Abstract
Plastid metabolism is critical in both photoautotrophic and heterotrophic plant cells. In chloroplasts, fructose-1,6-bisphosphate aldolase (FBA) catalyses the formation of both fructose 1,6-bisphosphate and sedoheptulose 1,7-bisphosphate within the Calvin-Benson cycle. Three Arabidopsis genes, AtFBA1-AtFBA3, encode plastidial isoforms of FBA, but the contribution of each isoform is unknown. Phylogenetic analysis indicates that FBA1 and FBA2 derive from a recently duplicated gene, while FBA3 is a more ancient paralog. fba1 mutants are phenotypically indistinguishable from the wild type, while both fba2 and fba3 have reduced growth. We show that FBA2 is the major isoform in leaves, contributing most of the measurable activity. Partial redundancy with FBA1 allows both single mutants to survive, but combining both mutations is lethal, indicating a block of photoautotrophy. In contrast, FBA3 is expressed predominantly in heterotrophic tissues, especially the leaf and root vasculature, but not in the leaf mesophyll. We show that the loss of FBA3 affects plastidial glycolytic metabolism of the root, potentially limiting the biosynthesis of essential compounds such as amino acids. However, grafting experiments suggest that fba3 is dysfunctional in leaf phloem transport, and we suggest that a block in photoassimilate export from leaves causes the buildup of high carbohydrate concentrations and retarded growth.
Highlights
The fixation of atmospheric CO2 into organic compounds by plants occurs via the Calvin–Benson cycle (Calvin, 1962).The cycle is organized into three phases: a CO2 fixation phase, a reduction phase and a regeneration phase
In Arabidopsis, FBA1 and FBA2 are located on chromosome II and IV, respectively, within syntenic zones (Fig. 1B) approximately 0.4 Mb in length containing similar sets of 56 genes
The plastidial localizations of FBA1, FBA2, and FBA3 were previously confirmed experimentally in Arabidopsis (Vidi et al, 2006;Ytterberg et al, 2006; Lu et al, 2012). Our analysis of their gene expression patterns and our functional studies show that FBA1 and FBA2 together fulfil the canonical, essential role of FBA within the Calvin–Benson cycle in the leaf mesophyll
Summary
The fixation of atmospheric CO2 into organic compounds by plants occurs via the Calvin–Benson cycle (Calvin, 1962).The cycle is organized into three phases: a CO2 fixation phase, a reduction phase and a regeneration phase. Five out of six triose-phosphates produced remain within the cycle for regeneration of the ribulose 1,5-bisphosphate for CO2 fixation, while one can be used to supply substrates for other metabolic processes. Several major pathways, such as sugar and starch production (Stitt and Zeeman, 2012) and the shikimate pathway (Henkes et al, 2001; Maeda and Dudareva, 2012), draw directly upon Calvin–Benson cycle intermediates.the concentrations of intermediates must be carefully managed to meet the demands of these pathways, while maintaining sufficient carbon for RuBP generation. Sugars derived from the Calvin–Benson cycle can be used locally as building blocks for leaf growth, but a large fraction is transported to heterotrophic sink tissues and catabolized there for energy generation and growth
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