Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress

Abstract Background Long non-coding RNAs (lncRNAs) play important roles in response to abiotic stresses in plants, by acting as cis- or trans-acting regulators of protein-coding genes. As a widely cultivated crop worldwide, maize is sensitive to salt stress particularly at the seedling stage. Howeve...

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Auteurs principaux: Peng Liu, Yinchao Zhang, Chaoying Zou, Cong Yang, Guangtang Pan, Langlang Ma, Yaou Shen
Format: Article
Langue:English
Publié: BMC 2022-01-01
Collection:BMC Genomics
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Accès en ligne:https://doi.org/10.1186/s12864-021-08286-7
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author Peng Liu
Yinchao Zhang
Chaoying Zou
Cong Yang
Guangtang Pan
Langlang Ma
Yaou Shen
author_facet Peng Liu
Yinchao Zhang
Chaoying Zou
Cong Yang
Guangtang Pan
Langlang Ma
Yaou Shen
author_sort Peng Liu
collection DOAJ
description Abstract Background Long non-coding RNAs (lncRNAs) play important roles in response to abiotic stresses in plants, by acting as cis- or trans-acting regulators of protein-coding genes. As a widely cultivated crop worldwide, maize is sensitive to salt stress particularly at the seedling stage. However, it is unclear how the expressions of protein-coding genes are affected by non-coding RNAs in maize responding to salt tolerance. Results The whole transcriptome sequencing was employed to investigate the differential lncRNAs and target transcripts responding to salt stress between two maize inbred lines with contrasting salt tolerance. We developed a flexible, user-friendly, and modular RNA analysis workflow, which facilitated the identification of lncRNAs and novel mRNAs from whole transcriptome data. Using the workflow, 12,817 lncRNAs and 8,320 novel mRNAs in maize seedling roots were identified and characterized. A total of 742 lncRNAs and 7,835 mRNAs were identified as salt stress-responsive transcripts. Moreover, we obtained 41 cis- and 81 trans-target mRNA for 88 of the lncRNAs. Among these target transcripts, 11 belonged to 7 transcription factor (TF) families including bHLH, C2H2, Hap3/NF-YB, HAS, MYB, WD40, and WRKY. The above 8,577 salt stress-responsive transcripts were further classified into 28 modules by weighted gene co-expression network analysis. In the salt-tolerant module, we constructed an interaction network containing 79 nodes and 3081 edges, which included 5 lncRNAs, 18 TFs and 56 functional transcripts (FTs). As a trans-acting regulator, the lncRNA MSTRG.8888.1 affected the expressions of some salt tolerance-relative FTs, including protein-serine/threonine phosphatase 2C and galactinol synthase 1, by regulating the expression of the bHLH TF. Conclusions The contrasting genetic backgrounds of the two inbred lines generated considerable variations in the expression abundance of lncRNAs and protein-coding transcripts. In the co-expression networks responding to salt stress, some TFs were targeted by the lncRNAs, which further regulated the salt tolerance-related functional transcripts. We constructed a regulatory pathway of maize seedlings to salt stress, which was mediated by the hub lncRNA MSTRG.8888.1 and participated by the bHLH TF and its downstream target transcripts. Future work will be focused on the functional revelation of the regulatory pathway.
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spelling doaj.art-0c0a4750ba0341dd9cf8c9c13e3b5c2c2022-12-22T04:09:14ZengBMCBMC Genomics1471-21642022-01-0123111610.1186/s12864-021-08286-7Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stressPeng Liu0Yinchao Zhang1Chaoying Zou2Cong Yang3Guangtang Pan4Langlang Ma5Yaou Shen6State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Maize Research Institute, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Maize Research Institute, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Maize Research Institute, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Maize Research Institute, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Maize Research Institute, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Maize Research Institute, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Maize Research Institute, Sichuan Agricultural UniversityAbstract Background Long non-coding RNAs (lncRNAs) play important roles in response to abiotic stresses in plants, by acting as cis- or trans-acting regulators of protein-coding genes. As a widely cultivated crop worldwide, maize is sensitive to salt stress particularly at the seedling stage. However, it is unclear how the expressions of protein-coding genes are affected by non-coding RNAs in maize responding to salt tolerance. Results The whole transcriptome sequencing was employed to investigate the differential lncRNAs and target transcripts responding to salt stress between two maize inbred lines with contrasting salt tolerance. We developed a flexible, user-friendly, and modular RNA analysis workflow, which facilitated the identification of lncRNAs and novel mRNAs from whole transcriptome data. Using the workflow, 12,817 lncRNAs and 8,320 novel mRNAs in maize seedling roots were identified and characterized. A total of 742 lncRNAs and 7,835 mRNAs were identified as salt stress-responsive transcripts. Moreover, we obtained 41 cis- and 81 trans-target mRNA for 88 of the lncRNAs. Among these target transcripts, 11 belonged to 7 transcription factor (TF) families including bHLH, C2H2, Hap3/NF-YB, HAS, MYB, WD40, and WRKY. The above 8,577 salt stress-responsive transcripts were further classified into 28 modules by weighted gene co-expression network analysis. In the salt-tolerant module, we constructed an interaction network containing 79 nodes and 3081 edges, which included 5 lncRNAs, 18 TFs and 56 functional transcripts (FTs). As a trans-acting regulator, the lncRNA MSTRG.8888.1 affected the expressions of some salt tolerance-relative FTs, including protein-serine/threonine phosphatase 2C and galactinol synthase 1, by regulating the expression of the bHLH TF. Conclusions The contrasting genetic backgrounds of the two inbred lines generated considerable variations in the expression abundance of lncRNAs and protein-coding transcripts. In the co-expression networks responding to salt stress, some TFs were targeted by the lncRNAs, which further regulated the salt tolerance-related functional transcripts. We constructed a regulatory pathway of maize seedlings to salt stress, which was mediated by the hub lncRNA MSTRG.8888.1 and participated by the bHLH TF and its downstream target transcripts. Future work will be focused on the functional revelation of the regulatory pathway.https://doi.org/10.1186/s12864-021-08286-7MaizeSalt stresslncRNATFsProtein-coding transcriptWGCNA
spellingShingle Peng Liu
Yinchao Zhang
Chaoying Zou
Cong Yang
Guangtang Pan
Langlang Ma
Yaou Shen
Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress
BMC Genomics
Maize
Salt stress
lncRNA
TFs
Protein-coding transcript
WGCNA
title Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress
title_full Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress
title_fullStr Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress
title_full_unstemmed Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress
title_short Integrated analysis of long non-coding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress
title_sort integrated analysis of long non coding rnas and mrnas reveals the regulatory network of maize seedling root responding to salt stress
topic Maize
Salt stress
lncRNA
TFs
Protein-coding transcript
WGCNA
url https://doi.org/10.1186/s12864-021-08286-7
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