Wei, Rishikesh Ghogare‬, Shyam Solanki, George Vandemark, Robert Brueggeman, Weidong Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2023.1189329/full
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author Vishnutej Ellur
Wei Wei
Rishikesh Ghogare‬
Shyam Solanki
George Vandemark
Robert Brueggeman
Weidong Chen
author_facet Vishnutej Ellur
Wei Wei
Rishikesh Ghogare‬
Shyam Solanki
George Vandemark
Robert Brueggeman
Weidong Chen
author_sort Vishnutej Ellur
collection DOAJ
description Polygalacturonase-inhibiting proteins (PGIPs) are cell wall proteins that inhibit pathogen polygalacturonases (PGs). PGIPs, like other defense-related proteins, contain extracellular leucine-rich repeats (eLRRs), which are required for pathogen PG recognition. The importance of these PGIPs in plant defense has been well documented. This study focuses on chickpea (Cicer arietinum) PGIPs (CaPGIPs) owing to the limited information available on this important crop. This study identified two novel CaPGIPs (CaPGIP3 and CaPGIP4) and computationally characterized all four CaPGIPs in the gene family, including the previously reported CaPGIP1 and CaPGIP2. The findings suggest that CaPGIP1, CaPGIP3, and CaPGIP4 proteins possess N-terminal signal peptides, ten LRRs, theoretical molecular mass, and isoelectric points comparable to other legume PGIPs. Phylogenetic analysis and multiple sequence alignment revealed that the CaPGIP1, CaPGIP3, and CaPGIP4 amino acid sequences are similar to the other PGIPs reported in legumes. In addition, several cis-acting elements that are typical of pathogen response, tissue-specific activity, hormone response, and abiotic stress-related are present in the promoters of CaPGIP1, CaPGIP3, and CaPGIP4 genes. Localization experiments showed that CaPGIP1, CaPGIP3, and CaPGIP4 are located in the cell wall or membrane. Transcript levels of CaPGIP1, CaPGIP3, and CaPGIP4 genes analyzed at untreated conditions show varied expression patterns analogous to other defense-related gene families. Interestingly, CaPGIP2 lacked a signal peptide, more than half of the LRRs, and other characteristics of a typical PGIP and subcellular localization indicated it is not located in the cell wall or membrane. The study’s findings demonstrate CaPGIP1, CaPGIP3, and CaPGIP4’s similarity to other legume PGIPs and suggest they might possess the potential to combat chickpea pathogens.
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spelling doaj.art-ef9a4489f6764b2c8dc8fbc3bd6e56c12023-06-05T05:04:07ZengFrontiers Media S.A.Frontiers in Genetics1664-80212023-06-011410.3389/fgene.2023.11893291189329Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpeaVishnutej Ellur0Wei Wei1Rishikesh Ghogare‬2Shyam Solanki3George Vandemark4Robert Brueggeman5Weidong Chen6Molecular Plant Science, Washington State University, Pullman, WA, United StatesDepartment of Plant Pathology, Washington State University, Pullman, WA, United StatesDepartment of Horticultural Sciences, Texas A&M University, College Station, TX, United StatesDepartment of Agronomy, Horticulture and Plant Science, South Dakota State University, Brookings, SD, United StatesGrain Legume Genetics Physiology Research, Pullman, WA, United StatesDepartment of Crop and Soil Science, Washington State University, Pullman, WA, United StatesGrain Legume Genetics Physiology Research, Pullman, WA, United StatesPolygalacturonase-inhibiting proteins (PGIPs) are cell wall proteins that inhibit pathogen polygalacturonases (PGs). PGIPs, like other defense-related proteins, contain extracellular leucine-rich repeats (eLRRs), which are required for pathogen PG recognition. The importance of these PGIPs in plant defense has been well documented. This study focuses on chickpea (Cicer arietinum) PGIPs (CaPGIPs) owing to the limited information available on this important crop. This study identified two novel CaPGIPs (CaPGIP3 and CaPGIP4) and computationally characterized all four CaPGIPs in the gene family, including the previously reported CaPGIP1 and CaPGIP2. The findings suggest that CaPGIP1, CaPGIP3, and CaPGIP4 proteins possess N-terminal signal peptides, ten LRRs, theoretical molecular mass, and isoelectric points comparable to other legume PGIPs. Phylogenetic analysis and multiple sequence alignment revealed that the CaPGIP1, CaPGIP3, and CaPGIP4 amino acid sequences are similar to the other PGIPs reported in legumes. In addition, several cis-acting elements that are typical of pathogen response, tissue-specific activity, hormone response, and abiotic stress-related are present in the promoters of CaPGIP1, CaPGIP3, and CaPGIP4 genes. Localization experiments showed that CaPGIP1, CaPGIP3, and CaPGIP4 are located in the cell wall or membrane. Transcript levels of CaPGIP1, CaPGIP3, and CaPGIP4 genes analyzed at untreated conditions show varied expression patterns analogous to other defense-related gene families. Interestingly, CaPGIP2 lacked a signal peptide, more than half of the LRRs, and other characteristics of a typical PGIP and subcellular localization indicated it is not located in the cell wall or membrane. The study’s findings demonstrate CaPGIP1, CaPGIP3, and CaPGIP4’s similarity to other legume PGIPs and suggest they might possess the potential to combat chickpea pathogens.https://www.frontiersin.org/articles/10.3389/fgene.2023.1189329/fullpolygalacturonase inhibitory proteins (PGIPs)gene familydefense-related genebiotic stress responseleucine-rich repeats (LRRs)promoter analysis
spellingShingle Vishnutej Ellur
Wei Wei
Rishikesh Ghogare‬
Shyam Solanki
George Vandemark
Robert Brueggeman
Weidong Chen
Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea
Frontiers in Genetics
polygalacturonase inhibitory proteins (PGIPs)
gene family
defense-related gene
biotic stress response
leucine-rich repeats (LRRs)
promoter analysis
title Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea
title_full Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea
title_fullStr Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea
title_full_unstemmed Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea
title_short Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea
title_sort unraveling the genomic reorganization of polygalacturonase inhibiting proteins in chickpea
topic polygalacturonase inhibitory proteins (PGIPs)
gene family
defense-related gene
biotic stress response
leucine-rich repeats (LRRs)
promoter analysis
url https://www.frontiersin.org/articles/10.3389/fgene.2023.1189329/full
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