ReviewImproved resource allocation and stabilization of yield under abiotic stress
Introduction
Source tissues are net-producers and sink tissues represent net-consumers of carbohydrates. The activity of source and sink tissues drives - and at the same time is driven by - growth and development of plants, in particular of crops. Through centuries of breeding, varieties with mostly increased gradients between source and sink have been selected (Lichthardt et al., 2020; Reynolds et al., 2009; Savage et al., 2015). Distantly located sink and source tissues are connected by the phloem system, which is transporting assimilated carbon mainly in form of non-reducing sugars, sugar alcohols and amino acids, but also different RNA species within a pressure-dependent mass flow. Recent reviews have discussed the trafficking of these individual compounds in detail (sugars: (Julius et al., 2017); amino acids: (Tegeder and Hammes, 2018); RNA: (Kehr and Kragler, 2018). The pressure required to induce mass flow is established by a concentrated and locally defined loading of solutes for transport into phloem sieve elements/companion cell complexes (SE/CCC) at the source (Slewinski et al., 2013; van Bel et al., 2002) and maintained over long distances by evolutionary adaptations of sieve element anatomy (Knoblauch et al., 2016). SE/CCCs are either exclusively connected to the assimilate-producing tissue via plasmodesmata (symplasmic phloem loading) or separated by an apoplasmic space, including only very few plasmodesmal bridges (apoplasmic phloem loading). The latter mechanism requires the mutual and coordinated activity of passive metabolite exporters and energy-dependent importers (Ludewig and Flügge, 2013). Apoplasmic phloem loading has been best understood and described for sucrose, the main transport form of carbon, and corresponding transport proteins have been characterized in many important crop species.
At the sink, sucrose might either be converted to storage compounds (e.g. starch or lipids) in respective storage organs (roots or tubers of e.g. potato, yam, or cassava, or seeds and fruits), or stored itself in storage vacuoles (e.g. in sugar beet taproots or sugarcane stem tissue). Correspondingly, sink strength of an organ or tissue may be adjusted by the rate of use or consumption of the source-delivered sugar (Herbers and Sonnewald, 1998; Ho, 1988). In addition, sucrose delivery and accumulation at sinks may be regulated by the activity of enzymes involved in the biosynthesis of the respective storage compounds, or by transport of sucrose across the vacuolar membrane (tonoplast) (Hedrich et al., 2015; Shiratake and Martinoia, 2007).
Biotechnological and breeding strategies target different key processes that might overcome source or sink limitation. Some of these approaches have been discussed in recent reviews (Fernie et al., 2020; Ludewig and Sonnewald, 2016; Pommerrenig et al., 2020; Sonnewald and Fernie, 2018). Others, like the potential of manipulating the subcellular distribution of sugars at the source to influence photosynthesis, carbon assimilation and transport, will be highlighted in this review. We will discuss how vacuolar sugar transport processes do not only contribute to the strength of sugar storing sinks, but also become relevant for source strength and phloem loading efficiency. Furthermore, we will explore connections between subcellular sugar homeostasis, long-distance transport and stress response. Subcellular carbohydrate partitioning is highly dependent on both, plant nutrient and stress levels and is regulated by activities of carbohydrate modifying enzymes, and specific transporter activities. Finally, we will shed light on stress-induced alternate carbon utilization, namely on biosynthesis of raffinose family oligosaccharides (RFOs) or fructans.
Section snippets
The fate of sucrose
Sucrose is the end product of photosynthesis and the major transport-carbohydrate in many plant species. Sucrose synthesis takes place in the cytosol of photosynthetic active plant cells and two enzymes are known to be rate-limiting, namely Sucrose-phosphate synthase (SPS) and Sucrose-phosphate phosphatase (SPP) (Ruan, 2014). SPS is the key-regulatory step in sucrose synthesis and its activity is influenced by several factors like the amount of protein, reversible protein phosphorylation as
Phloem loading as limiting step for the sugar utilization at the source
The successful loading of sugars depends largely on anatomic peculiarities of the involved cell types. While the filling through the symplasmic path is largely determined by the size exclusion limit (SEL) of connecting plasmodesmata, allowing an accelerated diffusion, the apoplasmic pathway involves energy-dependent loading of the phloem using proton gradients. Here we focus on the latter process, as it includes a multitude of adjustable transporters and enzymes, whose regulation is discussed
Abiotic stress influences sugar distribution
When plants grow under non-fluctuating environmental conditions, i.e. a fixed day length, constant humidity, temperature, and nutrient supply, their sugar and starch metabolism oscillate within very low margins dependent only on light/dark cycles and on endogenous genetic programming (Hummel et al., 2010; Klemens et al., 2014; Zeeman et al., 2007). However, growth in field or natural habitats likely occurs not so uneventful, and plants constantly employ a plethora of acclimation and adaptation
Box: outlook: improving resource allocation
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An altered sugar translocation almost immediately results in altered subcellular sugar concentrations, affecting photosynthesis and subcellular carbon partitioning. If cytosolic sugars drop, plants employ mechanisms to increase photosynthesis and carbon fixation. Adjustment of cellular sugars by targeted manipulation of subcellular sugar compartmentation either by modulation of sugar transporter activity or of sugar metabolism, might therefore represent an approach to steer development and
CRediT authorship contribution statement
Isabel Keller: Writing - original draft. Cristina Martins Rodrigues: Visualization, Writing - original draft. H. Ekkehard Neuhaus: Writing - review & editing. Benjamin Pommerrenig: Writing - original draft, Writing - review & editing.
Declaration of Competing Interest
The authors declare no conflict of interest.
Acknowledgements
This work was supported by a PhD grant from KWS Saat SE & Co. KGaA to I.K. (“Understanding of frost tolerance and frost resistance of meristematic tissues of sugar beet (Beta vulgaris) taproots”) and by the Bill and Melinda Gates Foundation through the grant OPP1113365 ‘Metabolic Engineering of Carbon Pathways to Enhance Yield of Root and Tuber Crops’ provided to H.E.N.
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