A systems genetics analysis in Eucalyptus reveals coordination of metabolic pathways associated with xylan modification in wood‐forming tissues

Wierzbicki, Martin Piotr; Christie, Nanette; Pinard, Desre; Mansfield, Shawn D.; Mizrachi, Eshchar; Myburg, Alexander Andrew

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A systems genetics analysis in Eucalyptus reveals coordination of metabolic pathways associated with xylan modification in wood‐forming tissues

Wierzbicki, Martin Piotr; Christie, Nanette; Pinard, Desre; Mansfield, Shawn D.; Mizrachi, Eshchar; Myburg, Alexander Andrew

URI: http://hdl.handle.net/2263/71579

Date: 2019-09

Abstract:

Acetyl‐ and methylglucuronic acid decorations of xylan, the dominant hemicellulose in secondary cell walls (SCWs) of woody dicots, affect its interaction with cellulose and lignin to determine SCW structure and extractability. Genes and pathways involved in these modifications may be targets for genetic engineering; however, little is known about the regulation of xylan modifications in woody plants. To address this, we assessed genetic and gene expression variation associated with xylan modification in developing xylem of Eucalyptus grandis × Eucalyptus urophylla interspecific hybrids. Expression quantitative trait locus (eQTL) mapping identified potential regulatory polymorphisms affecting gene expression modules associated with xylan modification. We identified 14 putative xylan modification genes that are members of five expression modules sharing seven trans‐eQTL hotspots. The xylan modification genes are prevalent in two expression modules. The first comprises nucleotide sugar interconversion pathways supplying the essential precursors for cellulose and xylan biosynthesis. The second contains genes responsible for phenylalanine biosynthesis and S‐adenosylmethionine biosynthesis required for glucuronic acid and monolignol methylation. Co‐expression and co‐regulation analyses also identified four metabolic sources of acetyl coenxyme A that appear to be transcriptionally coordinated with xylan modification. Our systems genetics analysis may provide new avenues for metabolic engineering to alter wood SCW biology for enhanced biomass processability.

Description:

Supplementary Material: Fig. S1 Phylogram representing a maximum likelihood analysis of RWA proteins in Arabidopsis, Eucalyptus and Populus coupled with relative and absolute percentile expression in xylem and leaf, and domain structure. Fig. S2 Phylogram representing a maximum likelihood analysis of GUX proteins in Arabidopsis, Eucalyptus and Populus coupled with relative and absolute percentile expression in xylem and leaf, and domain structure. Fig. S3 Phylogram representing a maximum likelihood analysis of DUF579/GXM proteins in Arabidopsis, Eucalyptus and Populus coupled with relative and absolute percentile expression in xylem and leaf, and domain structure. Fig. S4 Phylogram representing a maximum likelihood analysis of DUF231/TBL proteins from clade IV in Arabidopsis, Eucalyptus and Populus coupled with relative and absolute percentile expression in xylem and leaf, and domain structure. Fig. S5 Phylogram representing a maximum likelihood analysis of the full complement of DUF231/TBL proteins in Arabidopsis, Eucalyptus and Populus coupled with relative and absolute percentile expression in xylem and leaf, and domain structure. Fig. S6 F‐score threshold determined from the number of genes that each query gene included in the network by using a joint likelihood curve. Fig. S7 Co‐expression and clustering of 1136 genes obtained for genes which passed set criteria divided into five expression modules. Fig. S8 Seventy percent of genes co‐expressed with xylan modification were found to have at least one trans‐eQTL affecting its expression. Fig. S9 Identification of the seven highly enriched trans‐eQTL hotspot loci. Fig. S10 Principal component analysis of the five module eigengenes. Fig. S11 Model of genetic regulation that shapes the expression modules. Fig. S12 Numbers of genes affected by each of the seven hotspot loci and their expression module membership. Fig. S13 Nucleotide sugar interconversion is highly represented in EM5 and regulated primarily by HS_10.3 and HS_10.4. Fig. S14 Complete annotation of Fig. 3 containing genes which were not present in EMs or affected by hotspot loci. Fig. S15 Complete annotation of Fig. 5 containing genes which were not present in EMs or affected by hotspot loci. Methods S1 Network based co‐expression analysis and community detection clustering. Methods S2 Global eQTL mapping and hotspot locus detection. Notes S1 Protein sequences of GUX, DUF579, RWA and TBL proteins used for phylogenetic reconstruction.

Table S1 Arabidopsis, Eucalyptus and Populus genes potentially involved in xylan modification and cumulative evidence for naming of xylan modification genes in Populus and Eucalyptus. Table S2 Confirmed Arabidopsis SCW xylan modification genes and probable homologs in Eucalyptus. Table S3 Eucalyptus grandis query genes used for the co‐expression analysis and the subset that are probable xylan modification genes.

Table S4 1112 genes co‐expressed with 24 xylan modification genes. Table S5 Functional enrichment and annotation of genes present in the five expression modules produced by the co‐expression algorithm.

Table S6 Expression module genes corresponding to GO, KEGG and MM terms. Table S7 Eucalyptus grandis query genes which passed criteria set during co‐expression analysis, membership to an expression module and correlation with SCW associated genes.

Table S8 Identification of bins significantly enriched in trans‐eQTLs.

Table S9 Xylem expressed genes affected by seven hotspots.

Table S10 Overlap of hotspot loci identified in this study with previously identified global hotspots.

Table S11 Core set genes corresponding to enriched terms for GO, Kegg and MapMan.

Table S12 Genes corresponding to process categories on systems model.

Table S13 All genes affected by seven hotspot loci.

Table S14 Genes corresponding to numbered reaction steps on Fig. S13.

Table S15 Genes corresponding to numbered reaction steps on Fig. 3 as well as the genes missing from Fig. 3, indicated on Fig. S14.

Table S16 Genes linked to acetyl‐CoA production corresponding to the numbered reaction steps on Fig. 5 as well as the genes missing from Fig. 5, indicated on Fig. S15.

Table S17 Examples of how the systems model can be used as a tool to design and test new biotechnology approaches to alter cell wall structure and chemistry.

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