PGI1-mediated vascular pentose phosphate pathway activity determines growth, photosynthesis and metabolism through 2-C-methyl-D-erythritol 4-P pathway action in Arabidopsis

Resumen del trabajo presentado en el XVI Meeting of Plant Molecular Biology, celebrado en Sevilla (España), del 14 al 16 de septiembre de 2022Phosphoglucose isomerase is involved in the early steps of glycolysis and regeneration of glucose-6-phosphate pools in the pentose phosphate pathway (PPP). In Arabidopsis, plastidial phosphoglucose isomerase (PGI1) is an important determinant of growth, metabolism and photosynthesis, probably due to its involvement in the synthesis of 2-C-methyl-D-erythritol 4-P (MEP)-derived hormones in root tips and vascular tissues (Bahaji et al., 2015; Bahaji et al., 2018). To test this hypothesis, we conducted proteomic and metabolic characterization of PGI1-null pgi1-2 plants. We also characterized pgi1-2 plants ectopically expressing PGI1 under the control of a root tip- and vascular tissue-specific promoter. Furthermore, we characterized pfk4/pfk5 knockout plants impaired in the early steps of plastidial glycolysis, and pgl3-1 plants with reduced activity of the plastidial PPP enzyme 6-phosphogluconolactonase 3. The overall data obtained in this work provide strong evidence that root tip and vascular PGI1-mediated plastidial PPP determines growth, development and photosynthesis through MEP pathway action.This work was supported by the Ministerio de Ciencia e Innovación (MCIN) and Agencia Estatal de Investigación (AEI) / 10.13039/501100011033/ (grants BIO2016-78747-P, PID2019-104685GB-100) and the Ministry of Education, Youth and Sport of the Czech Republic and ERDF project entitled “Plants as a tool for sustainable global development” (No. CZ.02.1.01/0.0/0.0/16_019/0000827)

PGI1-mediated vascular oxidative pentose phosphate pathway modulates photosynthesis via long-distance cytokinin signaling

In Arabidopsis, the plastidial isoform of phosphoglucose isomerase, PGI1, mediates growth and photosynthesis, likely due to its involvement in the vascular production of cytokinins (CK). To examine this hypothesis, we characterized pgi1-2 knockout plants impaired in PGI1 and pgi1-2 plants specifically expressing PGI1 in root tips and vascular tissues. Moreover, to investigate whether the phenotype of pgi1-2 plants is due to impairments in the plastidial oxidative pentose phosphate pathway (OPPP) or the glycolytic pathway, we characterized pgl3-1 plants with reduced OPPP and pfk4pfk5 knockout plants impaired in plastidial glycolysis. Compared with wild-type (WT) leaves, pgi1-2 leaves exhibited weaker expression of photosynthesis- and 2-C-methyl-D-erythritol 4-P (MEP) pathway-related proteins, and stronger expression of oxidative stress protection-related enzymes. Consistently, pgi1-2 leaves accumulated lower levels of chlorophyll, and higher levels of tocopherols, flavonols and anthocyanins than the WT. Vascular- and root tip-specific PGI1 expression countered the reduced photosynthesis, low MEP pathway-derived CK content, dwarf phenotype and the metabolic characteristics of pgi1-2 plants, reverting them to WT-like levels. Moreover, pgl3-1, but not pfk4pfk5 plants phenocopied pgi1-2. Histochemical analyses of plants expressing GUS under the control of promoter regions of genes encoding plastidial OPPP enzymes exhibited strong GUS activity in root tips and vascular tissues. Overall, our findings show that root tip and vascular PGI1-mediated plastidial OPPP activity affects photosynthesis and growth through mechanisms involving long-distance modulation of the leaf proteome by MEP pathway-derived CKs.This work was supported by the Ministerio de Ciencia e Innovación (MCIN) and Agencia Estatal de Investigación (AEI)/10.13039/501100011033/(grants BIO2016-78747-P, PID2019-104685GB-100) and the Ministry of Education, Youth and Sport of the Czech Republic (No. CZ.02.1.01/0.0/0.0/16_019/0000827) within the program Research, Development, and Education (OP RDE).Peer reviewe