Photosynthesis regulation by sucrose metabolism under water deficit and source-sink alterations in sugarcane

Abstract

Water deficit stress is the major limiting factor for plant growth and development, constraining food production. In order to survive in such dry conditions, many biochemical and physiological changes must be triggered by plants. In general, the responses to drought are loss of water content, reductions of stomatal conductance and photosynthesis and increase of carbohydrates. Soluble sugars play a key role in plant metabolism, acting as substrates and modulators of enzyme activity in carbon-related pathways and controlling the expression of different genes related to carbon, lipid and nitrogen routs. However, the mechanisms involved with photosynthesis down-regulation by drought and sugars in C4 plants are not fully understood. The aim of this study was to investigate how drought and source-sink perturbation regulate photosynthesis in sugarcane plants. Therefore, two studies were conducted with sugarcane plants with four months old cultivated under greenhouse conditions. In the first study sugarcane plants (cv. IACSP94-2094) were subjected to water deficit for 5 days (WD) with concomitant spraying of 50 mM exogenous sucrose (WD + Suc). While in the second study source-sink relationship was perturbed in two sugarcane cultivars (cv. IACSP94-2094 and cv. IACSP95-5000) by imposing partial darkness, spraying 50 mM exogenous sucrose and their combination for 5 days. The negative effects of WD in the gas exchange and photochemical parameters were aggravated by exogenous sucrose. Photosynthesis reductions were related to both stomatal and biochemical limitations, but exogenous sucrose intensified metabolic restrictions mainly through down-regulation of Rubisco initial activity and PSII effective quantum efficiency in drought-stressed plants. In addition, Rubisco activation state was decreased by WD + Suc, indicating perhaps that the activity of this enzyme was reduced by tight-binding inhibitors, such as sugars phosphates. Sucrose metabolism enzymes and sugars amount were also differently altered by WD and WD + Suc in leaves, sheath and stalk in WD and WD +Suc plants. Interestingly, Sucrose/hexose ratio decreased in both leaf and sheath whereas it was increased in stalk, suggesting that sucrose and related sugars were intensely metabolized and transported in drought-stressed plants. In well-watered conditions, photosynthesis was inhibited by sucrose spraying in both genotypes, through decreases in maximum Rubisco carboxylation rate (Vcmax), initial slope of A-Ci curve (k), stomatal conductance (gs) and ATP production driven by electron transport (Jatp). The partial darkness and sucrose spraying combination did not change photosynthesis in both genotypes. Significant increases in Vcmax, gs and Jatp and marginal increases in k were noticed when combining partial darkness and sucrose spraying compared with sucrose spraying alone. Altogether, these results suggest that CO2 assimilation impairment is aggravated by exogenous sucrose in drought-stressed plants. This limitation was mainly related to biochemical restrictions, specially associated with Rubisco initial activity and PSII quantum efficiency. In contrast, in vitro PEPCase activity and amount were increased in sucrose-treated plants, suggesting that C4 cycle efficiency was reduced in vivo by C3 cycle inhibition under drought conditions. Moreover, sucrose amount was increased in the stalk, suggesting the feedback regulation from stalk to source leaves in drought-stressed plants. Our data also revealed that increases in sink strength due to partial darkness offset the inhibition of sugarcane photosynthesis caused by sucrose spraying, enhancing the knowledge on endogenous regulation of sugarcane photosynthesis through the source-sink relationship.