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GTR-mediated radial import directs accumulation of defensive glucosinolates to sulfur-rich cells (S-cells) in phloem cap of inflorescence stem of Arabidopsis thaliana

Xu, Deyang, Hunziker, Pascal, Koroleva, Olga, Blennow, Andreas, Crocoll, Christoph, Schulz, Alexander, Nour-Eldin, Hussam Hassan, Halkier, Barbara Ann
Molecular plant 2019
Arabidopsis thaliana, Lotus corniculatus var. japonicus, apoplast, biosynthesis, energy-dispersive X-ray analysis, glucosinolates, models, mutants, phloem, scanning electron microscopy
In the phloem cap region of Arabidopsis, sulfur-rich cells (S-cells) accumulate >100 mM glucosinolates (GLS), but are biosynthetically inactive. The source and route of S-cell-bound GLS remain elusive. Here we used single-cell sampling and scanning electron microscopy with Energy-dispersive X-ray analysis to show that the GLS importers NPF2.10/GTR1 and NPF2.11/GTR2 are critical for GLS accumulation in S-cells, although not localized to the S-cells. Analysis of S-cell GLS in homo- and heterografts of gtr1 gtr2, and biosynthetic null mutant on wild type indicate that S-cells accumulate GLS via symplasmic connections either directly from neighboring biosynthetic cells or indirectly to non-neighboring cells expressing GTRs. Distinct sources and transport routes exist for different types of GLS, and vary dependent on the position of S-cells in the inflorescence stem. Based on our data, we propose a model for GLS transport routes either directly from biosynthetic cells or via GTR-mediated import from apoplastic space radially into a symplasmic domain wherein the S-cells are the ultimate sink. Similarly, we observed accumulation of the cyanogenic glucoside defense compounds in high-turgor cells in phloem cap of Lotus japonicus, suggesting that storage of defense compounds in high-turgor cells may be a general mechanism for chemical protection of the phloem cap.