Establishment of Photosynthesis through Chloroplast Development Is Controlled by Two Distinct Regulatory Phases

Abstract

Chloroplasts develop from undifferentiated proplastids present in meristematic tissue. Thus, chloroplast biogenesis is closely connected to leaf development, which restricts our ability to study the process of chloroplast biogenesis per se. As a consequence, we know relatively little about the regulatory mechanisms behind the establishment of the photosynthetic reactions and how the activities of the two genomes involved are coordinated during chloroplast development. We developed a single cell-based experimental system from Arabidopsis () with high temporal resolution allowing for investigations of the transition from proplastids to functional chloroplasts. Using this unique cell line, we could show that the establishment of photosynthesis is dependent on a regulatory mechanism involving two distinct phases. The first phase is triggered by rapid light-induced changes in gene expression and the metabolome. The second phase is dependent on the activation of the chloroplast and generates massive changes in the nuclear gene expression required for the transition to photosynthetically functional chloroplasts. The second phase also is associated with a spatial transition of the chloroplasts from clusters around the nucleus to the final position at the cell cortex. Thus, the establishment of photosynthesis is a two-phase process with a clear checkpoint associated with the second regulatory phase allowing coordination of the activities of the nuclear and plastid genomes.

Seedling Establishment: A Dimmer Switch-Regulated Process between Dark and Light Signaling

“…Based on these observations, three different chloroplast developmental phases have been defined: a heterotrophic phase of cellular proliferation and growth; a transition phase of chloroplast biogenesis where proteins such as the plastid translation apparatus and plastid enzymes accumulate; and a maturation phase of photosynthetic protein accumulation and photosynthetic activity. Similar phases take place during dicot leaf development, although their spatial distribution is not as distinct (López-Juez et al, 2008;Charuvi et al, 2012;Dubreuil et al, 2018). During biogenesis, the photosynthetic pigments chlorophyll and carotenoid are synthesized through activation of the NADPHdependent POR that converts protochlorophyllide into chlorophyll, and the PSY central carotenoid biosynthesis gene (Toledo-Ortiz et al, 2010).…”

“…In Arabidopsis, chloroplast retrograde signals from the chloroplast to the nucleus are able to optimize photosynthetic capacity and growth, prevent photodamage in high light environments, and fine-tune circadian-regulated processes by releasing lightspecific signals (Strand and Hernandez-Verdeja, 2018;Waters et al, 2009;Martín et al, 2016a;Dubreuil et al, 2018; Box 3). …”

Photosynthetic performance and photosynthesis-related gene expression coordinated in a shade-tolerant species Panax notoginseng under nitrogen regimes

“…N deficiency exhibits small chloroplast with lower internal conductance (g i, ) [16], and a large chloroplast with well-developed grana under high-N application has been reported in summer maize [17]. Indeed, Photosynthesis-related components are strongly regulated by leaf N and photosynthetic capacity is closely related to N content since more than 50% of total leaf N is allocated to photosynthetic machinery and proteins of Calvin cycle represent the majority of leaf N [18][19][20][21]. In leaves of developing maize (Zea mays), N deficiency results in an obvious decrease in photosynthesis with an reduction in activities of phosphor enolpyruvate carboxylase (PEPC), pyruvate orthophosphate di-kinase (PPDK) and ribulose 1, 5bisphosphate carboxylase (Rubisco) [17,[22][23][24].…”

Non-canonical Features of Pentatricopeptide Repeat Protein-Facilitated RNA Editing in Arabidopsis Chloroplasts

“…In Arabidopsis, full-length CREF3 transcripts could not be amplified according to the gene annotation in TAIR10 (Figure 1b). RNA-seq datasets (Dubreuil et al, 2018) also suggest that there is no reads mapped to the first annotated exon and intron of CREF3. Therefore, rapid amplification of 5' cDNA ends (5'RACE) was performed to map the 5' end of CREF3 transcripts.…”