Empowering roots—Some current aspects of root bioenergetics

Abstract

Roots of higher plants provide the shoot with nutrients and water. In exchange, they receive photosynthates, which serve both as energy source and building blocks for maintenance and growth. While studies in plant bioenergetics used to focus on photosynthesis, several more recent findings also aroused or renewed interest in energy conversion and allocation in roots. Root building costs were identified as a long-undervalued trait, which turned out to be highly relevant for stress tolerance and nutrient use efficiency. Reduced building costs per root length (e.g., by aerenchyma formation or by increasing the cell size) are beneficial for exploring the soil for nutrient-rich patches, especially in low-input agrosystems. Also, an apparent mismatch was frequently found between the root energy budget in the form of the ATP pool on the one side and the apparent costs on the other side, particularly the costs of membrane transport under stress conditions, e.g., the Na+ detoxification costs resulting from Na+ sequestration at the plasma membrane. Ion transport across the plasma membrane (and also endomembranes) is coupled to the proton motive force usually believed to be exclusively generated by H+ ATPases. Recently, an alternative mechanism, the biochemical pH clamp, was identified which relies on H+ formation and binding in the apoplast and the cytosol, respectively, driven by metabolism (so-called active buffering). On this background, several aspects of root bioenergetics are discussed. These are (1) root respiration in soil, with a critical view on calorimetric vs. gas exchange measurements; (2) processes of energy conversion in mitochondria with a special focus on the role of the alternative oxidases, which allow adjusting carbon flow through metabolic pathways to membrane transport processes; and (3) energy allocation, in particular to transport across the plasma membrane forming the interface to soil solution. A concluding remark is dedicated to modeling root bioenergetics for optimizing further breeding strategies. Apparent “energy spoilers” may bestow the plant with a yet unidentified advantage only unfolding their beneficial effect under certain environmental conditions.

Root phenotypic plasticity: agronomic, breeding and modelling implications

“…Our experimental and modelling results indicate that some of these assumptions need revisiting. We showed that the intensity of water stress, as the result of the growing environment or intra-speci c plant competition, can affect both the maximum rooting depth and the depth at which crops will use water, indicating changes in resource allocation between above-and below-ground growth (Schneider 2022;Wegner 2022). By modifying the soil volume explorable by the rooting system in response to water stress, i.e.…”

“…This means that phenotypes that invest resources in deeper roots are likely to pro t from accessing deeper soil water at critical stages around owering and grain lling. We do not know whether the lower yield of hybrid A and B in the higher-yielding environment might be related to the cost of deep roots (Wegner 2022). Root respiration can consume up to 30% of the total plant sugars allocated to the roots (Lambers et al 2003), and faster respiration rates are associated with traits such as high speci c root length, high root nitrogen concentration and ne roots, compared to roots that have high tissue density (Han and Zhu 2021).…”

Study on the influence of fertilizers on the yield and quality of barley and potatoes

“…Its source is sugars -a product of photosynthesis occurring in green tissues. In turn, the root system is a "pump" that pumps water and a complex of nutrients from the soil necessary for the development of the above-ground part [1]. If both the "tops" and the "bottoms" work according to the optimal scenario, the agronomist will be satisfied with the crop yields.…”

Long‐term net H+ influx in maize roots and its potential role in salt tolerance

“…This involves intracellular metabolic processes 'consuming' H + (termed 'active buffering'), thus keeping the cytosolic pH in the narrow range slightly above 7 required for cell survival. Apoplastic H + can be mobilized by 'passive' buffering (the extracellular compartment which is in contact with soil solution outsizes the cytosol by several orders of magnitude) and by bicarbonate formation from CO 2 (for details, see Wegner & Shabala, 2020;Wegner et al, 2021;Wegner, 2022). Imposing mild, moderate and severe salinity stress, and using the noninvasive microelectrode ion flux estimation (MIFE) technique, we showed that salinity can induce a steady net H + influx across the root surface, providing first evidence for a key role of the biochemical pH clamp in salt tolerance in maize.…”