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Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L.

Brassica oleracea is one of the most important species of the Brassicaceae family encompassing several economically important vegetables produced and consumed worldwide. But its sustainability is challenged by a range of pathogens, among which black rot, caused by Xanthomonas campestris pv. campestr...

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Autores principales: Shaw, Ranjan K., Shen, Yusen, Wang, Jiansheng, Sheng, Xiaoguang, Zhao, Zhenqing, Yu, Huifang, Gu, Honghui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8687090/
https://www.ncbi.nlm.nih.gov/pubmed/34938304
http://dx.doi.org/10.3389/fpls.2021.742553
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author Shaw, Ranjan K.
Shen, Yusen
Wang, Jiansheng
Sheng, Xiaoguang
Zhao, Zhenqing
Yu, Huifang
Gu, Honghui
author_facet Shaw, Ranjan K.
Shen, Yusen
Wang, Jiansheng
Sheng, Xiaoguang
Zhao, Zhenqing
Yu, Huifang
Gu, Honghui
author_sort Shaw, Ranjan K.
collection PubMed
description Brassica oleracea is one of the most important species of the Brassicaceae family encompassing several economically important vegetables produced and consumed worldwide. But its sustainability is challenged by a range of pathogens, among which black rot, caused by Xanthomonas campestris pv. campestris (Xcc), is the most serious and destructive seed borne bacterial disease, causing huge yield losses. Host-plant resistance could act as the most effective and efficient solution to curb black rot disease for sustainable production of B. oleracea. Recently, ‘omics’ technologies have emerged as promising tools to understand the host-pathogen interactions, thereby gaining a deeper insight into the resistance mechanisms. In this review, we have summarized the recent achievements made in the emerging omics technologies to tackle the black rot challenge in B. oleracea. With an integrated approach of the omics technologies such as genomics, proteomics, transcriptomics, and metabolomics, it would allow better understanding of the complex molecular mechanisms underlying black rot resistance. Due to the availability of sequencing data, genomics and transcriptomics have progressed as expected for black rot resistance, however, other omics approaches like proteomics and metabolomics are lagging behind, necessitating a holistic and targeted approach to address the complex questions of Xcc-Brassica interactions. Genomic studies revealed that the black rot resistance is a complex trait and is mostly controlled by quantitative trait locus (QTL) with minor effects. Transcriptomic analysis divulged the genes related to photosynthesis, glucosinolate biosynthesis and catabolism, phenylpropanoid biosynthesis pathway, ROS scavenging, calcium signalling, hormonal synthesis and signalling pathway are being differentially expressed upon Xcc infection. Comparative proteomic analysis in relation to susceptible and/or resistance interactions with Xcc identified the involvement of proteins related to photosynthesis, protein biosynthesis, processing and degradation, energy metabolism, innate immunity, redox homeostasis, and defence response and signalling pathways in Xcc–Brassica interaction. Specifically, most of the studies focused on the regulation of the photosynthesis-related proteins as a resistance response in both early and later stages of infection. Metabolomic studies suggested that glucosinolates (GSLs), especially aliphatic and indolic GSLs, its subsequent hydrolysis products, and defensive metabolites synthesized by jasmonic acid (JA)-mediated phenylpropanoid biosynthesis pathway are involved in disease resistance mechanisms against Xcc in Brassica species. Multi-omics analysis showed that JA signalling pathway is regulating resistance against hemibiotrophic pathogen like Xcc. So, the bonhomie between omics technologies and plant breeding is going to trigger major breakthroughs in the field of crop improvement by developing superior cultivars with broad-spectrum resistance. If multi-omics tools are implemented at the right scale, we may be able to achieve the maximum benefits from the minimum. In this review, we have also discussed the challenges, future prospects, and the way forward in the application of omics technologies to accelerate the breeding of B. oleracea for disease resistance. A deeper insight about the current knowledge on omics can offer promising results in the breeding of high-quality disease-resistant crops.
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spelling pubmed-86870902021-12-21 Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L. Shaw, Ranjan K. Shen, Yusen Wang, Jiansheng Sheng, Xiaoguang Zhao, Zhenqing Yu, Huifang Gu, Honghui Front Plant Sci Plant Science Brassica oleracea is one of the most important species of the Brassicaceae family encompassing several economically important vegetables produced and consumed worldwide. But its sustainability is challenged by a range of pathogens, among which black rot, caused by Xanthomonas campestris pv. campestris (Xcc), is the most serious and destructive seed borne bacterial disease, causing huge yield losses. Host-plant resistance could act as the most effective and efficient solution to curb black rot disease for sustainable production of B. oleracea. Recently, ‘omics’ technologies have emerged as promising tools to understand the host-pathogen interactions, thereby gaining a deeper insight into the resistance mechanisms. In this review, we have summarized the recent achievements made in the emerging omics technologies to tackle the black rot challenge in B. oleracea. With an integrated approach of the omics technologies such as genomics, proteomics, transcriptomics, and metabolomics, it would allow better understanding of the complex molecular mechanisms underlying black rot resistance. Due to the availability of sequencing data, genomics and transcriptomics have progressed as expected for black rot resistance, however, other omics approaches like proteomics and metabolomics are lagging behind, necessitating a holistic and targeted approach to address the complex questions of Xcc-Brassica interactions. Genomic studies revealed that the black rot resistance is a complex trait and is mostly controlled by quantitative trait locus (QTL) with minor effects. Transcriptomic analysis divulged the genes related to photosynthesis, glucosinolate biosynthesis and catabolism, phenylpropanoid biosynthesis pathway, ROS scavenging, calcium signalling, hormonal synthesis and signalling pathway are being differentially expressed upon Xcc infection. Comparative proteomic analysis in relation to susceptible and/or resistance interactions with Xcc identified the involvement of proteins related to photosynthesis, protein biosynthesis, processing and degradation, energy metabolism, innate immunity, redox homeostasis, and defence response and signalling pathways in Xcc–Brassica interaction. Specifically, most of the studies focused on the regulation of the photosynthesis-related proteins as a resistance response in both early and later stages of infection. Metabolomic studies suggested that glucosinolates (GSLs), especially aliphatic and indolic GSLs, its subsequent hydrolysis products, and defensive metabolites synthesized by jasmonic acid (JA)-mediated phenylpropanoid biosynthesis pathway are involved in disease resistance mechanisms against Xcc in Brassica species. Multi-omics analysis showed that JA signalling pathway is regulating resistance against hemibiotrophic pathogen like Xcc. So, the bonhomie between omics technologies and plant breeding is going to trigger major breakthroughs in the field of crop improvement by developing superior cultivars with broad-spectrum resistance. If multi-omics tools are implemented at the right scale, we may be able to achieve the maximum benefits from the minimum. In this review, we have also discussed the challenges, future prospects, and the way forward in the application of omics technologies to accelerate the breeding of B. oleracea for disease resistance. A deeper insight about the current knowledge on omics can offer promising results in the breeding of high-quality disease-resistant crops. Frontiers Media S.A. 2021-12-06 /pmc/articles/PMC8687090/ /pubmed/34938304 http://dx.doi.org/10.3389/fpls.2021.742553 Text en Copyright © 2021 Shaw, Shen, Wang, Sheng, Zhao, Yu and Gu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Shaw, Ranjan K.
Shen, Yusen
Wang, Jiansheng
Sheng, Xiaoguang
Zhao, Zhenqing
Yu, Huifang
Gu, Honghui
Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L.
title Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L.
title_full Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L.
title_fullStr Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L.
title_full_unstemmed Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L.
title_short Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L.
title_sort advances in multi-omics approaches for molecular breeding of black rot resistance in brassica oleracea l.
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8687090/
https://www.ncbi.nlm.nih.gov/pubmed/34938304
http://dx.doi.org/10.3389/fpls.2021.742553
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