Arabidopsis hydathodes are sites of intense auxin metabolism and nutrient scavenging

Abstract

Hydathodes are small organs located on the leaf margins of all vascular plants. They release excess xylem sap through guttation when stomata are closed or when the humidity level is high. Many promoter analyses have suggested other hydathode functions in metabolite transport and auxin metabolism, but experimental demonstration is still lacking. Here, we compared the transcriptomic and metabolomic features of mature Arabidopsis hydathodes to the leaf blade. 1460 differentially-expressed genes were identified revealing that genes related to auxin metabolism, transport, stress, DNA, plant cell wall, RNA or wax were on average more expressed in hydathodes. On the other hand, genes involved in glucosinolate metabolism, sulfation pathway, metal handling or photosynthesis were downregulated in hydathodes. In hydathodes, there are an increased expression of auxin transcriptional regulators and biosynthetic genes, a lower expression of auxin transport genes and a differential expression of genes related to its vacuolar storage that is consistent with increased contents of free and conjugated auxin. We also found that ca. 78% of the total content of 52 xylem sap metabolites were removed from guttation fluid at the hydathode level. Using reverse genetics, we showed that the capture of nitrate and phosphate in the guttation fluid relies on theNRT2.1andPHT1;4transporters, respectively. Thus, hydathodes absorb a significant part of xylem sap nutrients, limiting the loss of valuable chemicals during guttation. Our transcriptomic and metabolomic analyses reveal an organ with its own transcriptomic and physiological identity and highlight hydathode biological processes that may impact the whole plant.One sentence summaryTranscriptome and physiological analysis of mature and healthy hydathodes of Arabidopsis demonstrates that those organs are sites of intense auxin metabolism and nutrient scavenging

M2WISH: an easy and efficient protocol for whole-mount mRNAin situhybridization that allows 3D cell resolution of gene expression inArabidopsis thaliana

“…Reconstruction of transversal sections revealed that PIN1 is preferentially expressed at the adaxial side of the leaf vasculature (Figure 3j). PIN1 transcripts were also detected in hydathodes, in agreement with transcriptomic analysis (Routaboul et al ., 2022) (Figure 3o-p), and at the tip of nascent serrations at the leaf margin (Figure 3l, n) (Bilsborough et al ., 2011). To our knowledge, this is the first time PIN1 transcripts was detected using WISH.…”

Cell specialization and coordination in Arabidopsis leaves upon pathogenic attack revealed by scRNA-seq

“… (B) Cluster-specific expression profiles of cell-type marker genes. The marker genes were selected from the literature ( Kim et al., 2021 ; Routaboul et al., 2022 ; Tenorio Berrío et al., 2022 ). GC, CC, EC, HC, MC, and SC stand for guard cells, companion cells, epidermal cells, hydathode cells, mesophyll cells, and vascular S cells, respectively.…”

The SAH7 Homologue of the Allergen Ole e 1 Interacts with the Putative Stress Sensor SBP1 (Selenium-Binding Protein 1) in Arabidopsis thaliana

“…Hydathodes are specialized organs that prevent the harmful effect of excess water and xylem sap [ 25 , 26 , 27 ]. Moreover, hydathodes are the auxin biosynthesis gene reservoir [ 28 , 29 , 30 , 31 , 32 , 33 , 34 ], while auxin has been observed in hydathodes via immunolocalization [ 29 ].…”