Functional Characterization of the GATA Transcription Factors GNC and CGA1 Reveals Their Key Role in Chloroplast Development, Growth, and Division in Arabidopsis    

Abstract

Chloroplasts develop from proplastids in a process that requires the interplay of nuclear and chloroplast genomes, but key steps in this developmental process have yet to be elucidated. Here, we show that the nucleus-localized transcription factors GATA NITRATE-INDUCIBLE CARBON-METABOLISM-INVOLVED (GNC) and CYTOKININ-RESPONSIVE GATA1 (CGA1) regulate chloroplast development, growth, and division in Arabidopsis (Arabidopsis thaliana). GNC and CGA1 are highly expressed in green tissues, and the phytohormone cytokinin regulates their expression. A gnc cga1 mutant exhibits a reduction in overall chlorophyll levels as well as in chloroplast size in the hypocotyl. Ectopic overexpression of either GNC or CGA1 promotes chloroplast biogenesis in hypocotyl cortex and root pericycle cells, based on increases in the number and size of the chloroplasts, and also results in expanded zones of chloroplast production into the epidermis of hypocotyls and cotyledons and into the cortex of roots. Ectopic overexpression also promotes the development of etioplasts from proplastids in dark-grown seedlings, subsequently enhancing the deetiolation process. Inducible expression of GNC demonstrates that GNCmediated chloroplast biogenesis can be regulated postembryonically, notably so for chloroplast production in cotyledon epidermal cells. Analysis of the gnc cga1 loss-of-function and overexpression lines supports a role for these transcription factors in regulating the effects of cytokinin on chloroplast division. These data support a model in which GNC and CGA1 serve as two of the master transcriptional regulators of chloroplast biogenesis, acting downstream of cytokinin and mediating the development of chloroplasts from proplastids and enhancing chloroplast growth and division in specific tissues.

Cross-Repressive Interactions between SOC1 and the GATAs GNC and GNL/CGA1 in the Control of Greening, Cold Tolerance, and Flowering Time in Arabidopsis

“…PIF3 is at least one member of the PIF family of transcription factors that controls GNC and GNL expression. As recently reported, the greening phenotype of gnc and gnl mutants may be explained by their role in directly and indirectly regulating the expression of chlorophyll biosynthetic genes and chloroplast development, growth, and division (Hudson et al, 2011;Chiang et al, 2012). GNC and GNL have also been identified as transcription repression targets of the floral homeotic genes APETALA3 and PISTILLATA (Mara and Irish, 2008).…”

“…Both GNC and GNL have recently been characterized as positive regulators of chlorophyll biosynthesis and chloroplast division (Richter et al, 2010;Hudson et al, 2011;Chiang et al, Figure 2. GNC and GNL act upstream of SOC1.…”

Rice Cytokinin GATA Transcription Factor1 Regulates Chloroplast Development and Plant Architecture

“…It is unclear whether Cga1 expression increases as a direct result of N application or indirectly increased through N-induced cytokinin production. However, results obtained in Arabidopsis indicate a requirement for functional cytokinin receptors and downstream ARRs for increased expression to occur (Naito et al, 2007;Hudson et al, 2011;Chiang et al, 2012). The rapid increase in Cga1 expression following cytokinin application indicates a higher degree of response to cytokinin than to N or light (Fig.…”

“…Transgenic Arabidopsis plants with altered expression of CGA1 have been shown to exhibit differences in germination, chlorophyll content, chloroplast number, leaf size, flowering time, and senescence (Mara and Irish, 2008;Richter et al, 2010;Hudson et al, 2011). This includes recent reports showing that ectopic overexpression promotes chloroplast biogenesis in cells where they are not typically found (Köllmer et al, 2011;Chiang et al, 2012). These data indicate that GNC and CGA1 function as key transcriptional regulators of chloroplast biogenesis in Arabidopsis.…”

Combined Large-Scale Phenotyping and Transcriptomics in Maize Reveals a Robust Growth Regulatory Network

“…However, two of the Arabidopsis orthologs of these ribosomal proteins, RPL21C and RPL3, were shown to be essential for plastid development and embryogenesis (Yin et al, 2012;Tiller and Bock, 2014), while reduced gene expression of the plastid-specific ribosomal protein PSRP5 resulted in severely delayed plant growth due to reduced plastid translation (Tiller et al, 2012). Additionally, this subnetwork contained one GATA TF (GRMZM2G039586) homologous to Arabidopsis GCN, described to function in chloroplast development, likely by regulating chloroplast division (Chiang et al, 2012). Interestingly, the majority of the other genes in this subnetwork were chloroplast targeted and involved in chloroplast development and/or functioning.…”