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Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings

BACKGROUND: Most plants rely on photosynthesis; therefore, albinism in plants with leaves that are white instead of green causes slow growth, dwarfing, and even death. Although albinism has been characterized in annual model plants, little is known about albino trees. Jackfruit (Artocarpus heterophy...

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Autores principales: Meng, Xiangxu, Xu, Jiahong, Zhang, Maoning, Du, Ruyue, Zhao, Wenxiu, Zeng, Qing, Tu, Zhihua, Chen, Jinhui, Chen, Beibei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8283932/
https://www.ncbi.nlm.nih.gov/pubmed/34271866
http://dx.doi.org/10.1186/s12864-021-07873-y
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author Meng, Xiangxu
Xu, Jiahong
Zhang, Maoning
Du, Ruyue
Zhao, Wenxiu
Zeng, Qing
Tu, Zhihua
Chen, Jinhui
Chen, Beibei
author_facet Meng, Xiangxu
Xu, Jiahong
Zhang, Maoning
Du, Ruyue
Zhao, Wenxiu
Zeng, Qing
Tu, Zhihua
Chen, Jinhui
Chen, Beibei
author_sort Meng, Xiangxu
collection PubMed
description BACKGROUND: Most plants rely on photosynthesis; therefore, albinism in plants with leaves that are white instead of green causes slow growth, dwarfing, and even death. Although albinism has been characterized in annual model plants, little is known about albino trees. Jackfruit (Artocarpus heterophyllus) is an important tropical fruit tree species. To gain insight into the mechanisms underlying the differential growth and development between albino jackfruit mutants and green seedlings, we analyzed root, stem, and leaf tissues by combining PacBio single-molecule real-time (SMRT) sequencing, high-throughput RNA-sequencing (RNA-seq), and metabolomic analysis. RESULTS: We identified 8,202 differentially expressed genes (DEGs), including 225 genes encoding transcription factors (TFs), from 82,572 full-length transcripts. We also identified 298 significantly changed metabolites (SCMs) in albino A. heterophyllus seedlings from a set of 692 metabolites in A. heterophyllus seedlings. Pathway analysis revealed that these DEGs were highly enriched in metabolic pathways such as ‘photosynthesis’, ‘carbon fixation in photosynthetic organisms’, ‘glycolysis/gluconeogenesis’, and ‘TCA cycle’. Analysis of the metabolites revealed 76 SCMs associated with metabolic pathways in the albino mutants, including L-aspartic acid, citric acid, succinic acid, and fumaric acid. We selected 225 differentially expressed TF genes, 333 differentially expressed metabolic pathway genes, and 76 SCMs to construct two correlation networks. Analysis of the TF–DEG network suggested that basic helix-loop-helix (bHLH) and MYB-related TFs regulate the expression of genes involved in carbon fixation and energy metabolism to affect light responses or photomorphogenesis and normal growth. Further analysis of the DEG–SCM correlation network and the photosynthetic carbon fixation pathway suggested that NAD-ME2 (encoding a malic enzyme) and L-aspartic acid jointly inhibit carbon fixation in the albino mutants, resulting in reduced photosynthetic efficiency and inhibited plant growth. CONCLUSIONS: Our preliminarily screening identified candidate genes and metabolites specifically affected in albino A. heterophyllus seedlings, laying the foundation for further study of the regulatory mechanism of carbon fixation during photosynthesis and energy metabolism. In addition, our findings elucidate the way genes and metabolites respond in albino trees. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07873-y.
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spelling pubmed-82839322021-07-19 Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings Meng, Xiangxu Xu, Jiahong Zhang, Maoning Du, Ruyue Zhao, Wenxiu Zeng, Qing Tu, Zhihua Chen, Jinhui Chen, Beibei BMC Genomics Research Article BACKGROUND: Most plants rely on photosynthesis; therefore, albinism in plants with leaves that are white instead of green causes slow growth, dwarfing, and even death. Although albinism has been characterized in annual model plants, little is known about albino trees. Jackfruit (Artocarpus heterophyllus) is an important tropical fruit tree species. To gain insight into the mechanisms underlying the differential growth and development between albino jackfruit mutants and green seedlings, we analyzed root, stem, and leaf tissues by combining PacBio single-molecule real-time (SMRT) sequencing, high-throughput RNA-sequencing (RNA-seq), and metabolomic analysis. RESULTS: We identified 8,202 differentially expressed genes (DEGs), including 225 genes encoding transcription factors (TFs), from 82,572 full-length transcripts. We also identified 298 significantly changed metabolites (SCMs) in albino A. heterophyllus seedlings from a set of 692 metabolites in A. heterophyllus seedlings. Pathway analysis revealed that these DEGs were highly enriched in metabolic pathways such as ‘photosynthesis’, ‘carbon fixation in photosynthetic organisms’, ‘glycolysis/gluconeogenesis’, and ‘TCA cycle’. Analysis of the metabolites revealed 76 SCMs associated with metabolic pathways in the albino mutants, including L-aspartic acid, citric acid, succinic acid, and fumaric acid. We selected 225 differentially expressed TF genes, 333 differentially expressed metabolic pathway genes, and 76 SCMs to construct two correlation networks. Analysis of the TF–DEG network suggested that basic helix-loop-helix (bHLH) and MYB-related TFs regulate the expression of genes involved in carbon fixation and energy metabolism to affect light responses or photomorphogenesis and normal growth. Further analysis of the DEG–SCM correlation network and the photosynthetic carbon fixation pathway suggested that NAD-ME2 (encoding a malic enzyme) and L-aspartic acid jointly inhibit carbon fixation in the albino mutants, resulting in reduced photosynthetic efficiency and inhibited plant growth. CONCLUSIONS: Our preliminarily screening identified candidate genes and metabolites specifically affected in albino A. heterophyllus seedlings, laying the foundation for further study of the regulatory mechanism of carbon fixation during photosynthesis and energy metabolism. In addition, our findings elucidate the way genes and metabolites respond in albino trees. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07873-y. BioMed Central 2021-07-16 /pmc/articles/PMC8283932/ /pubmed/34271866 http://dx.doi.org/10.1186/s12864-021-07873-y Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Meng, Xiangxu
Xu, Jiahong
Zhang, Maoning
Du, Ruyue
Zhao, Wenxiu
Zeng, Qing
Tu, Zhihua
Chen, Jinhui
Chen, Beibei
Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings
title Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings
title_full Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings
title_fullStr Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings
title_full_unstemmed Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings
title_short Third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings
title_sort third-generation sequencing and metabolome analysis reveal candidate genes and metabolites with altered levels in albino jackfruit seedlings
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8283932/
https://www.ncbi.nlm.nih.gov/pubmed/34271866
http://dx.doi.org/10.1186/s12864-021-07873-y
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