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Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize

BACKGROUND: Plant respiratory burst oxidase homolog (Rboh) gene family produces reactive oxygen species (ROS), and it plays key roles in plant–microbe interaction. Most Rboh gene family-related studies mainly focused on dicotyledonous plants; however, little is known about the roles of Rboh genes in...

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Autores principales: Wu, Fulang, Zhao, Manli, Zhang, Yajing, Si, Weina, Cheng, Beijiu, Li, Xiaoyu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10688149/
https://www.ncbi.nlm.nih.gov/pubmed/38030972
http://dx.doi.org/10.1186/s12870-023-04571-7
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author Wu, Fulang
Zhao, Manli
Zhang, Yajing
Si, Weina
Cheng, Beijiu
Li, Xiaoyu
author_facet Wu, Fulang
Zhao, Manli
Zhang, Yajing
Si, Weina
Cheng, Beijiu
Li, Xiaoyu
author_sort Wu, Fulang
collection PubMed
description BACKGROUND: Plant respiratory burst oxidase homolog (Rboh) gene family produces reactive oxygen species (ROS), and it plays key roles in plant–microbe interaction. Most Rboh gene family-related studies mainly focused on dicotyledonous plants; however, little is known about the roles of Rboh genes in gramineae. RESULTS: A total of 106 Rboh genes were identified in seven gramineae species, including Zea mays, Sorghum bicolor, Brachypodium distachyon, Oryza sativa, Setaria italica, Hordeum vulgare, and Triticum aestivum. The Rboh protein sequences showed high similarities, suggesting that they may have conserved functions across different species. Duplication mode analysis detected whole-genome/segmental duplication (WGD)/(SD) and dispersed in the seven species. Interestingly, two local duplication (LD, including tandem and proximal duplication) modes were found in Z. mays, S. italica and H. vulgare, while four LD were detected in T. aestivum, indicating that these genes may have similar functions. Collinearity analysis indicated that Rboh genes are at a stable evolution state in all the seven species. Besides, Rboh genes from Z. mays were closely related to those from S. bicolor, consistent with the current understanding of plant evolutionary history. Phylogenetic analysis showed that the genes in the subgroups I and II may participate in plant-AM fungus symbiosis. Cis-element analysis showed that different numbers of elements are related to fungal induction in the promoter region. Expression profiles of Rboh genes in Z. mays suggested that Rboh genes had distinct spatial expression patterns. By inoculation with AM fungi, our transcriptome analysis showed that the expression of Rboh genes varies upon AM fungal inoculation. In particularly, ZmRbohF was significantly upregulated after inoculation with AM fungi. pZmRbohF::GUS expression analyses indicated that ZmRbohF was induced by arbuscular mycorrhizal fungi in maize. By comparing WT and ZmRbohF mutant, we found ZmRbohF had limited impact on the establishment of maize-AM fungi symbiosis, but play critical roles in regulating the proper development of arbuscules. CONCLUSIONS: This study provides a comprehensive analysis of the evolution relationship of Rboh genes in seven gramineae species. Results showed that several Rboh genes regulate maize-AM fungal symbiosis process. This study provides valuable information for further studies of Rboh genes in gramineae. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04571-7.
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spelling pubmed-106881492023-11-30 Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize Wu, Fulang Zhao, Manli Zhang, Yajing Si, Weina Cheng, Beijiu Li, Xiaoyu BMC Plant Biol Research BACKGROUND: Plant respiratory burst oxidase homolog (Rboh) gene family produces reactive oxygen species (ROS), and it plays key roles in plant–microbe interaction. Most Rboh gene family-related studies mainly focused on dicotyledonous plants; however, little is known about the roles of Rboh genes in gramineae. RESULTS: A total of 106 Rboh genes were identified in seven gramineae species, including Zea mays, Sorghum bicolor, Brachypodium distachyon, Oryza sativa, Setaria italica, Hordeum vulgare, and Triticum aestivum. The Rboh protein sequences showed high similarities, suggesting that they may have conserved functions across different species. Duplication mode analysis detected whole-genome/segmental duplication (WGD)/(SD) and dispersed in the seven species. Interestingly, two local duplication (LD, including tandem and proximal duplication) modes were found in Z. mays, S. italica and H. vulgare, while four LD were detected in T. aestivum, indicating that these genes may have similar functions. Collinearity analysis indicated that Rboh genes are at a stable evolution state in all the seven species. Besides, Rboh genes from Z. mays were closely related to those from S. bicolor, consistent with the current understanding of plant evolutionary history. Phylogenetic analysis showed that the genes in the subgroups I and II may participate in plant-AM fungus symbiosis. Cis-element analysis showed that different numbers of elements are related to fungal induction in the promoter region. Expression profiles of Rboh genes in Z. mays suggested that Rboh genes had distinct spatial expression patterns. By inoculation with AM fungi, our transcriptome analysis showed that the expression of Rboh genes varies upon AM fungal inoculation. In particularly, ZmRbohF was significantly upregulated after inoculation with AM fungi. pZmRbohF::GUS expression analyses indicated that ZmRbohF was induced by arbuscular mycorrhizal fungi in maize. By comparing WT and ZmRbohF mutant, we found ZmRbohF had limited impact on the establishment of maize-AM fungi symbiosis, but play critical roles in regulating the proper development of arbuscules. CONCLUSIONS: This study provides a comprehensive analysis of the evolution relationship of Rboh genes in seven gramineae species. Results showed that several Rboh genes regulate maize-AM fungal symbiosis process. This study provides valuable information for further studies of Rboh genes in gramineae. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04571-7. BioMed Central 2023-11-30 /pmc/articles/PMC10688149/ /pubmed/38030972 http://dx.doi.org/10.1186/s12870-023-04571-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wu, Fulang
Zhao, Manli
Zhang, Yajing
Si, Weina
Cheng, Beijiu
Li, Xiaoyu
Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize
title Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize
title_full Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize
title_fullStr Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize
title_full_unstemmed Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize
title_short Systematic analysis of the Rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize
title_sort systematic analysis of the rboh gene family in seven gramineous plants and its roles in response to arbuscular mycorrhizal fungi in maize
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10688149/
https://www.ncbi.nlm.nih.gov/pubmed/38030972
http://dx.doi.org/10.1186/s12870-023-04571-7
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