Loss of Nuclear Gene Expression during the Phytochrome A-Mediated Far-Red Block of Greening Response

Abstract

We have examined the expression of the HEMA1 gene, which encodes the key chlorophyll synthesis enzyme glutamyl-tRNA reductase, during the phytochrome A-mediated far-red light (FR) block of greening response in Arabidopsis. Our results demonstrate that the FR block of greening comprises two separate responses: a white light (WL) intensity-independent response that requires 3 d of FR and is associated with a loss of expression of the nuclear genes HEMA1 and Lhcb following the transfer to WL (transcriptionally coupled response) and a WL intensity-dependent response that is induced by 1 d of FR and is transcriptionally uncoupled. Both responses required phytochrome A. The transcriptionally uncoupled response correlated with a deregulation of tetrapyrrole synthesis and potential photooxidative damage and was inhibited by cytokinin. The transcriptionally coupled FR response was additive with the loss of expression following Norflurazoninduced photobleaching and was absent in the presence of sucrose or after lower fluence rate (1 mol m Ϫ2 s Ϫ1 ) FR treatments. Both pathways leading to the loss of nuclear gene expression were inhibited by overexpression of NADPH: protochlorophyllide oxidoreductase, indicating a role for plastid signaling in the FR-mediated pathway. The significance of identifying a distinct phytochrome A-mediated plastid signaling pathway is discussed.The coordinated synthesis of chlorophylls and chlorophyll-binding proteins is critically important during emergence of the etiolated seedling into light, and is essential for the normal development of functional chloroplasts. The key regulatory step in chlorophyll synthesis is the formation of 5-aminolevulinic acid (ALA), which is rate limiting for the tetrapyrrole pathway (Beale and Castelfranco, 1974). As a consequence, inhibition of ALA synthesis through inhibitors or anti-sense approaches (Hö fgen et al., 1994;Kumar and Sö ll, 2000) has a dramatic effect on chloroplast development, resulting in plants that are highly susceptible to photobleaching. In a converse manner, excess ALA also affects chloroplast development (Kittsteiner et al., 1991) and leads to an overaccumulation of porphyrins, which can lead to severe photooxidative damage (Reinbothe et al., 1996).Uncoupling tetrapyrrole synthesis from chloroplast development may also be achieved by irradiating etiolated seedlings with far-red (FR) light (Barnes et al., 1996;Runge et al., 1996). Growth of Arabidopsis seedlings under continuous FR (FRc) can induce partial photomorphogenesis with reduced hypocotyl elongation growth and cotyledon expansion. These responses are characteristic of the FR-high-irradiance response (FR-HIR;Mancinelli, 1994), which is a specific function of phytochrome A (Smith, 1995). FRc irradiation can also activate many of the processes required for chloroplast development. These include the induction of nuclear genes encoding chlorophyll a/b-binding proteins and other photosynthetic proteins (Kuno et al., 2000;Tepperman et al., 2001) and the transcription of chloroplast genes ...

GUN4-Porphyrin Complexes Bind the ChlH/GUN5 Subunit of Mg-Chelatase and Promote Chlorophyll Biosynthesis inArabidopsis

“…These findings implicated Mg-chelatase, Mg-PPIX biosynthesis, or chloroplastic tetrapyrrole metabolism in the plastid-to-nucleus signaling that regulates photosynthesis-related gene expression (Mochizuki et al, 2001). Data generated using distinct experimental approaches provide evidence that Mg-chelatase, Mg-PPIX biosynthesis, or chloroplastic tetrapyrrole metabolism can affect gene expression in Arabidopsis and other plants (Oster et al, 1996;Papenbrock et al, 2000b;Vinti et al, 2000;La Rocca et al, 2001McCormac and Terry, 2002;Strand et al, 2003;Alawady and Grimm, 2005;Gadjieva et al, 2005;Ankele et al, 2007;Zhang et al, 2011), Chlamydomonas reinhardtii (Johanningmeier and Howell, 1984;Kropat et al, 1997Kropat et al, , 2000Falciatore et al, 2005;Vasileuskaya et al, 2005;von Gromoff et al, 2008), and Synechocystis (Osanai et al, 2009). Mg-PPIX also regulates DNA replication in Cyanidioschyzon merolae and tobacco (Nicotiana tabacum) BY-2 cell cultures (Kobayashi et al, 2009).…”

Tetrapyrrole Metabolism inArabidopsis thaliana

“…On the other hand, gun1 is a mutant of chloroplast localized pentatricopeptide protein, which appeared to act independently from tetrapyrrole pathway (Koussevitzky et al 2007). Interestingly, POR-overexpressing Arabidopsis also shows a gun phenotype (McCormac and Terry 2002b). Subsequently, it is reported that wild type plants accumulate high amounts of MgProto IX when grown on NF, whereas this accumulation occurs only partially or is absent in gun2 and gun5 mutants (Strand et al 2003).…”

PIF3 is a repressor of chloroplast development

“…Misregulation of the tetrapyrrole synthesis pathway commonly leads to a photobleaching phenotype (e.g., refs. 29 and 30), and overac- cumulation of Pchlide is well established as leading to photooxidative damage (29), for example, in the FR block of greening response (31).…”