Transcriptional Regulation of Tetrapyrrole Biosynthesis in Arabidopsis thaliana

Abstract

Biosynthesis of chlorophyll (Chl) involves many enzymatic reactions that share several first steps for biosynthesis of other tetrapyrroles such as heme, siroheme, and phycobilins. Chl allows photosynthetic organisms to capture light energy for photosynthesis but with simultaneous threat of photooxidative damage to cells. To prevent photodamage by Chl and its highly photoreactive intermediates, photosynthetic organisms have developed multiple levels of regulatory mechanisms to coordinate tetrapyrrole biosynthesis (TPB) with the formation of photosynthetic and photoprotective systems and to fine-tune the metabolic flow with the varying needs of Chl and other tetrapyrroles under various developmental and environmental conditions. Among a wide range of regulatory mechanisms of TPB, this review summarizes transcriptional regulation of TPB genes during plant development, with focusing on several transcription factors characterized in Arabidopsis thaliana. Key TPB genes are tightly coexpressed with other photosynthesis-associated nuclear genes and are induced by light, oscillate in a diurnal and circadian manner, are coordinated with developmental and nutritional status, and are strongly downregulated in response to arrested chloroplast biogenesis. LONG HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs, which are positive and negative transcription factors with a wide range of light signaling, respectively, target many TPB genes for light and circadian regulation. GOLDEN2-LIKE transcription factors directly regulate key TPB genes to fine-tune the formation of the photosynthetic apparatus with chloroplast functionality. Some transcription factors such as FAR-RED ELONGATED HYPOCOTYL3, REVEILLE1, and scarecrow-like transcription factors may directly regulate some specific TPB genes, whereas other factors such as GATA transcription factors are likely to regulate TPB genes in an indirect manner. Comprehensive transcriptional analyses of TPB genes and detailed characterization of key transcriptional regulators help us obtain a whole picture of transcriptional control of TPB in response to environmental and endogenous cues.

Keywords: Arabidopsis thaliana; chlorophyll; chloroplast; gene expression; heme; photosynthesis; porphyrin; tetrapyrrole.

FIGURE 1

Structures of major tetrapyrroles in plants. Chlorophylls contain magnesium (Mg) for the central metal, whereas hemes and siroheme contain iron (Fe). Phytochromobilin is a linear tetrapyrrole functioning as a chromophore of phytochromes.

FIGURE 2

The tetrapyrrole biosynthesis pathway (TPB) and TPB genes in Arabidopsis. TPB genes are classified into four clusters (c1, c2, c3, and c4 in red, green, gray, and blue boxes, respectively) based on Matsumoto et al. (2004) and the ATTED-II coexpression database (Obayashi et al., 2007). Possible direct regulation of TPB genes by HY5 (Lee J. et al., 2007) and GLKs (Waters et al., 2009) is indicated by orange and purple circles, respectively, with initial letters of each regulator. Detail information for each gene is in Supplementary Table S1. GGPP, geranylgeranyl pyrophosphate; Phytyl PP, phytyl pyrophosphate.

FIGURE 3

Coexpression networks of Arabidopsis genes involved in TPB. Coexpression networks of (A) TPB genes in cl (red), c2 (green), c3 (gray), and c4 (blue) clusters, (B) FLUORESCENT IN BLUE LIGHT (FLU, At3g14110), and (C) GluTR-binding protein (GBP, At3g21200) formed with photosynthesis-associated nuclear genes (PhANGs, orange), plastid ribosome-related genes (purple) and other nuclear genes (white). The coexpression networks were drawn by using the NetworkDrawer of the ATTED-II database v8.0 (Aoki et al., 2016; http://atted.jp/) with “add a few genes” and “Draw PPIs” options. Query genes are (A) all TPB genes listed in Supplementary Table S1, (B) FLU and its top 10 coexpressed genes (Supplementary Table S2) and (C) GBP and its top 10 coexpressed genes (Supplementary Table S3). Orange lines indicate highly reliable coexpression that is repeatedly detected in multiple coexpression data sets. Red dotted lines show links at protein–protein interaction levels. Query genes are in bold. Locus codes of PhANGs: ABC1K8, At5g64940; CLA1, At4g15560; cpSRP43, At2g47450; ECHID, At1g60550; GLK2, At5g44190; HCF107, At3g17040; LIL3:1, At4g17600; LIL3:2, At5g47110; PSBP1, At1g06680.

FIGURE 4

A model for regulating TPB genes (A) in the dark and (B) under light. The pathway for Chl biosynthesis is shown with important intermediates and enzymatic steps indicated by arrowheads. Key genes for the pathway shown in boxes are connected to each step that they involved. Arrows and bars represent positive and negative regulation, respectively. Dotted lines indicate indirect effects. Black and light blue colors represent activated and inactivated status, respectively. CK, cytokinin; CRY, cryptochrome; GA, gibberellic acid; PHY; phytochrome; SL, strigolactone.

FIGURE 5

Expression of TPB genes during leaf senescence. Gene expression data in Arabidopsis were obtained from the AtGenExpress Visualization Tool (http://jsp.weigelworld.org/expviz/expviz.jsp) in the public transcriptome database. The expression of each gene in senesced leaves of 35-day-old plants was normalized to that in the sixth true leaves of 17-day-old seedlings (dotted line).