Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming
Plant lignocellulosic biomass, mostly composed of polysaccharide-rich secondary cell walls (SCWs), provides fermentable sugars that may be used to produce biofuels and biomaterials. However, the complex chemical composition and physical structure of SCWs hinder efficient processing of plant biomass....
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2020-12-01
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doaj-82dcd1c56aaa4006ac0743dafdb324c02021-01-15T06:42:34ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-12-011110.3389/fpls.2020.617020617020Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional ReprogrammingMarcella Siqueira Simões0Sávio Siqueira Ferreira1Adriana Grandis2Jorge Rencoret3Staffan Persson4Staffan Persson5Staffan Persson6Staffan Persson7Eny Iochevet Segal Floh8André Ferraz9José C. del Río10Marcos Silveira Buckeridge11Marcos Silveira Buckeridge12Igor Cesarino13Igor Cesarino14Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, BrazilDepartamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, BrazilDepartamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, BrazilInstituto de Recursos Naturales y Agrobiología de Sevilla, CSIC, Seville, SpainSchool of Biosciences, University of Melbourne, Melbourne, VIC, AustraliaDepartment of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, DenmarkCopenhagen Plant Science Center, University of Copenhagen, Frederiksberg, DenmarkJoint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaDepartamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, BrazilDepartamento de Biotecnologia, Escola de Engenharia de Lorena, Universidade de São Paulo, Lorena, BrazilInstituto de Recursos Naturales y Agrobiología de Sevilla, CSIC, Seville, SpainDepartamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, BrazilSynthetic and Systems Biology Center, InovaUSP, São Paulo, BrazilDepartamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, BrazilSynthetic and Systems Biology Center, InovaUSP, São Paulo, BrazilPlant lignocellulosic biomass, mostly composed of polysaccharide-rich secondary cell walls (SCWs), provides fermentable sugars that may be used to produce biofuels and biomaterials. However, the complex chemical composition and physical structure of SCWs hinder efficient processing of plant biomass. Understanding the molecular mechanisms underlying SCW deposition is, thus, essential to optimize bioenergy feedstocks. Here, we establish a xylogenic culture as a model system to study SCW deposition in sugarcane; the first of its kind in a C4 grass species. We used auxin and brassinolide to differentiate sugarcane suspension cells into tracheary elements, which showed metaxylem-like reticulate or pitted SCW patterning. The differentiation led to increased lignin levels, mainly caused by S-lignin units, and a rise in p-coumarate, leading to increased p-coumarate:ferulate ratios. RNAseq analysis revealed massive transcriptional reprogramming during differentiation, with upregulation of genes associated with cell wall biogenesis and phenylpropanoid metabolism and downregulation of genes related to cell division and primary metabolism. To better understand the differentiation process, we constructed regulatory networks of transcription factors and SCW-related genes based on co-expression analyses. Accordingly, we found multiple regulatory modules that may underpin SCW deposition in sugarcane. Our results provide important insights and resources to identify biotechnological strategies for sugarcane biomass optimization.https://www.frontiersin.org/articles/10.3389/fpls.2020.617020/fullC4 grassesco-expression networkligninsystems biologytranscriptomicsxylogenic culture |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Marcella Siqueira Simões Sávio Siqueira Ferreira Adriana Grandis Jorge Rencoret Staffan Persson Staffan Persson Staffan Persson Staffan Persson Eny Iochevet Segal Floh André Ferraz José C. del Río Marcos Silveira Buckeridge Marcos Silveira Buckeridge Igor Cesarino Igor Cesarino |
spellingShingle |
Marcella Siqueira Simões Sávio Siqueira Ferreira Adriana Grandis Jorge Rencoret Staffan Persson Staffan Persson Staffan Persson Staffan Persson Eny Iochevet Segal Floh André Ferraz José C. del Río Marcos Silveira Buckeridge Marcos Silveira Buckeridge Igor Cesarino Igor Cesarino Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming Frontiers in Plant Science C4 grasses co-expression network lignin systems biology transcriptomics xylogenic culture |
author_facet |
Marcella Siqueira Simões Sávio Siqueira Ferreira Adriana Grandis Jorge Rencoret Staffan Persson Staffan Persson Staffan Persson Staffan Persson Eny Iochevet Segal Floh André Ferraz José C. del Río Marcos Silveira Buckeridge Marcos Silveira Buckeridge Igor Cesarino Igor Cesarino |
author_sort |
Marcella Siqueira Simões |
title |
Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming |
title_short |
Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming |
title_full |
Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming |
title_fullStr |
Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming |
title_full_unstemmed |
Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming |
title_sort |
differentiation of tracheary elements in sugarcane suspension cells involves changes in secondary wall deposition and extensive transcriptional reprogramming |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Plant Science |
issn |
1664-462X |
publishDate |
2020-12-01 |
description |
Plant lignocellulosic biomass, mostly composed of polysaccharide-rich secondary cell walls (SCWs), provides fermentable sugars that may be used to produce biofuels and biomaterials. However, the complex chemical composition and physical structure of SCWs hinder efficient processing of plant biomass. Understanding the molecular mechanisms underlying SCW deposition is, thus, essential to optimize bioenergy feedstocks. Here, we establish a xylogenic culture as a model system to study SCW deposition in sugarcane; the first of its kind in a C4 grass species. We used auxin and brassinolide to differentiate sugarcane suspension cells into tracheary elements, which showed metaxylem-like reticulate or pitted SCW patterning. The differentiation led to increased lignin levels, mainly caused by S-lignin units, and a rise in p-coumarate, leading to increased p-coumarate:ferulate ratios. RNAseq analysis revealed massive transcriptional reprogramming during differentiation, with upregulation of genes associated with cell wall biogenesis and phenylpropanoid metabolism and downregulation of genes related to cell division and primary metabolism. To better understand the differentiation process, we constructed regulatory networks of transcription factors and SCW-related genes based on co-expression analyses. Accordingly, we found multiple regulatory modules that may underpin SCW deposition in sugarcane. Our results provide important insights and resources to identify biotechnological strategies for sugarcane biomass optimization. |
topic |
C4 grasses co-expression network lignin systems biology transcriptomics xylogenic culture |
url |
https://www.frontiersin.org/articles/10.3389/fpls.2020.617020/full |
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