Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signalling

Abstract

Lhcb and other nuclear genes for chloroplastic proteins are regulated by several signals. Among them, light and retrograde signals from the plastid itself appear to act through closely related mechanisms. To investigate this interaction, we analysed an Arabidopsis mutant, hy1, deficient in plastidic heme oxygenase. hy1 is defective in phytochrome chromophore biosynthesis, which has other indirect effects on tetrapyrrole metabolism. We generated double mutants between hy1-6.2, genetically a null mutation, and three known gun (genome uncoupled) mutants, defective in retrograde plastid signalling. Recent molecular evidence shows GUN5 to be involved in tetrapyrrole metabolism (N. Mochizuki and J. Chory, manuscript in preparation). We observed hy1gun4 to be semi-albino plants, and hy1gun5 albino lethal, in a high-light-sensitive manner. Both double mutants showed defective greening and chloroplast development, and expressed Lhcb at reduced levels specifically in high light. Their degree of 'genome uncoupling' (Lhcb expression in the absence of functional chloroplasts) was similar to that observed in single mutants. These results can be interpreted as a metabolic (rather than genetic) interaction between HY1 and GUN4 or GUN5, and this in turn supports the involvement of tetrapyrroles as plastid signals. The tetrapyrrole precursor 5-aminolevulinic acid (ALA) inhibited Lhcb expression in hy1. Surprisingly, ALA also rescued photomorphogenesis of hy1. We speculate that either one tetrapyrrole intermediate, which can accumulate anomalously in hy1, or an altered ratio between two intermediates, plays a role as a repressor of Lhcb expression. gun1 did not exacerbate the plastid or Lhcb expression phenotype of hy1. This can be interpreted as a role for gun1 strictly on the same pathway as hy1 or, more likely, as evidence for the existence of at least one separate, non-tetrapyrrole related plastid signal.

Regulatory network of tetrapyrrole biosynthesis - studies of intracellular signalling involved in metabolic and developmental control of plastids

“…Their degree of`genome uncoupling' (Lhcb expression in the absence of functional chloroplasts) was similar to that observed in single mutants. These results can be interpreted as a metabolic (rather than genetic) interaction between HY1 and the GUN gene products (Vinti et al 2000). Several of the GUN loci were identi®ed.…”

Arabidopsis genomes uncoupled 5 ( GUN5 ) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction

“…We have found that gun2 and gun3 are alleles of hy1 and hy2, respectively, and that hy1-1 and hy2-1 (28) are gun mutants. hy1-6.2, a null allele (34), is also a gun mutant (48). HY1 and HY2 are required for the synthesis of phytochromobilin (P⌽B) from heme.…”

“…HY1 encodes a heme oxygenase that converts heme to biliverdin IX␣ (BV; refs. 35 and 36), and HY2 is thought to encode a P⌽B synthase that converts BV to 3(Z)-P⌽B (37 (48). Because gun2 is an allele of hy1, and because gun2 and gun3 affect chlorophyll accumulation like gun4 and gun5, it is likely that gun2-gun5 mutations affect the same plastid-to-nucleus signaling pathway by perturbing tetrapyrrole synthesis.…”

Arabidopsis cue mutants with defective plastids are impaired primarily in the photocontrol of expression of photosynthesis-associated nuclear genes

“…The hy1-6.2 mutant has also been described (Vinti et al, 2000). These mutants are available through the Nottingham Arabidopsis Stock Centre.…”

“…Lhcb1, in particular, has been found to be under the control of a variety of signals, including hormones, sugar, and particularly the circadian clock (Millar and Kay, 1996) and a signal through which nuclear gene expression responds to the physiological status of the plastid (plastid retrograde signals, Oelmu¨ller et al, 1986, Surpin et al, 2002. At least one class of 'plastid signals' has now been identified as a tetrapyrrole intermediary metabolite produced by plastids (Vinti et al, 2000;La Rocca et al, 2001;Mochizuki et al, 2001), specifically Mg-Proto (Strand et al, 2003). Very close connections appear to exist between both light and circadian clock responses of Lhcb (Wang and Tobin, 1998;Ma´s et al, 2003), and between light and 'plastid-signal' responses (Argu¨ello-Astorga and Herrera-Estrella, 1998;Lo´pez-Juez et al, 1998).…”