Commentary
Sucrose synthase – an enzyme with a central role in the source-sink coordination and carbon flow in trees.
There is an intense discussion on whether the carbon (C) balance of trees, and thus forest ecosystems, is mainly driven by the availability of assimilates provided by photosynthesis or by the metabolic activity of sink tissues (Körner, 2015). The more traditional view is that growth and biomass accumulation of trees and forests is governed by their photosynthetic capacity. More recent research, however, indicates control of plant C allocation but also of C assimilation by sink metabolic activity. As a consequence, and especially to understand tree growth in a changing environment and under stressful conditions, more detailed knowledge on the mechanisms that convey sink control and source–sink coordination is necessary. In a recently published paper in New Phytologist, Dominguez et al. (2020; doi:
10.1111/nph.16721) provide evidence that sucrose synthase (SUS) activity influences C allocation to developing and growing woody tissues and also feeds back on the whole tree C balance. In their approach the authors not only looked at changes in growth or sugar pools in a particular sink tissue, but they applied a smart combination of analysing the metabolite pools and tracking the fate of 13C label in metabolites in source, sink and transport tissues of transgenic aspen with reduced SUS expression and activity. Moreover, they linked these detailed analyses performed with seedlings in a glasshouse with growth assessments in field grown 5-year-old trees.
‘… under naturally varying stressful conditions and complete phenological cycles, functional SUS is needed for normal growth and development.’
This document is the accepted manuscript version of the following article:
Gessler, A. (2021). Sucrose synthase – an enzyme with a central role in the source–
sink coordination and carbon flow in trees. New Phytologist, 229(1), 8-10.
https://doi.org/10.1111/nph.16998
Besides roots and their associated microbiome, stems are the major sink tissues in trees and also provide the main commercial value, i.e., timber. Sink and source tissues in plants are connected via the phloem. The phloem is the transport tissue for C compounds (in most cases sucrose, but in some species also sugar alcohols; Rennie & Turgeon, 2009) from the sites of production to the sites of demand, where sucrose (as the main transport form) is broken down for further use. The sucrose breakdown is achieved by either SUS or invertase (Stein & Granot, 2019) and these enzymes thus play an important role in the connection of C producing and C consuming tissues keeping the concentration and thereby the pressure gradient in the phloem operational. While there is some evidence that the sink strength of storage organs or fruits of crops is determined by SUS (D’Aoust et al., 1999; Xu et al., 2012), there is less information available for stems of long-lived plants such as trees. It might be assumed that in different species, plant organs and at different times during the growing season, the relative importance of SUS versus invertase activity changes and that SUS is thus not always playing a predominant role in supplying hexoses for further sink metabolic processes. In their study, Dominguez et al. assessed SUS mRNA abundance and SUS activity in RNAi transgenic lines and wildtype but also the activity of neutral and acidic invertase. In two of the three transgenic lines assessed, the activity of the acidic invertase was increased. Thus, a partial compensation of the reduced SUS sucrose cleavage activity by acidic invertase might explain the mild phenotype in the glasshouse-grown seedlings with no changes in stem fresh weight (and only a reduction of dry weight in one transgenic line) and root traits. The fact, however, that the C content and the 13C label of sucrose and other central metabolites in the developing wood were reduced in the RNAi lines, clearly indicates that SUS plays a central role for the C supply in this tissue. Additional support for this assumption is provided by the lower 13C label of cell
wall polymers and by the strongly reduced growth in the field grown trees. Especially the latter finding indicates that under naturally varying stressful conditions and complete phenological cycles, functional SUS is needed for normal growth and development.
Another important finding of the Dominguez et al. paper is that the reduced sink activity (induced by the reduced SUS activity) feeds back on phloem loading and transport, and might thus play a central role in whole plant source–sink coordination. It is known that reduced C sink strength can not only reduce phloem transport but can even lead to a down-regulation of photosynthesis (Gavito et al., 2019). In trees, this was assumed to be a result of the acclimation of C assimilation to the reduced sink demand and lower phloem transport (Hagedorn et al., 2016) probably as result of leaf sucrose accumulation (cf. Fabre et al., 2019).
Such effects on the photosynthetic system were not observed in the seedings in the present paper but it is known that feedbacks from changed sink activity on source activity occur with delays (Hagedorn et al., 2016) and the partial compensation by invertase might also be a reason for the lack of photosynthetic feedback. In this respect, it will be interesting to compare the photosynthetic activity between transgenic lines and wildtype in the field settings. In line with the potential of SUS to feedback on C assimilation, previous findings have shown that increased SUS activity in tobacco leads to higher photosynthetic activity (Nguyen et al., 2016).
Environmental conditions strongly affect growth of plants and productivity of ecosystems and especially global change-induced (hot) droughts are known to have a strong negative effect on primary productivity (Ciais et al., 2005). It has often been assumed that such extreme events reduce growth via direct impacts on photosynthesis mediated by the closure of
stomata or induced by the reduced ribulose bisphosphate regeneration and ATP synthesis (Flexas & Medrano, 2002). There is, however, more and more evidence that environmental stresses, such as drought events, can also directly affect the sink activity of plants (Körner, 2015), for example by impairing growth at low turgor (Steppe et al., 2015), and the subsequently reduced C demand leads to a down-regulation of photosynthetic activity in the source organs (Gessler & Grossiord, 2019).
The findings of Dominguez et al. that SUS activity plays a central role in coordinating sink activity with whole plant C allocation now raises the question as to whether this is also the case – and if this is even more pronounced – under environmental stress (see Fig. 1). The authors speculate that environmental stress conditions might have contributed to the growth reduction in field grown SUSRNAi aspen. It has been previously observed that drought reduced SUS activity in soybean nodules (González et al., 1995) and it was assumed that the impaired potential to metabolize sucrose lead to decreased nitrogen fixing activity (Gordon et al., 1997).
Still, the mechanism driving sink control of the C metabolism during stress events such as droughts remains elusive. An increase in sucrose concentration has also been observed in the roots of drought exposed trees and was related to reduced root respiratory activity (Hagedorn et al., 2016). These authors concluded, based on the framework of McDowell et al. (2011), that reduced water availability and thus a more negative water potential first reduces sink tissue growth (cell expansion, cell wall production) and primary and secondary metabolic pathways (Fig. 1 – growth-mediated sink control). This reduced activity would lead to a reduced demand for UDP-Glucose, which, in turn, might negatively feedback on SUS activity.
However, if SUS was particularly sensitive to reduced water availability it might become a bottleneck for the C supply of sink tissues before their general metabolic activity ceases (Fig.
1 – SUS-mediated sink control). Knowledge on the SUS function under stress is even more important since it is known that high SUS expression under reduced water availability can enhance drought tolerance (Pelah et al., 1997). This might be related to the ability to increase tissue sugar concentrations and thus to adjust the osmotic potential (Yang et al., 2019).
Therefore, impaired SUS activity under drought might not only negatively affect growth but also osmoregulation. Exposing trees with increased and reduced expression and activity of SUS to drought or other stressful conditions in future experiments could be extremely helpful in disentangling the role of SUS in plant stress tolerance and provide further indications on the mechanism controlling the C balance of plants under variable environmental conditions.
ORCID
Arthur Gessler https://orcid.org/0000-0002-1910-9589
Arthur Gessler1,2
1 Ecosystem Ecology, Swiss Federal Research Institute WSL, Zürcherstr. 111, 8903 Birmensdorf, Switzerland.
2 Institute of Terrestrial Ecosystems, ETH Zurich, Department of Environmental Systems Science, Universitätstrasse 16, 8092 Zurich, Switzerland.
(email: arthur.gessler@wsl.ch)
Figures
Fig. 1 Potential role of sucrose synthase (SUS) in the source–sink coordination in trees. In the study of Dominguez et al. (2020; doi: 10.1111/nph.16721) in the recently published article in New Phytologist, SUSRNAi lines of aspen were studied which had reduced SUS activity especially in the growing stem tissues. Reduced SUS activity lead to reduced carbon (C) fluxes through the primary metabolic pathways in the stem and to a reduced incorporation of recent assimilates into cell wall material. At the same time, reduced phloem loading was assumed.
Over the long-term the authors observed reduced biomass production in the stem. On such longer time scales, it might be also assumed (though not examined by Dominguez et al. and thus shown in brackets) that C assimilation acclimates to lower sink activity. Environmental stress such as drought events have been shown to exert sink control over the whole tree C balance (e.g. Hagedorn et al., 2016). Here, also SUS-mediated sink control might act. SUS activity might be sensitive to reduced water availability (González et al., 1995) and thus effects comparable to the ones observed for the SUSRNAi lines might occur in trees exposed to
drought, reducing the availability of metabolites for osmotic adjustment and growth in sink tissues, and leading to an adjustment of leaf assimilate export and C assimilation.
Environmental stress might, however, also act directly on the growth of sink tissues (e.g. under drought via the turgor-dependency of cell elongation) thus exerting growth-mediated sink control. Under such a scenario, reduced growth results in lower C demand and thus lower C flux through sink metabolic networks. Any reduction of SUS activity might then be indirectly induced by stress, for example via feedback inhibition by the reaction product fructose (Stein
& Granot, 2019). In a same way as in the SUS-mediated sink control, phloem transport and photosynthesis could be negatively affected. The black arrows in the figure depict the C flow.
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Key words: carbon allocation, carbon assimilation, climate change, metabolic activity, photosynthesis, source-sink coordination, sucrose synthase, trees.
