Expression profiles of cell-wall related genes vary broadly between two common maize inbreds during stem development

Authors: Penning, Bryan; SHIGA, TANIA - Purdue University; KLIMEK, JOHN - Purdue University; SAN MIGUEL, PHILIP - Purdue University; SHREVE, JACOB - Purdue University; THIMMAPURAM, JYOTHI - Purdue University; SYKES, ROBERT - National Renewable Energy Laboatory; DAVIS, MARK - National Renewable Energy Laboatory; MCCANN, MAUREEN - Purdue University; CARPITA, NICHOLAS - Purdue University

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/20/2019
Publication Date: 10/29/2019
Citation: Penning, B., Shiga, T.M., Klimek, J.F., San-Miguel, P., Shreve, J., Thimmapuram, J., Sykes, R.W., Davis, M.F., McCann, M.C., Carpita, N.C. 2019. Expression profiles of cell-wall related genes vary broadly between two common maize inbreds during stem development. BMC Genomics. 20, Article #785. https://doi.org/10.1186/s12864-019-6117-z.
DOI: https://doi.org/10.1186/s12864-019-6117-z

Interpretive Summary: Background: Grass species stem residues are a world-wide raw material for bioenergy and many other bioproducts. Their cell walls are distinct from many model plants such as Arabidopsis used most often to understand plant physical properties and genetics. These differences can impact end-quality and conversion efficiency to bioproducts. To better understand what genes may impact differences in cell walls, experiments were conducted in maize and compared to Arabidopsis. Maize is known to have a lot of genetic diversity so two different varieties of maize were tested at key development points of the stem. Findings: Functions of this large set of gene families (>1200) responsible for making and maintaining cell walls are identified and their relative expression in the model grass, maize, and the model dicot, Arabidopsis, are observed for different stages of cell wall development. A few gene families were found to be conserved in potential function based on sequence and expression between maize and Arabidopsis, but the majority of families of genes were not which may play a role in differences between cell walls of different plants such as grasses compared to dicots such as poplar also used for bioproducts. Models were developed using genes known to be expressed at specific times in the production of the maize cell wall and used to identify new genes that may be involved in cell wall production. Two different varieties of maize were tested and it was found that many genes were expressed at different levels between the varieties. In several cases, two different genes in the same gene family show high expression levels providing expression in the gene family but with different genes between maize varieties. In some cases sequence differences were identified that could lead to the expression differences. Genes thought to be involved in the thickening of the cell wall were expressed earlier in one variety. Early thickening was confirmed by showing key components of the cell wall associated with the thickening stage of the early-expressing variety were observed earlier at key stem developmental time-points than the late expressing variety. Conclusions: A better understanding of what genes are present, expressed, utilized, and what function they perform provided by this study can be used to modify plant cell walls in grasses that lead to improvement of end-use quality of bioproducts by other researchers. There were important differences between the most-studied model plant, Arabidopsis, compared to maize, a model for grasses used to make bioproducts. This illustrates the need by researchers and industry to use grass species to test hypotheses about grass species-related bioproducts. Differences in the two maize varieties tested both in physical composition and gene expression indicate earlier formation of the secondary cell wall stage in one variety that could be important to generate biomass faster or improve end-use quality of the material for some bioproducts useful for industry. These expression differences will be useful in future studies of cell wall genes by other researchers.

Technical Abstract: Background: The cellular machinery for cell wall synthesis and metabolism is encoded by members of large multi-gene families. Maize is both a genetic model for grass species and a potential source of lignocellulosic biomass from crop residues. Genetic improvement of maize for its utility as a bioenergy feedstock depends on identification of the specific gene family members expressed during secondary wall development in stems. Results: High-throughput sequencing of transcripts expressed in developing rind tissues of stem internodes provided a comprehensive inventory of cell wall-related genes in maize (Zea mays, cultivar B73). Of 1239 of these genes, 695 were expressed. Grasses have cell wall compositions distinct from non-commelinid species; only one-quarter of maize cell wall-related genes expressed in stems were putatively orthologous with those of the eudicot Arabidopsis. Using a slope-metric algorithm, five distinct patterns for sub-sets of co-expressed genes were defined across a time course of stem development. For the subset of genes associated with secondary wall formation, fifteen sequence motifs in five groups were found in promoter regions. The same members of gene families were often expressed in two maize inbreds, B73 and Mo17, but levels of gene expression between them varied, with 30% of the entire genome exhibiting at least a 5-fold difference at any stage. Although presence-absence and copy-number variation accounted for some of the differences, fold-changes of expression of a CADa and a FLA11 gene were attributed to polymorphisms in promoter response elements. Conclusions: Large genetic variation in maize as a species precludes the extrapolation of cell wall-related gene expression networks even from one common inbred line to another. Elucidation of genotype-specific expression patterns and their regulatory controls will be needed for association panels of inbreds and landraces to fully exploit genetic variation in maize and other bioenergy grass species.