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Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet

Downy mildew of foxtail millet is an important oomycete disease caused by Sclerospora graminicola, affecting the yield and quality of the crop. Foxtail millet infected with S. graminicola exhibit symptoms of leaf yellowing and leaf cracking. To uncover the pathogenic mechanism of this disease, we ex...

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Autores principales: Zhang, Baojun, Liu, Xu, Sun, Yurong, Xu, Lin, Ren, Zhixian, Zhao, Yaofei, Han, Yuanhuai
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9317951/
https://www.ncbi.nlm.nih.gov/pubmed/35903230
http://dx.doi.org/10.3389/fpls.2022.928040
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author Zhang, Baojun
Liu, Xu
Sun, Yurong
Xu, Lin
Ren, Zhixian
Zhao, Yaofei
Han, Yuanhuai
author_facet Zhang, Baojun
Liu, Xu
Sun, Yurong
Xu, Lin
Ren, Zhixian
Zhao, Yaofei
Han, Yuanhuai
author_sort Zhang, Baojun
collection PubMed
description Downy mildew of foxtail millet is an important oomycete disease caused by Sclerospora graminicola, affecting the yield and quality of the crop. Foxtail millet infected with S. graminicola exhibit symptoms of leaf yellowing and leaf cracking. To uncover the pathogenic mechanism of this disease, we explored the effects on chlorophyll synthesis and photosynthesis of foxtail millet leaves infected by S. graminicola. An elite foxtail millet variety, JG21, susceptible to S. graminicola, was used as for this study. S. graminicola inhibited chlorophyll synthesis and caused loose mesophyll cell arrangement. In addition, some cells were severely vacuolated in S. graminicola-infected foxtail millet leaves at the early stages of infection. S. graminicola could invade the mesophyll cells through haustoria which destroyed the chloroplast structure at the middle stages of infection causing significant accumulation of osmiophilic particles (OPs) and disintegrated chloroplast grana lamellae. Furthermore, foxtail millet leaves split longitudinally at the later stages of infection. Chlorophyll and carotenoid contents in infected leaves decreased significantly compared with those in the control. Net photosynthetic rate (Pn) of leaves and stomatal conductance showed a downward trend, and intercellular carbon dioxide concentrations increased significantly following the infection with S. graminicola. A total of 1,618 differentially expressed genes (DEGs) were detected between the control group and the treatment groups using RNA sequencing (RNA-Seq) among S1–S5 stages. DEGs associated with “photosynthesis” and “light reaction” were enriched. Gene expression patterns showed that 91.3% of 23 genes related to chlorophyll synthesis and photosynthesis, were significantly down-regulated than the control during S1–S5 stages. Based on the gene expression dataset, weighed gene co-expression network analysis (WGCNA) with 19 gene co-expression modules related to photosynthesis revealed six hub genes related to chlorophyll synthesis, which were suppressed during infection. The results suggest that infection of S. graminicola led to weak chlorophyll synthesis and rapid chloroplasts disappearance in foxtail millet. The defense responses and resistance of foxtail millet to S. graminicola were inhibited because chloroplast structure and function were destroyed in leaves, and the sexual reproduction in S. graminicola could be completed rapidly.
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spelling pubmed-93179512022-07-27 Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet Zhang, Baojun Liu, Xu Sun, Yurong Xu, Lin Ren, Zhixian Zhao, Yaofei Han, Yuanhuai Front Plant Sci Plant Science Downy mildew of foxtail millet is an important oomycete disease caused by Sclerospora graminicola, affecting the yield and quality of the crop. Foxtail millet infected with S. graminicola exhibit symptoms of leaf yellowing and leaf cracking. To uncover the pathogenic mechanism of this disease, we explored the effects on chlorophyll synthesis and photosynthesis of foxtail millet leaves infected by S. graminicola. An elite foxtail millet variety, JG21, susceptible to S. graminicola, was used as for this study. S. graminicola inhibited chlorophyll synthesis and caused loose mesophyll cell arrangement. In addition, some cells were severely vacuolated in S. graminicola-infected foxtail millet leaves at the early stages of infection. S. graminicola could invade the mesophyll cells through haustoria which destroyed the chloroplast structure at the middle stages of infection causing significant accumulation of osmiophilic particles (OPs) and disintegrated chloroplast grana lamellae. Furthermore, foxtail millet leaves split longitudinally at the later stages of infection. Chlorophyll and carotenoid contents in infected leaves decreased significantly compared with those in the control. Net photosynthetic rate (Pn) of leaves and stomatal conductance showed a downward trend, and intercellular carbon dioxide concentrations increased significantly following the infection with S. graminicola. A total of 1,618 differentially expressed genes (DEGs) were detected between the control group and the treatment groups using RNA sequencing (RNA-Seq) among S1–S5 stages. DEGs associated with “photosynthesis” and “light reaction” were enriched. Gene expression patterns showed that 91.3% of 23 genes related to chlorophyll synthesis and photosynthesis, were significantly down-regulated than the control during S1–S5 stages. Based on the gene expression dataset, weighed gene co-expression network analysis (WGCNA) with 19 gene co-expression modules related to photosynthesis revealed six hub genes related to chlorophyll synthesis, which were suppressed during infection. The results suggest that infection of S. graminicola led to weak chlorophyll synthesis and rapid chloroplasts disappearance in foxtail millet. The defense responses and resistance of foxtail millet to S. graminicola were inhibited because chloroplast structure and function were destroyed in leaves, and the sexual reproduction in S. graminicola could be completed rapidly. Frontiers Media S.A. 2022-07-12 /pmc/articles/PMC9317951/ /pubmed/35903230 http://dx.doi.org/10.3389/fpls.2022.928040 Text en Copyright © 2022 Zhang, Liu, Sun, Xu, Ren, Zhao and Han. 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
Zhang, Baojun
Liu, Xu
Sun, Yurong
Xu, Lin
Ren, Zhixian
Zhao, Yaofei
Han, Yuanhuai
Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet
title Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet
title_full Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet
title_fullStr Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet
title_full_unstemmed Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet
title_short Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet
title_sort sclerospora graminicola suppresses plant defense responses by disrupting chlorophyll biosynthesis and photosynthesis in foxtail millet
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9317951/
https://www.ncbi.nlm.nih.gov/pubmed/35903230
http://dx.doi.org/10.3389/fpls.2022.928040
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