Photosynthesis in cells around veins of the C₃ plant Arabidopsis thaliana is important for both the shikimate pathway and leaf senescence as well as contributing to plant fitness

Abstract

SUMMARYCells associated with veins of C 3 species often contain significant amounts of chlorophyll, and radiotracer analysis shows that carbon present in the transpiration stream may be used for photosynthesis in these cells. It is not clear whether CO 2 is also supplied to these cells close to veins via stomata, nor whether this veinal photosynthesis supplies carbon skeletons to particular metabolic pathways. In addition, it has not been possible to determine whether photosynthesis in cells close to veins of C 3 plants is quantitatively important for growth or fitness. To investigate the role of photosynthesis in cells in and around the veins of C 3 plants, we have trans-activated a hairpin construct to the chlorophyll synthase gene (CS) using an Arabidopsis thaliana enhancer trap line specific to veins. CS is responsible for addition of the phytol chain to the tetrapyrolle head group of chlorophyll, and, as a result of cell-specific trans-activation of the hairpin to CS, chlorophyll accumulation is reduced around veins. We use these plants to show that, under steady-state conditions, the extent to which CO 2 is supplied to cells close to veins via stomata is limited. Fixation by minor veins of CO 2 supplied to the xylem stream and the amount of specific metabolites associated with carbohydrate metabolism and the shikimate pathway were all reduced. In addition, an abundance of transcripts encoding components of pathways that generate phosphoenolpyruvate were altered. Leaf senescence, growth rate and seed size were all reduced in the lines with lower photosynthetic ability in veins and in cells close to veins.

Tomato Fruit Photosynthesis Is Seemingly Unimportant in Primary Metabolism and Ripening But Plays a Considerable Role in Seed Development

“…Despite the fact that a wide number of fruit mutants have been characterized that contain altered pigmentation (Isaacson et al, 2002;Barry and Giovannoni, 2006;Galpaz et al, 2008;Nashilevitz et al, 2010), we chose to manipulate the chlorophyll content by antisense inhibition of GSA in an attempt to minimize the influence of pleiotropic effects. This same approach has already been successfully applied to a number of species (Kannangara and Gough, 1978;Hö fgen et al, 1994;Ilag et al, 1994;Chen et al, 2003), while addressing the functionality of photosynthesis in the cells surrounding the veins of C3 plants was recently achieved using an analogous approach, but different target enzyme, in Arabidopsis (Janacek et al, 2009). Table I.…”

“…With restricted photosynthesis in cells surrounding the veins of Arabidopsis, following an analogous approach to that described here, Janacek et al (2009) suggested a role for photosynthesis in shikimate biosynthesis in this tissue. Similarly, Rubisco was demonstrated to operate, in isolation from the CalvinBenson cycle enzymes, as part of a more efficient route of fatty acid biosynthesis in developing embryos of Brassica napus (Schwender et al, 2004).…”

“…Previous studies have demonstrated that, even within C3 plants, the role of photosynthesis (Janacek et al, 2009) or at least a subset of its reactions (Schwender et al, 2004) varies in a tissue-dependent manner. With restricted photosynthesis in cells surrounding the veins of Arabidopsis, following an analogous approach to that described here, Janacek et al (2009) suggested a role for photosynthesis in shikimate biosynthesis in this tissue.…”

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

“…It is estimated that chloroplasts in BS and M cells of rice contain similar amounts of RuBisCO [47]. Downregulation of chlorophyll synthase in cells associated with the vasculature of C 3 Arabidopsis thaliana showed that photosynthetic capacity of these cells makes an important contribution to plant growth and seed production [48]. Thus, although the BS in C 3 species is most commonly associated with controlling fluxes of nitrogen, sulfur and water into and out of the leaf [49,50], these results suggest photosynthetic activity contributes significantly to plant fitness.…”

Functions of maize genes encoding pyruvate phosphate dikinase in developing endosperm

“…Cytosolic PPDK also functions in gluconeogenesis during Arabidopsis seed germination, using pyruvate from amino acid catabolism (14). Another function is to provide PEP to the shikimate pathway in cells surrounding the vasculature, using pyruvate from decarboxylation of organic acids in the transpiration stream (15).…”