7-Hydroxymethyl chlorophyll a reductase functions in metabolic channeling of chlorophyll breakdown intermediates during leaf senescence

Sakuraba, Yasuhito; Kim, Ye-Sol; Yoo, Soo-Cheul; Hörtensteiner, Stefan; Paek, Nam‐Chon

doi:10.1016/j.bbrc.2012.11.050

Cited by 69 publications

(87 citation statements)

References 30 publications

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“…3A) is reminiscent of trimerization of LHC-II in plants (52). Because chlorophyll b degradation is essential for LHC-II turnover (11)(12)(13), and HCAR directly interacts with LHC-II (14), it is plausible that their similarity reflects a biological function (Fig. 9A).…”

Section: Discussionmentioning

confidence: 99%

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Crystal Structure and Catalytic Mechanism of 7-Hydroxymethyl Chlorophyll a Reductase

Wang

Liu

2016

Journal of Biological Chemistry

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7-Hydroxymethyl chlorophyll a reductase (HCAR) catalyzes the second half-reaction in chlorophyll b to chlorophyll a conversion. HCAR is required for the degradation of light-harvesting complexes and is necessary for efficient photosynthesis by balancing the chlorophyll a/b ratio. Reduction of the hydroxymethyl group uses redox cofactors [4Fe-4S] cluster and FAD to transfer electrons and is difficult because of the strong carbonoxygen bond. Here, we report the crystal structure of Arabidopsis HCAR at 2.7-Å resolution and reveal that two [4Fe-4S] clusters and one FAD within a very short distance form a consecutive electron pathway to the substrate pocket. In vitro kinetic analysis confirms the ferredoxin-dependent electron transport chain, thus supporting a proton-activated electron transfer mechanism. HCAR resembles a partial reconstruction of an archaeal F 420 -reducing [NiFe] hydrogenase, which suggests a common mode of efficient proton-coupled electron transfer through conserved cofactor arrangements. Furthermore, the trimeric form of HCAR provides a biological clue of its interaction with light-harvesting complex II.The balance of chlorophyll metabolism is vital for plants to ensure an efficient photosynthesis and to support various biological processes (1). To this end, chlorophyll biosynthesis and degradation need to cooperate with the chlorophyll cycle, a process of interconversion between chlorophyll a and chlorophyll b (2-5). The chlorophyll a/b ratio is important for stabilization of the light-harvesting complexes (LHCs).2 In general, an increase of the chlorophyll b level correlates with accumulation of LHCs and thus improvement of light usage efficiency in normal condition; excessive chlorophyll b, however, could impair the energy transfer pathway by replacing chlorophyll a in LHCs (6). In the chlorophyll cycle, both the forward (from chlorophyll a to chlorophyll b) and the backward conversions use 7-hydroxymethyl chlorophyll a (HMChl) as the intermediate (see Fig. 1A). Chlorophyll a oxygenase catalyzes two sequential oxidation reactions from the 7-methyl to the 7-formyl group (7, 8); chlorophyll b reductase and HMChl reductase (HCAR) catalyze the reverse two sequential reduction reactions (9, 10). In addition, the reverse reduction reactions are essential for LHC-II turnover because chlorophyll degradation precedes degradation of the LHC-II apoprotein, and the chlorophyll catabolic process starts from chlorophyll a (11-13). Direct interaction between HCAR and LHC-II has been observed in senescing chloroplasts (14).HCAR is the last identified enzyme of the chlorophyll cycle (10). Bioinformatic studies have discovered that the HCAR homologues range from archaea to plants (15). They perform different roles, such as the Here, the crystal structure of Arabidopsis HCAR reveals the ligating cysteines of the two [4Fe-4S] clusters, residues involved in FAD binding, and a deep substrate pocket adjacent to the flavin ring. We established a quantitative in vitro assay, confirmed the reduced ferredoxin (Fd red )-...

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Section: Discussionmentioning

confidence: 99%

“…In addition, the reverse reduction reactions are essential for LHC-II turnover because chlorophyll degradation precedes degradation of the LHC-II apoprotein, and the chlorophyll catabolic process starts from chlorophyll a (11)(12)(13). Direct interaction between HCAR and LHC-II has been observed in senescing chloroplasts (14).…”

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confidence: 99%

Crystal Structure and Catalytic Mechanism of 7-Hydroxymethyl Chlorophyll a Reductase

Wang

Liu

2016

Journal of Biological Chemistry

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“…3). When plants are placed in the dark for 3 days, the level of NYC1 mRNA increases by over 10-fold (Sakuraba et al 2013). During senescence, the entire plant is organized for reproduction, whereas the light conditions primarily affect photosynthesis.…”

Section: Discussionmentioning

confidence: 99%

“…NYC1 is expressed during dark-induced or natural senescence. Conversely, the NOL level is independent of the plant conditions (Sakuraba et al 2013). …”

Section: Introductionmentioning

confidence: 99%

Chlorophyll b degradation by chlorophyll b reductase under high-light conditions

2015

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After the high-light treatment, the maximum quantum efficiency of the photosystem II photochemistry was lower in nyc1 and nyc1/nol plants than in wild-type and nol plants. A larger light-harvesting system would damage photosystem II in nyc1 and nyc1/nol plants. The fluorescence spectroscopy of the leaves indicated that photosystem I was also damaged by the excess LHCII in nyc1/nol plants. These observations suggest that chlorophyll b degradation by NYC1 is the initial reaction for the optimization of the light-harvesting capacity under high-light conditions.

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“…We previously proposed that differences in their capacities to interact with CCEs cause the divergent functions of three SGR homologs (Sakuraba et al 2015b). SGR1 and SGRL can interact with six CCEs (NYC1, NOL, HCAR, PPH, PAO, and RCCR) and the light-harvesting complexes II (LHCII; Sakuraba et al 2012Sakuraba et al , 2013Sakuraba et al , 2014b. Although SGR2 also interacts with LHCII proteins, it hardly interacts with CCEs (Sakuraba et al 2014c), leading to the interruption of formation of SGR1-CCE or SGRL-CCE complexes at LHCII.…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription

et al. 2015

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The Arabidopsis transcriptional factor NAC016 directly activates chlorophyll degradation during leaf senescence by binding to the promoter of SGR1 and upregulating its transcription. During leaf senescence or abiotic stress in Arabidopsis thaliana, STAYGREEN1 (SGR1) promotes chlorophyll (Chl) degradation, acting with Chl catabolic enzymes, but the mechanism regulating SGR1 transcription remains largely unknown. Here, we show that the Arabidopsis senescence-associated NAC transcription factor NAC016 directly activates SGR1 transcription. Under senescence-promoting conditions, the expression of SGR1 was downregulated in nac016-1 mutants and upregulated in NAC016-overexpressing (NAC016-OX) plants. By yeast one-hybrid and chromatin immunoprecipitation assays, we found that NAC016 directly binds to the SGR1 promoter, which contains the NAC016-specific binding motif (termed the NAC016BM). Furthermore, nac016-1 SGR1-OX plants showed an early leaf yellowing phenotype, similar to SGR1-OX plants, confirming that NAC016 directly activates SGR1 expression in the leaf senescence regulatory cascade. Although we found that NAC016 activates SGR1 expression in senescing leaves, this transcriptional regulation is considerably weaker in maturing seeds; the seeds of sgr1-1 mutants (also known as nonyellowing1-1, nye1-1) stayed green, while the seeds of nac016-1 mutants turned from green to yellow normally. We also found that the abscisic acid (ABA) signaling-related transcription factor genes ABI5 and EEL and the ABA biosynthesis gene AAO3, which activate SGR1 expression directly or indirectly, were significantly downregulated in nac016-1 mutants and upregulated in NAC016-OX plants. However, the NAC016BM does not exist in their promoter regions, indicating that NAC016 may indirectly activate these ABA signaling and biosynthesis genes, probably by directly activating transcriptional cascades regulated by the NAC transcription factor NAP. The NAC016-mediated regulatory cascades of SGR1 and other Chl degradation-related genes are discussed. and chromatin immunoprecipitation assays, we found that NAC016 directly binds to the SGR1 21 promoter, which contains the NAC016-specific binding motif (termed the NAC016BM). 22Furthermore, nac016-1 SGR1-OX plants showed an early leaf yellowing phenotype, similar to 23 SGR1-OX plants, confirming that NAC016 directly activates SGR1 expression in the leaf 24 senescence regulatory cascade. Although we found that NAC016 activates SGR1 expression in 25 senescing leaves, this transcriptional regulation is considerably weaker in maturing seeds; the 26 seeds of sgr1-1 mutants (also known as nonyellowing1-1, nye1-1) stayed green, while the seeds of 27 nac016-1 mutants turned from green to yellow normally. We also found that the abscisic acid (ABA) 28 signaling-related transcription factor genes ABI5 and EEL and the ABA biosynthesis gene AAO3, 29 which activate SGR1 expression directly or indirectly, were significantly downregulated in nac016-1 30 mutants and upregulated in NAC016-OX plants. Howeve...

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7-Hydroxymethyl chlorophyll a reductase functions in metabolic channeling of chlorophyll breakdown intermediates during leaf senescence

Cited by 69 publications

References 30 publications

Crystal Structure and Catalytic Mechanism of 7-Hydroxymethyl Chlorophyll a Reductase

Crystal Structure and Catalytic Mechanism of 7-Hydroxymethyl Chlorophyll a Reductase

Chlorophyll b degradation by chlorophyll b reductase under high-light conditions

Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription

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