The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression

Summary Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the secondary salt damage by improper fertilization and irrigation. To expand the cultivation area of apple (Malus domestica) and select salt‐r...

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Published inPlant biotechnology journal Vol. 19; no. 2; pp. 311 - 323
Main Authors Ma, Yue, Xue, Hao, Zhang, Feng, Jiang, Qiu, Yang, Shuang, Yue, Pengtao, Wang, Feng, Zhang, Yuanyan, Li, Linguang, He, Ping, Zhang, Zhihong
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.02.2021
John Wiley and Sons Inc
Subjects
Abiotic stress
apple
Apples
biotechnology
Crop yield
Cultivation
cultivation area
Developmental stages
Embryogenesis
Embryonic growth stage
Empirical analysis
Fertilization
flowering
Flowers & plants
Fruit cultivation
Fruits
Gene expression
gene expression regulation
Gene Expression Regulation, Plant - genetics
genes
Genetic resources
Genetic transformation
irrigation
Kinases
Life cycles
Malus - genetics
Malus - metabolism
Malus domestica
microRNA
microRNA156
MicroRNAs
MicroRNAs - genetics
miRNA
Modules
Morphogenesis
Phylogenetics
Plant growth
Plant Proteins - genetics
Plant Proteins - metabolism
Plant resistance
Proteins
Salinity tolerance
Salt Stress
Salt tolerance
Salt Tolerance - genetics
sequence analysis
Sorghum
SQUAMOSA PROMOTER BINDING PROTEIN‐LIKE 13
Standard deviation
stress tolerance
Transcription factors
Transcription Factors - genetics
WRKY100
salt tolerance
apple
SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 13
WRKY100
microRNA156
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Abstract Summary Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the secondary salt damage by improper fertilization and irrigation. To expand the cultivation area of apple (Malus domestica) and select salt‐resistant varieties, the mechanism of salt tolerance in apple is necessary to be clarified. The miR156/SPL regulatory module plays key roles in embryogenesis, morphogenesis, life cycle stage transformation, flower formation and other processes. However, its roles in the mechanisms of salt tolerance are unknown. In order to elucidate the mechanism of 156/SPL regulating salt stress in apple, we performed RLM‐5’ RACE and stable genetic transformation technology to verify that both mdm‐MIR156a and MdSPL13 responded to salt stress in apple and that the latter was the target of the former. MIR156a overexpression weakened salt resistance in apple whereas MdSPL13 overexpression strengthened it. A total of 6094 differentially expressed genes relative to nontransgenic apple plants were found by RNA‐Seq analysis of MdSPL13OE. Further verification indicated that MdSPL13 targeted the MdWRKY100 gene promoter. Moreover, MdWRKY100 overexpression enhanced salt tolerance in apple. Our results revealed that the miR156/SPL module regulates salt tolerance by up‐regulating MdWRKY100 in apple. This study is the first to elucidate the mechanism underlying the miRNA network response to salt stress in apple and provides theoretical and empirical bases and genetic resources for the molecular breeding of salt tolerance in apple.
AbstractList Summary Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the secondary salt damage by improper fertilization and irrigation. To expand the cultivation area of apple (Malus domestica) and select salt‐resistant varieties, the mechanism of salt tolerance in apple is necessary to be clarified. The miR156/SPL regulatory module plays key roles in embryogenesis, morphogenesis, life cycle stage transformation, flower formation and other processes. However, its roles in the mechanisms of salt tolerance are unknown. In order to elucidate the mechanism of 156/SPL regulating salt stress in apple, we performed RLM‐5’ RACE and stable genetic transformation technology to verify that both mdm‐MIR156a and MdSPL13 responded to salt stress in apple and that the latter was the target of the former. MIR156a overexpression weakened salt resistance in apple whereas MdSPL13 overexpression strengthened it. A total of 6094 differentially expressed genes relative to nontransgenic apple plants were found by RNA‐Seq analysis of MdSPL13OE. Further verification indicated that MdSPL13 targeted the MdWRKY100 gene promoter. Moreover, MdWRKY100 overexpression enhanced salt tolerance in apple. Our results revealed that the miR156/SPL module regulates salt tolerance by up‐regulating MdWRKY100 in apple. This study is the first to elucidate the mechanism underlying the miRNA network response to salt stress in apple and provides theoretical and empirical bases and genetic resources for the molecular breeding of salt tolerance in apple.
Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the secondary salt damage by improper fertilization and irrigation. To expand the cultivation area of apple (Malus domestica) and select salt‐resistant varieties, the mechanism of salt tolerance in apple is necessary to be clarified. The miR156/SPL regulatory module plays key roles in embryogenesis, morphogenesis, life cycle stage transformation, flower formation and other processes. However, its roles in the mechanisms of salt tolerance are unknown. In order to elucidate the mechanism of 156/SPL regulating salt stress in apple, we performed RLM‐5’ RACE and stable genetic transformation technology to verify that both mdm‐MIR156a and MdSPL13 responded to salt stress in apple and that the latter was the target of the former. MIR156a overexpression weakened salt resistance in apple whereas MdSPL13 overexpression strengthened it. A total of 6094 differentially expressed genes relative to nontransgenic apple plants were found by RNA‐Seq analysis of MdSPL13OE. Further verification indicated that MdSPL13 targeted the MdWRKY100 gene promoter. Moreover, MdWRKY100 overexpression enhanced salt tolerance in apple. Our results revealed that the miR156/SPL module regulates salt tolerance by up‐regulating MdWRKY100 in apple. This study is the first to elucidate the mechanism underlying the miRNA network response to salt stress in apple and provides theoretical and empirical bases and genetic resources for the molecular breeding of salt tolerance in apple.
Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the secondary salt damage by improper fertilization and irrigation. To expand the cultivation area of apple ( Malus domestica ) and select salt‐resistant varieties, the mechanism of salt tolerance in apple is necessary to be clarified. The miR156/SPL regulatory module plays key roles in embryogenesis, morphogenesis, life cycle stage transformation, flower formation and other processes. However, its roles in the mechanisms of salt tolerance are unknown. In order to elucidate the mechanism of 156/SPL regulating salt stress in apple, we performed RLM‐5’ RACE and stable genetic transformation technology to verify that both mdm‐ MIR156a and MdSPL13 responded to salt stress in apple and that the latter was the target of the former. MIR156a overexpression weakened salt resistance in apple whereas MdSPL13 overexpression strengthened it. A total of 6094 differentially expressed genes relative to nontransgenic apple plants were found by RNA‐Seq analysis of MdSPL13OE. Further verification indicated that MdSPL13 targeted the MdWRKY100 gene promoter. Moreover, MdWRKY100 overexpression enhanced salt tolerance in apple. Our results revealed that the miR156/SPL module regulates salt tolerance by up‐regulating MdWRKY100 in apple. This study is the first to elucidate the mechanism underlying the miRNA network response to salt stress in apple and provides theoretical and empirical bases and genetic resources for the molecular breeding of salt tolerance in apple.
Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the secondary salt damage by improper fertilization and irrigation. To expand the cultivation area of apple (Malus domestica) and select salt-resistant varieties, the mechanism of salt tolerance in apple is necessary to be clarified. The miR156/SPL regulatory module plays key roles in embryogenesis, morphogenesis, life cycle stage transformation, flower formation and other processes. However, its roles in the mechanisms of salt tolerance are unknown. In order to elucidate the mechanism of 156/SPL regulating salt stress in apple, we performed RLM-5' RACE and stable genetic transformation technology to verify that both mdm-MIR156a and MdSPL13 responded to salt stress in apple and that the latter was the target of the former. MIR156a overexpression weakened salt resistance in apple whereas MdSPL13 overexpression strengthened it. A total of 6094 differentially expressed genes relative to nontransgenic apple plants were found by RNA-Seq analysis of MdSPL13OE. Further verification indicated that MdSPL13 targeted the MdWRKY100 gene promoter. Moreover, MdWRKY100 overexpression enhanced salt tolerance in apple. Our results revealed that the miR156/SPL module regulates salt tolerance by up-regulating MdWRKY100 in apple. This study is the first to elucidate the mechanism underlying the miRNA network response to salt stress in apple and provides theoretical and empirical bases and genetic resources for the molecular breeding of salt tolerance in apple.Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the secondary salt damage by improper fertilization and irrigation. To expand the cultivation area of apple (Malus domestica) and select salt-resistant varieties, the mechanism of salt tolerance in apple is necessary to be clarified. The miR156/SPL regulatory module plays key roles in embryogenesis, morphogenesis, life cycle stage transformation, flower formation and other processes. However, its roles in the mechanisms of salt tolerance are unknown. In order to elucidate the mechanism of 156/SPL regulating salt stress in apple, we performed RLM-5' RACE and stable genetic transformation technology to verify that both mdm-MIR156a and MdSPL13 responded to salt stress in apple and that the latter was the target of the former. MIR156a overexpression weakened salt resistance in apple whereas MdSPL13 overexpression strengthened it. A total of 6094 differentially expressed genes relative to nontransgenic apple plants were found by RNA-Seq analysis of MdSPL13OE. Further verification indicated that MdSPL13 targeted the MdWRKY100 gene promoter. Moreover, MdWRKY100 overexpression enhanced salt tolerance in apple. Our results revealed that the miR156/SPL module regulates salt tolerance by up-regulating MdWRKY100 in apple. This study is the first to elucidate the mechanism underlying the miRNA network response to salt stress in apple and provides theoretical and empirical bases and genetic resources for the molecular breeding of salt tolerance in apple.
Author Ma, Yue
Yang, Shuang
Yue, Pengtao
Jiang, Qiu
Zhang, Yuanyan
Zhang, Zhihong
Li, Linguang
He, Ping
Xue, Hao
Zhang, Feng
Wang, Feng
AuthorAffiliation 5 Shandong Institute of Pomology Taian Shandong China
3 College of Bioscience and Biotechnology Shenyang Agricultural University Shenyang China
4 College of Plant Protection Shenyang Agricultural University Shenyang China
1 College of Horticulture Shenyang Agricultural University Shenyang China
2 College of Horticulture Anhui Agricultural University Hefei China
AuthorAffiliation_xml – name: 2 College of Horticulture Anhui Agricultural University Hefei China
– name: 5 Shandong Institute of Pomology Taian Shandong China
– name: 3 College of Bioscience and Biotechnology Shenyang Agricultural University Shenyang China
– name: 1 College of Horticulture Shenyang Agricultural University Shenyang China
– name: 4 College of Plant Protection Shenyang Agricultural University Shenyang China
Author_xml – sequence: 1
  givenname: Yue
  surname: Ma
  fullname: Ma, Yue
  organization: Shenyang Agricultural University
– sequence: 2
  givenname: Hao
  surname: Xue
  fullname: Xue, Hao
  organization: Anhui Agricultural University
– sequence: 3
  givenname: Feng
  orcidid: 0000-0002-3200-5506
  surname: Zhang
  fullname: Zhang, Feng
  organization: Shenyang Agricultural University
– sequence: 4
  givenname: Qiu
  surname: Jiang
  fullname: Jiang, Qiu
  organization: Shenyang Agricultural University
– sequence: 5
  givenname: Shuang
  surname: Yang
  fullname: Yang, Shuang
  organization: Shenyang Agricultural University
– sequence: 6
  givenname: Pengtao
  surname: Yue
  fullname: Yue, Pengtao
  organization: Shenyang Agricultural University
– sequence: 7
  givenname: Feng
  surname: Wang
  fullname: Wang, Feng
  organization: Shenyang Agricultural University
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  fullname: Zhang, Yuanyan
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– sequence: 9
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  orcidid: 0000-0001-5935-1567
  surname: Zhang
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  email: zhangz@syau.edu.cn
  organization: Shenyang Agricultural University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32885918$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2020 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2020 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: 2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Issue 2
Keywords salt tolerance
apple
SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 13
WRKY100
microRNA156
Language English
License Attribution
2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Snippet Summary Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of...
Salt stress dramatically impedes plant growth and development as well as crop yield. The apple production regions are reduced every year, because of the...
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StartPage 311
SubjectTerms Abiotic stress
apple
Apples
biotechnology
Crop yield
Cultivation
cultivation area
Developmental stages
Embryogenesis
Embryonic growth stage
Empirical analysis
Fertilization
flowering
Flowers & plants
Fruit cultivation
Fruits
Gene expression
gene expression regulation
Gene Expression Regulation, Plant - genetics
genes
Genetic resources
Genetic transformation
irrigation
Kinases
Life cycles
Malus - genetics
Malus - metabolism
Malus domestica
microRNA
microRNA156
MicroRNAs
MicroRNAs - genetics
miRNA
Modules
Morphogenesis
Phylogenetics
Plant growth
Plant Proteins - genetics
Plant Proteins - metabolism
Plant resistance
Proteins
Salinity tolerance
Salt Stress
Salt tolerance
Salt Tolerance - genetics
sequence analysis
Sorghum
SQUAMOSA PROMOTER BINDING PROTEIN‐LIKE 13
Standard deviation
stress tolerance
Transcription factors
Transcription Factors - genetics
WRKY100
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Title The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.13464
https://www.ncbi.nlm.nih.gov/pubmed/32885918
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Volume 19
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