Transcriptional regulation of thylakoid galactolipid biosynthesis coordinated with chlorophyll biosynthesis during the development of chloroplasts in Arabidopsis.

Koichi Kobayashi,Hiroyuki Ohta,Shinsuke Baba,Tatsuru Masuda,Hajime Wada,Sho Fujii,Daichi Sasaki

doi:10.3389/fpls.2014.00272

Abstract

Biogenesis of thylakoid membranes in chloroplasts requires the coordinated synthesis of chlorophyll and photosynthetic proteins with the galactolipids monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), which constitute the bulk of the thylakoid lipid matrix. MGD1 and DGD1 are the key enzymes of MGDG and DGDG synthesis, respectively. We investigated the expression profiles of MGD1 and DGD1 in Arabidopsis to identify the transcriptional regulation that coordinates galactolipid synthesis with the synthesis of chlorophyll and photosynthetic proteins during chloroplast biogenesis. The expression of both MGD1 and DGD1 was repressed in response to defects in chlorophyll synthesis. Moreover, these genes were downregulated by norflurazon-induced chloroplast malfunction via the GENOMES-UNCOUPLED1-mediated plastid signaling pathway. Similar to other photosynthesis-associated nuclear genes, the expression of MGD1 and DGD1 was induced by light, in which both cytokinin signaling and LONG HYPOCOTYL5-mediated light signaling played crucial roles. The expression of these galactolipid-synthesis genes, and particularly that of DGD1 under continuous light, was strongly affected by the activities of the GOLDEN2-LIKE transcription factors, which are potent regulators of chlorophyll synthesis and chloroplast biogenesis. These results suggest tight transcriptional coordination of galactolipid synthesis with the formation of the photosynthetic chlorophyll–protein complexes during leaf development. Meanwhile, unlike the photosynthetic genes, the galactolipid synthesis genes were not upregulated during chloroplast biogenesis in the roots, even though the galactolipids accumulated with chlorophylls, indicating the importance of post-transcriptional regulation of galactolipid synthesis during root greening. Our data suggest that plants utilize complex regulatory mechanisms to modify galactolipid synthesis with chloroplast development during plant growth.

Highlights

Autotrophic plant growth depends on photosynthesis, which takes place in the photosynthetic plastids, i.e., the chloroplasts
TRANSCRIPTIONAL COORDINATION OF GALACTOLIPID SYNTHESIS WITH CHLOROPHYLL SYNTHESIS AND CHLOROPLAST DEVELOPMENT In our previous study, we reported that galactolipid biosynthetic activities profoundly influence gene expression related to photosynthesis and chlorophyll synthesis; a lack of galactolipid synthesis in the mgd1-2 mutant caused a marked downregulation of the photosynthesis-associated genes, whereas partial complementation of galactolipid synthesis in mgd1-2 by the alternative MGD2/MGD3 pathway attenuated the downregulation of these genes (Kobayashi et al, 2013a)
As with many photosynthesis-associated genes, MGD1 and DGD1 expression was regulated by plastid signaling, in which GUN1 played a pivotal role (Figure 2A)

Summary

Introduction

Autotrophic plant growth depends on photosynthesis, which takes place in the photosynthetic plastids, i.e., the chloroplasts. At the onset of chloroplast biogenesis, enzymes involved in chlorophyll synthesis are actively expressed together with nuclearencoded photosynthetic proteins, and are transported to the chloroplasts where chlorophyll synthesis takes place. Because chlorophylls and their intermediates are strong photosensitizers and are phototoxic, plant cells strictly regulate their metabolism to coincide with the development of the photosynthetic machinery. When chloroplast function is severely impaired, the expression of chlorophyll synthesis genes is downregulated globally along with nuclear photosynthetic genes, through plastid-to-nucleus retrograde signaling (Strand et al, 2003; Moulin et al, 2008)

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