Optimization of Light-Harvesting Pigment Improves Photosynthetic Efficiency

Maximizing light capture by light-harvesting pigment optimization represents an attractive but challenging strategy to improve photosynthetic efficiency. Here, we report that loss of a previously uncharacterized gene, HIGH PHOTOSYNTHETIC EFFICIENCY1 (HPE1), optimizes light-harvesting pigments, leading to improved photosynthetic efficiency and biomass production. Arabidopsis (Arabidopsis thaliana) hpe1 mutants show faster electron transport and increased contents of carbohydrates. HPE1 encodes a chloroplast protein containing an RNA recognition motif that directly associates with and regulates the splicing of target RNAs of plastid genes. HPE1 also interacts with other plastid RNA-splicing factors, including CAF1 and OTP51, which share common targets with HPE1. Deficiency of HPE1 alters the expression of nucleus-encoded chlorophyll-related genes, probably through plastid-to-nucleus signaling, causing decreased total content of chlorophyll (a+b) in a limited range but increased chlorophyll a/b ratio. Interestingly, this adjustment of light-harvesting pigment reduces antenna size, improves light capture, decreases energy loss, mitigates photodamage, and enhances photosynthetic quantum yield during photosynthesis. Our findings suggest a novel strategy to optimize light-harvesting pigments that improves photosynthetic efficiency and biomass production in higher plants.The tremendous increase in world population and environmental deterioration pose serious challenges to agricultural production and food security (Ray et al., 2013). To meet this challenge, crops with high yield potential need to be developed (Long et al., 2015). However, the yield traits that have played key roles during the green revolution have had their potential nearly exhausted; thus, new strategies are needed. Photosynthesis, the unique biological process responsible for the conversion of light energy to chemical forms, is the ultimate basis of crop yield (Zhu et al., 2010). Theoretically, enhancing photosynthetic efficiency should be an excellent strategy to increase crop yield. However, the improvement of photosynthetic efficiency has played only a minor role in the remarkable crop productivity improvement achieved in the last half-century (Zhu et al., 2010; Ort et al., 2015).In the light reactions of photosynthesis, light energy is used by chlorophyll and associated pigments, water is split, and electron transport on the chloroplast membrane reduces NADP, resulting in a proton gradient that powers the phosphorylation of ADP. NADPH and ATP power the Calvin cycle, which assimilates and reduces carbon dioxide to carbohydrate (Ort et al., 2015). Strategies to improve photosynthesis mainly include the optimization of light capture, light energy conversion in the light reaction, and carbon capture and conversion in the dark reaction (Ort et al., 2015). Previous research focused mainly on the optimization of dark reactions through the improvement of carbon capture and conversion to directly increase biomass (Miyagawa et al., 2001; Kebeish et al., 2007; Lin et al., 2014; Ort et al., 2015). However, less effort has been spent to optimize light capture and light energy conversion in the light reactions to improve the whole photosynthetic efficiency (Ort et al., 2015).Maximizing light capture by the adjustment of antenna size can optimize light capture and light energy conversion, but it is difficult to achieve (Blankenship and Chen, 2013). Antenna in photosynthetic systems typically consist of pigments specifically bound to membrane-associated proteins. These antenna pigment-protein complexes closely associate with the reaction center complexes and deliver absorbed energy to the reaction centers, where some of the energy originally in the photon is captured by electron-transfer processes (Blankenship, 2002; Green and Parson, 2003). However, light saturation could take place at intensities much lower than would be expected if every chlorophyll was able to carry out photosynthesis by itself (Blankenship, 2002). The light saturation problem also has been addressed from the antenna perspective, and many efforts are under way to truncate the antenna system in photosynthetic microorganisms. A smaller antenna associated with each reaction center will, in principle, also shift the light-response curve, so that light saturation sets in at higher intensities, thereby reducing excess light and increasing productive light. While the concept of increased efficiency due to reduced antenna size is simple, reaching this goal has not yet been achieved (Blankenship and Chen, 2013). In green algae, the reduction of light-harvesting pigments by decreasing the expression of the chlorophyll a oxygenase gene, which is responsible for the synthesis of chlorophyll b via the oxidation of chlorophyll a (Czarnecki and Grimm, 2012), led to efficient photosynthesis due to the balance between captured light and photochemical reactions (Perrine et al., 2012). However, there is still no success in higher plants.In this study, we performed a large-scale genetic screen using the model organism Arabidopsis (Arabidopsis thaliana) and identified two independent alleles of an uncharacterized gene that we named HIGH PHOTOSYNTHETIC EFFICIENCY1 (HPE1), whose mutation confers improved photosynthetic efficiency by optimizing light-harvesting pigment. A deficiency of HPE1 shows higher light reaction activity of photosynthesis, more efficient carbon fixation, and significantly increased biomass production. Interestingly, HPE1 encodes a chloroplast protein containing an RNA recognition motif and regulates the splicing of RNAs of plastid genes by directly associating with target RNAs. HPE1 mutation results in a splicing deficiency of plastid genes that may alter the expression of chlorophyll-related genes, probably through plastid-to-nucleus signaling. Altered expression of chlorophyll-related genes changes the content of light-harvesting pigments and optimizes the light-harvesting system. Our characterization of HPE1 mutants suggests a novel strategy to optimize light harvesting and improve photosynthetic efficiency in higher plants.