Biosynthesis of cellulose‐enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis

Abstract

SummaryStems and branches of angiosperm trees form tension wood (TW) when exposed to a gravitational stimulus. One of the main characteristics of TW, which distinguishes it from normal wood, is the formation of fibers with a thick inner gelatinous cell wall layer mainly composed of crystalline cellulose. Hence TW is enriched in cellulose, and deficient in lignin and hemicelluloses. An expressed sequence tag library made from TW-forming tissues in Populus tremula (L.) · tremuloides (Michx.) and data from transcript profiling using microarray and metabolite analysis were obtained during TW formation in Populus tremula (L.) in two growing seasons. The data were examined with the aim of identifying the genes responsible for the change in carbon (C) flow into various cell wall components, and the mechanisms important for the formation of the gelatinous cell wall layer (G-layer). A specific effort was made to identify carbohydrate-active enzymes with a putative function in cell wall biosynthesis. An increased C flux to cellulose was suggested by a higher abundance of sucrose synthase transcripts. However, genes related to the cellulose biosynthetic machinery were not generally affected, although the expression of secondary wall-specific CesA genes was modified in both directions. Other pathways for which the data suggested increased activity included lipid and glucosamine biosynthesis and the pectin degradation machinery. In addition, transcripts encoding fasciclin-like arabinogalactan proteins were particularly increased and found to lack true Arabidopsis orthologs. Major pathways for which the transcriptome and metabolome analysis suggested decreased activity were the pathway for C flux through guanosine 5¢-diphosphate (GDP) sugars to mannans, the pentose phosphate pathway, lignin biosynthesis, and biosynthesis of cell wall matrix carbohydrates. Several differentially expressed auxin-and ethylene-related genes and transcription factors were also identified.

A comparative transcriptomic approach to understanding the formation of cork

“…In fact the plastidial pyruvate kinase has been involved in fatty acid synthesis in Arabidopsis seeds (Andre et al 2007;Baud et al 2007) and sucrose synthase is involved in oil accumulation, suggesting a coordination between glycolytic and fatty acid biosynthetic pathways (Troncoso-Ponce et al 2011). However, the upregulation of sucrose synthases in cork could also be a consequence of a higher demand of cell wall synthesis (Andersson-Gunnerås et al 2006;Wei et al 2015). In addition, we found several contigs showing significant homology with HXXXDmotif/BAHD acyltransferases and GDSL-like genes that are upregulated in cork oak outer bark (Table S6A) and although their role in the biosynthesis of suberin has not yet been described, they could also be relevant for the accumulation of this polyester according to the role of some members of these gene families (Girard et al 2012;Molina and Kosma 2015).…”

Association Genetics of Wood Physical Traits in the Conifer White Spruce and Relationships With Gene Expression

“…It has been suggested that the prevalence of neutral PMEs in active cells would allow cell wall expansion (Guglielmino et al 1996). Pectinesterase transcripts were among the differentially regulated and most strongly expressed genes in tension wood of Populus (Andersson-Gunneras et al 2006) and in the juvenile cambial region of E. grandis (Gallo De Carvalho et al 2008). A pectin methyl esterase from wood-forming tissues of hybrid aspen (P. tremula x tremuloides Michx.)…”

Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus

“…TW is formed on the upper side of the leaning stem, resulting in characteristic asymmetric growth, and it serves to correct the stem position (4). In addition to the striking increase in cambial cell divisions, TW has an altered anatomy, and the fibers form an additional inner, cellulose-rich, gelatinous secondary cell wall layer (G layer) (5).…”