Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae

Verticillium wilt of olive (VWO), caused by the soil-borne vascular pathogen Verticillium dahliae, is one of the most devastating diseases affecting olive, the woody crop. One of the best VWO management measures is the use of tolerant cultivars. Yet, our knowledge about defense mechanisms that operate at the root level to explain tolerance to this disease is incomplete. Moreover, most of the approaches so far followed focus only on a specific mechanistic level (e.g., genetic, physiological, or biochemical) rather than on a holistic/multilevel perspective. In this study, eighteen root functional traits, the time-course expression of nine defense-related genes, the root lignin content, and the root membrane permeability were evaluated in six olive varieties differing in their level of tolerance/susceptibility to VWO. The aim was to find links between the level of tolerance to VWO and specific root defense mechanisms at the structural, genetic, biochemical, and physiological levels. Tolerant and susceptible cultivars showed substantial differences in the root system architecture and root lignin content. VWO-susceptible cultivars presented roots with higher specific length and area, but lower diameter and larger number of forks and tips compared to tolerant varieties that also showed less branched roots, higher root diameter, and larger basal content of lignin. Interestingly, VWO-tolerant varieties significantly increased their root lignin content and root membrane permeability after inoculation with V. dahliae. These results were seldom (or not at all) observed in the susceptible plants. At the genetic level, genes related to defense mechanisms, such as cell wall lignin biosynthesis (C4H and CO-MT), production of hydrolytic enzymes able to degrade the fungal cell wall (β-1.3-glucanase), and activation of innate immunity (BAK1 and WRKY5) increased their expression in tolerant cultivars from early moments after inoculation, in contrast to the susceptible ones. These results showed that differences in the root system architecture and lignin content may greatly determine the performance of olive against colonization and invasion by V. dahliae. Moreover, the increase in root membrane permeability in the presence of the pathogen was a typical response of tolerant cultivars. Finally, VWO-tolerant cultivars were able to mount a more intense and rapid defense-related genetic response to respond to the attack by V. dahliae.

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Main Authors: Cardoni, Martina, Gómez-Lama Cabanás, Carmen, Valverde-Corredor, Antonio, Villar, Rafael, Mercado-Blanco, Jesús
Other Authors: Ministerio de Ciencia e Innovación (España)
Format: artículo biblioteca
Language:English
Published: Frontiers Media 2022-04-25
Subjects:Specific root length, Olea europaea, Verticillium wilt, Functional traits, Host defense response, Lignin content, Olive root architecture, Root membrane permeability,
Online Access:http://hdl.handle.net/10261/286911
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100004837
http://dx.doi.org/10.13039/501100011011
https://api.elsevier.com/content/abstract/scopus_id/85129919999
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id dig-ias-es-10261-286911
record_format koha
institution IAS ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-ias-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IAS España
language English
topic Specific root length
Olea europaea
Verticillium wilt
Functional traits
Host defense response
Lignin content
Olive root architecture
Root membrane permeability
Specific root length
Olea europaea
Verticillium wilt
Functional traits
Host defense response
Lignin content
Olive root architecture
Root membrane permeability
spellingShingle Specific root length
Olea europaea
Verticillium wilt
Functional traits
Host defense response
Lignin content
Olive root architecture
Root membrane permeability
Specific root length
Olea europaea
Verticillium wilt
Functional traits
Host defense response
Lignin content
Olive root architecture
Root membrane permeability
Cardoni, Martina
Gómez-Lama Cabanás, Carmen
Valverde-Corredor, Antonio
Villar, Rafael
Mercado-Blanco, Jesús
Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae
description Verticillium wilt of olive (VWO), caused by the soil-borne vascular pathogen Verticillium dahliae, is one of the most devastating diseases affecting olive, the woody crop. One of the best VWO management measures is the use of tolerant cultivars. Yet, our knowledge about defense mechanisms that operate at the root level to explain tolerance to this disease is incomplete. Moreover, most of the approaches so far followed focus only on a specific mechanistic level (e.g., genetic, physiological, or biochemical) rather than on a holistic/multilevel perspective. In this study, eighteen root functional traits, the time-course expression of nine defense-related genes, the root lignin content, and the root membrane permeability were evaluated in six olive varieties differing in their level of tolerance/susceptibility to VWO. The aim was to find links between the level of tolerance to VWO and specific root defense mechanisms at the structural, genetic, biochemical, and physiological levels. Tolerant and susceptible cultivars showed substantial differences in the root system architecture and root lignin content. VWO-susceptible cultivars presented roots with higher specific length and area, but lower diameter and larger number of forks and tips compared to tolerant varieties that also showed less branched roots, higher root diameter, and larger basal content of lignin. Interestingly, VWO-tolerant varieties significantly increased their root lignin content and root membrane permeability after inoculation with V. dahliae. These results were seldom (or not at all) observed in the susceptible plants. At the genetic level, genes related to defense mechanisms, such as cell wall lignin biosynthesis (C4H and CO-MT), production of hydrolytic enzymes able to degrade the fungal cell wall (β-1.3-glucanase), and activation of innate immunity (BAK1 and WRKY5) increased their expression in tolerant cultivars from early moments after inoculation, in contrast to the susceptible ones. These results showed that differences in the root system architecture and lignin content may greatly determine the performance of olive against colonization and invasion by V. dahliae. Moreover, the increase in root membrane permeability in the presence of the pathogen was a typical response of tolerant cultivars. Finally, VWO-tolerant cultivars were able to mount a more intense and rapid defense-related genetic response to respond to the attack by V. dahliae.
author2 Ministerio de Ciencia e Innovación (España)
author_facet Ministerio de Ciencia e Innovación (España)
Cardoni, Martina
Gómez-Lama Cabanás, Carmen
Valverde-Corredor, Antonio
Villar, Rafael
Mercado-Blanco, Jesús
format artículo
topic_facet Specific root length
Olea europaea
Verticillium wilt
Functional traits
Host defense response
Lignin content
Olive root architecture
Root membrane permeability
author Cardoni, Martina
Gómez-Lama Cabanás, Carmen
Valverde-Corredor, Antonio
Villar, Rafael
Mercado-Blanco, Jesús
author_sort Cardoni, Martina
title Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae
title_short Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae
title_full Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae
title_fullStr Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae
title_full_unstemmed Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae
title_sort unveiling differences in root defense mechanisms between tolerant and susceptible olive cultivars to verticillium dahliae
publisher Frontiers Media
publishDate 2022-04-25
url http://hdl.handle.net/10261/286911
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100004837
http://dx.doi.org/10.13039/501100011011
https://api.elsevier.com/content/abstract/scopus_id/85129919999
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spelling dig-ias-es-10261-2869112024-05-18T20:40:26Z Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae Cardoni, Martina Gómez-Lama Cabanás, Carmen Valverde-Corredor, Antonio Villar, Rafael Mercado-Blanco, Jesús Ministerio de Ciencia e Innovación (España) Agencia Estatal de Investigación (España) European Commission Junta de Andalucía Specific root length Olea europaea Verticillium wilt Functional traits Host defense response Lignin content Olive root architecture Root membrane permeability Verticillium wilt of olive (VWO), caused by the soil-borne vascular pathogen Verticillium dahliae, is one of the most devastating diseases affecting olive, the woody crop. One of the best VWO management measures is the use of tolerant cultivars. Yet, our knowledge about defense mechanisms that operate at the root level to explain tolerance to this disease is incomplete. Moreover, most of the approaches so far followed focus only on a specific mechanistic level (e.g., genetic, physiological, or biochemical) rather than on a holistic/multilevel perspective. In this study, eighteen root functional traits, the time-course expression of nine defense-related genes, the root lignin content, and the root membrane permeability were evaluated in six olive varieties differing in their level of tolerance/susceptibility to VWO. The aim was to find links between the level of tolerance to VWO and specific root defense mechanisms at the structural, genetic, biochemical, and physiological levels. Tolerant and susceptible cultivars showed substantial differences in the root system architecture and root lignin content. VWO-susceptible cultivars presented roots with higher specific length and area, but lower diameter and larger number of forks and tips compared to tolerant varieties that also showed less branched roots, higher root diameter, and larger basal content of lignin. Interestingly, VWO-tolerant varieties significantly increased their root lignin content and root membrane permeability after inoculation with V. dahliae. These results were seldom (or not at all) observed in the susceptible plants. At the genetic level, genes related to defense mechanisms, such as cell wall lignin biosynthesis (C4H and CO-MT), production of hydrolytic enzymes able to degrade the fungal cell wall (β-1.3-glucanase), and activation of innate immunity (BAK1 and WRKY5) increased their expression in tolerant cultivars from early moments after inoculation, in contrast to the susceptible ones. These results showed that differences in the root system architecture and lignin content may greatly determine the performance of olive against colonization and invasion by V. dahliae. Moreover, the increase in root membrane permeability in the presence of the pathogen was a typical response of tolerant cultivars. Finally, VWO-tolerant cultivars were able to mount a more intense and rapid defense-related genetic response to respond to the attack by V. dahliae. This work was supported by the Spanish Ministerio de Ciencia e Innovación/Agencia Estatal de Investigación (grant PID2019-106283RB-I00) and projects UCO-FEDER 18 REF 27943 MOD B and P18-RT-3455 from Junta de Andalucía (Spain). All co-funded with EU FEDER funds. Peer reviewed 2023-01-17T07:20:35Z 2023-01-17T07:20:35Z 2022-04-25 artículo http://purl.org/coar/resource_type/c_6501 Frontiers in Plant Science 13: 863055 (2022) http://hdl.handle.net/10261/286911 10.3389/fpls.2022.863055 1664-462X http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100011011 35548299 2-s2.0-85129919999 https://api.elsevier.com/content/abstract/scopus_id/85129919999 en Publisher's version Cardoni, Martina; Gómez-Lama Cabanás, Carmen; Valverde-Corredor, Antonio; Villar, Rafael; Mercado-Blanco, Jesús; 2022; Data_Sheet_1_Unveiling Differences in Root Defense Mechanisms Between Tolerant and Susceptible Olive Cultivars to Verticillium dahliae.docx [Dataset]; Frontiers Media; https://doi.org/10.3389/fpls.2022.863055.s001 https://doi.org/10.3389/fpls.2022.863055 Sí open application/pdf Frontiers Media