Analysis of companion cell and phloem metabolism using a transcriptome-guided model of Arabidopsis metabolism

Abstract

Companion cells and sieve elements play an essential role in vascular plants and yet the details of the metabolism that underpins their function remain largely unknown. Here we construct a tissue-scale flux balance analysis (FBA) model to describe the metabolism of phloem loading in a mature Arabidopsis (Arabidopsis thaliana) leaf. We explore the potential metabolic interactions between mesophyll cells, companion cells, and sieve elements based on the current understanding of the physiology of phloem tissue and through the use of cell-type-specific transcriptome data as a weighting in our model. We find that companion cell chloroplasts likely play a very different role to mesophyll chloroplasts. Our model suggests that, rather than carbon capture, the most crucial function of companion cell chloroplasts is to provide photosynthetically-generated ATP to the cytosol. Additionally, our model predicts that the metabolites imported into the companion cell are not necessarily the same metabolites that are exported in phloem sap; phloem loading is more efficient if certain amino acids are synthesised in the phloem tissue. Surprisingly, in our model predictions the proton pumping pyrophosphatase (H + -PPiase) is a more efficient contributor to the energisation of the companion cell plasma membrane than the H + -ATPase. A computational model provides insight into the metabolism behind Arabidopsis phloem loading, predicting a crucial role for companion cell chloroplasts in phloem loading energy metabolism. kiad154_Supplementary_Data.zip

Lessons from combined metabolic model of mesophyll and guard cells

“…The six phase combined diel model of GC and MC successfully explains many experimental observations and computational predictions. This combined model would help to integrate and model metabolism of all the cells present in a leaf and to explain physiological process starting from gaseous exchange to biosynthesis and transfer of photosynthates to phloem sap (Hunt et al ., 2023). The inclusion of malate transport from MC to GC (Lee, 2010; Lawson et al ., 2014, Daloso et al ., 2017), population based study of GC and MC considering the different numbers of GCs and MCs in a leaf, integration of omics data, dependencies on CO 2 concentration, restriction on vacuolar size, regulation of hormones like abscisic acid (ABA), roles of calcium signalling etc.…”

The Interplay between Enucleated Sieve Elements and Companion Cells

“…It will be important to demonstrate at what stage in the life of the SE the proteasomal proteins appear. Small proteins (20-70 KDa) from companion cells to SEs may explain the plethora of macromolecules identified in phloem sap [43]. In addition, the majority of molecules found in the phloem stream may simply be the product of macromolecular leakage from companion cells.…”

“…As the authors of the review point out, it will be interesting to determine the physiological significance of the spatial separation of the proteins within SE plasmalemma. Similarly, genes involved in the initiation of companion cell development have not been determined with certainty thus far [43]. SE/companion cell complexes arise from (pro)cambial mother cells induced by key genes known to be decisive for SE differentiation [24].…”

The Arabidopsis leaf quantitative atlas: a cellular and subcellular mapping through unified data integration

“…We provide illustrations of how this data compendium can be used to calculate membrane surface areas at the leaf level and to convert metabolite amounts in the various units used in the literature to a common unit, taking metabolite subcellular localisation into account. This quantitative atlas could be useful in many different contexts where quantitative parameters are required: for example, knowledge of cell/organelle volumes was essential for modelling in Beauvoit et al ( 2014 ), Shameer et al ( 2020 ) and Topfer et al ( 2020 ), and knowledge of cell type and number was used in Scheunemann et al ( 2018 ) and Hunt et al ( 2023 ). Furthermore, this quantitative atlas can also feed into other integrative approaches such as the Plant Cell Atlas initiative (Fahlgren et al, 2023 ; Jha et al, 2021 ).…”