Chloroplast development in green plant tissues: the interplay between light, hormone, and transcriptional regulation

Abstract

Chloroplasts are best known for their role in photosynthesis, but they also allow nitrogen and sulphur assimilation, amino acid, fatty acid, nucleotide and hormone synthesis. How chloroplasts develop is therefore relevant to these diverse and fundamental biological processes, but also to attempts at their rational redesign. Light is strictly required for chloroplast formation in all angiosperms and directly regulates the expression of hundreds of chloroplast-related genes. Light also modulates the levels of several hormones including brassinosteriods, cytokinins, auxins and gibberellins, which themselves control chloroplast development particularly during early stages of plant development. Transcription factors such as GOLDENLIKE1&2 (GLK1&2), GATA NITRATE-INDUCIBLE CARBON METABOLISM-INVOLVED (GNC) and CYTOKININ-RESPONSIVE GATA FACTOR 1 (CGA1) act downstream of both light and phytohormone signalling to regulate chloroplast development. Thus, in green tissues transcription factors, light signalling and hormone signalling form a complex network regulating the transcription of chloroplast-and photosynthesis-related genes to control the development and number of chloroplasts per cell. We use this conceptual framework to identify points of regulation that could be harnessed to modulate chloroplast abundance and increase photosynthetic efficiency of crops, and to highlight future avenues to overcome gaps in current knowledge.

Correlated retrograde and developmental regulons implicate multiple retrograde signals as coordinators of chloroplast development in maize

“…The expression dynamics of maize orthologs of CGA and GNC (Figure 7) are consistent with the possibility that they are up-regulated by CIA2/CIL, and that they, in turn, up-regulate genes involved in PEPmediated transcription and plastid translation. The expression dynamics of G2 and GLK1 are similar to that of PhANGs, supporting the current view that they activate PhANGs relatively late in the chloroplast biogenesis program (Waters et al, 2009;Cackett et al, 2021). Each gene in this hypothetical regulatory cascade is impacted by retrograde signals: g2, glk1, cia2/cil, and one cga1/gnc homolog are down-regulated in our mutants, whereas the other cga1/gnc homolog is up-regulated (Figure 3B,Supplementary Dataset S5).…”

Auxin Plays a Role in the Adaptation of Rice to Anaerobic Germination and Seedling Establishment

“…In submerged fields, rapid coleoptile emergence results in the appearance of a coleoptile tip above the soil during AG; meanwhile, coleoptile elongation and seedling establishment were affected by light (Biswas and Yamauchi, 1997). Light is known to control various physiological processes in the plant, such as leaf expansion, shade-avoidance response, seed germination, the greening of seedlings, and chloroplast development (Salazar-Iribe and De-la-Peña, 2020; Cackett et al, 2021; Wang et al, 2022). It has been demonstrated that phytochrome B (phyB) is involved in these processes by regulating auxin levels in response to light conditions (Zhang et al, 2014).…”

“…On the contrary, earlier greening timing was observed when IAA function was inhibited, suggesting that the greening of the coleoptile in response to auxin signaling might play a vital role in influencing seed germination and seedling establishment under submergence in rice. It has been reported that chloroplast development and photomorphogenesis in green plant tissues depend on the interplay between light and phytohormones signaling pathways, including auxin signaling (Salazar-Iribe and De-la-Peña, 2020; Cackett et al, 2021; Wang et al, 2022) but the interplay underlying these signaling pathways in modulating AG tolerance is still unclear. Moreover, whether sugar could affect the accumulation of endogenous free IAA to influence AG and seedling establishment in rice remains elusive.…”

The FtsH-Inactive Protein FtsHi5 Is Required for Chloroplast Development and Protein Accumulation in Chloroplasts at Low Ambient Temperature in Arabidopsis

“…Chloroplasts in de-etiolated plants are developed from proplastids which are small and undifferentiated plastids. Upon light, the biogenesis of thylakoids begins immediately accompanied by the coordinated synthesis and assembly of proteins, chlorophylls and lipids in both space and time (Cackett et al, 2021). The plastid retains a functional genome which encodes about 100 proteins, while most of the other ∼2,000-3,000 proteins within chloroplasts are imported from the cytosol via the translocon at the outer envelope membrane of chloroplasts (TOC) and translocon at the inner envelope membrane of chloroplasts (TIC) systems (Li and Chiu, 2010;Jarvis and Lopez-Juez, 2013).…”

“…Light-regulating chloroplast development requires transcription factors such as ELONGATED HYPOCOTYL 5 (HY5), GOLDEN2-LIKEs (GLKs), GATA NITRATE-INDUCIBLE CARBON-METABOLISM-INVOLVED (GNC) which appear to regulate the expression of genes essential for chloroplast development, chlorophyll biosynthesis, and photosynthesis (Chen et al, 2016;Gangappa and Botto, 2016;Cackett et al, 2021). At the same time, chloroplast development is regulated by environmental temperatures.…”