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Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants

BACKGROUND: Maize brown midrib (bm) mutants associated with impaired lignin biosynthesis are a potential source for the breed of novel germplasms with improved cell wall digestibility. The spontaneous bm5 mutants had been identified since 2008. However, the gene responsible for the bm5 locus, and th...

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Autores principales: Xiong, Wangdan, Wu, Zhenying, Liu, Yuchen, Li, Yu, Su, Kunlong, Bai, Zetao, Guo, Siyi, Hu, Zhubing, Zhang, Zhiming, Bao, Yan, Sun, Juan, Yang, Guofeng, Fu, Chunxiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6456989/
https://www.ncbi.nlm.nih.gov/pubmed/31007716
http://dx.doi.org/10.1186/s13068-019-1421-z
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author Xiong, Wangdan
Wu, Zhenying
Liu, Yuchen
Li, Yu
Su, Kunlong
Bai, Zetao
Guo, Siyi
Hu, Zhubing
Zhang, Zhiming
Bao, Yan
Sun, Juan
Yang, Guofeng
Fu, Chunxiang
author_facet Xiong, Wangdan
Wu, Zhenying
Liu, Yuchen
Li, Yu
Su, Kunlong
Bai, Zetao
Guo, Siyi
Hu, Zhubing
Zhang, Zhiming
Bao, Yan
Sun, Juan
Yang, Guofeng
Fu, Chunxiang
author_sort Xiong, Wangdan
collection PubMed
description BACKGROUND: Maize brown midrib (bm) mutants associated with impaired lignin biosynthesis are a potential source for the breed of novel germplasms with improved cell wall digestibility. The spontaneous bm5 mutants had been identified since 2008. However, the gene responsible for the bm5 locus, and the comprehensive effects of bm5 mutation on lignin biosynthesis, soluble phenolics accumulation, and cell wall degradation have yet to be elucidated. RESULTS: The bm5 locus was identified to encode a major 4-coumarate: coenzyme A ligase (Zm4CL1) through analyzing MutMap-assisted gene mapping data. Two alleles of Zm4CL1 isolated from bm5 mutants contained two transposons inserted in the first exon and the second intron, respectively, and consequently, the activities of 4CLs in the crude enzyme extracts from bm5 midribs were reduced by 51–62% compared with the wild type. Furthermore, five 4CLs were retrieved from maize genome, and Zm4CL1 was the most highly expressed one in the lignified tissues. Mutation of Zm4CL1 mainly impeded the biosynthesis of guaiacyl (G) lignins and increased the level of soluble feruloyl derivatives without impacting maize growth and development. Moreover, both neutral detergent fiber digestibility and saccharification efficiency of cell walls were significantly elevated in the bm5 mutant. CONCLUSIONS: Zm4CL1 was identified as the Bm5 gene, since two independent alleles of Zm4CL1 were associated with the same mutant phenotype. Mutation of Zm4CL1 mainly affected G lignin biosynthesis and soluble feruloyl derivatives accumulation in maize lignified tissues. The reduced recalcitrance of the bm5 mutant suggests that Zm4CL1 is an elite target for cell wall engineering, and genetic manipulation of this gene will facilitate the utilization of crop straw and stover that have to be dealt with for environmental protection. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-019-1421-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-64569892019-04-19 Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants Xiong, Wangdan Wu, Zhenying Liu, Yuchen Li, Yu Su, Kunlong Bai, Zetao Guo, Siyi Hu, Zhubing Zhang, Zhiming Bao, Yan Sun, Juan Yang, Guofeng Fu, Chunxiang Biotechnol Biofuels Research BACKGROUND: Maize brown midrib (bm) mutants associated with impaired lignin biosynthesis are a potential source for the breed of novel germplasms with improved cell wall digestibility. The spontaneous bm5 mutants had been identified since 2008. However, the gene responsible for the bm5 locus, and the comprehensive effects of bm5 mutation on lignin biosynthesis, soluble phenolics accumulation, and cell wall degradation have yet to be elucidated. RESULTS: The bm5 locus was identified to encode a major 4-coumarate: coenzyme A ligase (Zm4CL1) through analyzing MutMap-assisted gene mapping data. Two alleles of Zm4CL1 isolated from bm5 mutants contained two transposons inserted in the first exon and the second intron, respectively, and consequently, the activities of 4CLs in the crude enzyme extracts from bm5 midribs were reduced by 51–62% compared with the wild type. Furthermore, five 4CLs were retrieved from maize genome, and Zm4CL1 was the most highly expressed one in the lignified tissues. Mutation of Zm4CL1 mainly impeded the biosynthesis of guaiacyl (G) lignins and increased the level of soluble feruloyl derivatives without impacting maize growth and development. Moreover, both neutral detergent fiber digestibility and saccharification efficiency of cell walls were significantly elevated in the bm5 mutant. CONCLUSIONS: Zm4CL1 was identified as the Bm5 gene, since two independent alleles of Zm4CL1 were associated with the same mutant phenotype. Mutation of Zm4CL1 mainly affected G lignin biosynthesis and soluble feruloyl derivatives accumulation in maize lignified tissues. The reduced recalcitrance of the bm5 mutant suggests that Zm4CL1 is an elite target for cell wall engineering, and genetic manipulation of this gene will facilitate the utilization of crop straw and stover that have to be dealt with for environmental protection. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-019-1421-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-04-10 /pmc/articles/PMC6456989/ /pubmed/31007716 http://dx.doi.org/10.1186/s13068-019-1421-z Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Xiong, Wangdan
Wu, Zhenying
Liu, Yuchen
Li, Yu
Su, Kunlong
Bai, Zetao
Guo, Siyi
Hu, Zhubing
Zhang, Zhiming
Bao, Yan
Sun, Juan
Yang, Guofeng
Fu, Chunxiang
Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
title Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
title_full Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
title_fullStr Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
title_full_unstemmed Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
title_short Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
title_sort mutation of 4-coumarate: coenzyme a ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6456989/
https://www.ncbi.nlm.nih.gov/pubmed/31007716
http://dx.doi.org/10.1186/s13068-019-1421-z
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