Plastid-Targeted Cyanobacterial Flavodiiron Proteins Maintain Carbohydrate Turnover and Enhance Drought Stress Tolerance in Barley

Abstract

Chloroplasts, the sites of photosynthesis in higher plants, have evolved several means to tolerate short episodes of drought stress through biosynthesis of diverse metabolites essential for plant function, but these become ineffective when the duration of the stress is prolonged. Cyanobacteria are the closest bacterial homologs of plastids with two photosystems to perform photosynthesis and to evolve oxygen as a byproduct. The presence of Flv genes encoding flavodiiron proteins has been shown to enhance stress tolerance in cyanobacteria. In an attempt to support the growth of plants exposed to drought, the Synechocystis genes Flv1 and Flv3 were expressed in barley with their products being targeted to the chloroplasts. The heterologous expression of both Flv1 and Flv3 accelerated days to heading, increased biomass, promoted the number of spikes and grains per plant, and improved the total grain weight per plant of transgenic lines exposed to drought. Improved growth correlated with enhanced availability of soluble sugars, a higher turnover of amino acids and the accumulation of lower levels of proline in the leaf. Flv1 and Flv3 maintained the energy status of the leaves in the stressed plants by converting sucrose to glucose and fructose, immediate precursors for energy production to support plant growth under drought. The results suggest that sugars and amino acids play a fundamental role in the maintenance of the energy status and metabolic activity to ensure growth and survival under stress conditions, that is, water limitation in this particular case. Engineering chloroplasts by Flv genes into the plant genome, therefore, has the potential to improve plant productivity wherever drought stress represents a significant production constraint.

Here comes the sun: How optimization of photosynthetic light reactions can boost crop yields

“…In angiosperms, in which FDPs are absent, introduction of two FDPs could therefore possibly replace several ROS scavenging enzymes and reactions, thus saving energy and nitrogen sources or adding extra protection. Indeed, transgenic lines of tobacco, Arabidopsis and barley expressing cyanobacterial Flv1/3 or Flv2/4 proteins in chloroplasts showed that FDPs are able to act as additional electron sinks in plants as well, particularly under stress conditions, such as drought and fluctuating light stress, thereby improving photosynthetic performance (Gómez et al, 2018; Tula et al, 2020; Shahinnia et al, 2021; Vicino et al, 2021). In other instances, two FDPs from the moss Physcomitrella patens were introduced into Arabidopsis and rice, revealing similar effects of FDPs and CET in maintaining the pmf under unfavorable growth conditions (Yamamoto et al, 2016; Wada et al, 2018).…”

“…The heterodimer Flv1/3 is conserved in all cyanobacteria and is responsible for oxygen photoreduction downstream of PSI in a Mehler-like reaction that does not produce ROS (Allahverdiyeva et al, 2013), whereas the heterodimer Flv2/4 is only present in β-cyanobacteria and was reported to be involved in photoprotection of both PSII and PSI (Zhang et al, 2009(Zhang et al, , 2012Bersanini et al, 2014Bersanini et al, , 2017Chukhutsina et al, 2015;Santana-Sanchez et al, 2019). In angiosperms, in which FDPs are absent, introduction of two FDPs could therefore possibly replace Tognetti et al, 2006Tognetti et al, , 2007aTognetti et al, , 2007bZurbriggen et al, 2008;Shvaleva et al, 2009;Coba de la Peña et al 2010;Giró et al, 2011;Ceccoli et al, 2012;Lodeyro et al, 2012;Gharechahi et al, 2015;Mayta et al, 2018;Gómez et al, 2020;Niazian et al, 2021 Overexpression of cyanobacterial and moss FDPs AET Arabidopsis, tobacco, barley, rice Yes Drought/ fluctuating light stress Yamamoto et al, 2016;Gómez et al, 2018;Wada et al, 2018;Tula et al, 2020;Shahinnia et al, 2021;Vicino et al, 2021 Abbreviations: AET, alternative electron transfer; ATP, adenosine triphosphate; LHC, light-harvesting complex; NPQ, nonphotochemical quenching.…”

Engineering Climate-Change-Resilient Crops: New Tools and Approaches

“…Better growth was correlated with enhanced availability of soluble sugars, a higher turnover of amino acids and the accumulation of lower levels of proline in the leaf. Flv1/Flv3 maintained the energy status of the leaves in the stressed plants by converting sucrose to glucose and fructose, immediate precursors for energy production to support plant growth under drought [85]. The results suggest that sugars and amino acids play a fundamental role in the maintenance of energy status and metabolic activity to ensure growth and survival of plants exposed to drought (Figure 1).…”

“…To evaluate the contribution of Flv1/Flv3 to the growth of plants exposed to drought in crops, the Synechocystis genes encoding these two proteins were expressed in barley, with their products being targeted to chloroplasts (Figure 1). The heterologous expression of Flv1/Flv3 accelerated days to heading, increased biomass, promoted the number of spikes and grains per plant, and improved the total grain weight per plant of transgenic lines exposed to drought [85]. Better growth was correlated with enhanced availability of soluble sugars, a higher turnover of amino acids and the accumulation of lower levels of proline in the leaf.…”

Photosystems under high light stress: throwing light on mechanism and adaptation

“…In angiosperms, in which FDPs are absent, the introduction of FDPs could therefore possibly replace several ROS-scavenging enzymes and reactions, thus saving energy and nitrogen sources or adding extra protection. Transgenic lines of tobacco, Arabidopsis and barley expressing cyanobacterial Flv1/3 or Flv2/4 proteins in chloroplasts showed that FDPs can act as additional electron sinks in plants as well, particularly under fluctuating light stress, thereby improving photosynthetic performance (Gómez et al 2018, Tula et al 2020, Shahinnia et al 2021, Vicino et al 2021.…”