GLK transcription factors regulate chloroplast development in a cell‐autonomous manner

Abstract

SummaryIn a number of land plants, Golden2-like (GLK) genes encode a pair of partially redundant nuclear transcription factors that are required for the expression of nuclear photosynthetic genes and for chloroplast development. As chloroplast biogenesis depends on close co-operation between the nuclear and plastid compartments, GLK gene function must be dependent on tight intracellular control. However, the extent to which GLK-mediated chloroplast development depends on intercellular communication is not known. Here we used sector analysis to show that GLK proteins operate cell-autonomously in leaf mesophyll cells. To establish whether GLK proteins are able to influence adjacent cell layers, we used tissue-specific promoters to restrict GLK gene expression to the epidermis and to the phloem. GLK genes driven by the Arabidopsis epidermal FIDDLEHEAD (FDH) and MERISTEM LAYER1 (AtML1) promoters failed to rescue the pale-green Atglk1 Atglk2 mutant phenotype, confirming the suggestion that GLK proteins can only influence chloroplast development intracellularly. An exception to this rule was seen in lines in which GLK genes were expressed in the phloem. However, we believe that the partial complementation of the mutant phenotype that was observed resulted from phloem unloading, as opposed to inherent properties of GLK proteins. We conclude that GLK proteins act in a cell-autonomous manner to coordinate and maintain the photosynthetic apparatus within individual cells. Significantly, this suggests that GLK proteins provide a means to fine-tune photosynthesis according to the differential requirements of cells within the leaf.

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

“…Both the GNC/CGA1 and GLK families play roles in chloroplast development. Like the gnc cga1 double mutant, the glk1 glk2 double mutant exhibits a decrease in chlorophyll levels (Fitter et al, 2002), the defect in the glk1 glk2 mutant being primarily owed to a decreased abundance of thylakoid membranes and grana (Waters et al, 2008). Overexpression of both GNC/CGA1 and GLK family members leads to an increase of chlorophyll content compared with wild-type plants (Waters et al, 2008;Hudson et al, 2011), but the ectopic production of chloroplasts in the epidermis and roots has only been reported in the GNC/CGA1 overexpression lines.…”

“…Like the gnc cga1 double mutant, the glk1 glk2 double mutant exhibits a decrease in chlorophyll levels (Fitter et al, 2002), the defect in the glk1 glk2 mutant being primarily owed to a decreased abundance of thylakoid membranes and grana (Waters et al, 2008). Overexpression of both GNC/CGA1 and GLK family members leads to an increase of chlorophyll content compared with wild-type plants (Waters et al, 2008;Hudson et al, 2011), but the ectopic production of chloroplasts in the epidermis and roots has only been reported in the GNC/CGA1 overexpression lines. However, overexpression of rice GLK1 (OsGLK1) induces chloroplast development in nongreen rice callus cells (Nakamura et al, 2009), consistent with both GLK and GNC/CGA1 transcription factors serving to positively regulate chloroplast development from proplastids, although the conditions under which this has been observed differ.…”

“…Three transcription factor families (GNC/CGA1, GLK, and CRF) are now implicated in directly and positively regulating chloroplast biogenesis (Bi et al, 2005;Naito et al, 2007;Mara and Irish, 2008;Waters et al, 2008Okazaki et al, 2009;Richter et al, 2010;Hudson et al, 2011;Köllmer et al, 2011;Fig. 9).…”

Network Inference Analysis Identifies an APRR2-Like Gene Linked to Pigment Accumulation in Tomato and Pepper Fruits

“…In Arabidopsis (Arabidopsis thaliana) leaf tissue, Golden2-like (GLK2) transcription factors are necessary to coregulate and synchronize the expression of a suite of nuclear photosynthetic genes, and GLKoverexpressing lines in Arabidopsis accumulate higher amounts of chlorophyll (Waters et al, 2008(Waters et al, , 2009. Recently, the up-regulation of a GLK2-like transcription factor in tomato has also been shown to elevate levels of chlorophyll and carotenoids in tomato, and a lesion in this gene is responsible for the uniform ripening phenotype (Powell et al, 2012).…”

Retrograde Signals Navigate the Path to Chloroplast Development

“…The GLK transcription factors have been shown to be implicated in fruit development, for 404 example through the pale siliques of the Arabidopsis glk2 mutant or the identification of GLK2 405 as the locus affected in the uniform ripening (u) mutation that results in uniformly green 406 tomatoes (Waters et al, 2008;Powell et al, 2012;Nguyen et al, 2014). Similarly, a correlation 407 was reported between CaGLK2 and variation in chlorophyll content and colour in pepper fruit 408 (Brand et al, 2014).…”