Tangled evolutionary processes with commonality and diversity in plastidial glycolipid synthesis in photosynthetic organisms

Abstract

In photosynthetic organisms, the photosynthetic membrane constitutes a scaffold for light-harvesting complexes and photosynthetic reaction centers. Three kinds of glycolipids, namely monogalactosyldiacylglycerol, digalactosyldiacylglycerol, and sulfoquinovosyldiacylglycerol, constitute approximately 80-90% of photosynthetic membrane lipids and are well conserved from tiny cyanobacteria to the leaves of huge trees. These glycolipids perform a wide variety of functions beyond biological membrane formation. In particular, the capability of adaptation to harsh environments through regulation of membrane glycolipid composition is essential for healthy growth and development of photosynthetic organisms. The genome analysis and functional genetics of the model seed plant Arabidopsis thaliana have yielded many new findings concerning the biosynthesis, regulation, and functions of glycolipids. Nevertheless, it remains to be clarified how the complex biosynthetic pathways and well-organized functions of glycolipids evolved in early and primitive photosynthetic organisms, such as cyanobacteria, to yield modern photosynthetic organisms like land plants. Recently, genome data for many photosynthetic organisms have been made available as the fruit of the rapid development of sequencing technology. We also have reported the draft genome sequence of the charophyte alga Klebsormidium flaccidum, which is an intermediate organism between green algae and land plants. Here, we performed a comprehensive phylogenic analysis of glycolipid biosynthesis genes in oxygenic photosynthetic organisms including K. flaccidum. Based on the results together with membrane lipid analysis of this alga, we discuss the evolution of glycolipid synthesis in photosynthetic organisms. This article is part of a Special Issue entitled: Plant Lipid Biology edited by Kent D. Chapman and Ivo Feussner.

Configuration of the sugar head of glycolipids in thylakoid membranes

“…These galactolipids are highly conserved, i.e., from the thylakoid membranes of cyanobacteria to the chloroplasts of algae and land plants (Boudière et al, 2014;Hori et al, 2016). MGDG and DGDG comprise up to 50 mol% and 30 mol%, respectively, of thylakoid membrane lipids of these photosynthetic organisms.…”

Lipid remodeling regulator 1 (LRL1) is differently involved in the phosphorus‐depletion response from PSR1 in Chlamydomonas reinhardtii

“…During the RNA‐seq analysis, another change was observed in genes involved in sulfolipid synthesis. Upregulation of sulfoquinovosyl diacylglycerol (SQDG) biosynthesis genes is a major event in the adaptation response to P‐starvation in photosynthetic organisms (Shimojima, ; Hori et al ., ) and generally occurs under low P conditions to substitute for phospholipid breakdown (Essigmann et al ., ; Hartel et al ., ). CrSQD1 and CrSQD2 were repressed in lrl1‐1 under P‐depletion (Figure ).…”

“…It is well understood that to maintain Pi-homeostasis in cells exposed to P-depletion, the expression of genes encoding various phosphatases and those responsible for phospholipid degradation are increased (Nakamura, 2013). Synthesis of SQDG is also enhanced to compensate for phospholipid degradation and to maintain membrane integrity throughout oxygenic photosynthetic organisms (Hori et al, 2016). The RNA-seq comparison and confirmation by real-time PCR suggested that the P-starvation response, including SQDG synthesis is suppressed in lrl1-1.…”

“…The use of a low PiÀresponsive promoter and a TF such as PSR1 for TAG overproduction has shed some light on the clarification of regulatory mechanisms involved in TAG synthesis under P-starvation in C. reinhardtii (Ngan et al, 2015;Bajhaiya et al, 2016). Concomitantly with TAG accumulation, membrane remodeling is a typical response under P-starvation and occurs widely throughout oxygenic photosynthetic organisms from cyanobacteria and phytoplankton to land plants (Nakamura et al, 2009;Hori et al, 2016;Shemi et al, 2016). In this response, phospholipids are replaced by non-P glycolipids and/or betaine lipids, which releases inorganic phosphate from membranes, thus providing phosphate to other important cellular processes (Shimojima et al, 2013;Hori et al, 2016).…”

“…Concomitantly with TAG accumulation, membrane remodeling is a typical response under P-starvation and occurs widely throughout oxygenic photosynthetic organisms from cyanobacteria and phytoplankton to land plants (Nakamura et al, 2009;Hori et al, 2016;Shemi et al, 2016). In this response, phospholipids are replaced by non-P glycolipids and/or betaine lipids, which releases inorganic phosphate from membranes, thus providing phosphate to other important cellular processes (Shimojima et al, 2013;Hori et al, 2016). Moreover, a regulatory gene involved in the transition from N-depleted to N-replete conditions, Compromised Hydrolysis of Triacylglycerols 7 (CHT7), which may be a repressor of cellular quiescence, provides a mechanistic insight into how cells exit quiescence after nutrient deprivation (Tsai et al, 2014).…”