Catalyzes conversion of folates to polyglutamate derivatives allowing concentration of folate compounds in the cell and the intracellular retention of these cofactors, which are important substrates for most of the folate-dependent enzymes that are involved in one-carbon transfer reactions involved in purine, pyrimidine and amino acid synthesis. Essential for organellar and whole-plant folate homeostasis. Required for postembryonic root development. Generates polyglutamylated folate cofactors to support C1 metabolism required for meristem maintenance and cell expansion during postembryonic root development. (6S)-5,6,7,8-tetrahydrofolyl-(gamma-L-Glu)(n) + ATP + L-glutamate = (6S)-5,6,7,8-tetrahydrofolyl-(gamma-L-Glu)(n+1) + ADP + H(+) + phosphate A monovalent cation. Cofactor biosynthesis; tetrahydrofolylpolyglutamate biosynthesis. Expressed in both shoots and roots, but expression in roots is higher compared with shoots. Distinct expression in the quiescent center (QC) region of the root tip. Also expressed in vascular tissues of the cotyledons and hypocotyls, and the first true leaves of 7 days old seedlings. Has short primary roots. Root hairs are also short and wavy. Epidermal cells of wild-type roots are two times longer than epidermal cells of the mutant roots. Short primary roots of the mutant are impaired in F-actin organization due to extensive bundling. Reduced primary root growth of mutants indicate defects in both cell division and cell expansion. Total folate content does not significantly change between the wild-type and mutant in either shoots or roots. However, differences in the accumulation patterns of some folate classes, and general changes in the contribution of each folate class to the total folate pool are found. A considerable increase in total monoglutamylated folates in mutant roots when compared with wild-type is found. This difference is not observed in shoots. Total polyglutamylated folate content is not altered in either tissue. Nucleotides and amino acids are generally depleted in mutant. Vegetative phenotype does not differ visually from wild-type. Polyglutamylated folates are still detectable in the disruption mutant. In comparison to wild-type, the plastid and mitochondrial folate levels are reduced by approximately 50 and 25%, respectively. Folate polyglutamylation levels are significantly reduced but not abolished within the respective compartments. Combined loss of FPGS1 and FPGS2 result in embryo lethality. This double mutant has abnormal seeds that are readily distinguishable as albinos which do not proceed beyond the globular stage of embryogenesis. The absence of a developing embryo lead to collapse of seed walls, leaving shrivelled seed reamnants. FPGS1 and FPGS3 double mutant exhibits dwarfed leaves, late flowering (approximately 13 days after wild-type), reduced fecundity and delayed senescence. Pollination with FPGS1 and FPGS3 double mutant pollen yield at most one or two seeds per silique compared to the yield of full siliques when wild-type stigmas are pollinated with wild-type pollen. There is a 40% reduction in the total of 5-CH(3)-THF pool in FPGS1 and FPGS3 double mutant leaf tissue. FPGS1 and FPGS3 double mutants have 70% lower methionine content than wild-type. Belongs to the folylpolyglutamate synthase family.