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 GNC-mediated 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.
Highlights
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
The transcriptional response to cytokinin is mediated by the type-B Arabidopsis response regulators (ARRs; Sakai et al, 2001; Mason et al, 2005; Argyros et al, 2008), with ARR1, ARR10, and ARR12 regulating the majority of this transcriptional response (Argyros et al, 2008)
Wild-type and arr1-3 arr12-1 seedlings were treated with 10 mM BA or a dimethyl sulfoxide (DMSO) vehicle control for up to 4 h, and the expression of both GATA NITRATE-INDUCIBLE CARBON-METABOLISM-INVOLVED (GNC) and CYTOKININ-RESPONSIVE GATA1 (CGA1) was analyzed in the shoot by quantitative reverse transcription (qRT)-PCR (Fig. 1B)
Summary
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. Analysis of the gnc cga loss-of-function and overexpression lines supports a role for these transcription factors in regulating the effects of cytokinin on chloroplast division. Far, a detailed picture of the physiological function of this GATA family of transcriptional regulators is lacking We hypothesize that these transcription factors are part of a pathway that links light and cytokinin signaling with the differentiation of photosynthetically active chloroplasts from proplastids and their proliferation throughout plant development. To characterize these two proteins functionally and to place them into the pathway that mediates chloroplast development, we performed an extensive physiological analysis of both loss- and gain-of-function lines. We propose a model in which GNC and CGA1 serve as key positive regulators of chloroplast biogenesis, integrating both light and cytokinin inputs to mediate chloroplast development, growth, and division
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