Search
2024 Volume 4
Article Contents
REVIEW   Open Access    

Regulatory mechanism of a light-dependent protochlorophyllide oxidoreductase in chlorophyll biosynthesis and environmental adaptation

More Information
  • Chlorophyll is a vital component of photosynthesis and must be produced throughout the plant life cycle. Light-dependent protochlorophyllide oxidoreductase (LPOR) is a pivotal enzyme in the chlorophyll biosynthesis pathway, catalyzing the conversion of Pchlide to Chlide. The presence of different types of LPOR ensures the efficient synthesis of chlorophyll in photosynthetic organisms during the dark-light transition. In addition to the transcriptional, translational, and post-translational regulation of LPOR function under different abiotic stresses, the nature of the substrate also influences LPOR function. Here, a perspective on chlorophyll synthesis and the development of chloroplasts is offered, the importance of LPOR in safeguarding plant light energy utilization is summarized, the gene expression pattern and structural-functional features of LPOR are outlined, as well as the role of LPOR in abiotic stress tolerance response, the catalytic mechanism of LPOR as well as the modulation of LPOR by light signals and other environmental factors are discussed. The aim is to provide references for the cultivation and innovation of plant germplasm resources with stress tolerance.
  • 加载中
  • [1]

    Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA. 2012. Recent patterns of crop yield growth and stagnation. Nature Communications 3:1293

    doi: 10.1038/ncomms2296

    CrossRef   Google Scholar

    [2]

    Ray DK, Mueller ND, West PC, Foley JA. 2013. Yield trends are insufficient to double global crop production by 2050. PLoS One 8:e66428

    doi: 10.1371/journal.pone.0066428

    CrossRef   Google Scholar

    [3]

    Zhu XG, Long SP, Ort DR. 2010. Improving photosynthetic efficiency for greater yield. Annual Review of Plant Biology 61:235−61

    doi: 10.1146/annurev-arplant-042809-112206

    CrossRef   Google Scholar

    [4]

    Hatfield JL. 2014. Radiation use efficiency: evaluation of cropping and management systems. Agronomy Journal 106:1820−27

    doi: 10.2134/agronj2013.0310

    CrossRef   Google Scholar

    [5]

    Reynolds M, Foulkes MJ, Slafer GA, Berry P, Parry MAJ, et al. 2009. Raising yield potential in wheat. Journal of Experimental Botany 60:1899−918

    doi: 10.1093/jxb/erp016

    CrossRef   Google Scholar

    [6]

    Bailey-Serres J, Parker JE, Ainsworth EA, Oldroyd GED, Schroeder JI. 2019. Genetic strategies for improving crop yields. Nature 575:109−18

    doi: 10.1038/s41586-019-1679-0

    CrossRef   Google Scholar

    [7]

    Calvin M, Benson AA. 1948. The path of carbon in photosynthesis. Science 107:476−80

    doi: 10.1126/science.107.2784.476

    CrossRef   Google Scholar

    [8]

    Simkin AJ, Kapoor L, Doss CGP, Hofmann TA, Lawson T, et al. 2022. The role of photosynthesis related pigments in light harvesting, photoprotection and enhancement of photosynthetic yield in planta. Photosynthesis Research 152:23−42

    doi: 10.1007/s11120-021-00892-6

    CrossRef   Google Scholar

    [9]

    Tanaka R, Tanaka A. 2011. Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807:968−76

    doi: 10.1016/j.bbabio.2011.01.002

    CrossRef   Google Scholar

    [10]

    Wietrzynski W, Engel BD. 2021. Chlorophyll biogenesis sees the light. Nature Plants 7:380−81

    doi: 10.1038/s41477-021-00900-6

    CrossRef   Google Scholar

    [11]

    Stenbaek A, Jensen PE. 2010. Redox regulation of chlorophyll biosynthesis. Phytochemistry 71:853−59

    doi: 10.1016/j.phytochem.2010.03.022

    CrossRef   Google Scholar

    [12]

    Aarti PD, Tanaka R, Tanaka A. 2006. Effects of oxidative stress on chlorophyll biosynthesis in cucumber (Cucumis sativus) cotyledons. Physiologia Plantarum 128:186−97

    doi: 10.1111/j.1399-3054.2006.00720.x

    CrossRef   Google Scholar

    [13]

    Holtorf H, Reinbothe S, Reinbothe C, Bereza B, Apel K. 1995. Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.). Proceedings of the National Academy of Sciences of the United States of America 92:3254−8

    doi: 10.1073/pnas.92.8.3254

    CrossRef   Google Scholar

    [14]

    Selstam E, Sandelius AS. 1984. A Comparison between Prolamellar Bodies and Prothylakoid Membranes of Etioplasts of Dark-Grown Wheat Concerning Lipid and Polypeptide Composition. Plant Physiology 76:1036−40

    doi: 10.1104/pp.76.4.1036

    CrossRef   Google Scholar

    [15]

    Solymosi K, Schoefs B. 2010. Etioplast and etio-chloroplast formation under natural conditions: the dark side of chlorophyll biosynthesis in angiosperms. Photosynthesis Research 105:143−66

    doi: 10.1007/s11120-010-9568-2

    CrossRef   Google Scholar

    [16]

    Fujita Y. 1996. Protochlorophyllide reduction: a key step in the greening of plants. Plant and Cell Physiology 37:411−21

    doi: 10.1093/oxfordjournals.pcp.a028962

    CrossRef   Google Scholar

    [17]

    Heyes DJ, Zhang S, Taylor A, Johannissen LO, Hardman SJO, et al. 2021. Photocatalysis as the 'master switch' of photomorphogenesis in early plant development. Nature Plants 7:268−76

    doi: 10.1038/s41477-021-00866-5

    CrossRef   Google Scholar

    [18]

    Yamazaki S, Nomata J, Fujita Y. 2006. Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana. Plant Physiology 142:911−22

    doi: 10.1104/pp.106.086090

    CrossRef   Google Scholar

    [19]

    Vedalankar P, Tripathy BC. 2019. Evolution of light-independent protochlorophyllide oxidoreductase. Protoplasma 256:293−312

    doi: 10.1007/s00709-018-1317-y

    CrossRef   Google Scholar

    [20]

    Chernomor O, Peters L, Schneidewind J, Loeschcke A, Knieps-Grünhagen E, et al. 2021. Complex Evolution of Light-Dependent protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: origin, Phylogeny, and Function. Molecular Biology and Evolution 38:819−37

    doi: 10.1093/molbev/msaa234

    CrossRef   Google Scholar

    [21]

    Kaschner M, Loeschcke A, Krause J, Minh BQ, Heck A, et al. 2014. Discovery of the first light-dependent protochlorophyllide oxidoreductase in anoxygenic phototrophic bacteria. Molecular Microbiology 93:1066−78

    doi: 10.1111/mmi.12719

    CrossRef   Google Scholar

    [22]

    Stolárik T, Nožková V, Nosek L, Pavlovič A. 2018. Dark chlorophyll synthesis may provide a potential for shade tolerance as shown by a comparative study with seedlings of European larch (Larix decidua) and Norway spruce (Picea abies). Trees 32:951−65

    doi: 10.1007/s00468-018-1688-x

    CrossRef   Google Scholar

    [23]

    Gabruk M, Mysliwa-Kurdziel B. 2020. The origin, evolution and diversification of multiple isoforms of light-dependent protochlorophyllide oxidoreductase (LPOR): focus on angiosperms. Biochemical Journal 477:2221−36

    doi: 10.1042/BCJ20200323

    CrossRef   Google Scholar

    [24]

    Yang J, Cheng Q. 2004. Origin and evolution of the light-dependent protochlorophyllide oxidoreductase (LPOR) genes. Plant Biology 6:537−44

    doi: 10.1055/s-2004-821270

    CrossRef   Google Scholar

    [25]

    Paddock T, Lima D, Mason ME, Apel K, Armstrong GA. 2012. Arabidopsis light-dependent protochlorophyllide oxidoreductase A (PORA) is essential for normal plant growth and development. Plant Molecular Biology 78:447−60

    doi: 10.1007/s11103-012-9873-6

    CrossRef   Google Scholar

    [26]

    Erdei AL, Kósa A, Kovács-Smirová L, Böddi B. 2016. Wavelength-dependent photooxidation and photoreduction of protochlorophyllide and protochlorophyll in the innermost leaves of cabbage (Brassica oleracea var. capitata L.). Photosynthesis Research 128:73−83

    doi: 10.1007/s11120-015-0200-3

    CrossRef   Google Scholar

    [27]

    Kwon CT, Kim SH, Song G, Kim D, Paek NC. 2017. Two NADPH: Protochlorophyllide Oxidoreductase (POR) isoforms play distinct roles in environmental adaptation in rice. Rice 10:1

    doi: 10.1186/s12284-016-0141-2

    CrossRef   Google Scholar

    [28]

    Buhr F, Lahroussi A, Springer A, Rustgi S, von Wettstein D, et al. 2017. NADPH: protochlorophyllide oxidoreductase B (PORB) action in Arabidopsis thaliana revisited through transgenic expression of engineered barley PORB mutant proteins. Plant Molecular Biology 94:45−59

    doi: 10.1007/s11103-017-0592-x

    CrossRef   Google Scholar

    [29]

    Millerd A, McWilliam JR. 1968. Studies on a maize mutant sensitive to low temperature I. Influence of temperature and light on the production of chloroplast pigments. Plant Physiology 43:1967−72

    doi: 10.1104/pp.43.12.1967

    CrossRef   Google Scholar

    [30]

    Talaat NB. 2013. RNAi based simultaneous silencing of all forms of light-dependent NADPH: protochlorophyllide oxidoreductase genes result in the accumulation of protochlorophyllide in tobacco (Nicotiana tabacum). Plant Physiology and Biochemistry 71:31−36

    doi: 10.1016/j.plaphy.2013.06.025

    CrossRef   Google Scholar

    [31]

    Fusada N, Masuda T, Kuroda H, Shiraishi T, Shimada H, et al. 2000. NADPH-protochlorophyllide oxidoreductase in cucumber is encoded by a single gene and its expression is transcriptionally enhanced by illumination. Photosynthesis Research 64:147−54

    doi: 10.1023/A:1006418608647

    CrossRef   Google Scholar

    [32]

    Erdei N, Barta C, Hideg E, Böddi B. 2005. Light-induced wilting and its molecular mechanism in epicotyls of dark-germinated pea (Pisum sativum L.) seedlings. Plant and Cell Physiology 46:185−91

    doi: 10.1093/pcp/pci012

    CrossRef   Google Scholar

    [33]

    Huq E, Al-Sady B, Hudson M, Kim C, Apel K, et al. 2004. PHYTOCHROME-INTERACTING FACTOR 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305:1937−41

    doi: 10.1126/science.1099728

    CrossRef   Google Scholar

    [34]

    Kojima K, Oshita M, Nanjo Y, Kasai K, Tozawa Y, et al. 2007. Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Molecular Microbiology 65:936−47

    doi: 10.1111/j.1365-2958.2007.05836.x

    CrossRef   Google Scholar

    [35]

    Oosawa N, Masuda T, Awai K, Fusada N, Shimada H, et al. 2000. Identification and light-induced expression of a novel gene of NADPH-protochlorophyllide oxidoreductase isoform in Arabidopsis thaliana. FEBS Letters 474:133−36

    doi: 10.1016/S0014-5793(00)01568-4

    CrossRef   Google Scholar

    [36]

    Armstrong GA, Runge S, Frick G, Sperling U, Apel K. 1995. Identification of NADPH: protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiology 108:1505−17

    doi: 10.1104/pp.108.4.1505

    CrossRef   Google Scholar

    [37]

    Su Q, Frick G, Armstrong G, Apel K. 2001. POR C of Arabidopsis thaliana: a third light- and NADPH-dependent protochlorophyllide oxidoreductase that is differentially regulated by light. Plant Molecular Biology 47:805−13

    doi: 10.1023/A:1013699721301

    CrossRef   Google Scholar

    [38]

    Matsumoto F, Obayashi T, Sasaki-Sekimoto Y, Ohta H, Takamiya K, et al. 2004. Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system. Plant Physiology 135:2379−91

    doi: 10.1104/pp.104.042408

    CrossRef   Google Scholar

    [39]

    Paddock TN, Mason ME, Lima DF, Armstrong GA. 2010. Arabidopsis protochlorophyllide oxidoreductase A (PORA) restores bulk chlorophyll synthesis and normal development to a porB porC double mutant. Plant Molecular Biology 72:445−57

    doi: 10.1007/s11103-009-9582-y

    CrossRef   Google Scholar

    [40]

    Ji S, Grimm B, Wang P. 2023. Chloroplast SRP43 and SRP54 independently promote thermostability and membrane binding of light-dependent protochlorophyllide oxidoreductases. The Plant Journal 115:1583−98

    doi: 10.1111/tpj.16339

    CrossRef   Google Scholar

    [41]

    Zhao Y, Han Q, Ding C, Huang Y, Liao J, et al. 2020. Effect of low temperature on chlorophyll biosynthesis and chloroplast biogenesis of rice seedlings during greening. International Journal of Molecular Sciences 21:1390

    doi: 10.3390/ijms21041390

    CrossRef   Google Scholar

    [42]

    Reinbothe S, Reinbothe C, Holtorf H, Apel K. 1995. Two NADPH: protochlorophyllide oxidoreductases in barley: evidence for the selective disappearance of PORA during the light-induced greening of etiolated seedlings. The Plant Cell 7:1933−40

    doi: 10.2307/3870200

    CrossRef   Google Scholar

    [43]

    Reinbothe C, Pollmann S, Desvignes C, Weigele M, Beck E, et al. 2004. LHPP, the light-harvesting NADPH: protochlorophyllide (Pchlide) oxidoreductase: Pchlide complex of etiolated plants, is developmentally expressed across the barley leaf gradient. Plant Science 167:1027−41

    doi: 10.1016/j.plantsci.2004.05.044

    CrossRef   Google Scholar

    [44]

    Reinbothe C, Buhr F, Bartsch S, Desvignes C, Quigley F, et al. 2006. In vitro-mutagenesis of NADPH: protochlorophyllide oxidoreductase B: two distinctive protochlorophyllide binding sites participate in enzyme catalysis and assembly. Molecular Genetics and Genomics 275:540−52

    doi: 10.1007/s00438-006-0109-9

    CrossRef   Google Scholar

    [45]

    Menon BRK, Hardman SJO, Scrutton NS, Heyes DJ. 2016. Multiple active site residues are important for photochemical efficiency in the light-activated enzyme protochlorophyllide oxidoreductase (POR). Journal of Photochemistry and Photobiology B-Biology 161:236−43

    doi: 10.1016/j.jphotobiol.2016.05.029

    CrossRef   Google Scholar

    [46]

    Kavanagh KL, Jörnvall H, Persson B, Oppermann U. 2008. Medium- and short-chain dehydrogenase/reductase gene and protein families : the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cellular and Molecular Life Sciences 65:3895−906

    doi: 10.1007/s00018-008-8588-y

    CrossRef   Google Scholar

    [47]

    Zhang S, Heyes DJ, Feng L, Sun W, Johannissen LO, et al. 2019. Structural basis for enzymatic photocatalysis in chlorophyll biosynthesis. Nature 574:722−25

    doi: 10.1038/s41586-019-1685-2

    CrossRef   Google Scholar

    [48]

    Taylor A, Zhang S, Johannissen LO, Sakuma M, Phillips RS, et al. 2024. Mechanistic implications of the ternary complex structural models for the photoenzyme protochlorophyllide oxidoreductase. The FEBS Journal 291:1404−21

    doi: 10.1111/febs.17025

    CrossRef   Google Scholar

    [49]

    Schneidewind J, Krause F, Bocola M, Stadler AM, Davari MD, et al. 2019. Consensus model of a cyanobacterial light-dependent protochlorophyllide oxidoreductase in its pigment-free apo-form and photoactive ternary complex. Communications Biology 2:351

    doi: 10.1038/s42003-019-0590-4

    CrossRef   Google Scholar

    [50]

    Floris D, Kühlbrandt W. 2021. Molecular landscape of etioplast inner membranes in higher plants. Nature Plants 7:514−23

    doi: 10.1038/s41477-021-00896-z

    CrossRef   Google Scholar

    [51]

    Savchenko GE, Klyuchareva EA, Stupak AP. 2003. Fluorescence of the protein of the prolamellar bodies of etioplasts. Journal of Applied Spectroscopy 70:907−12

    doi: 10.1023/B:JAPS.0000016310.66731.0e

    CrossRef   Google Scholar

    [52]

    Cazzonelli CI, Hou X, Alagoz Y, Rivers J, Dhami N, et al. 2020. A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development. eLife 9:e45310

    doi: 10.7554/eLife.45310

    CrossRef   Google Scholar

    [53]

    Myśliwa-Kurdziel B, Turek E, Malec P. 2013. Protochlorophyllide forms in etiolated seedlings of photoreceptor mutants of Arabidopsis thaliana — Is chlorophyll biosynthesis controlled by cooperation between phytochromes and phototropins? In Photosynthesis Research for Food, Fuel and the Future. Advanced Topics in Science and Technology in China. Berlin, Heidelberg: Springer. pp. 381−84. DOI: 10.1007/978-3-642-32034-7_79

    [54]

    Heyes DJ, Hardman SJO, Hedison TM, Hoeven R, Greetham GM, et al. 2015. Excited-state charge separation in the photochemical mechanism of the light-driven enzyme protochlorophyllide oxidoreductase. Angewandte Chemie International Edition 54:1512−15

    doi: 10.1002/anie.201409881

    CrossRef   Google Scholar

    [55]

    Reinbothe S, Gray J, Rustgi S, von Wettstein D, Reinbothe C. 2015. Cell growth defect factor 1 is crucial for the plastid import of NADPH: protochlorophyllide oxidoreductase A in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 112:5838−43

    doi: 10.1073/pnas.1506339112

    CrossRef   Google Scholar

    [56]

    Kim C, Ham H, Apel K. 2005. Multiplicity of different cell- and organ-specific import routes for the NADPH-protochlorophyllide oxidoreductases A and B in plastids of Arabidopsis seedlings. The Plant Journal 42:329−40

    doi: 10.1111/j.1365-313X.2005.02374.x

    CrossRef   Google Scholar

    [57]

    Aronsson H, Sundqvist C, Dahlin C. 2003. POR hits the road: import and assembly of a plastid protein. Plant Molecular Biology 51:1−7

    doi: 10.1023/A:1020795415631

    CrossRef   Google Scholar

    [58]

    Reinbothe S, Pollmann S, Springer A, James RJ, Tichtinsky G, et al. 2005. A role of Toc33 in the protochlorophyllide-dependent plastid import pathway of NADPH: protochlorophyllide oxidoreductase (POR) A. The Plant Journal 42:1−12

    doi: 10.1111/j.1365-313X.2005.02353.x

    CrossRef   Google Scholar

    [59]

    Reinbothe S, Bartsch S, Rossig C, Davis MY, Yuan S, et al. 2019. A protochlorophyllide (Pchlide) a oxygenase for plant viability. Frontiers in Plant Science 10:593

    doi: 10.3389/fpls.2019.00593

    CrossRef   Google Scholar

    [60]

    Lee JY, Lee HS, Song JY, Jung YJ, Reinbothe S, et al. 2013. Cell growth defect factor1/CHAPERONE-LIKE PROTEIN OF POR1 plays a role in stabilization of light-dependent protochlorophyllide oxidoreductase in Nicotiana benthamiana and Arabidopsis. The Plant Cell 25:3944−60

    doi: 10.1105/tpc.113.111096

    CrossRef   Google Scholar

    [61]

    Herbst J, Pang X, Roling L, Grimm B. 2024. A novel tetratricopeptide-repeat protein, TTP1, forms complexes with glutamyl-tRNA reductase and protochlorophyllide oxidoreductase during tetrapyrrole biosynthesis. Journal of Experimental Botany 75:2027−45

    doi: 10.1093/jxb/erad491

    CrossRef   Google Scholar

    [62]

    Hanf R, Fey S, Schmitt M, Hermann G, Dietzek B, et al. 2012. Catalytic efficiency of a photoenzyme − an adaptation to natural light conditions. ChemPhysChem 13:2013−15

    doi: 10.1002/cphc.201200194

    CrossRef   Google Scholar

    [63]

    Kósa A, Böddi B. 2012. Dominance of a 675 nm chlorophyll(ide) form upon selective 632.8 or 654 nm laser illumination after partial protochlorophyllide phototransformation. Photosynthesis Research 114:111−20

    doi: 10.1007/s11120-012-9782-1

    CrossRef   Google Scholar

    [64]

    Lebedev N, Karginova O, McIvor W, Timko MP. 2001. Tyr275 and Lys279 stabilize NADPH within the catalytic site of NADPH: protochlorophyllide oxidoreductase and are involved in the formation of the enzyme photoactive state. Biochemistry 40:12562−74

    doi: 10.1021/bi0105025

    CrossRef   Google Scholar

    [65]

    Menon BRK, Davison PA, Hunter CN, Scrutton NS, Heyes DJ. 2010. Mutagenesis alters the catalytic mechanism of the light-driven enzyme protochlorophyllide oxidoreductase. Journal of Biological Chemistry 285:2113−19

    doi: 10.1074/jbc.M109.071522

    CrossRef   Google Scholar

    [66]

    Liu R, Wang L, Meng Y, Li F, Nie H, Lu H. 2022. Role of thylakoid lipids in protochlorophyllide oxidoreductase activation: allosteric mechanism elucidated by a computational study. International Journal of Molecular Sciences 24:307

    doi: 10.3390/ijms24010307

    CrossRef   Google Scholar

    [67]

    Fujii S, Kobayashi K, Nagata N, Masuda T, Wada H. 2018. Digalactosyldiacylglycerol Is Essential for Organization of the Membrane Structure in Etioplasts. Plant Physiology 177:1487−97

    doi: 10.1104/pp.18.00227

    CrossRef   Google Scholar

    [68]

    Kauss D, Bischof S, Steiner S, Apel K, Meskauskiene R. 2012. FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++-branch of this pathway. FEBS Letters 586:211−16

    doi: 10.1016/j.febslet.2011.12.029

    CrossRef   Google Scholar

    [69]

    Hey D, Rothbart M, Herbst J, Wang P, Müller J, et al. 2017. LIL3, a Light-Harvesting Complex Protein, Links Terpenoid and Tetrapyrrole Biosynthesis in Arabidopsis thaliana. Plant Physiology 174:1037−50

    doi: 10.1104/pp.17.00505

    CrossRef   Google Scholar

    [70]

    Kovacheva S, Ryberg M, Sundqvist C. 2000. ADP/ATP and protein phosphorylation dependence of phototransformable protochlorophyllide in isolated etioplast membranes. Photosynthesis Research 64:127−36

    doi: 10.1023/A:1006451824312

    CrossRef   Google Scholar

    [71]

    Wang F, Yan J, Chen X, Jiang C, Liu Y, et al. 2019. Light regulation of chlorophyll biosynthesis in plants. Journal of Horticulture 46:975−94

    Google Scholar

    [72]

    Valdés AE, Rizzardi K, Johannesson H, Para A, Sundås-Larsson A, et al. 2012. Arabidopsis thaliana TERMINAL FLOWER2 is involved in light-controlled signalling during seedling photomorphogenesis. Plant, Cell and Environment 35:1013−25

    doi: 10.1111/j.1365-3040.2011.02468.x

    CrossRef   Google Scholar

    [73]

    Brouwer B, Gardeström P, Keech O. 2014. In response to partial plant shading, the lack of phytochrome A does not directly induce leaf senescence but alters the fine-tuning of chlorophyll biosynthesis. Journal of Experimental Botany 65:4037−49

    doi: 10.1093/jxb/eru060

    CrossRef   Google Scholar

    [74]

    Lim J, Park JH, Jung S, Hwang D, Nam HG, et al. 2018. Antagonistic roles of PhyA and PhyB in far-red light-dependent leaf senescence in Arabidopsis thaliana. Plant & Cell Physiology 59:1753−64

    doi: 10.1093/pcp/pcy153

    CrossRef   Google Scholar

    [75]

    Alameldin HF, Oh S, Hernandez AP, Montgomery BL. 2020. Nuclear-encoded sigma factor 6 (SIG6) is involved in the block of greening response in Arabidopsis thaliana. American Journal of Botany 107:329−38

    doi: 10.1002/ajb2.1423

    CrossRef   Google Scholar

    [76]

    Liang M, Gu D, Lie Z, Yang Y, Lu L, et al. 2023. Regulation of chlorophyll biosynthesis by light-dependent acetylation of NADPH: protochlorophyll oxidoreductase A in Arabidopsis. Plant Science 330:111641

    doi: 10.1016/j.plantsci.2023.111641

    CrossRef   Google Scholar

    [77]

    Moon J, Zhu L, Shen H, Huq E. 2008. PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 105:9433−38

    doi: 10.1073/pnas.0803611105

    CrossRef   Google Scholar

    [78]

    Liu X, Chen CY, Wang KC, Luo M, Tai R, et al. 2013. PHYTOCHROME INTERACTING FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. The Plant Cell 25:1258−73

    doi: 10.1105/tpc.113.109710

    CrossRef   Google Scholar

    [79]

    Cheminant S, Wild M, Bouvier F, Pelletier S, Renou JP, et al. 2011. DELLAs regulate chlorophyll and carotenoid biosynthesis to prevent photooxidative damage during seedling deetiolation in Arabidopsis. The Plant Cell 23:1849−60

    doi: 10.1105/tpc.111.085233

    CrossRef   Google Scholar

    [80]

    Ma Z, Hu X, Cai W, Huang W, Zhou X, et al. 2014. Arabidopsis miR171-targeted scarecrow-like proteins bind to GT cis-elements and mediate gibberellin-regulated chlorophyll biosynthesis under light conditions. PLoS Genetics 10:e1004519

    doi: 10.1371/journal.pgen.1004519

    CrossRef   Google Scholar

    [81]

    Toledo-Ortiz G, Johansson H, Lee KP, Bou-Torrent J, Stewart K, et al. 2014. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genetics 10:e1004416

    doi: 10.1371/journal.pgen.1004416

    CrossRef   Google Scholar

    [82]

    Sperling U, Franck F, van Cleve B, Frick G, Apel K, et al. 1998. Etioplast differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. The Plant Cell 10:283−96

    doi: 10.1105/tpc.10.2.283

    CrossRef   Google Scholar

    [83]

    Cackett L, Luginbuehl LH, Schreier TB, Lopez-Juez E, Hibberd JM. 2022. Chloroplast development in green plant tissues: the interplay between light, hormone, and transcriptional regulation. New Phytologist 233:2000−16

    doi: 10.1111/nph.17839

    CrossRef   Google Scholar

    [84]

    Zhong S, Zhao M, Shi T, Shi H, An F, et al. 2009. EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proceedings of the National Academy of Sciences of the United States of America 106:21431−36

    doi: 10.1073/pnas.0907670106

    CrossRef   Google Scholar

    [85]

    Kusnetsov V, Herrmann RG, Kulaeva ON, Oelmüller R. 1998. Cytokinin stimulates and abscisic acid inhibits greening of etiolated Lupinus luteus cotyledons by affecting the expression of the light-sensitive protochlorophyllide oxidoreductase. Molecular & General Genetics 259:21−28

    doi: 10.1007/pl00008626

    CrossRef   Google Scholar

    [86]

    Luo WG, Liang QW, Su Y, Huang C, Mo BX, et al. 2023. Auxin inhibits chlorophyll accumulation through ARF7-IAA14-mediated repression of chlorophyll biosynthesis genes in Arabidopsis. Frontiers in Plant Science 14:1172059

    doi: 10.3389/fpls.2023.1172059

    CrossRef   Google Scholar

    [87]

    Zhong S, Shi H, Xue C, Wei N, Guo H, et al. 2014. Ethylene-orchestrated circuitry coordinates a seedling's response to soil cover and etiolated growth. Proceedings of the National Academy of Sciences of the United States of America 111:3913−20

    doi: 10.1073/pnas.1402491111

    CrossRef   Google Scholar

    [88]

    Xu G, Guo H, Zhang D, Chen D, Jiang Z, et al. 2015. REVEILLE1 promotes NADPH: protochlorophyllide oxidoreductase A expression and seedling greening in Arabidopsis. Photosynthesis Research 126:331−40

    doi: 10.1007/s11120-015-0146-5

    CrossRef   Google Scholar

    [89]

    Turan S, Tripathy BC. 2015. Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiologia Plantarum 153:477−91

    doi: 10.1111/ppl.12250

    CrossRef   Google Scholar

    [90]

    Dalal VK, Tripathy BC. 2012. Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. Plant, Cell & Environment 35:1685−703

    doi: 10.1111/j.1365-3040.2012.02520.x

    CrossRef   Google Scholar

    [91]

    Wen B, Liu W, Yang W. 2019. Two strategies of plants facing shade: advances in the mechanisms of shade avoidance and shade tolerance responses. Molecular Plant Breeding 17:1028−33

    doi: 10.13271/j.mpb.017.001028

    CrossRef   Google Scholar

    [92]

    Fan Y, Chen J, Wang Z, Tan T, Li S, et al. 2019. Soybean (Glycine max L. Merr.) seedlings response to shading: leaf structure, photosynthesis and proteomic analysis. BMC Plant Biology 19:34

    doi: 10.1186/s12870-019-1633-1

    CrossRef   Google Scholar

    [93]

    Yang F, Liu Q, Cheng Y, Feng L, Wu X, et al. 2020. Low red/far-red ratio as a signal promotes carbon assimilation of soybean seedlings by increasing the photosynthetic capacity. BMC Plant Biology 20:148

    doi: 10.1186/s12870-020-02352-0

    CrossRef   Google Scholar

    [94]

    Yang F, Feng L, Liu Q, Wu X, Fan Y, et al. 2018. Effect of interactions between light intensity and red-to- far-red ratio on the photosynthesis of soybean leaves under shade condition. Environmental and Experimental Botany 150:79−87

    doi: 10.1016/j.envexpbot.2018.03.008

    CrossRef   Google Scholar

    [95]

    Liu X, Li L, Li M, Su L, Lian S, et al. 2018. AhGLK1 affects chlorophyll biosynthesis and photosynthesis in peanut leaves during recovery from drought. Scientific Reports 8:2250

    doi: 10.1038/s41598-018-20542-7

    CrossRef   Google Scholar

    [96]

    Li YH, Sun ZL, Xu XL, Jin M, Liu YJ, et al. 2010. Influence of low temperatures on photosystem II photochemistry and expression of the NADPH: protochlorophyllide oxidoreductase in the alpine, subnival perennial, Chorispora bungeana. Photosynthetica 48:457−68

    doi: 10.1007/s11099-010-0060-1

    CrossRef   Google Scholar

    [97]

    Mohanty S, Grimm B, Tripathy BC. 2006. Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. Planta 224:692−99

    doi: 10.1007/s00425-006-0248-6

    CrossRef   Google Scholar

    [98]

    Wu Q, Chen Z, Sun W, Deng T, Chen M. 2016. De novo sequencing of the leaf transcriptome reveals complex light-responsive regulatory networks in Camellia sinensis cv. Baijiguan. Frontiers in Plant Science 7:332

    doi: 10.3389/fpls.2016.00332

    CrossRef   Google Scholar

    [99]

    Wang Q, Ning Z, Awan SA, Gao J, Chen J, et al. 2023. Far-red light mediates light energy capture and distribution in soybeans (Glycine max L.) under the shade. Plant Physiology and Bioche mistry 204:108130

    doi: 10.1016/j.plaphy.2023.108130

    CrossRef   Google Scholar

    [100]

    Sakuraba Y, Rahman ML, Cho SH, Kim YS, Koh HJ, et al. 2013. The rice faded green leaf locus encodes protochlorophyllide oxidoreductase B and is essential for chlorophyll synthesis under high light conditions. The Plant Journal 74:122−33

    doi: 10.1111/tpj.12110

    CrossRef   Google Scholar

    [101]

    Kumar Tewari A, Charan Tripathy B. 1998. Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiology 117:851−58

    doi: 10.1104/pp.117.3.851

    CrossRef   Google Scholar

    [102]

    Zhao M, Yuan L, Wang J, Xie S, Zheng Y, et al. 2019. Transcriptome analysis reveals a positive effect of brassinosteroids on the photosynthetic capacity of wucai under low temperature. BMC Genomics 20:810

    doi: 10.1186/s12864-019-6191-2

    CrossRef   Google Scholar

    [103]

    Wang H, Liu Z, Luo S, Li J, Zhang J, et al. 2021. 5-Aminolevulinic acid and hydrogen sulphide alleviate chilling stress in pepper (Capsicum annuum L.) seedlings by enhancing chlorophyll synthesis pathway. Plant Physiology and Biochemistry 167:567−76

    doi: 10.1016/j.plaphy.2021.08.031

    CrossRef   Google Scholar

    [104]

    Zhou S, Hu Z, Zhu M, Zhang B, Deng L, et al. 2013. Biochemical and molecular analysis of a temperature-sensitive albino mutant in kale named “White Dove”. Plant Growth Regulation 71:281−94

    doi: 10.1007/s10725-013-9829-0

    CrossRef   Google Scholar

    [105]

    Liu XG, Xu H, Zhang JY, Liang GW, Liu YT, et al. 2012. Effect of low temperature on chlorophyll biosynthesis in albinism line of wheat (Triticum aestivum) FA85. Physiologia Plantarum 145:384−94

    doi: 10.1111/j.1399-3054.2012.01604.x

    CrossRef   Google Scholar

    [106]

    Catalá R, Medina J, Salinas J. 2011. Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 108:16475−80

    doi: 10.1073/pnas.1107161108

    CrossRef   Google Scholar

    [107]

    Yuan L, Zhang L, Wu Y, Zheng Y, Nie L, et al. 2021. Comparative transcriptome analysis reveals that chlorophyll metabolism contributes to leaf color changes in wucai (Brassica campestris L.) in response to cold. BMC Plant Biology 21:438

    doi: 10.1186/s12870-021-03218-9

    CrossRef   Google Scholar

    [108]

    Du J, Wang J, Shan S, Mi T, Song Y, et al. 2023. Low-Temperature-Mediated Promoter Methylation Relates to the Expression of TaPOR2D, Affecting the Level of Chlorophyll Accumulation in Albino Wheat (Triticum aestivum L.). International Journal of Molecular Sciences 24:14697

    doi: 10.3390/ijms241914697

    CrossRef   Google Scholar

    [109]

    Mishra D, Shekhar S, Chakraborty S, Chakraborty N. 2021. Wheat 2-Cys peroxiredoxin plays a dual role in chlorophyll biosynthesis and adaptation to high temperature. The Plant Journal 105:1374−89

    doi: 10.1111/tpj.15119

    CrossRef   Google Scholar

    [110]

    Xing X, Ding Y, Jin J, Song A, Chen S, et al. 2021. Physiological and Transcripts Analyses Reveal the Mechanism by Which Melatonin Alleviates Heat Stress in Chrysanthemum Seedlings. Frontiers in Plant Science 12:673236

    doi: 10.3389/fpls.2021.673236

    CrossRef   Google Scholar

    [111]

    Ha JH, Lee HJ, Jung JH, Park CM. 2017. Thermo-induced maintenance of photo-oxidoreductases underlies plant autotrophic development. Developmental Cell 41:170−179.e4

    doi: 10.1016/j.devcel.2017.03.005

    CrossRef   Google Scholar

    [112]

    Abdelaziz ME, Atia MAM, Abdelsattar M, Abdelaziz SM, Ibrahim TAA, et al. 2021. Unravelling the role of Piriformospora indica in combating water deficiency by modulating physiological performance and chlorophyll metabolism-related genes in Cucumis sativus. Horticulturae 7:399

    doi: 10.3390/horticulturae7100399

    CrossRef   Google Scholar

    [113]

    Shah AA, Yasin NA, Mudassir M, Ramzan M, Hussain I, et al. 2022. Iron oxide nanoparticles and selenium supplementation improve growth and photosynthesis by modulating antioxidant system and gene expression of chlorophyll synthase (CHLG) and protochlorophyllide oxidoreductase (POR) in arsenic-stressed Cucumis melo. Environmental Pollution 307:119413

    doi: 10.1016/j.envpol.2022.119413

    CrossRef   Google Scholar

  • Cite this article

    Wang Q, Gao J, Chen J, Tan X, Liu C, et al. 2024. Regulatory mechanism of a light-dependent protochlorophyllide oxidoreductase in chlorophyll biosynthesis and environmental adaptation. Technology in Agronomy 4: e023 doi: 10.48130/tia-0024-0019
    Wang Q, Gao J, Chen J, Tan X, Liu C, et al. 2024. Regulatory mechanism of a light-dependent protochlorophyllide oxidoreductase in chlorophyll biosynthesis and environmental adaptation. Technology in Agronomy 4: e023 doi: 10.48130/tia-0024-0019

Figures(3)  /  Tables(1)

Article Metrics

Article views(1337) PDF downloads(292)

REVIEW   Open Access    

Regulatory mechanism of a light-dependent protochlorophyllide oxidoreductase in chlorophyll biosynthesis and environmental adaptation

Technology in Agronomy  4 Article number: e023  (2024)  |  Cite this article

Abstract: Chlorophyll is a vital component of photosynthesis and must be produced throughout the plant life cycle. Light-dependent protochlorophyllide oxidoreductase (LPOR) is a pivotal enzyme in the chlorophyll biosynthesis pathway, catalyzing the conversion of Pchlide to Chlide. The presence of different types of LPOR ensures the efficient synthesis of chlorophyll in photosynthetic organisms during the dark-light transition. In addition to the transcriptional, translational, and post-translational regulation of LPOR function under different abiotic stresses, the nature of the substrate also influences LPOR function. Here, a perspective on chlorophyll synthesis and the development of chloroplasts is offered, the importance of LPOR in safeguarding plant light energy utilization is summarized, the gene expression pattern and structural-functional features of LPOR are outlined, as well as the role of LPOR in abiotic stress tolerance response, the catalytic mechanism of LPOR as well as the modulation of LPOR by light signals and other environmental factors are discussed. The aim is to provide references for the cultivation and innovation of plant germplasm resources with stress tolerance.

    • The demand for food has sharply increased because of the growing population[1,2]. Improving the LUE of crops represents the primary option for increasing crop yield potential[3]. LUE refers to the efficiency by which a crop produces biomass from absorbed light energy, which is measured by the accumulation rate of photosynthetically active radiation in relation to biomass per unit of intercepted or absorbed light[4]. The improvement of LUE depends on the rate of photosynthesis and the efficiency of converting light energy into fixed carbon[5]. The principal methods of improving LUE include (i) extending photosynthetic time, (ii) increasing the area of photosynthesis, and (iii) increasing the rate of photosynthesis. Therefore, enhancing photosynthetic efficiency is crucial for increasing yield[6]. Photosynthesis is the process by which plants and photosynthetic bacteria use light energy and CO2 to produce carbohydrates and O2[7]. During photosynthesis, plants convert light energy into chemical energy, which is used for plant growth. Chlorophyll plays an important role in photosynthesis in higher plants and has multiple functions in this process[8]. Related proteins bind with chlorophyll and form complexes that capture, convert, and redirect light energy[8]. Chl a and Chl b are the primary substances of the core protein complex and light-harvesting antenna protein complex of photosystems, respectively[9].

    • Chlorophyll biosynthesis is a complex process completed by multiple enzymes (Fig. 1). Accurate and stable chlorophyll synthesis is critical for plant growth and development because free chlorophyll and its precursors, the tetrapyrrole compounds can be photosensitive and phototoxic to cells. This effect is most pronounced in the photosystem II reaction center, which is highly exposed to oxidative damage[1012]. Chlorophyll synthesis consists of two parts. The first part is the common pathway of tetrapyrrole substance synthesis, starting from the synthesis of glutamyl tRNA and ending with Pro. This pathway involves the enzymes glutamine tRNA reductase, delta-amino ketones pentanoic acid dehydratase, uroporphyrinogen III synthase, coproporphyrinogen III oxidase, and protoporphyrinogen oxidase. The second aspect involves Pro chelation with Mg2+ in the chlorophyll synthesis pathway, requiring involved enzymes Mg-chelatase, Mg-protoporphyrin IX methyltransferase, POR, chlorophyllide a oxygenase, chlorophyll synthase, and chlorophyllase. The rate-limiting enzyme POR performs a crucial catalytic role in chlorophyll synthesis by transforming Pchlide into Chlide[13]. LPOR also participates in chloroplast development and serves as the primary protein component in PLBs of etioplasts[14,15]. Two types of POR exist in nature: DPOR (EC 1.3.7.7) and LPOR (EC 1.3.1.33)[16]. From evolutionary terms, DPOR is the older enzyme, a multisubunit enzyme containing three separate subunits, and very similar to nitrogen-fixing enzymes. DPOR catalyzes Pchlide reduction in an ATP-dependent manner and is oxygen-sensitive, and is present in non-flowering land plants, algae, and cyanobacteria[17]; LPORs are thought to have evolved in cyanobacteria about 2 billion years ago as a result of increased atmospheric oxygen levels and are not sensitive to oxygen[18]. LPOR is present in a wide range of organisms, including plants, algae, cyanobacteria, and anaerobic photosynthetic bacteria[1921]. However, only LPOR is present in angiosperms, indicating that induction with light is necessary for angiosperms to produce chlorophyll[22,23]. These characteristics make LPOR essential in chlorophyll biosynthesis and chloroplast development in angiosperms.

      Figure 1. 

      Chlorophyll biosynthesis pathway. 1: glutamine-tRNA reductase, 2: delta-amino ketones pentanoic acid dehydratase, 3: urinary porphyrins original III synthetase, 4: coproporphyrin III oxidase, 5: protoporphyrin oxidase, 6: Mg-chelating enzyme, 7: Mg-protoporphyrin IX methyltransferase, 8: the original chlorophyll acid ester oxidoreductase, 9: chlorophyll acid ester a oxygenase, 10: chlorophyll synthase, 11: chlorophyllase, 12: chlorophyllide a oxygenase, 13: ferrous chelase.

      A multitude of investigations have demonstrated that LPOR plays a pivotal role in the response to abiotic stress, influencing the biosynthesis of chlorophyll, and exhibiting a certain level of stress resistance. A synthesis was conducted of the research conducted domestically and internationally on LPOR, encompassing its structural characteristics, catalytic reaction mechanism, optical signal, temperature, moisture, and the factors influencing its activity.

    • LPOR is a single polypeptidase that is encoded within the nucleus. It has a transporter protein segment at its N-terminus. This transporter protein segment transports LPOR into the plastid after it is transcribed. LPOR is highly similar to the SDR family and needs photoactivation to reduce Pchlide and perform biological functions[24]. Previous studies investigated LPOR in several species, including Arabidopsis thaliana[25], Brassica oleracea[26], Oryza sativa[27], Hordeum vulgare[28], Zea mays[29], Nicotiana tabacum[30], Cucumis sativus[31], and Pisum sativum[32]. Pchlide, the precursor of chlorophyll synthesis, failed to undergo the requisite reduction in time, thereby allowing the production of a substantial amount of ROS upon exposure to light, which resulted in the oxidative damage and chlorophyll bleaching of the seedling[33]. In addition, the accumulation of ROS in chloroplasts also impairs the de novo synthesis of protein D1 (also known as photosystem b-a or PsbA), which is essential for PSII repair[34]. The enzyme LPOR catalyzes the conversion of pchlide into chlide, a process which enables the developing seedling to gain the capacity to perform photosynthesis[35]. The production of chlorophyll is thus facilitated, thus allowing the seedling to grow in an autotrophic manner[15].

      The different gene expression patterns of LPOR subtypes prevent direct photooxidative harm in yellow seedlings when exposed to light. In Arabidopsis, three LPOR subtypes, namely, LPORA, LPORB, and LPORC were identified[36,37]. At the early stage of plant development, AtPORA and AtPORB are expressed during etiolation in Arabidopsis seedlings[35]. AtPORB and AtPORC are synthesized abundantly in slightly mature seedlings and, subsequently, in mature plants[35]. Upon light exposure, the expression levels of AtPORB and AtPORC are directly correlated to Chl a content and the stacking of thylakoids in seedlings[38,39]. The cpSRP43 as a chaperone, stabilizes the enzyme and provides the optimal quantity of PORB during leaf greening and heat shock[40]. In contrast, cpSRP54 enhances its binding to the thylakoid membrane, thus ensuring a sufficient level of metabolic flux during late chlorophyll biosynthesis[40]. Two LPOR subtypes, namely, OsPORA and OsPORB, were identified in rice[27]. During early leaf development, OsPORA is expressed in darkness, whereas OsPORB is expressed throughout the entire leaf development process regardless of light conditions[41]. Previous studies demonstrated that although OsPORA and OsPORB have overlapping biochemical functions, the response of OsPORB to constant light or physiological functions during reproductive growth cannot be substituted with OsPORA[27]. Barley also has two LPOR subtypes[13]. In vitro measurement revealed that HvPORA is expressed in etiolated seedlings, and its expression is downregulated after light exposure[42]. On the contrary, HvPORB is expressed during morphogenesis in leaf development regardless of light conditions[42]. In addition, barley etioplast contains a distinctive light-harvesting complex called LHPP, of which HvPORA is an essential component[42]. The LHPP complex is prepared in advance for the LPOR-catalyzed transformation of Pchlide under light to prevent the free Pchlide phototoxicity after light exposure, which causes photobleaching of seedlings[43].

    • A comparison of the amino acid sequences of LPOR in barley and Synechocystis reveals that the conserved Cys residue sequence is closely linked to the binding and catalysis of substrate Pchlide conversion. Point mutation experiments on various Cys residues revealed that Cys276 is the active site for Pchlide binding. Additionally, Cys303 functions as a pigment-binding site with low affinity. Both Cys residues participate in the assembly and stabilization of PORB in the etioplast[44,45].

      LPOR’s structure, along with other SDR family members[24], contains the Rossmann-fold structure that binds dinucleotides[46]. The structure has three flexible regions positioned at amino acid residues 146–160, 228–255, and 284–291. Binding to the NADPH binding site of LPOR is closely associated with amino acid residues 146–160 and 228–255, whereas amino acid residues 284–291 plays a crucial role in regulating substrate Pchlide binding. In contrast to the other SDR family members, the SDR proteins stand out for utilizing Asn-Ser-Tyr-Lys to facilitate proton transfer from tetrads, leading to the production of stable reaction intermediates[46]. However, LPOR employs Thr residues, particularly Thr145, to replace the Ser residues. The structural modeling of the ternary enzyme-substrate complexes constructed from crystal and electron microscopy data also confirmed the differences in the orientation of LPOR to the substrate Pchlide and the structure of the LPOR active site[4749]. Further results indicate that the conserved Tyr and Gln residues in LPOR are essential for Pchlide binding, while the active site Cys residue is crucial for both hydride and proton transfer reactions in LPOR[48].

      LPOR participates in both chlorophyll biosynthesis and chloroplast development[50]. Chloroplasts originate from proplastids, and etioplasts are transitional forms of chloroplast development. Etioplasts are characterized by the lack of chlorophyll and possession of a distinctive membrane structure called PLBs[15]. LPOR is the main protein constituent of PLBs, comprising more than 90% of the total protein content of PLBs[51]. Carotenoids act in parallel with DET1 to regulate the transcriptional formation of LPOR and plastids PLBs, thereby controlling chloroplast development[52]. PLBs have diverse LHPP complexes with distinct absorption spectra, namely, LPOR-Pchlide633, LPOR-Pchlide640, and LPOR-Pchlide655, with peak absorptions at 633, 640, and 655 nm, respectively[26,53]. The photoactive binary complex of LPOR-Pchlide655 binds to NADPH after light detection and catalyzes Pchlide reduction, leading to light conversion and gradual formation of Chl[53]. Moreover, the decomposition of the PLB lattice structure initiates grana stacking, leading to the complete development of chloroplasts[50]. Nonetheless, LPOR-Pchlide633, which is not photoactive, can degrade after exposure to light, thereby triggering an outburst of ROS in chloroplasts. Severe instances of such degradations may result in cell death[32].

    • In plants, Pchlide reduction is an important rate-limiting step within the chlorophyll synthesis pathway. In angiosperms lacking DPOR, chlorotic seedlings rely on LPOR to turn green. LPOR requires light-induced NADPH as a reducing agent to catalyze the Pchlide conversion. In regular plant development, LPOR-Pchlide-NADPH forms a ternary complex that accumulates during the dark morphogenesis of the etioplast; the NADPH hydride on the nicotinamide ring is transferred to the C17 position of Pchlide through light induction (Fig. 2). Then, the conserved Tyr residue transfers a proton to the C18 position of Pchlide. Thus, the C17 and C18 double bonds of the Pchlide-D ring are reduced, resulting in the creation of Chlide. Then, Chlide undergoes esterification and further modifications to form Chl a and Chl b[47,54].

      Figure 2. 

      The C17–C18 double bond of Pchlide is restored to chlorophyll by light.

    • LPOR is a protein encoded in the nucleus, synthesized into large pPORs in the cytoplasm, and then modified to enter the plastid[55] (Fig. 3). The process of LPORs entering chloroplasts is distinct[56]. Prior studies verified that pPORA relies on substrates to enter chloroplasts, whereas pPORB does not require any substrate for entry[57]. TOC33 is an essential core component in the complex of PORA and PORB import channels in cotyledons and leaves[56,58]. PTC52 is a unique Pchlide a oxygenase complex located in the plastid envelope. It is responsible for associating the synthesis of Pchlide b with the import of pPORA[59]. In RNAi plants lacking PTC52 transcripts and proteins, pPORA cannot be imported to plastids normally. This phenomenon causes an excessive accumulation of Pchlide and leads to ROS accumulation and cell death during greening[59]. In addition, CDF1 present on thylakoids and capsules interacts with the LPOR subtype and plays a crucial role in the introduction and stability of LPOR[55]. Deletion of CDF1 leads to a decrease in LPOR protein accumulation, which normally hinders chlorophyll synthesis, damages PLB formation, affects chloroplast development under light, causes photobleaching of plants under light, and inhibits plant growth[55,60]. Various pathways of LPOR import into plastids guarantee normal chloroplast development and chlorophyll biosynthesis. This finding suggests that factors beyond the components of the core complex of the import channel participates in the transportation of nuclear-encoded plastid proteins. Plastid-localized membrane-bound factors, such as TTP1, play a role in LPOR-directed import into chloroplasts. TTP1 deficiency leads to the accumulation of glutamate receptors, enhances pentosamine ketoglutarate synthesis and reduces POR levels, which in turn leads to increased sensitivity to reactive oxygen species and slower greening of yellowing seedlings[61].

      Figure 3. 

      Regulatory networks of the PORA, PORB, and PORC genes in A. thaliana. Positive interactions are indicated by arrows, negative interactions by blunt ends, and the direction of protein movement by arched arrows. Helices represent mRNA, and ellipses represent proteins.

    • For the reduction of Pchlide to occur, LPOR catalysis requires photoactivation[23]. The catalytic efficiency of the reaction varies with different light qualities, and the quantum yield of the reaction is 3–7 times higher under red light (647 nm) than under blue light (407 nm)[62]. Moreover, LPOR's catalytic reaction efficiency varies when combined with different substrates. Several studies suggested that cabbage’s photobleaching is primarily caused by short-wavelength light (625–630 nm) of 7 μmol photons m−2∙s−1. Light with wavelengths longer than 630–640 nm causes bleaching and photoreduction, whereas that with wavelengths higher than 640 nm predominantly causes photoreduction[26]. Similar conclusions can be reached through various methods, such as behavioral spectroscopy, pigment content measurement, and kinetic analysis. These studies indicated that under low light intensity, the excitation energy of the short-wavelength-absorption-type Pchlide causes the photoreduction of long-wavelength-absorption-type Pchlide; in comparison, photobleaching occurs under high photochemical light[63].

      The active site of LPOR plays a critical role in its catalytic activity. Tyr275 and Lys279, which are essential active sites of LPOR, along with four conserved Cys residues involved in substrate binding, have a very important function in the operation of LPOR. Tyr275 and Lys279 regulate the efficiency of LPOR photoactive state formation by participating in the coordination of NADPH and Pchlide at enzyme catalytic sites[64]. LPOR photoactivity is regulated by several Cys binding sites with different substrate affinities[58]. Any mutation at these sites can affect LPOR photoactivity[65].

      Furthermore, proteins interacting with LPOR regulate their enzyme activity in various ways. The structural stability of the LHPP complex is crucial for plant greening. The presence of TLs has been demonstrated to influence the activation of LPORs in response to regulators[66]. Research indicated that galactosyl diacylglycerol impacts the catalytic reaction of LPOR by influencing the creation and breakdown of the Pchlide-LPOR-NADPH complex, which affects the biosynthesis of plant chlorophyll[67]. Feedback regulation is usual in chlorophyll biosynthesis. Fluorescent protein is one of the tetrapyrrole biosynthesis negative feedback regulators in higher plants. It directly interacts with LPOR and cooperates with LPOR negative feedback to regulate chlorophyll biosynthesis[68]. The protein LIL3 regulates plant greening through direct interaction with LPOR. The mutation in lil3 causes a considerable loss of LPOR protein, affecting its posttranslational modifications, which lead to abnormal chlorophyll synthesis[69]. Pchlide transformation catalyzed by LPOR involves protein phosphorylation. Previous research demonstrated that certain plastid ADP-dependent kinase impacts the membrane association of LPOR via reversible protein phosphorylation regulates PLB formation, promotes light-dependent diffusion, and ultimately facilitates chloroplast development[70].

    • Light is necessary for angiosperms to turn green, and the reaction involved is Pchlide reduction[56]. Several researchers examined prevalent transcription factors in light signaling, and they summarized and predicted the availability of multiple light response elements on the promoter of genes involved in chlorophyll biosynthesis, further highlighting the importance of light signaling in chlorophyll synthesis in plants[71]. Under dark conditions, PORC expression is extremely reduced or completely inhibited because of the suppression of PIF3, histone deacetylase 1, and SCL proteins. Research indicated that the phytochrome proteins PHYA and PHYB, which are photosensitive receptors found in plants, play a role in chlorophyll biosynthesis. When exposed to white light, PHYA and PHYB positively regulates LPOR, promoting chlorophyll biosynthesis[33]. Terminal flower 2 protein located downstream of the PHYA signal regulates the expression of PORA and promotes chlorophyll synthesis[72]. Under shading or low-intensity far-red light, the expression levels of PORB and PORC in the phyA mutant is substantially suppressed[73,74]. Far-red light exposure leads to the far-red-blocked greening phenomenon in plants. PHYA suppresses LPOR gene expression under far-red light, resulting in irreversible plastid damage that restrains proper greening ability of seedlings[75]. The sigma factor is a nuclear-encoded protein regulated by PHYA that participates in the regulation gene expression in chloroplasts and influences reverse signaling from plastids to nuclei to promote plant greening and plastid development[75].

      In the dark, PORA activity is initiated by acetylation in the presence of HDAC, which regulates chlorophyll synthesis[76]. Meanwhile, phytochrome interacting factor 1 binds to the G-box DNA sequence element (CACGTG) of the PORC promoter and positively regulates PORC expression[77] (Fig. 3). After exposure to light, PIF3 is phosphorylated and inactivated, and histone H4 is acetylated[78]. Moreover, light facilitates the expression of miR171 and hinders gibberellic acid synthesis, thereby promoting the expression of DELLA protein. However, miR171 and DELLA inhibit the SCL transcription, resulting in a significant increase in the PORC expression under light[79,80] (Fig. 3). In addition, light positively regulates the expression of the transcription factor HY5, which binds directly to PORC to promote its gene expression[81]. HY5 interacts with PHYB in the dark through COP1/SPA1; after exposure to light, the transcription factor HY5 is released. HY5 cooperates with the biological clock of PIFs to regulate the transcription level of PORC[81,82] (Fig. 3).

      The dark-to-light transition enables plants to transition from the skotomorphogenesis to the photomorphogenesis state. This process is often accompanied by changes in phytohormones, which regulate the expression of different PORs in different ways[83]. EIN 3 and EIN 3-like 1 positively regulate PORA and PORB[84]. Cytokinins significantly enhance the transcription of POR mRNA and accelerate plant greening, whereas abscisic acid has the opposite effect[85]. Auxin binds to the promoters of PORA and GUN5 through ARF2 and ARF7 to inhibit their expression directly, with the help of IAA14[86]. Additionally, growth hormones are known to inhibit chlorophyll biosynthesis. Inhibition of their expression directly inhibits chlorophyll biosynthesis[86]. In Arabidopsis, the structures of PORA and PORB are mostly the same, except for the initial transit peptide. However, they perform different functions and cannot replace each other. PORA solely performs during the initial stage of light exposure in yellowing seedlings, and light significantly inhibits PORA. Following light exposure, the expression of PORA declines rapidly, whereas PORB stays constantly expressed.[25].

      The regulatory mechanisms of PORA, PORB, and PORC are interconnected and not completely independent. When ethylene is applied under light, EIN3 regulates the transfer of COP1 from the cytoplasm to the nucleus. Thus, the activity of extranuclear COP1 is blocked, and the expression of PORC is inhibited. When ethylene is absent under light, COP1 mainly exists in the cytoplasm, and HY5 initiates PORC transcription[87] (Fig. 3).

      The expression of LPOR mRNA exhibits noteworthy cyclic variations[88]. Reveille 1 directly binds to the PORA promoter through the EE motif (AAAATATCT) and regulates the transcription of PORA[88] (Fig. 3). AtPORB expression is regulated by the biological clock, whereas AtPORC expression is independent of the biological clock. This finding corresponds to the regulation of OsPORB expression observed in rice grown under short-day conditions. The LPOR enzyme in cucumber is encoded by a single gene, with its expression under light being six times greater than that under dark treatment[31]. Upon exposure to light, the LPOR level decreases slightly, followed by a gradual increase in LPOR expression from 3 to 12 h[31].

      Research on light signal regulation of LPOR primarily focuses on plants turning green during the transition from darkness to light. Further experiments must be conducted to determine whether changes occur in the expression, content, and enzyme activity of LPOR during shading (including changes in light intensity and quality) and whether it is an essential enzyme affecting chlorophyll biosynthesis during variations in the light environment.

    • Changes in LPOR enzyme activity are one of the important factors affecting chlorophyll biosynthesis under abiotic stress[89,90] (Table 1). Shading environments are ubiquitous in nature. Increasing the content of photosynthetic pigments and reducing Chl a/b are important shade tolerance mechanisms for plants[91]. However, the molecular mechanism regulating chlorophyll synthesis under shade has not yet been studied. Previous proteomic studies indicated that compared with the level of LPOR protein in the soybean seedling leaves grown under normal light, that in the soybean seedling leaves grown under shade increases[9294]. This increase may be a significant reason for the augmentation observed in plants’ chlorophyll content under shade conditions.

      Table 1.  Effects of different stresses on the LPOR activity, protein, and transcription levels.

      Abiotic stress Species Response to stress (transcript and protein expression and enzyme activity) Ref.
      Water Rice LPOR content decreases. [90]
      Salt/drought Peanut The expression of AhPORA is downregulated during drought and upregulated during postdrought recovery through AhGLK. [95]
      Rice LPOR activity is downregulated by 60% in salt-treated seedlings. [89]
      Chill Rice and LPOR activity is downregulated. [41]
      Corydalis bungeana Turcz. LPOR's transcript and protein content slightly decline at 4 °C but dramatically decrease at −4 °C with time. [96]
      Wheat and cucumber LPOR level is not reduced in light-exposed chill-stressed seedlings. [97]
      Heat Wheat and cucumber LPOR content is greatly reduced in response to light in heat-stressed seedlings. [97]
      Shade Camellia sinensis L. and soybean LPOR is significantly upregulated after shading, but downregulated by low R/FR ratio [93,98,99]
      Rice OsPORA expression is repressed by light, and OsPORB expression is rapidly upregulated by high-light treatment. [100]

      When plants undergo the process of greening, low temperatures significantly hinder chlorophyll biosynthesis, leading to a decline in chlorophyll accumulation. However, the extent of this decline differs between various species[97]. One of the primary factors contributing to this phenomenon is the inhibition of the conversion of Pchlide to Chlide, which significantly diminishes LPOR activity and downregulates protein and transcriptional expression levels at low temperatures[41,97,101], This results in the obstruction of chlorophyll synthesis and the accumulation of ROS at low temperatures[41]. These ROS subsequently have the potential to cause oxidative damage during the greening process[41]. However, spraying exogenous carotenoids can improve the downregulation of LPOR transcriptional levels at low temperatures, thereby reducing their impact on chlorophyll biosynthesis[102]. Furthermore, the exogenous application of ALA and H2S was found to significantly enhance the content of chlorophyll and its upstream precursors[103]. Previous research showed that LPOR plays an important role in the cold resistance of plants[96,104,105]. CbPORB is resistant to cold in Chorispora bungeana[105]. CbPORB transcription and protein content decrease slightly at 4 °C but significantly decrease over time at −4 °C. Conversely, in A. thaliana[106] and wheat[107], low temperatures upregulate the HY5 expression at the transcriptional level, and HY5 regulates the transfer of COP1 from the nucleus to the cytoplasm, thereby promoting PORC expression (Fig. 3). A comparison of winter wheat XN1376 with its albino line XN1376B revealed that the expression of TaPOR2D in albino leaves with methylation of its promoter at low temperatures was an important factor influencing chlorophyll accumulation at low temperatures[108]. The restricted decrease in Pchlide is the primary cause of the impact on chlorophyll biosynthesis during periods of high-temperature stress[97,101,109,110]. Although the activity of the LPOR enzyme in green seedlings increases under high-temperature conditions[101], the LPOR protein content decreases significantly[97], resulting in a decrease in chlorophyll content. Developing seedlings could regulate the balance between ROS and Chl levels by regulating the production of LPOR enzymes[111]. PORB plays a significant role in the thermoregulation of chlorophyll biosynthesis in phototrophic seedlings and FCA (Flowering Control Locus A) induces the expression of PORA and PORB by promoting the DNA accessibility of RNA polymerase II to the gene promoters, thereby maintaining protein levels at a constant temperature[111]. Some studies suggest that melatonin can enhance plant stress resistance and improve the impact of heat stress on plant chlorophyll synthesis by upregulating the PORA expression[110]. A high-temperature stress-responsive protein, Ta2CP, was discovered in a heat-adapted wheat variety that is also involved in regulating chlorophyll biosynthesis under high-temperature stress[109]. The results indicated that Ta2CP positively regulates chlorophyll biosynthesis via interaction with TaPORB. Silencing Ta2CP expression downregulates TaPORB expression and decreases chlorophyll content, whereas Ta2CP overexpression upregulates TaPORB expression and increases chlorophyll content.

      Under salt stress, the decrease in LPOR enzyme activity is a key contributor to the decline in chlorophyll levels[89]. The expression of genes related to chlorophyll synthesis and photosynthesis in peanuts (Arachis hypogaea) decreases significantly under drought stress. During recovery, the transcript and protein expression levels of AhPORA upregulate significantly, leading to the recovery of chlorophyll biosynthesis and photosynthesis[95]. This finding is consistent with the results observed in rice, where the accumulation of chlorophyll in seedlings developed under water stress is significantly reduced because of a decrease in the accumulation of intermediate precursors for chlorophyll synthesis. In particular, the decrease in the activity of LPOR enzymes, protein, and gene expression leads to damage to the Shibata shift, resulting in a decrease in Pchlide photoreduction[90]. Similarly, when cucumbers experience water stress, the LPOR enzyme content and the transcriptional content directly impact chlorophyll accumulation[112]. Arsenic significantly reduced the growth rate, chlorophyll content, and photosynthetic rate of melon plants. In contrast, iron oxide nanoparticles and selenium treatments up-regulated the expression of chlorophyll synthase and LPOR and increased the chlorophyll content of melon plants under arsenic stress[113]. In summary, LPOR plays a crucial role in regulating chlorophyll biosynthesis during adverse conditions. Plants improve their stress response capability by regulating their LPOR transcription, protein level expression, and enzyme activity. However, the regulatory mechanism is not completely clear. Thus, further exploration is needed.

    • In angiosperms, chlorophyll synthesis is dependent on light-induced activity of LPOR, which reduces Pchlide (Fig. 2) and promotes chloroplast development. Different types of LPOR were identified in multiple species, with varying expression patterns. The different expression patterns and the dependence of LPOR activity on the type of substrate can optimize preparations in the dark to ensure efficient chlorophyll synthesis with minimal impact on photosynthesis. The current research on light has focused on the greening process during the transition from darkness to light. A large number of studies have gradually revealed the regulatory mechanisms of light signaling factors. However, the complexity of light variations in natural environments, such as shaded or densely planted areas in forests, as well as cultivation techniques including strip cropping, result in varying degrees of light intensity and light quality. The precise regulation of LPOR in a variable environment and the efficient synthesis of the optimal amount of chlorophyll to ensure the utilization of light energy by plants remain unclear. Additionally, numerous studies have demonstrated that LPOR plays a pivotal role in abiotic stress response by regulating chlorophyll synthesis at the transcriptional and protein levels (Fig. 3, Table 1). However, the regulatory mechanisms at the posttranslational level have not been extensively investigated. Consequently, further investigation will provide a theoretical foundation for the breeding and development of plant germplasm resources with stress tolerance.

    • The authors confirm contribution to the paper as follows: draft manuscript preparation: Wang Q; manuscript revision: Gao J, Chen J, Tan X, Liu C, Yu L, Yang F, Yang W; conceptualization, funding acquision: Yang F, Yang W. All authors reviewed the results and approved the final version of the manuscript.

    • Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

      • This work was supported by the National Natural Science Foundation of China (32071963).

      • The authors declare that they have no conflict of interest.

      • Copyright: © 2024 by the author(s). Published by Maximum Academic Press, Fayetteville, GA. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (3)  Table (1) References (113)
  • About this article
    Cite this article
    Wang Q, Gao J, Chen J, Tan X, Liu C, et al. 2024. Regulatory mechanism of a light-dependent protochlorophyllide oxidoreductase in chlorophyll biosynthesis and environmental adaptation. Technology in Agronomy 4: e023 doi: 10.48130/tia-0024-0019
    Wang Q, Gao J, Chen J, Tan X, Liu C, et al. 2024. Regulatory mechanism of a light-dependent protochlorophyllide oxidoreductase in chlorophyll biosynthesis and environmental adaptation. Technology in Agronomy 4: e023 doi: 10.48130/tia-0024-0019

Catalog

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return