Abstract
Vascular tissues essentially regulate water, nutrient, photo-assimilate, and phytohormone logistics throughout the plant body. Boron (B) is crucial for the development of the vascular tissue in many dicotyledonous plant taxa and B deficiency particularly affects the integrity of phloem and xylem vessels, and, therefore, functionality of long-distance transport. We hypothesize that changes in the plants’ B nutritional status evoke differential responses of the vasculature and the mesophyll. However, direct analyses of the vasculature in response to B deficiency are lacking, due to the experimental inaccessibility of this tissue. Here, we generated biochemical and physiological understanding of B deficiency response reactions in common plantain (Plantago major L.), from which pure and intact vascular bundles can be extracted. Low soil B concentrations affected quantitative distribution patterns of various phytohormones, sugars and macro-, and micronutrients in a tissue-specific manner. Vascular sucrose levels dropped, and sucrose loading into the phloem was reduced under low B supply. Phytohormones responded selectively to B deprivation. While concentrations of abscisic acid and salicylic acid decreased at low B supply, cytokinins and brassinosteroids increased in the vasculature and the mesophyll, respectively. Our results highlight the biological necessity to analyze nutrient deficiency responses in a tissue- rather organ-specific manner.
Highlights
Boron (B) is an essential micronutrient for seed plant species
Polyamines and polyamine biosynthesis in P. major and A. thaliana have been shown to be specific for the vascular tissue [23], and the observed increase of S in the mesophyll cannot be fully explained by an increased demand of these compounds
2c.o4n.3d.iStiaolnic(yFligcuArceid7).(SSAtu)dies addressing systemic acquired resistance signaling demonstrated that SA is involved in the transmission of biotic stress responses via the phloem, but did not represent the SA levels decreased to about one fifth in the mesophyll tissue of plants grown under low B when compared to the B-sufficient soil condition
Summary
Boron (B) is an essential micronutrient for seed plant species. Boron serves as a structural element in the cell wall’s pectin layer where boric acid links two rhamnogalacturonan II (RG-II) monomers via di-ester bonds with RG-II intrinsic apiose sugar residues. The damaging impact of B deficiency on the plant vasculature was reported [5,6], and veins from B-deprived leaves often adopt a serpentine shape-like growth behavior leading to the reduced longitudinal growth of leaf blades and cell expansion within the leaf mesophyll [1,7] Such phenotypes can in part be explained by the lack of stability of cell walls in B-deprived organs leading to a collapse of cell layers and transport vessels. During manual extraction of the vascular bundles, surrounding mesophyll tissue cells detach from the endodermal vascular border and isolated vascular strands from common plantain are, almost free from cellular mesophyll contaminations [13] Such isolated vascular (and the remaining leaf) tissue were used for vascular- versus non-vascular-specific analyses of physiological parameters [18], gene expression and transcriptomics [19,20,21], and secondary metabolites [22,23]. The usage of the by us developed soil substrate cultivation system allows for a more natural growth analysis than, e.g., hydroponic culture growth assays in which a physiologically and plant nutritionally-relevant rhizosphere is absent
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