Abstract

A pyruvate-phosphate dikinase (C4-PPDK) gene was cloned from Suaeda monoica, which had a single-cell C4 photosynthesis pathway without Kranz anatomy and was functionally validated in a C3 model plant under different abiotic stress conditions in an ambient and elevated CO2 environment. Overexpression of SmPPDK promoted growth of C3 transgenic plants, enhancing their photosynthesis (CO2 assimilation) by lowering photorespiration under stress conditions. Transgenic plants also showed an improved physiological status, with higher relative water content (RWC), membrane integrity, concentration of glycine betaine, total soluble sugars, free amino acids, polyphenols and antioxidant activity, and lower electrolyte leakage, lipid peroxidation, free radical accumulation, and generation of reactive oxygen species (ROS), compared to control plants. Moreover, SmPPDK transgenic plants exhibited earlier flowering and higher dry biomass compared to controls. These results suggested that the C4-PPDK gene was appropriate for improvement of carbon assimilation, and it also played an important role in adaption to salinity and severe drought-induced stress. More intriguingly, an elevated CO2 environment alleviated the adverse effects of abiotic stress, particularly caused by drought through coordination of osmoprotectants and antioxidant defense systems. The molecular, physiological, metabolic, and biochemical indicators ameliorated the overall performance of model C3 plants overexpressing the C4-PPDK gene in an elevated CO2 environment, by lowering photorespiration metabolic processes, however, further studies are needed to confirm its precise role in C3 plants as protection against future climate change.

Highlights

  • Global climate changes such as increasing temperature, atmospheric CO2 concentration and salinization, and altered precipitation are among the primary constraints on crop improvement, including biomass production and yield (Dhir, 2018)

  • T1 transgenic lines were further confirmed by histochemical GUS assay (Figure 1B) and polymerase chain reaction (PCR) (Figure 1C), in comparison with the controls

  • Quantitative real-time-based analysis confirmed that all transgenic lines (L1, L20, L32, L33, and L40) contained a single integration event (Supplementary Figure S3)

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Summary

Introduction

Global climate changes such as increasing temperature, atmospheric CO2 concentration and salinization, and altered precipitation are among the primary constraints on crop improvement, including biomass production and yield (Dhir, 2018). Global CO2 concentrations have increased from a preindustrial level of 285 μmol mol−1 to the current level of 384 μmol mol−1, and they have been predicted to reach 936 μmol mol−1 by the year 2100, with an increase in global atmospheric temperature of about 6.4◦C (IPCC, 2014) These stresses will likely affect the productivity of plants, influencing the sequestration and assimilation of atmospheric CO2 through photosynthesis. Various studies on elevated CO2 concentrations have shown a close relationship between improvements to photosynthesis and increases in yield and total biomass of plants (Kellner et al, 2019; Pastore et al, 2019) This provides an attractive approach to enhancing yield by increasing photosynthesis of a particular crop species (Zhang et al, 2014; Yadav et al, 2018). Genera Suaeda and Bienertia have broken the dualcell paradigm that Kranz anatomy is essential for C4 carbon assimilation (Freitag and Stichler, 2002; Voznesenskaya et al, 2002; Akhani et al, 2005)

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