Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic Analyses

Ramie (<i>Boehmeria nivea</i> [L.] Gaud.), a nutritious animal feed, is rich in protein and produces a variety of secondary metabolites that increase its palatability and functional composition. Ethylene (ETH) is an important plant hormone that regulates the growth and development of var...

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Main Authors: Hongdong Jie, Pengliang He, Long Zhao, Yushen Ma, Yucheng Jie
Format: Article
Language:English
Published: MDPI AG 2023-11-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/12/22/3899
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author Hongdong Jie
Pengliang He
Long Zhao
Yushen Ma
Yucheng Jie
author_facet Hongdong Jie
Pengliang He
Long Zhao
Yushen Ma
Yucheng Jie
author_sort Hongdong Jie
collection DOAJ
description Ramie (<i>Boehmeria nivea</i> [L.] Gaud.), a nutritious animal feed, is rich in protein and produces a variety of secondary metabolites that increase its palatability and functional composition. Ethylene (ETH) is an important plant hormone that regulates the growth and development of various crops. In this study, we investigated the impact of ETH sprays on the growth and metabolism of forage ramie. We explored the mechanism of ETH regulation on the growth and secondary metabolites of forage ramie using transcriptomic and metabolomic analyses. Spraying ramie with ETH elevated the contents of flavonoids and chlorogenic acid and decreased the lignin content in the leaves and stems. A total of 1076 differentially expressed genes (DEGs) and 51 differentially expressed metabolites (DEMs) were identified in the leaves, and 344 DEGs and 55 DEMs were identified in the stems. The DEGs that affect phenylpropanoid metabolism, including <i>BGLU41</i>, <i>LCT</i>, <i>PER63</i>, <i>PER42</i>, <i>PER12</i>, <i>PER10</i>, <i>POD</i>, <i>BAHD1</i>, <i>SHT</i>, and <i>At4g26220</i> were significantly upregulated in the leaves. Ethylene sprays downregulated tyrosine and chlorogenic acid (3-<i>O</i>-caffeoylquinic acid) in the leaves, but lignin biosynthesis <i>HCT</i> genes, including <i>ACT</i>, <i>BAHD1</i>, and <i>SHT</i>, were up- and downregulated. These changes in expression may ultimately reduce lignin biosynthesis. In addition, the upregulation of caffeoyl CoA-<i>O</i>-methyltransferase (CCoAOMT) may have increased the abundance of its flavonoids. Ethylene significantly downregulated metabolites, affecting phenylpropanoid metabolism in the stems. The differential 4CL and HCT metabolites were downregulated, namely, phenylalanine and tyrosine. Additionally, ETH upregulated 2-hydroxycinnamic acid and the cinnamyl hydroxyl derivatives (caffeic acid and <i>p</i>-coumaric acid). Cinnamic acid is a crucial intermediate in the shikimic acid pathway, which serves as a precursor for the biosynthesis of flavonoids and lignin. The ETH-decreased gene expression and metabolite alteration reduced the lignin levels in the stem. Moreover, the <i>HCT</i> downregulation may explain the inhibited lignin biosynthesis to promote flavonoid biosynthesis. In conclusion, external ETH application can effectively reduce lignin contents and increase the secondary metabolites of ramie without affecting its growth and development. These results provide candidate genes for improving ramie and offer theoretical and practical guidance for cultivating ramie for forage.
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spelling doaj.art-1c5c2993fc754e56b5ad2dd7fad1fe042023-11-24T15:02:10ZengMDPI AGPlants2223-77472023-11-011222389910.3390/plants12223899Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic AnalysesHongdong Jie0Pengliang He1Long Zhao2Yushen Ma3Yucheng Jie4College of Agronomy, Hunan Agricultural University, Changsha 410128, ChinaCollege of Agronomy, Hunan Agricultural University, Changsha 410128, ChinaCollege of Agronomy, Hunan Agricultural University, Changsha 410128, ChinaCollege of Agronomy, Hunan Agricultural University, Changsha 410128, ChinaCollege of Agronomy, Hunan Agricultural University, Changsha 410128, ChinaRamie (<i>Boehmeria nivea</i> [L.] Gaud.), a nutritious animal feed, is rich in protein and produces a variety of secondary metabolites that increase its palatability and functional composition. Ethylene (ETH) is an important plant hormone that regulates the growth and development of various crops. In this study, we investigated the impact of ETH sprays on the growth and metabolism of forage ramie. We explored the mechanism of ETH regulation on the growth and secondary metabolites of forage ramie using transcriptomic and metabolomic analyses. Spraying ramie with ETH elevated the contents of flavonoids and chlorogenic acid and decreased the lignin content in the leaves and stems. A total of 1076 differentially expressed genes (DEGs) and 51 differentially expressed metabolites (DEMs) were identified in the leaves, and 344 DEGs and 55 DEMs were identified in the stems. The DEGs that affect phenylpropanoid metabolism, including <i>BGLU41</i>, <i>LCT</i>, <i>PER63</i>, <i>PER42</i>, <i>PER12</i>, <i>PER10</i>, <i>POD</i>, <i>BAHD1</i>, <i>SHT</i>, and <i>At4g26220</i> were significantly upregulated in the leaves. Ethylene sprays downregulated tyrosine and chlorogenic acid (3-<i>O</i>-caffeoylquinic acid) in the leaves, but lignin biosynthesis <i>HCT</i> genes, including <i>ACT</i>, <i>BAHD1</i>, and <i>SHT</i>, were up- and downregulated. These changes in expression may ultimately reduce lignin biosynthesis. In addition, the upregulation of caffeoyl CoA-<i>O</i>-methyltransferase (CCoAOMT) may have increased the abundance of its flavonoids. Ethylene significantly downregulated metabolites, affecting phenylpropanoid metabolism in the stems. The differential 4CL and HCT metabolites were downregulated, namely, phenylalanine and tyrosine. Additionally, ETH upregulated 2-hydroxycinnamic acid and the cinnamyl hydroxyl derivatives (caffeic acid and <i>p</i>-coumaric acid). Cinnamic acid is a crucial intermediate in the shikimic acid pathway, which serves as a precursor for the biosynthesis of flavonoids and lignin. The ETH-decreased gene expression and metabolite alteration reduced the lignin levels in the stem. Moreover, the <i>HCT</i> downregulation may explain the inhibited lignin biosynthesis to promote flavonoid biosynthesis. In conclusion, external ETH application can effectively reduce lignin contents and increase the secondary metabolites of ramie without affecting its growth and development. These results provide candidate genes for improving ramie and offer theoretical and practical guidance for cultivating ramie for forage.https://www.mdpi.com/2223-7747/12/22/3899ethephontranscriptomemetabolomeflavonoidsligninchlorogenic acid
spellingShingle Hongdong Jie
Pengliang He
Long Zhao
Yushen Ma
Yucheng Jie
Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic Analyses
Plants
ethephon
transcriptome
metabolome
flavonoids
lignin
chlorogenic acid
title Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic Analyses
title_full Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic Analyses
title_fullStr Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic Analyses
title_full_unstemmed Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic Analyses
title_short Molecular Mechanisms Regulating Phenylpropanoid Metabolism in Exogenously-Sprayed Ethylene Forage Ramie Based on Transcriptomic and Metabolomic Analyses
title_sort molecular mechanisms regulating phenylpropanoid metabolism in exogenously sprayed ethylene forage ramie based on transcriptomic and metabolomic analyses
topic ethephon
transcriptome
metabolome
flavonoids
lignin
chlorogenic acid
url https://www.mdpi.com/2223-7747/12/22/3899
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AT penglianghe molecularmechanismsregulatingphenylpropanoidmetabolisminexogenouslysprayedethyleneforageramiebasedontranscriptomicandmetabolomicanalyses
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AT yushenma molecularmechanismsregulatingphenylpropanoidmetabolisminexogenouslysprayedethyleneforageramiebasedontranscriptomicandmetabolomicanalyses
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