Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding

Huanglongbing (HLB) is a devastating citrus disease that threatens the citrus industry worldwide. HLB is associated with the bacteria Candidatus Liberibacter asiaticus (CLas) and as of today, there are no tools for economically viable disease management. Several wild Australian limes have been ident...

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Main Authors: Jianyang Liu, Khushwant Singh, Matthew Huff, Christopher Gottschalk, Michael Do, Margaret Staton, Manjunath L. Keremane, Robert Krueger, Chandrika Ramadugu, Chris Dardick
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1503030/full
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author Jianyang Liu
Khushwant Singh
Matthew Huff
Christopher Gottschalk
Michael Do
Margaret Staton
Manjunath L. Keremane
Robert Krueger
Chandrika Ramadugu
Chris Dardick
author_facet Jianyang Liu
Khushwant Singh
Matthew Huff
Christopher Gottschalk
Michael Do
Margaret Staton
Manjunath L. Keremane
Robert Krueger
Chandrika Ramadugu
Chris Dardick
author_sort Jianyang Liu
collection DOAJ
description Huanglongbing (HLB) is a devastating citrus disease that threatens the citrus industry worldwide. HLB is associated with the bacteria Candidatus Liberibacter asiaticus (CLas) and as of today, there are no tools for economically viable disease management. Several wild Australian limes have been identified to be HLB resistant and their resistance is hypothesized to be conferred by resistance genes (R-genes), which mediate pathogen-specific defense responses. The aim of this study was to gain insight into the genomic features of R-genes in Australian limes, in comparison to susceptible citrus cultivars. In this study, we used five citrus genomes, including three Australian limes (Citrus australasica, C. glauca and C. inodora) and two cultivated citrus species (C. clementina and C. sinensis). Our results indicate up to 70% of the R-genes were identified in the unannotated regions in the original genome annotation of each species, owing to the use of a R-gene specific pipeline. Surprisingly, the two cultivated species harbored 15.8 to 104% more R-genes than the Australian limes. In all species, over 75% of the R-genes occurred in clusters and nearly 80% were concentrated in three chromosomes (Chr3, 5 and 7). The syntenic R-gene based phylogenic classification grouped the five species according to their HLB-resistance levels, reflecting the association between these R-genes and their distinct Australian origins. Domain structure analysis revealed substantial similarities in the R-genes between wild Australian limes and cultivated citrus. Investigation of chromosomal sites underlying Australian specific R genes revealed diversifying selection signatures on several chromosomal regions. The findings in this study will aid in the development of tools for genome-assisted breeding for HLB-resistant varieties.
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spelling doaj-art-0f18177717264915ad3f38d1ff99eadc2025-02-03T12:04:54ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-01-011510.3389/fpls.2024.15030301503030Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breedingJianyang Liu0Khushwant Singh1Matthew Huff2Christopher Gottschalk3Michael Do4Margaret Staton5Manjunath L. Keremane6Robert Krueger7Chandrika Ramadugu8Chris Dardick9Innovative Fruit Production, Improvement, and Protection, Appalachian Fruit Research Station, U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS), Kearneysville, WV, United StatesDepartment of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United StatesDepartment of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN, United StatesInnovative Fruit Production, Improvement, and Protection, Appalachian Fruit Research Station, U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS), Kearneysville, WV, United StatesInnovative Fruit Production, Improvement, and Protection, Appalachian Fruit Research Station, U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS), Kearneysville, WV, United StatesDepartment of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN, United StatesNational Clonal Germplasm Repository for Citrus and Dates, U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS), Riverside, CA, United StatesNational Clonal Germplasm Repository for Citrus and Dates, U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS), Riverside, CA, United StatesDepartment of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United StatesInnovative Fruit Production, Improvement, and Protection, Appalachian Fruit Research Station, U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS), Kearneysville, WV, United StatesHuanglongbing (HLB) is a devastating citrus disease that threatens the citrus industry worldwide. HLB is associated with the bacteria Candidatus Liberibacter asiaticus (CLas) and as of today, there are no tools for economically viable disease management. Several wild Australian limes have been identified to be HLB resistant and their resistance is hypothesized to be conferred by resistance genes (R-genes), which mediate pathogen-specific defense responses. The aim of this study was to gain insight into the genomic features of R-genes in Australian limes, in comparison to susceptible citrus cultivars. In this study, we used five citrus genomes, including three Australian limes (Citrus australasica, C. glauca and C. inodora) and two cultivated citrus species (C. clementina and C. sinensis). Our results indicate up to 70% of the R-genes were identified in the unannotated regions in the original genome annotation of each species, owing to the use of a R-gene specific pipeline. Surprisingly, the two cultivated species harbored 15.8 to 104% more R-genes than the Australian limes. In all species, over 75% of the R-genes occurred in clusters and nearly 80% were concentrated in three chromosomes (Chr3, 5 and 7). The syntenic R-gene based phylogenic classification grouped the five species according to their HLB-resistance levels, reflecting the association between these R-genes and their distinct Australian origins. Domain structure analysis revealed substantial similarities in the R-genes between wild Australian limes and cultivated citrus. Investigation of chromosomal sites underlying Australian specific R genes revealed diversifying selection signatures on several chromosomal regions. The findings in this study will aid in the development of tools for genome-assisted breeding for HLB-resistant varieties.https://www.frontiersin.org/articles/10.3389/fpls.2024.1503030/fullcitrusHonglongbing (HLB)R-genesAustralian limesresistance
spellingShingle Jianyang Liu
Khushwant Singh
Matthew Huff
Christopher Gottschalk
Michael Do
Margaret Staton
Manjunath L. Keremane
Robert Krueger
Chandrika Ramadugu
Chris Dardick
Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding
Frontiers in Plant Science
citrus
Honglongbing (HLB)
R-genes
Australian limes
resistance
title Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding
title_full Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding
title_fullStr Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding
title_full_unstemmed Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding
title_short Deep R-gene discovery in HLB resistant wild Australian limes uncovers evolutionary features and potentially important loci for hybrid breeding
title_sort deep r gene discovery in hlb resistant wild australian limes uncovers evolutionary features and potentially important loci for hybrid breeding
topic citrus
Honglongbing (HLB)
R-genes
Australian limes
resistance
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1503030/full
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