In plants, genes involved in photosynthesis are encoded separately in nuclei and plastids, and tight cooperation between these two genomes is therefore required for the development of functional chloroplasts. Golden2-like (GLK) transcription factors are involved in chloroplast development, directly targeting photosynthesis-associated nuclear genes for up-regulation. Although overexpression of GLKs leads to chloroplast development in non-photosynthetic organs, the mechanisms of coordination between the nuclear gene expression influenced by GLKs and the photosynthetic processes inside chloroplasts are largely unknown. To elucidate the impact of GLK-induced expression of photosynthesis-associated nuclear genes on the construction of photosynthetic systems, chloroplast morphology and photosynthetic characteristics in greenish roots of Arabidopsis thaliana lines overexpressing GLKs were compared with those in wild-type roots and leaves. Overexpression of GLKs caused up-regulation of not only their direct targets but also non-target nuclear and plastid genes, leading to global induction of chloroplast biogenesis in the root. Large antennae relative to reaction centers were observed in wild-type roots and were further enhanced by GLK overexpression due to the increased expression of target genes associated with peripheral light-harvesting antennae. Photochemical efficiency was lower in the root chloroplasts than in leaf chloroplasts, suggesting that the imbalance in the photosynthetic machinery decreases the efficiency of light utilization in root chloroplasts. Despite the low photochemical efficiency, root photosynthesis contributed to carbon assimilation in Arabidopsis. Moreover, GLK overexpression increased CO₂ fixation and promoted phototrophic performance of the root, showing the potential of root photosynthesis to improve effective carbon utilization in plants.
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.
The development of plant chloroplasts is regulated by various developmental, environmental, and hormonal cues. In Arabidopsis (), chloroplast development is repressed in roots via auxin signaling. However, roots develop chloroplasts when they are detached from the shoot. In contrast to auxin, cytokinin positively affects chloroplast development in roots, but the role and signaling pathway of cytokinin in the root greening response remain unclear. To understand the regulatory pathways of chloroplast development in the plant stress response, we examined the mechanisms underlying the conditional greening of detached roots. In wild-type Arabidopsis roots, shoot removal activates type B ARABIDOPSIS RESPONSE REGULATOR (ARR)-mediated cytokinin signaling and induces chlorophyll accumulation and photosynthetic remodeling. ARR1 and ARR12 are essential for up-regulating nucleus- and plastid-encoded genes associated with chloroplast development in detached roots. In this process, WOUND INDUCED DEDIFFERENTIATION1 and class B GATA transcription factors (B-GATAs) act upstream and downstream of ARRs, respectively. Overexpression of B-GATAs promotes root greening, as does shoot removal, dependent on a light signaling transcription factor, LONG HYPOCOTYL5. Auxin represses the root greening response independent of ARR signaling. (), a B-GATA, is strongly up-regulated in detached roots via ARR1 and ARR12 but is repressed by auxin, so may function at the point of convergence of cytokinin and auxin signaling in the root greening response.
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