<i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf Blight

The rapid evolution of pathogens and the limited genetic diversity of hosts are two major factors contributing to the plant pathogenic phenomenon known as the loss of disease resistance in maize (<i>Zea mays</i> L.). It has emerged as a significant biological stressor threatening the glo...

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Main Authors: Bo Su, Xiaolan Yang, Rui Zhang, Shijie Dong, Ying Liu, Hubiao Jiang, Guichun Wu, Ting Ding
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Current Issues in Molecular Biology
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Online Access:https://www.mdpi.com/1467-3045/47/7/573
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author Bo Su
Xiaolan Yang
Rui Zhang
Shijie Dong
Ying Liu
Hubiao Jiang
Guichun Wu
Ting Ding
author_facet Bo Su
Xiaolan Yang
Rui Zhang
Shijie Dong
Ying Liu
Hubiao Jiang
Guichun Wu
Ting Ding
author_sort Bo Su
collection DOAJ
description The rapid evolution of pathogens and the limited genetic diversity of hosts are two major factors contributing to the plant pathogenic phenomenon known as the loss of disease resistance in maize (<i>Zea mays</i> L.). It has emerged as a significant biological stressor threatening the global food supplies and security. Based on previous cross-species homologous gene screening assays conducted in the laboratory, this study identified the maize disease-resistance candidate gene <i>ZmNLR-7</i> to investigate the maize immune regulation mechanism against <i>Bipolaris maydis</i>. Subcellular localization assays confirmed that the ZmNLR-7 protein is localized in the plasma membrane and nucleus, and phylogenetic analysis revealed that it contains a conserved NB-ARC domain. Analysis of tissue expression patterns revealed that <i>ZmNLR-7</i> was expressed in all maize tissues, with the highest expression level (5.11 times) exhibited in the leaves, and that its transcription level peaked at 11.92 times 48 h post <i>Bipolaris maydis</i> infection. Upon inoculating the <i>ZmNLR-7</i> EMS mutants with <i>Bipolaris maydis</i>, the disease index was increased to 33.89 and 43.33, respectively, and the lesion expansion rate was higher than that in the wild type, indicating enhanced susceptibility to southern corn leaf blight. Physiological index measurements revealed a disturbance of ROS metabolism in <i>ZmNLR-7</i> EMS mutants, with SOD activity decreased by approximately 30% and 55%, and POD activity decreased by 18% and 22%. Moreover, H<sub>2</sub>O<sub>2</sub> content decreased, while lipid peroxide MDA accumulation increased. Transcriptomic analysis revealed a significant inhibition of the expression of the key genes <i>NPR1</i> and <i>ACS6</i> in the SA/ET signaling pathway and a decrease in the expression of disease-related genes <i>ERF1</i> and <i>PR1</i>. This study established a new paradigm for the study of NLR protein-mediated plant immune mechanisms and provided target genes for molecular breeding of disease resistance in maize. Overall, these findings provide the first evidence that <i>ZmNLR-7</i> confers resistance to southern corn leaf blight in maize by synergistically regulating ROS homeostasis, SA/ET signal transduction, and downstream defense gene expression networks.
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spelling doaj-art-754994b2a8b74c1389f46a43d8cc151b2025-08-20T03:58:31ZengMDPI AGCurrent Issues in Molecular Biology1467-30371467-30452025-07-0147757310.3390/cimb47070573<i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf BlightBo Su0Xiaolan Yang1Rui Zhang2Shijie Dong3Ying Liu4Hubiao Jiang5Guichun Wu6Ting Ding7School of Plant Protection, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, Anhui Agricultural University, Anhui Province Key Laboratory of Integrated Pest Management on Crops, Hefei 230036, ChinaSchool of Plant Protection, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, Anhui Agricultural University, Anhui Province Key Laboratory of Integrated Pest Management on Crops, Hefei 230036, ChinaSchool of Plant Protection, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, Anhui Agricultural University, Anhui Province Key Laboratory of Integrated Pest Management on Crops, Hefei 230036, ChinaSchool of Plant Protection, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, Anhui Agricultural University, Anhui Province Key Laboratory of Integrated Pest Management on Crops, Hefei 230036, ChinaSchool of Plant Protection, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, Anhui Agricultural University, Anhui Province Key Laboratory of Integrated Pest Management on Crops, Hefei 230036, ChinaSchool of Plant Protection, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, Anhui Agricultural University, Anhui Province Key Laboratory of Integrated Pest Management on Crops, Hefei 230036, ChinaNational Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural University, Hefei 230036, ChinaSchool of Plant Protection, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, Anhui Agricultural University, Anhui Province Key Laboratory of Integrated Pest Management on Crops, Hefei 230036, ChinaThe rapid evolution of pathogens and the limited genetic diversity of hosts are two major factors contributing to the plant pathogenic phenomenon known as the loss of disease resistance in maize (<i>Zea mays</i> L.). It has emerged as a significant biological stressor threatening the global food supplies and security. Based on previous cross-species homologous gene screening assays conducted in the laboratory, this study identified the maize disease-resistance candidate gene <i>ZmNLR-7</i> to investigate the maize immune regulation mechanism against <i>Bipolaris maydis</i>. Subcellular localization assays confirmed that the ZmNLR-7 protein is localized in the plasma membrane and nucleus, and phylogenetic analysis revealed that it contains a conserved NB-ARC domain. Analysis of tissue expression patterns revealed that <i>ZmNLR-7</i> was expressed in all maize tissues, with the highest expression level (5.11 times) exhibited in the leaves, and that its transcription level peaked at 11.92 times 48 h post <i>Bipolaris maydis</i> infection. Upon inoculating the <i>ZmNLR-7</i> EMS mutants with <i>Bipolaris maydis</i>, the disease index was increased to 33.89 and 43.33, respectively, and the lesion expansion rate was higher than that in the wild type, indicating enhanced susceptibility to southern corn leaf blight. Physiological index measurements revealed a disturbance of ROS metabolism in <i>ZmNLR-7</i> EMS mutants, with SOD activity decreased by approximately 30% and 55%, and POD activity decreased by 18% and 22%. Moreover, H<sub>2</sub>O<sub>2</sub> content decreased, while lipid peroxide MDA accumulation increased. Transcriptomic analysis revealed a significant inhibition of the expression of the key genes <i>NPR1</i> and <i>ACS6</i> in the SA/ET signaling pathway and a decrease in the expression of disease-related genes <i>ERF1</i> and <i>PR1</i>. This study established a new paradigm for the study of NLR protein-mediated plant immune mechanisms and provided target genes for molecular breeding of disease resistance in maize. Overall, these findings provide the first evidence that <i>ZmNLR-7</i> confers resistance to southern corn leaf blight in maize by synergistically regulating ROS homeostasis, SA/ET signal transduction, and downstream defense gene expression networks.https://www.mdpi.com/1467-3045/47/7/573<i>ZmNLR-7</i>maize<i>Bipolaris maydis</i>plant disease susceptibility
spellingShingle Bo Su
Xiaolan Yang
Rui Zhang
Shijie Dong
Ying Liu
Hubiao Jiang
Guichun Wu
Ting Ding
<i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf Blight
Current Issues in Molecular Biology
<i>ZmNLR-7</i>
maize
<i>Bipolaris maydis</i>
plant disease susceptibility
title <i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf Blight
title_full <i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf Blight
title_fullStr <i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf Blight
title_full_unstemmed <i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf Blight
title_short <i>ZmNLR</i><i>-7</i>-Mediated Synergistic Regulation of ROS, Hormonal Signaling, and Defense Gene Networks Drives Maize Immunity to Southern Corn Leaf Blight
title_sort i zmnlr i i 7 i mediated synergistic regulation of ros hormonal signaling and defense gene networks drives maize immunity to southern corn leaf blight
topic <i>ZmNLR-7</i>
maize
<i>Bipolaris maydis</i>
plant disease susceptibility
url https://www.mdpi.com/1467-3045/47/7/573
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