Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperatures

Fusarium verticillioides and Fusarium graminearum are important pathogens causing disease in maize (Zea mays) worldwide. The distributions of these fungal pathogens vary greatly in different regions and in different years, and are influenced by environmental and climatic conditions. Temperature has...

Full description

Bibliographic Details
Main Authors: Ning Liu, Yue Chen, Jing Liu, Qianfu Su, Bin Zhao, Manli Sun, Hui Jia, Zhiyan Cao, Jingao Dong
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1030523/full
_version_ 1797988029540859904
author Ning Liu
Ning Liu
Ning Liu
Yue Chen
Jing Liu
Qianfu Su
Bin Zhao
Bin Zhao
Bin Zhao
Manli Sun
Manli Sun
Manli Sun
Hui Jia
Zhiyan Cao
Zhiyan Cao
Zhiyan Cao
Jingao Dong
Jingao Dong
Jingao Dong
author_facet Ning Liu
Ning Liu
Ning Liu
Yue Chen
Jing Liu
Qianfu Su
Bin Zhao
Bin Zhao
Bin Zhao
Manli Sun
Manli Sun
Manli Sun
Hui Jia
Zhiyan Cao
Zhiyan Cao
Zhiyan Cao
Jingao Dong
Jingao Dong
Jingao Dong
author_sort Ning Liu
collection DOAJ
description Fusarium verticillioides and Fusarium graminearum are important pathogens causing disease in maize (Zea mays) worldwide. The distributions of these fungal pathogens vary greatly in different regions and in different years, and are influenced by environmental and climatic conditions. Temperature has significant effects on the growth and mycotoxin production of Fusarium species. In this study, the effects of temperature on the growth and pathogenicity of F. verticillioides and F. graminearum were investigated. F. verticillioides grew fastest and exhibited the strongest pathogenicity to maize stems and grains at 30°C, while F. graminearum grew best at 20°C. Both species produced more toxins at 20°C than at 30°C. To explain the interspecific differences in the relationship of growth and temperature, RNA-seq was used to compare F. verticillioides and F. graminearum cultivated for 4 d at the optimum temperatures of 30°C and 20°C, respectively. Samples of F. verticillioides were also cultivated for 9 d (to maximize toxin production) at 20°C and 30°C and analyzed by RNA-seq to investigate the influence of temperature for different growth stages. The differently expressed genes (DEGs) were identified by comparison of cultures grown for the same amount of time but at different temperatures. GO enrichment analysis showed high enrichment of DEGs in categories of membrane part, catalytic activity, metabolic process, and growth at warmer temperature resulted in more down-regulated DEGs enriched in membrane components in all groups. KEGG analysis revealed enrichment of DEGs related to different temperatures in carbohydrate and amino acid metabolism pathways. For both species, there was decreased expression of many DEGs related to amino acid metabolism when cultivated at warm temperature, such as genes related to beta-alanine metabolism and arginine and proline metabolism. However, changes in genes related to glyoxylate and dicarboxylate metabolism and fatty acid degradation were more related to the growth state. The results showing different responses pattern of these pathways provides a foundation for further investigation of the molecular mechanisms underlying distinct thermal ecological niches of F. verticillioides and F. graminearum.
first_indexed 2024-04-11T07:56:13Z
format Article
id doaj.art-bf875ebebf734881816545e9cd5899e1
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-11T07:56:13Z
publishDate 2022-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-bf875ebebf734881816545e9cd5899e12022-12-22T04:35:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-12-011310.3389/fmicb.2022.10305231030523Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperaturesNing Liu0Ning Liu1Ning Liu2Yue Chen3Jing Liu4Qianfu Su5Bin Zhao6Bin Zhao7Bin Zhao8Manli Sun9Manli Sun10Manli Sun11Hui Jia12Zhiyan Cao13Zhiyan Cao14Zhiyan Cao15Jingao Dong16Jingao Dong17Jingao Dong18State Key Laboratory of North China Crop Improvement and Regulation, Baoding, ChinaHebei Key Laboratory of Plant Physiology and Molecular Pathology, Baoding, ChinaPlant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Agricultural University, Baoding, ChinaPlant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Agricultural University, Baoding, ChinaPlant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Agricultural University, Baoding, ChinaJilin Academy of Agricultural Sciences, Changchun, ChinaState Key Laboratory of North China Crop Improvement and Regulation, Baoding, ChinaHebei Key Laboratory of Plant Physiology and Molecular Pathology, Baoding, ChinaPlant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Agricultural University, Baoding, ChinaState Key Laboratory of North China Crop Improvement and Regulation, Baoding, ChinaHebei Key Laboratory of Plant Physiology and Molecular Pathology, Baoding, ChinaPlant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Agricultural University, Baoding, ChinaState Key Laboratory of North China Crop Improvement and Regulation, Baoding, ChinaState Key Laboratory of North China Crop Improvement and Regulation, Baoding, ChinaHebei Key Laboratory of Plant Physiology and Molecular Pathology, Baoding, ChinaPlant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Agricultural University, Baoding, ChinaState Key Laboratory of North China Crop Improvement and Regulation, Baoding, ChinaHebei Key Laboratory of Plant Physiology and Molecular Pathology, Baoding, ChinaPlant Pathogenic Mycotoxin and Molecular Plant Pathology Laboratory, Hebei Agricultural University, Baoding, ChinaFusarium verticillioides and Fusarium graminearum are important pathogens causing disease in maize (Zea mays) worldwide. The distributions of these fungal pathogens vary greatly in different regions and in different years, and are influenced by environmental and climatic conditions. Temperature has significant effects on the growth and mycotoxin production of Fusarium species. In this study, the effects of temperature on the growth and pathogenicity of F. verticillioides and F. graminearum were investigated. F. verticillioides grew fastest and exhibited the strongest pathogenicity to maize stems and grains at 30°C, while F. graminearum grew best at 20°C. Both species produced more toxins at 20°C than at 30°C. To explain the interspecific differences in the relationship of growth and temperature, RNA-seq was used to compare F. verticillioides and F. graminearum cultivated for 4 d at the optimum temperatures of 30°C and 20°C, respectively. Samples of F. verticillioides were also cultivated for 9 d (to maximize toxin production) at 20°C and 30°C and analyzed by RNA-seq to investigate the influence of temperature for different growth stages. The differently expressed genes (DEGs) were identified by comparison of cultures grown for the same amount of time but at different temperatures. GO enrichment analysis showed high enrichment of DEGs in categories of membrane part, catalytic activity, metabolic process, and growth at warmer temperature resulted in more down-regulated DEGs enriched in membrane components in all groups. KEGG analysis revealed enrichment of DEGs related to different temperatures in carbohydrate and amino acid metabolism pathways. For both species, there was decreased expression of many DEGs related to amino acid metabolism when cultivated at warm temperature, such as genes related to beta-alanine metabolism and arginine and proline metabolism. However, changes in genes related to glyoxylate and dicarboxylate metabolism and fatty acid degradation were more related to the growth state. The results showing different responses pattern of these pathways provides a foundation for further investigation of the molecular mechanisms underlying distinct thermal ecological niches of F. verticillioides and F. graminearum.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1030523/fullFusarium verticillioidesFusarium graminearumoptimum temperaturetranscriptome analysisthermal ecological niches
spellingShingle Ning Liu
Ning Liu
Ning Liu
Yue Chen
Jing Liu
Qianfu Su
Bin Zhao
Bin Zhao
Bin Zhao
Manli Sun
Manli Sun
Manli Sun
Hui Jia
Zhiyan Cao
Zhiyan Cao
Zhiyan Cao
Jingao Dong
Jingao Dong
Jingao Dong
Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperatures
Frontiers in Microbiology
Fusarium verticillioides
Fusarium graminearum
optimum temperature
transcriptome analysis
thermal ecological niches
title Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperatures
title_full Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperatures
title_fullStr Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperatures
title_full_unstemmed Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperatures
title_short Transcriptional differences between major Fusarium pathogens of maize, Fusarium verticillioides and Fusarium graminearum with different optimum growth temperatures
title_sort transcriptional differences between major fusarium pathogens of maize fusarium verticillioides and fusarium graminearum with different optimum growth temperatures
topic Fusarium verticillioides
Fusarium graminearum
optimum temperature
transcriptome analysis
thermal ecological niches
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1030523/full
work_keys_str_mv AT ningliu transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT ningliu transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT ningliu transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT yuechen transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT jingliu transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT qianfusu transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT binzhao transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT binzhao transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT binzhao transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT manlisun transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT manlisun transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT manlisun transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT huijia transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT zhiyancao transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT zhiyancao transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT zhiyancao transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT jingaodong transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT jingaodong transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures
AT jingaodong transcriptionaldifferencesbetweenmajorfusariumpathogensofmaizefusariumverticillioidesandfusariumgraminearumwithdifferentoptimumgrowthtemperatures