Dataset Information

Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis.

ABSTRACT: A fundamental limitation of photosynthetic carbon fixation is the availability of CO2. In C4 plants, primary carboxylation occurs in mesophyll cytosol, and little is known about the role of CO2 diffusion in facilitating C4 photosynthesis. We have examined the expression, localization, and functional role of selected plasma membrane intrinsic aquaporins (PIPs) from Setaria italica (foxtail millet) and discovered that SiPIP2;7 is CO2-permeable. When ectopically expressed in mesophyll cells of Setaria viridis (green foxtail), SiPIP2;7 was localized to the plasma membrane and caused no marked changes in leaf biochemistry. Gas exchange and C18O16O discrimination measurements revealed that targeted expression of SiPIP2;7 enhanced the conductance to CO2 diffusion from the intercellular airspace to the mesophyll cytosol. Our results demonstrate that mesophyll conductance limits C4 photosynthesis at low pCO2 and that SiPIP2;7 is a functional CO2 permeable aquaporin that can improve CO2 diffusion at the airspace/mesophyll interface and enhance C4 photosynthesis.

SUBMITTER: Ermakova M

PROVIDER: S-EPMC8648302 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

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Publications

Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis.

Ermakova Maria M Osborn Hannah H Groszmann Michael M Bala Soumi S Bowerman Andrew A McGaughey Samantha S Byrt Caitlin C Alonso-Cantabrana Hugo H Tyerman Steve S Furbank Robert T RT Sharwood Robert E RE von Caemmerer Susanne S

eLife 20211129

A fundamental limitation of photosynthetic carbon fixation is the availability of CO2. In C4 plants, primary carboxylation occurs in mesophyll cytosol, and little is known about the role of CO2 diffusion in facilitating C4 photosynthesis. We have examined the expression, localization, and functional role of selected plasma membrane intrinsic aquaporins (PIPs) from Setaria italica (foxtail millet) and discovered that SiPIP2;7 is CO2-pe ...[more]

PMID: 34842138

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Project description:BACKGROUND:Recently, there has been interest in establishing a monocot C4 model species with a small genome, short lifecycle, and capacity for genetic transformation. Setaria viridis has been adopted to fill this role, since reports of Agrobacterium-mediated transformation in 2010, and sequencing of its genome in 2012. To date, S. viridis has primarily been used to further our understanding of C4 photosynthesis, but is also an ideal system for the study of biomass crops, which are almost exclusively C4 panicoid grasses. Biogenesis of stem tissue, its cell wall composition, and soluble sugar content are important determinants of bioenergy crop yields. Here we show that a developing S. viridis internode is a valuable experimental system for gene discovery in relation to these important bioenergy feedstock traits. RESULTS:The rate of maximal stem biomass accumulation in S. viridis A10 under long day growth was at the half-head emergence developmental stage. At this stage of development, internode 5 (of 7) was found to be rapidly expanding with an active meristem, a zone of cell expansion (primary cell walls), a transitional zone where cell expansion ceased and secondary cell wall deposition was initiated, and a mature zone that was actively accumulating soluble sugars. A simple method for identifying these zones was established allowing rapid dissection and snap-freezing for RNAseq analysis. A transcriptome profile was generated for each zone showing a transition from cell division and nucleic acid synthesis/processing in the meristem, to metabolism, energy synthesis, and primary cell wall synthesis in the cell expansion zone, to secondary cell wall synthesis in the transitional zone, to sugar transport, and photosynthesis in the mature zone. CONCLUSION:The identification of these zones has provided a valuable experimental system for investigating key bioenergy traits, including meristematic activity, cell wall biosynthesis, and soluble sugar accumulation, in a C4 panicoid grass that has genetic resources, a short life cycle, and small stature allowing controlled experimental conditions in growth cabinets. Here we have presented a comprehensive map of gene expression and metabolites in this experimental system to facilitate gene discovery and controlled hypothesis testing for bioenergy research in S. viridis.

Project description:Setaria viridis has emerged as a model species for the larger C4 grasses. Here the cellulose synthase (CesA) superfamily has been defined, with an emphasis on the amounts and distribution of (1,3;1,4)-?-glucan, a cell wall polysaccharide that is characteristic of the grasses and is of considerable value for human health.Orthologous relationship of the CesA and Poales-specific cellulose synthase-like (Csl) genes among Setaria italica (Si), Sorghum bicolor (Sb), Oryza sativa (Os), Brachypodium distachyon (Bradi) and Hordeum vulgare (Hv) were compared using bioinformatics analysis. Transcription profiling of Csl gene families, which are involved in (1,3;1,4)-?-glucan synthesis, was performed using real-time quantitative PCR (Q-PCR). The amount of (1,3;1,4)-?-glucan was measured using a modified Megazyme assay. The fine structures of the (1,3;1,4)-?-glucan, as denoted by the ratio of cellotriosyl to cellotetraosyl residues (DP3:DP4 ratio) was assessed by chromatography (HPLC and HPAEC-PAD). The distribution and deposition of the MLG was examined using the specific antibody BG-1 and captured using fluorescence and transmission electron microscopy (TEM).The cellulose synthase gene superfamily contains 13 CesA and 35 Csl genes in Setaria. Transcript profiling of CslF, CslH and CslJ gene families across a vegetative tissue series indicated that SvCslF6 transcripts were the most abundant relative to all other Csl transcripts. The amounts of (1,3;1,4)-?-glucan in Setaria vegetative tissues ranged from 0.2% to 2.9% w/w with much smaller amounts in developing grain (0.003% to 0.013% w/w). In general, the amount of (1,3;1,4)-?-glucan was greater in younger than in older tissues. The DP3:DP4 ratios varied between tissue types and across developmental stages, and ranged from 2.4 to 3.0:1. The DP3:DP4 ratios in developing grain ranged from 2.5 to 2.8:1. Micrographs revealing the distribution of (1,3;1,4)-?-glucan in walls of different cell types and the data were consistent with the quantitative (1,3;1,4)-?-glucan assays.The characteristics of the cellulose synthase gene superfamily and the accumulation and distribution of (1,3;1,4)-?-glucans in Setaria are similar to those in other C4 grasses, including sorghum. This suggests that Setaria is a suitable model plant for cell wall polysaccharide biology in C4 grasses.

Dataset Information

Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis.

Publications

Expression of a CO<sub>2</sub>-permeable aquaporin enhances mesophyll conductance in the C<sub>4</sub> species <i>Setaria viridis</i>.

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