Abstract
Starch synthesis and degradation require the participation of many enzymes, occur in both photosynthetic and nonphotosynthetic tissues, and are subject to environmental and developmental regulation. We examine the distribution of starch in vegetative tissues of Arabidopsis (Arabidopsis thaliana) and the expression of genes encoding core enzymes for starch synthesis. Starch is accumulated in plastids of epidermal, mesophyll, vascular, and root cap cells but not in root proper cells. We also identify cells that can synthesize starch heterotrophically in albino mutants. Starch synthesis in leaves is regulated by developmental stage and light. Expression of gene promoter-beta-glucuronidase fusion constructs in transgenic seedlings shows that starch synthesis genes are transcriptionally active in cells with starch synthesis and are inactive in root proper cells except the plastidial phosphoglucose isomerase. In addition, ADG2 (for ADPG PYROPHOSPHORYLASE2) is not required for starch synthesis in root cap cells. Expression profile analysis reveals that starch metabolism genes can be clustered into two sets based on their tissue-specific expression patterns. Starch distribution and expression pattern of core starch synthesis genes are common in Arabidopsis and rice (Oryza sativa), suggesting that the regulatory mechanism for starch metabolism genes may be conserved evolutionarily. We conclude that starch synthesis in Arabidopsis is achieved by spatial coexpression of core starch metabolism genes regulated by their promoter activities and is fine-tuned by cell-specific endogenous and environmental controls.
Highlights
Starch synthesis and degradation require the participation of many enzymes, occur in both photosynthetic and nonphotosynthetic tissues, and are subject to environmental and developmental regulation
We demonstrate that PGM1, APS1, APL1, and SS1 promoters are transcriptionally inactive in cells without starch synthesis
Our results suggest that starch synthesis in Arabidopsis requires spatial coexpression of core starch metabolism genes, which are regulated by their promoter activities
Summary
Starch synthesis and degradation require the participation of many enzymes, occur in both photosynthetic and nonphotosynthetic tissues, and are subject to environmental and developmental regulation. In previous studies on starch synthesis, several Arabidopsis (Arabidopsis thaliana) mutants with low or aberrant starch in their leaves have been characterized They are nucleus-encoded recessive mutants (e.g. pgi, pgm, adg, adg, isa isa, ss1, ss, be2, and be3), indicating that plastidial phosphoglucose isomerase (PGI), phosphoglucose mutase (PGM), ADP-Glc pyrophosphorylase (AGPase), debranching enzymes (ISA), members of the starch synthase (SSs) family, and branching enzymes (BE) are required for normal starch synthesis in photosynthetic. The Arabidopsis pgi mutant is deficient in plastidial PGI and lacks starch in mesophyll cells, but the starch synthesis in root cap cells and guard cells is not affected (Yu et al, 2000) This phenotype suggests that in the absence of plastidial PGI, cytosolic G6P can be transported into chloroplasts of guard cells and amyloplasts of root cap cells for starch synthesis, while chloroplasts of mesophyll cells cannot import G6P efficiently. It has been suggested that APL1 homologs (APL2, APL3, and APL4) may form heterotetramers with APS1 based on the presence of specific isoforms and play roles in starch metabolism in response to various metabolic states of tissues (Crevillen et al, 2005)
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