Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic Diazotroph

Some sugarcane germplasms can absorb higher amounts of nitrogen via atmospheric nitrogen fixation through the bacterial diazotrophs. Most endophytic diazotrophs usually penetrate through the root, colonize inside the plant, and fix the nitrogen. To assess the plant’s bacterial association during roo...

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Main Authors: Qian Nong, Mukesh Kumar Malviya, Manoj Kumar Solanki, Anjali Chandrol Solanki, Li Lin, Jinlan Xie, Zhanghong Mo, Zeping Wang, Xiu-Peng Song, Xin Huang, Shalini Rai, Changning Li, Yang-Rui Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.924283/full
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author Qian Nong
Qian Nong
Mukesh Kumar Malviya
Manoj Kumar Solanki
Anjali Chandrol Solanki
Li Lin
Jinlan Xie
Zhanghong Mo
Zeping Wang
Xiu-Peng Song
Xin Huang
Shalini Rai
Changning Li
Yang-Rui Li
author_facet Qian Nong
Qian Nong
Mukesh Kumar Malviya
Manoj Kumar Solanki
Anjali Chandrol Solanki
Li Lin
Jinlan Xie
Zhanghong Mo
Zeping Wang
Xiu-Peng Song
Xin Huang
Shalini Rai
Changning Li
Yang-Rui Li
author_sort Qian Nong
collection DOAJ
description Some sugarcane germplasms can absorb higher amounts of nitrogen via atmospheric nitrogen fixation through the bacterial diazotrophs. Most endophytic diazotrophs usually penetrate through the root, colonize inside the plant, and fix the nitrogen. To assess the plant’s bacterial association during root colonization, strain GXS16 was tagged with a plasmid-bear green fluorescent protein (GFP) gene. The results demonstrated that the strain can colonize roots all the way to the maturation zone. The strain GXS16 showed maximum nitrogenase enzyme activity at pH 8 and 30°C, and nitrogenase activity is less affected by different carbon sources. Further, strain GXS16 colonization response was investigated through plant hormones analysis and RNAseq. The results showed that the bacterial colonization gradually increased with time, and the H2O2 and malondialdehyde (MDA) content significantly increased at 1 day after inoculation. There were no substantial changes noticed in proline content, and the ethylene content was detected initially, but it decreased with time. The abscisic acid (ABA) content showed significant increases of 91.9, 43.9, and 18.7%, but conversely, the gibberellin (GA3) content decreased by 12.9, 28.5, and 45.2% at 1, 3, and 5 days after inoculation, respectively. The GXS16 inoculation significantly increased the activities of catalase (CAT), superoxide dismutase (SOD), polyphenol oxidase (PPO), ascorbate peroxidase (APX), and glutathione reductase (GR) at different timepoint. In contrast, the peroxisome (POD) activity had no changes detected during the treatment. In the case of RNAseq analysis, 2437, 6678, and 4568 differentially expressed genes (DEGs) were identified from 1, 3, and 5 days inoculated root samples, and 601 DEGs were shared in all samples. The number or the expression diversity of DEGs related to ethylene was much higher than that of ABA or GA, which indicated the critical role of ethylene in regulating the sugarcane roots response to GXS16 inoculation.
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spelling doaj.art-8e2fae9caa75499db6a08992a09085b52022-12-22T02:33:36ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-06-011310.3389/fmicb.2022.924283924283Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic DiazotrophQian Nong0Qian Nong1Mukesh Kumar Malviya2Manoj Kumar Solanki3Anjali Chandrol Solanki4Li Lin5Jinlan Xie6Zhanghong Mo7Zeping Wang8Xiu-Peng Song9Xin Huang10Shalini Rai11Changning Li12Yang-Rui Li13Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaPlant Protection Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaPlant Cytogenetics and Molecular Biology Group, Institute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, Katowice, PolandDepartment of Agriculture Science, Mansarovar Global University, Bhopal, IndiaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaDepartment of Biotechnology, Society of Higher Education and Practical Application (SHEPA), Varanasi, IndiaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaKey Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Sugarcane Research Center, Chinese Academy of Agricultural Sciences, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaSome sugarcane germplasms can absorb higher amounts of nitrogen via atmospheric nitrogen fixation through the bacterial diazotrophs. Most endophytic diazotrophs usually penetrate through the root, colonize inside the plant, and fix the nitrogen. To assess the plant’s bacterial association during root colonization, strain GXS16 was tagged with a plasmid-bear green fluorescent protein (GFP) gene. The results demonstrated that the strain can colonize roots all the way to the maturation zone. The strain GXS16 showed maximum nitrogenase enzyme activity at pH 8 and 30°C, and nitrogenase activity is less affected by different carbon sources. Further, strain GXS16 colonization response was investigated through plant hormones analysis and RNAseq. The results showed that the bacterial colonization gradually increased with time, and the H2O2 and malondialdehyde (MDA) content significantly increased at 1 day after inoculation. There were no substantial changes noticed in proline content, and the ethylene content was detected initially, but it decreased with time. The abscisic acid (ABA) content showed significant increases of 91.9, 43.9, and 18.7%, but conversely, the gibberellin (GA3) content decreased by 12.9, 28.5, and 45.2% at 1, 3, and 5 days after inoculation, respectively. The GXS16 inoculation significantly increased the activities of catalase (CAT), superoxide dismutase (SOD), polyphenol oxidase (PPO), ascorbate peroxidase (APX), and glutathione reductase (GR) at different timepoint. In contrast, the peroxisome (POD) activity had no changes detected during the treatment. In the case of RNAseq analysis, 2437, 6678, and 4568 differentially expressed genes (DEGs) were identified from 1, 3, and 5 days inoculated root samples, and 601 DEGs were shared in all samples. The number or the expression diversity of DEGs related to ethylene was much higher than that of ABA or GA, which indicated the critical role of ethylene in regulating the sugarcane roots response to GXS16 inoculation.https://www.frontiersin.org/articles/10.3389/fmicb.2022.924283/fullsugarcane rootphysiological functiongene expressionendophytic diazotrophinoculation
spellingShingle Qian Nong
Qian Nong
Mukesh Kumar Malviya
Manoj Kumar Solanki
Anjali Chandrol Solanki
Li Lin
Jinlan Xie
Zhanghong Mo
Zeping Wang
Xiu-Peng Song
Xin Huang
Shalini Rai
Changning Li
Yang-Rui Li
Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic Diazotroph
Frontiers in Microbiology
sugarcane root
physiological function
gene expression
endophytic diazotroph
inoculation
title Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic Diazotroph
title_full Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic Diazotroph
title_fullStr Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic Diazotroph
title_full_unstemmed Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic Diazotroph
title_short Sugarcane Root Transcriptome Analysis Revealed the Role of Plant Hormones in the Colonization of an Endophytic Diazotroph
title_sort sugarcane root transcriptome analysis revealed the role of plant hormones in the colonization of an endophytic diazotroph
topic sugarcane root
physiological function
gene expression
endophytic diazotroph
inoculation
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.924283/full
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