Plastid glucose-6-phosphate dehydrogenase 3 is involved in root system reshaping under low phosphorus stress through regulating auxin and cytokinin signaling in Arabidopsis.

Phosphorus (P) deficiency severely limits crop yield. Plastid glucose-6-phosphate dehydrogenase 3 (G6PD3) is extensively involved in plant adaptation to abiotic stresses. However, little is known regarding the G6PD3 roles in plant adaptation to low P environments. Among G6PD family gene mutants, g6pd3 seedlings have the shortest primary root length under low P stress. G6PD3 transcription was markedly induced by low P stress, especially in the meristematic and elongation zones of primary roots and lateral root primordia. G6PD3 mutation increased the lateral root number but decreased the primary root length and the root/shoot ratio compared with WT, G6PD3 overexpression lines, disturbing root system architecture (RSA) reshaping induced by low P conditions. g6pd3 plants also exhibited other low P-sensitive phenotypes, such as high hydrogen peroxide (H2O2) levels and NADP+/NADPH ratio, reduced biomass, and delayed seed germination. qRT-PCR results further showed that the transcriptions of P-starvation responsive (PSR) genes (PHR1, Pht1;4/PT2 and Pht1;1/PT1) were markedly down-regulated in g6pd3 roots. Meanwhile, G6PD3 mutation down-regulated the expressions of genes related to auxin (IAA) synthesis, polar transport and signaling pathway, but up-regulated the expressions of cytokinin (CTK) synthetic genes under low P stress. This ultimately resulted in low IAA levels and high CTK levels in g6pd3 roots. Exogenous application of reduced glutathione (GSH) effectively alleviated the inhibition of primary root growth in g6pd3 seedlings under low P stress. Taken together, G6PD3 mutation disturbes RSA reshaping through affecting plant hormone (IAA and CTK) signals and H2O2 homeostasis, ultimately increasing the sensitivity of Arabidopsis to low P environments.