Improved resource allocation and stabilization of yield under abiotic stress

Abstract

Sugars are the main building blocks for carbohydrate storage, but also serve as signaling molecules and protective compounds during abiotic stress responses. Accordingly, sugar transport proteins fulfill multiple roles as they mediate long distance sugar allocation, but also shape the subcellular and tissue-specific carbohydrate profiles by balancing the levels of these molecules in various compartments. Accordingly, transporter activity represents a target by classical or directed breeding approaches, to either, directly increase phloem loading or to increase sink strength in crop species. The relative subcellular distribution of sugars is critical for molecular signaling affecting yield-relevant processes like photosynthesis, onset of flowering and stress responses, while controlled long-distance sugar transport directly impacts development and productivity of plants. However, long-distance transport is prone to become unbalanced upon adverse environmental conditions. Therefore, we highlight the influence of stress stimuli on sucrose transport in the phloem and include the role of stress induced cellular carbohydrate sinks, like raffinose or fructans, which possess important roles to build up tolerance against challenging environmental conditions. In addition, we report on recent breeding approaches that resulted in altered source and sink capacities, leading to increased phloem sucrose shuttling in crops. Finally, we present strategies integrating the need of cellular stress-protection into the general picture of long-distance transport under abiotic stress, and point to possible approaches improving plant performance and resource allocation under adverse environmental conditions, leading to stabilized or even increased crop yield.

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.