Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple Roots

Apple replant disease (ARD), incited by a pathogen complex including Pythium ultimum, causes stunted growth or death of newly planted trees at replant sites. Development and deployment of resistant or tolerant rootstocks offers a cost-effective, ecologically friendly, and durable approach for ARD ma...

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Main Authors: Yanmin Zhu, Guanliang Li, Jugpreet Singh, Awais Khan, Gennaro Fazio, Melody Saltzgiver, Rui Xia
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.629776/full
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spelling doaj-ba2a4ad78e554d45b88234ae787331d42021-09-07T06:28:11ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-09-011210.3389/fpls.2021.629776629776Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple RootsYanmin Zhu0Guanliang Li1Jugpreet Singh2Awais Khan3Gennaro Fazio4Melody Saltzgiver5Rui Xia6Tree Fruit Research Laboratory, USDA-ARS, Wenatchee, WA, United StatesCollege of Horticulture, South China Agricultural University, Guangzhou, ChinaPlant Pathology and Plant-Microbe Biology Section, Cornell University, Geneva, NY, United StatesPlant Pathology and Plant-Microbe Biology Section, Cornell University, Geneva, NY, United StatesPlant Genetic Resources Unit, USDA-ARS, Geneva, NY, United StatesTree Fruit Research Laboratory, USDA-ARS, Wenatchee, WA, United StatesCollege of Horticulture, South China Agricultural University, Guangzhou, ChinaApple replant disease (ARD), incited by a pathogen complex including Pythium ultimum, causes stunted growth or death of newly planted trees at replant sites. Development and deployment of resistant or tolerant rootstocks offers a cost-effective, ecologically friendly, and durable approach for ARD management. Maximized exploitation of natural resistance requires integrated efforts to identify key regulatory mechanisms underlying resistance traits in apple. In this study, miRNA profiling and degradome sequencing identified major miRNA pathways and candidate genes using six apple rootstock genotypes with contrasting phenotypes to P. ultimum infection. The comprehensive RNA-seq dataset offered an expansive view of post-transcriptional regulation of apple root defense activation in response to infection from P. ultimum. Several pairs of miRNA families and their corresponding targets were identified for their roles in defense response in apple roots, including miR397-laccase, miR398-superoxide dismutase, miR10986-polyphenol oxidase, miR482-resistance genes, and miR160-auxin response factor. Of these families, the genotype-specific expression patterns of miR397 indicated its fundamental role in developing defense response patterns to P. ultimum infection. Combined with other identified copper proteins, the importance of cellular fortification, such as lignification of root tissues by the action of laccase, may critically contribute to genotype-specific resistance traits. Our findings suggest that quick and enhanced lignification of apple roots may significantly impede pathogen penetration and minimize the disruption of effective defense activation in roots of resistant genotypes. The identified target miRNA species and target genes consist of a valuable resource for subsequent functional analysis of their roles during interaction between apple roots and P. ultimum.https://www.frontiersin.org/articles/10.3389/fpls.2021.629776/fullapple rootsoilborne pathogensdefense activationplant resistancesmall RNA profilingdegradome sequencing
collection DOAJ
language English
format Article
sources DOAJ
author Yanmin Zhu
Guanliang Li
Jugpreet Singh
Awais Khan
Gennaro Fazio
Melody Saltzgiver
Rui Xia
spellingShingle Yanmin Zhu
Guanliang Li
Jugpreet Singh
Awais Khan
Gennaro Fazio
Melody Saltzgiver
Rui Xia
Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple Roots
Frontiers in Plant Science
apple root
soilborne pathogens
defense activation
plant resistance
small RNA profiling
degradome sequencing
author_facet Yanmin Zhu
Guanliang Li
Jugpreet Singh
Awais Khan
Gennaro Fazio
Melody Saltzgiver
Rui Xia
author_sort Yanmin Zhu
title Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple Roots
title_short Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple Roots
title_full Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple Roots
title_fullStr Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple Roots
title_full_unstemmed Laccase Directed Lignification Is One of the Major Processes Associated With the Defense Response Against Pythium ultimum Infection in Apple Roots
title_sort laccase directed lignification is one of the major processes associated with the defense response against pythium ultimum infection in apple roots
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-09-01
description Apple replant disease (ARD), incited by a pathogen complex including Pythium ultimum, causes stunted growth or death of newly planted trees at replant sites. Development and deployment of resistant or tolerant rootstocks offers a cost-effective, ecologically friendly, and durable approach for ARD management. Maximized exploitation of natural resistance requires integrated efforts to identify key regulatory mechanisms underlying resistance traits in apple. In this study, miRNA profiling and degradome sequencing identified major miRNA pathways and candidate genes using six apple rootstock genotypes with contrasting phenotypes to P. ultimum infection. The comprehensive RNA-seq dataset offered an expansive view of post-transcriptional regulation of apple root defense activation in response to infection from P. ultimum. Several pairs of miRNA families and their corresponding targets were identified for their roles in defense response in apple roots, including miR397-laccase, miR398-superoxide dismutase, miR10986-polyphenol oxidase, miR482-resistance genes, and miR160-auxin response factor. Of these families, the genotype-specific expression patterns of miR397 indicated its fundamental role in developing defense response patterns to P. ultimum infection. Combined with other identified copper proteins, the importance of cellular fortification, such as lignification of root tissues by the action of laccase, may critically contribute to genotype-specific resistance traits. Our findings suggest that quick and enhanced lignification of apple roots may significantly impede pathogen penetration and minimize the disruption of effective defense activation in roots of resistant genotypes. The identified target miRNA species and target genes consist of a valuable resource for subsequent functional analysis of their roles during interaction between apple roots and P. ultimum.
topic apple root
soilborne pathogens
defense activation
plant resistance
small RNA profiling
degradome sequencing
url https://www.frontiersin.org/articles/10.3389/fpls.2021.629776/full
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