Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>

Salinization of soil is a major environmental risk factor to plant functions, leading to a reduction of productivity of crops and forage. <i>Epichloë gansuensis</i>, seed-borne endophytic fungi, establishes a mutualistic symbiotic relationship with <i>Achnatherum inebrians</i>...

Full description

Bibliographic Details
Main Authors: Chao Wang, Rong Huang, Jianfeng Wang, Jie Jin, Kamran Malik, Xueli Niu, Rong Tang, Wenpeng Hou, Chen Cheng, Yinglong Liu, Jie Liu
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/8/10/1092
_version_ 1797472227540598784
author Chao Wang
Rong Huang
Jianfeng Wang
Jie Jin
Kamran Malik
Xueli Niu
Rong Tang
Wenpeng Hou
Chen Cheng
Yinglong Liu
Jie Liu
author_facet Chao Wang
Rong Huang
Jianfeng Wang
Jie Jin
Kamran Malik
Xueli Niu
Rong Tang
Wenpeng Hou
Chen Cheng
Yinglong Liu
Jie Liu
author_sort Chao Wang
collection DOAJ
description Salinization of soil is a major environmental risk factor to plant functions, leading to a reduction of productivity of crops and forage. <i>Epichloë gansuensis</i>, seed-borne endophytic fungi, establishes a mutualistic symbiotic relationship with <i>Achnatherum inebrians</i> and confers salt tolerance in the host plants. In this study, analysis of transcriptome and metabolome was used to explore the potential molecular mechanism underlying the salt-adaptation of <i>A. inebrians</i> roots mediated by <i>E. gansuensis</i>. We found that <i>E. gansuensis</i> played an important role in the gene expression of the host’s roots and regulated multiple pathways involved in amino acid metabolism, carbohydrate metabolism, TCA cycle, secondary metabolism, and lipid metabolism in the roots of <i>A. inebrians</i>. Importantly, <i>E. gansuensis</i> significantly induced the biological processes, including exocytosis, glycolytic process, fructose metabolic process, and potassium ion transport in roots of host plants at transcriptional levels, and altered the pathways, including inositol phosphate metabolism, galactose metabolism, starch, and sucrose metabolism at metabolite levels under NaCl stress. These findings provided insight into the molecular mechanism of salt resistance in roots of <i>A. inebrians</i> mediated by <i>E. gansuensis</i> and could drive progress in the cultivation of new salt-resistance breeds with endophytes.
first_indexed 2024-03-09T20:00:09Z
format Article
id doaj.art-8fee66308fac4c8aba5dbbd4735d9aa5
institution Directory Open Access Journal
issn 2309-608X
language English
last_indexed 2024-03-09T20:00:09Z
publishDate 2022-10-01
publisher MDPI AG
record_format Article
series Journal of Fungi
spelling doaj.art-8fee66308fac4c8aba5dbbd4735d9aa52023-11-24T00:47:49ZengMDPI AGJournal of Fungi2309-608X2022-10-01810109210.3390/jof8101092Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>Chao Wang0Rong Huang1Jianfeng Wang2Jie Jin3Kamran Malik4Xueli Niu5Rong Tang6Wenpeng Hou7Chen Cheng8Yinglong Liu9Jie Liu10State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaSchool of Life Science and Technology, Lingnan Normal University, Zhanjiang 524048, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, Center for Grassland Microbiome, Collaborative Innovation Center for Western Ecological Safety, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, ChinaSalinization of soil is a major environmental risk factor to plant functions, leading to a reduction of productivity of crops and forage. <i>Epichloë gansuensis</i>, seed-borne endophytic fungi, establishes a mutualistic symbiotic relationship with <i>Achnatherum inebrians</i> and confers salt tolerance in the host plants. In this study, analysis of transcriptome and metabolome was used to explore the potential molecular mechanism underlying the salt-adaptation of <i>A. inebrians</i> roots mediated by <i>E. gansuensis</i>. We found that <i>E. gansuensis</i> played an important role in the gene expression of the host’s roots and regulated multiple pathways involved in amino acid metabolism, carbohydrate metabolism, TCA cycle, secondary metabolism, and lipid metabolism in the roots of <i>A. inebrians</i>. Importantly, <i>E. gansuensis</i> significantly induced the biological processes, including exocytosis, glycolytic process, fructose metabolic process, and potassium ion transport in roots of host plants at transcriptional levels, and altered the pathways, including inositol phosphate metabolism, galactose metabolism, starch, and sucrose metabolism at metabolite levels under NaCl stress. These findings provided insight into the molecular mechanism of salt resistance in roots of <i>A. inebrians</i> mediated by <i>E. gansuensis</i> and could drive progress in the cultivation of new salt-resistance breeds with endophytes.https://www.mdpi.com/2309-608X/8/10/1092<i>Epichloë gansuensis</i>transcriptomemetabolomedifferentially expressed genesdifferentially expressed metabolitesalt tolerance
spellingShingle Chao Wang
Rong Huang
Jianfeng Wang
Jie Jin
Kamran Malik
Xueli Niu
Rong Tang
Wenpeng Hou
Chen Cheng
Yinglong Liu
Jie Liu
Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>
Journal of Fungi
<i>Epichloë gansuensis</i>
transcriptome
metabolome
differentially expressed genes
differentially expressed metabolite
salt tolerance
title Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>
title_full Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>
title_fullStr Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>
title_full_unstemmed Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>
title_short Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of <i>Achnatherum inebrians</i> Mediated by <i>Epichloë gansuensis</i>
title_sort comprehensive analysis of transcriptome and metabolome elucidates the molecular regulatory mechanism of salt resistance in roots of i achnatherum inebrians i mediated by i epichloe gansuensis i
topic <i>Epichloë gansuensis</i>
transcriptome
metabolome
differentially expressed genes
differentially expressed metabolite
salt tolerance
url https://www.mdpi.com/2309-608X/8/10/1092
work_keys_str_mv AT chaowang comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT ronghuang comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT jianfengwang comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT jiejin comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT kamranmalik comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT xueliniu comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT rongtang comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT wenpenghou comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT chencheng comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT yinglongliu comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi
AT jieliu comprehensiveanalysisoftranscriptomeandmetabolomeelucidatesthemolecularregulatorymechanismofsaltresistanceinrootsofiachnatheruminebriansimediatedbyiepichloegansuensisi