A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora

Plants have complex and dynamic immune systems that have evolved to resist pathogens. Humans have worked to enhance these defenses in crops through breeding. However, many crops harbor only a fraction of the genetic diversity present in wild relatives. Increased utilization of diverse germplasm to s...

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Main Authors: Winters, Noah P, Wafula, Eric K, Knollenberg, Benjamin J, Leandro-Muñoz, Mariela E
Format: Artículo
Language:Inglés
Published: BMC Biology 2024
Subjects:
Online Access:https://repositorio.catie.ac.cr/handle/11554/12638
id RepoCATIE12638
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spelling RepoCATIE126382024-04-13T00:26:16Z A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora Winters, Noah P Wafula, Eric K Knollenberg, Benjamin J Leandro-Muñoz, Mariela E Mejoramiento genético||genetic improvement||melhoramento genético||undefined mejora de cultivos||crop improvement||undefined||amélioration des cultures Diversidad genética (como recurso)||genetic diversity (as resource)||diversidade genética (como recurso)||diversité génétique (comme ressource) Germoplasma||germplasm||germoplasma||germoplasme Theobroma cacao||Theobroma cacao||Theobroma cacao||Theobroma cacao Phytophthora palmivora||Phytophthora palmivora||Phytophthora palmivora||Phytophthora palmivora Antimicrobianos||antimicrobials||antimicrobiano||antimicrobien Reacciones de defensa de plantas||plant defence reactions||reacção de defesa das plantas||réaction de défense des plantes Evolución||evolution||evolução||évolution Secuencia de ARN||RNA sequence||Sequência do ARN||séquence d'arn genómica||genomics||undefined||génomique Cacao Sede Central ODS 15 - Vida de ecosistemas terrestres Plants have complex and dynamic immune systems that have evolved to resist pathogens. Humans have worked to enhance these defenses in crops through breeding. However, many crops harbor only a fraction of the genetic diversity present in wild relatives. Increased utilization of diverse germplasm to search for desirable traits, such as disease resistance, is therefore a valuable step towards breeding crops that are adapted to both current and emerging threats. Here, we examine diversity of defense responses across four populations of the long-generation tree crop Theobroma cacao L., as well as four non-cacao Theobroma species, with the goal of identifying genetic elements essential for protection against the oomycete pathogen Phytophthora palmivora. We began by creating a new, highly contiguous genome assembly for the P. palmivora-resistant genotype SCA 6 (Additional file 1: Tables S1-S5), deposited in GenBank under accessions CP139290-CP139299. We then used this high-quality assembly to combine RNA and whole-genome sequencing data to discover several genes and pathways associated with resistance. Many of these are unique, i.e., differentially regulated in only one of the four populations (diverged 40 k–900 k generations). Among the pathways shared across all populations is phenylpropanoid biosynthesis, a metabolic pathway with well-documented roles in plant defense. One gene in this pathway, caffeoyl shikimate esterase (CSE), was upregulated across all four populations following pathogen treatment, indicating its broad importance for cacao’s defense response. Further experimental evidence suggests this gene hydrolyzes caffeoyl shikimate to create caffeic acid, an antimicrobial compound and known inhibitor of Phytophthora spp. Our results indicate most expression variation associated with resistance is unique to populations. Moreover, our findings demonstrate the value of using a broad sample of evolutionarily diverged populations for revealing the genetic bases of cacao resistance to P. palmivora. This approach has promise for further revealing and harnessing valuable genetic resources in this and other long-generation plants. 2024-04-11T20:28:25Z 2024-04-11T20:28:25Z 2024 Artículo https://repositorio.catie.ac.cr/handle/11554/12638 openAccess en BMC Biology 24 páginas application/pdf BMC Biology
institution Centro Agronómico Tropical de Investigación y Enseñanza
collection Repositorio CATIE
language Inglés
topic Mejoramiento genético||genetic improvement||melhoramento genético||undefined
mejora de cultivos||crop improvement||undefined||amélioration des cultures
Diversidad genética (como recurso)||genetic diversity (as resource)||diversidade genética (como recurso)||diversité génétique (comme ressource)
Germoplasma||germplasm||germoplasma||germoplasme
Theobroma cacao||Theobroma cacao||Theobroma cacao||Theobroma cacao
Phytophthora palmivora||Phytophthora palmivora||Phytophthora palmivora||Phytophthora palmivora
Antimicrobianos||antimicrobials||antimicrobiano||antimicrobien
Reacciones de defensa de plantas||plant defence reactions||reacção de defesa das plantas||réaction de défense des plantes
Evolución||evolution||evolução||évolution
Secuencia de ARN||RNA sequence||Sequência do ARN||séquence d'arn
genómica||genomics||undefined||génomique
Cacao
Sede Central
ODS 15 - Vida de ecosistemas terrestres
spellingShingle Mejoramiento genético||genetic improvement||melhoramento genético||undefined
mejora de cultivos||crop improvement||undefined||amélioration des cultures
Diversidad genética (como recurso)||genetic diversity (as resource)||diversidade genética (como recurso)||diversité génétique (comme ressource)
Germoplasma||germplasm||germoplasma||germoplasme
Theobroma cacao||Theobroma cacao||Theobroma cacao||Theobroma cacao
Phytophthora palmivora||Phytophthora palmivora||Phytophthora palmivora||Phytophthora palmivora
Antimicrobianos||antimicrobials||antimicrobiano||antimicrobien
Reacciones de defensa de plantas||plant defence reactions||reacção de defesa das plantas||réaction de défense des plantes
Evolución||evolution||evolução||évolution
Secuencia de ARN||RNA sequence||Sequência do ARN||séquence d'arn
genómica||genomics||undefined||génomique
Cacao
Sede Central
ODS 15 - Vida de ecosistemas terrestres
Winters, Noah P
Wafula, Eric K
Knollenberg, Benjamin J
Leandro-Muñoz, Mariela E
A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora
description Plants have complex and dynamic immune systems that have evolved to resist pathogens. Humans have worked to enhance these defenses in crops through breeding. However, many crops harbor only a fraction of the genetic diversity present in wild relatives. Increased utilization of diverse germplasm to search for desirable traits, such as disease resistance, is therefore a valuable step towards breeding crops that are adapted to both current and emerging threats. Here, we examine diversity of defense responses across four populations of the long-generation tree crop Theobroma cacao L., as well as four non-cacao Theobroma species, with the goal of identifying genetic elements essential for protection against the oomycete pathogen Phytophthora palmivora. We began by creating a new, highly contiguous genome assembly for the P. palmivora-resistant genotype SCA 6 (Additional file 1: Tables S1-S5), deposited in GenBank under accessions CP139290-CP139299. We then used this high-quality assembly to combine RNA and whole-genome sequencing data to discover several genes and pathways associated with resistance. Many of these are unique, i.e., differentially regulated in only one of the four populations (diverged 40 k–900 k generations). Among the pathways shared across all populations is phenylpropanoid biosynthesis, a metabolic pathway with well-documented roles in plant defense. One gene in this pathway, caffeoyl shikimate esterase (CSE), was upregulated across all four populations following pathogen treatment, indicating its broad importance for cacao’s defense response. Further experimental evidence suggests this gene hydrolyzes caffeoyl shikimate to create caffeic acid, an antimicrobial compound and known inhibitor of Phytophthora spp. Our results indicate most expression variation associated with resistance is unique to populations. Moreover, our findings demonstrate the value of using a broad sample of evolutionarily diverged populations for revealing the genetic bases of cacao resistance to P. palmivora. This approach has promise for further revealing and harnessing valuable genetic resources in this and other long-generation plants.
format Artículo
author Winters, Noah P
Wafula, Eric K
Knollenberg, Benjamin J
Leandro-Muñoz, Mariela E
author_facet Winters, Noah P
Wafula, Eric K
Knollenberg, Benjamin J
Leandro-Muñoz, Mariela E
author_sort Winters, Noah P
title A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora
title_short A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora
title_full A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora
title_fullStr A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora
title_full_unstemmed A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora
title_sort combination of conserved and diverged responses underlies theobroma cacao’s defense response to phytophthora palmivora
publisher BMC Biology
publishDate 2024
url https://repositorio.catie.ac.cr/handle/11554/12638
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