Advances from chlorophyll biosynthesis to photosynthetic adaptation, evolution and signaling

Abstract

Chlorophyll (Chl)-mediated oxygenic photosynthesis supports life on earth. From a view of evolution, ‘survival of the fittest’ facilitates oxygenic photosynthetic organisms evolved from cyanobacteria to higher plants by ever more sophisticated photosystems including antennae, Chls, and carotenoids. Increasing advances highlight (1) the H subunit of magnesium chelatase (CHLH)-mediated Chl biosynthesis at the branch point that also channels to heme biosynthesis by the common tetrapyrrole pathway, associated to various GUN (genomes uncoupled) anterograde signals; (2) the multiple functions of carotenoids generated by mevalonic acid (MVA) and methylerythritol phosphate (MEP) pathways, also linked to several hormonal and anterograde signals; (3) the size and composition of the modularly-assembled pigment-protein supercomplexes vary with green lineages adaptive to growth niches at genetic and structural levels, showing more Chls with more growth and fitness. Under favorable environments, the photosynthetic electron transfer chain (PETC) is responsible for sugar biosynthesis, fundamental to plant growth by auxin and cytokinin. While under stressful environments, the impeded PETC triggers ROS, consequently triggering both phytohormone signaling (ABA, SA, JA, and Eth) and retrograde signaling (PAP, MEcPP, and GUNs). These regulators weave a crosstalk network between nucleus-to-plastid anterograde signaling and plastid-to-nucleus retrograde signaling, finally fine-tuning plant development and adaptation. In this review, we outline photosystematic evolution and chloroplast-derived signals, paving the way to understanding plant survival and fitness by optimizing sugar biosynthesis and utilization.