Differentiation of Tracheary Elements in Sugarcane Suspension Cells Involves Changes in Secondary Wall Deposition and Extensive Transcriptional Reprogramming

Author(s)

Simoes, Marcella Siqueira ^[1] ; Ferreira, Savio Siqueira ^{[1, 2, 3]} ; Grandis, Adriana ^[1] ; Rencoret, Jorge ^[4] ; Persson, Staffan ^{[5, 6, 7, 8]} ; Floh, Eny Iochevet Segal ^[1] ; Ferraz, Andre ^[9] ; del Rio, Jose C. ^[4] ; Buckeridge, Marcos Silveira ^{[1, 10]} ; Cesarino, Igor ^{[1, 10]}

Affiliation

^[1] Univ Sao Paulo, Inst Biociencias, Dept Bot, Sao Paulo - Brazil

^[2] Univ North Texas, Dept Biol Sci, Denton, TX 76203 - USA

^[3] Univ North Texas, BioDiscovery Inst, Denton, TX 76203 - USA

^[4] CSIC, Inst Recursos Nat & Agrobiol Sevilla, Seville - Spain

^[5] Univ Copenhagen, Dept Plant & Environm Sci, Frederiksberg - Denmark

^[6] Univ Melbourne, Sch BioSci, Melbourne, Vic - Australia

^[7] Univ Copenhagen, Copenhagen Plant Sci Ctr, Frederiksberg - Denmark

^[8] Shanghai Jiao Tong Univ, Sch Life Sci & Biotechnol, Joint Int Res Lab Metab & Dev Sci, State Key Lab Hybrid Rice, Shanghai - Peoples R China

^[9] Univ Sao Paulo, Escola Engn Lorena, Dept Biotecnol, Lorena - Brazil

^[10] InovaUSP, Synthet & Syst Biol Ctr, Sao Paulo - Brazil

• Document type: Journal article
• Source: FRONTIERS IN PLANT SCIENCE; v. 11, DEC 18 2020.
• Web of Science Citations: 1

Abstract

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. (AU)

• FAPESP's process: 14/50884-5 - INCT 2014: National Institute of Science and Technology of Bioethanol
• Grantee: Marcos Silveira Buckeridge
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 16/50189-0 - Can we control how plants produce their biomass?
• Grantee: Igor Cesarino
• Support Opportunities: Regular Research Grants
• FAPESP's process: 15/02527-1 - Development of model systems in sorghum and a systems biology approach to unravel the molecular mechanisms controlling lignin metabolism in grasses
• Grantee: Igor Cesarino
• Support Opportunities: Program for Research on Bioenergy (BIOEN) - Young Investigators Grants
• FAPESP's process: 19/13936-0 - The role of xyloglucan in the cell wall architecture determination in sugarcane
• Grantee: Adriana Grandis
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 15/18361-5 - Establishment of an inducible suspension cell culture for tracheary element differentiation in Sorghum bicolor L.
• Grantee: Marcella Siqueira Simões
• Support Opportunities: Scholarships in Brazil - Master
• FAPESP's process: 16/06917-1 - Transcriptomic analysis and co-expression network construction in model systems for identification of genes involved in secondary cell wall deposition and lignin metabolism in grasses
• Grantee: Sávio de Siqueira Ferreira
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 16/17541-2 - From stress to embryos: molecular and physiological mechanisms associated to somatic embryogenesis
• Grantee: Eny Iochevet Segal Floh
• Support Opportunities: Regular Research Grants