PROGRAMMED CELL DEATH8 interacts with tetrapyrrole biosynthesis enzymes and ClpC1 to maintain homeostasis of tetrapyrrole metabolites in Arabidopsis.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
06 2023
Historique:
received: 02 01 2023
accepted: 19 03 2023
medline: 19 5 2023
pubmed: 28 3 2023
entrez: 27 3 2023
Statut: ppublish

Résumé

Tetrapyrrole biosynthesis (TBS) is a dynamically and strictly regulated process. Disruptions in tetrapyrrole metabolism influence many aspects of plant physiology, including photosynthesis, programmed cell death (PCD), and retrograde signaling, thus affecting plant growth and development at multiple levels. However, the genetic and molecular basis of TBS is not fully understood. We report here PCD8, a newly identified thylakoid-localized protein encoded by an essential gene in Arabidopsis. PCD8 knockdown causes a necrotic phenotype due to excessive chloroplast damage. A burst of singlet oxygen that results from overaccumulated tetrapyrrole intermediates upon illumination is suggested to be responsible for cell death in the knockdown mutants. Genetic and biochemical analyses revealed that PCD8 interacts with ClpC1 and a number of TBS enzymes, such as HEMC, CHLD, and PORC of TBS. Taken together, our findings uncover the function of chloroplast-localized PCD8 and provide a new perspective to elucidate molecular mechanism of how TBS is finely regulated in plants.

Identifiants

pubmed: 36967598
doi: 10.1111/nph.18906
doi:

Substances chimiques

Tetrapyrroles 0
Arabidopsis Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2545-2560

Informations de copyright

© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.

Références

Adhikari ND, Froehlich JE, Strand DD, Buck SM, Kramer DM, Larkin RM. 2011. GUN4-porphyrin complexes bind the ChlH/GUN5 subunit of Mg-Chelatase and promote chlorophyll biosynthesis in Arabidopsis. Plant Cell 23: 1449-1467.
Albus CA, Ruf S, Schottler MA, Lein W, Kehr J, Bock R. 2010. Y3IP1, a nucleus-encoded thylakoid protein, cooperates with the plastid-encoded Ycf3 protein in photosystem I assembly of tobacco and Arabidopsis. Plant Cell 22: 2838-2855.
Apitz J, Nishimura K, Schmied J, Wolf A, Hedtke B, van Wijk KJ, Grimm B. 2016. Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiology 170: 2040-2051.
Ayliffe MA, Agostino A, Clarke BC, Furbank R, von Caemmerer S, Pryor AJ. 2009. Suppression of the barley uroporphyrinogen III synthase gene by a Ds activation tagging element generates developmental photosensitivity. Plant Cell 21: 814-831.
Brzezowski P, Richter AS, Grimm B. 2015. Regulation and function of tetrapyrrole biosynthesis in plants and algae. Biochimica et Biophysica Acta 1847: 968-985.
Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16: 735-743.
Czarnecki O, Grimm B. 2012. Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. Journal of Experimental Botany 63: 1675-1687.
D'Alessandro S, Beaugelin I, Havaux M. 2020. Tanned or sunburned: how excessive light triggers plant cell death. Molecular Plant 2: 1545-1555.
D'Alessandro S, Ksas B, Havaux M. 2018. Decoding β-cyclocitral-mediated retrograde signaling reveals the role of a detoxification response in plant tolerance to photooxidative stress. Plant Cell 30: 2495-2511.
De Pinto MC, Locato V, De Gara L. 2012. Redox regulation in plant programmed cell death. Plant, Cell & Environment 35: 234-244.
Demmig-Adams B, Adams WW III. 2000. Harvesting sunlight safely. Nature 403: 373-374.
Dogra V, Li MY, Singh S, Li MP, Kim C. 2019. Oxidative post-translational modification of EXECUTER1 is required for singlet oxygen sensing in plastids. Nature Communications 10: 2834.
Dogra V, Singh RM, Li M, Li M, Singh S, Kim C. 2022. EXECUTER2 modulates the EXECUTER1 signalosome through its singlet oxygen-dependent oxidation. Molecular Plant 15: 438-453.
Gonzalez-Perez S, Gutierrez J, Garcia-Garcia F, Osuna D, Dopazo J, Lorenzo O, Revuelta JL, Arellano JB. 2011. Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. Plant Physiology 156: 1439-1456.
Hilson P, Allemeersch J, Altmann T, Aubourg S, Avon A, Beynon J, Bhalerao RP, Bitton F, Caboche M, Cannoot B et al. 2004. Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Research 14: 2176-2189.
Hu G, Yalpani N, Briggs SP, Johal GS. 1998. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10: 1095-1105.
Huang C, Yu QB, Li ZR, Ye LS, Xu L, Yang ZN. 2017. Porphobilinogen deaminase HEMC interacts with the PPR-protein AtECB2 for chloroplast RNA editing. The Plant Journal 92: 546-556.
Huang M, Slewinski TL, Baker RF, Janick-Buckner D, Buckner B, Johal GS, Braun DM. 2009. Camouflage patterning in maize leaves results from a defect in porphobilinogen deaminase. Molecular Plant 2: 773-789.
Huysmans M, Lema AS, Coll NS, Nowack MK. 2017. Dying two deaths - programmed cell death regulation in development and disease. Current Opinion in Plant Biology 35: 37-44.
Inaba T, Ito-Inaba Y. 2010. Versatile roles of plastids in plant growth and development. Plant Cell Physiology 51: 1847-1853.
Ishikawa A, Okamoto H, Iwasaki Y, Asahi T. 2001. A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis. The Plant Journal 27: 89-99.
Izumi M, Ishida H, Nakamura S, Hidema J. 2017. Entire photodamaged chloroplasts are transported to the central vacuole by autophagy. Plant Cell 29: 377-394.
Jarvis P, Lopez-Juez E. 2013. Biogenesis and homeostasis of chloroplasts and other plastids. Nature Reviews Molecular Cell Biology 14: 787-802.
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: 211-216.
Kim C, Apel K. 2013b. Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynthesis Research 116: 455-464.
Kim C, Lee KP, Baruah A, Nater M, Gobel C, Feussner I, Apel K. 2009. 1O2-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid. Proceedings of the National Academy of Sciences, USA 106: 9920-9924.
Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M, Blajecka K, Herrfurth C, Feussner I, Apel K. 2012. Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. Plant Cell 24: 3026-3039.
Kovacheva S, Bédard J, Wardle A, Patel R, Jarvis P. 2007. Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. The Plant Journal 50: 364-379.
Kruse E, Mock HP, Grimm B. 1995. Reduction of coproporphyrinogen oxidase level by antisense RNA synthesis leads to deregulated gene expression of plastid proteins and affects the oxidative defense system. EMBO Journal 14: 3712-3720.
Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K. 2007. Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104: 672-677.
Larkin RM, Alonso JM, Ecker JR, Chory J. 2003. GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902-906.
Lee KP, Kim C, Landgraf F, Apel K. 2007. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104: 10270-10275.
Lichtenthaler HK. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148: 350-382.
Lv R, Li Z, Li M, Dogra V, Lv S, Liu R, Lee KP, Kim C. 2019. Uncoupled expression of nuclear and plastid photosynthesis-associated genes contributes to cell death in a lesion mimic mutant. Plant Cell 31: 210-230.
Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K. 2001. FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 98: 12826-12831.
Miernyk JA, Thelen JJ. 2008. Biochemical approaches for discovering protein-protein interactions. The Plant Journal 53: 597-609.
Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. 2001. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proceedings of the National Academy of Sciences, USA 98: 2053-2058.
Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ. 2010. The cell biology of tetrapyrroles: a life and death struggle. Trends in Plant Science 15: 488-498.
Mock HP, Grimm B. 1997. Reduction of uroporphyrinogen decarboxylase by antisense RNA expression affects activities of other enzymes involved in tetrapyrrole biosynthesis and leads to light-dependent necrosis. Plant Physiology 113: 1101-1112.
Mock HP, Heller W, Molinai A, Neubohn B, Sandermann H Jr, Grimm B. 1999. Expression of uroporphyrinogen decarboxylase or coproporphyrinogen oxidase antisense RNA in tobacco induces pathogen defense responses conferring increased resistance to tobacco mosaic virus. Journal of Biological Chemistry 274: 4231-4238.
Nakagawara E, Sakuraba Y, Yamasato A, Tanaka R, Tanaka A. 2007. Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. The Plant Journal 49: 800-809.
Neuhaus HE, Emes MJ. 2000. Nonphotosynthetic metabolism in plastids. Annual Review of Plant Physiology and Plant Molecular Biology 51: 111-140.
Pennell RI, Lamb C. 1997. Programmed cell death in plants. Plant Cell 9: 1157-1168.
Quesada V, Sarmiento-Manus R, Gonzalez-Bayon R, Hricova A, Ponce MR, Micol JL. 2013. PORPHOBILINOGEN DEAMINASE deficiency alters vegetative and reproductive development and causes lesions in Arabidopsis. PLoS ONE 8: e53378.
Rabino I, Mancinelli AL. 1986. Light, temperature, and anthocyanin production. Plant Physiology 81: 922-924.
Richter AS, Peter E, Rothbart M, Schlicke H, Toivola J, Rintamaki E, Grimm B. 2013. Posttranslational influence of NTRC on enzymes in tetrapyrrole synthesis. Plant Physiology 162: 63-73.
Rodriguez-Concepcion M, D'Andrea L, Pulido P. 2019. Control of plastidial metabolism by the Clp protease complex. Journal of Experimental Botany 70: 2049-2058.
Salvi D, Rolland N, Joyard J, Ferro M. 2008. Purification and proteomic analysis of chloroplasts and their sub-organellar compartments. Methods in Molecular Biology 432: 19-36.
Shumbe L, Chevalier A, Legeret B, Taconnat L, Monnet F, Havaux M. 2016. Singlet oxygen-induced cell death in Arabidopsis under high-light stress is controlled by OXI1 kinase. Plant Physiology 170: 1757-1771.
Sjögren LL, MacDonald TM, Sutinen S, Clarke AK. 2004. Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiology 136: 4114-4126.
Stenbaek A, Jensen PE. 2010. Redox regulation of chlorophyll biosynthesis. Phytochemistry 71: 853-859.
Tang W, Wang W, Chen D, Ji Q, Jing Y, Wang H, Lin R. 2012. Transposase-derived proteins FHY3/FAR1 interact with PHYTOCHROME-INTERACTING FACTOR1 to regulate chlorophyll biosynthesis by modulating HEMB1 during deetiolation in Arabidopsis. Plant Cell 24: 1984-2000.
Triantaphylides C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ. 2008. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology 148: 960-968.
Vacca RA, Valenti D, Bobba A, Merafina RS, Passarella S, Marra E. 2006. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco bright-yellow 2 cells en route to heat shock-induced cell death. Plant Physiology 141: 208-219.
Van Aken O, Van Breusegem F. 2015. Licensed to kill: mitochondria, chloroplasts, and cell death. Trends in Plant Science 20: 754-766.
Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inze D, Van Breusegem F. 2005. Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiology 139: 806-821.
Wang J, Bayles KW. 2013. Programmed cell death in plants: lessons from bacteria? Trends in Plant Science 18: 133-139.
Wang L, Leister D, Guan L, Zheng Y, Schneider K, Lehmann M, Apel K, Kleine T. 2020. The Arabidopsis SAFEGUARD1 suppresses singlet oxygen-induced stress responses by protecting grana margins. Proceedings of the National Academy of Sciences, USA 117: 6918-6927.
Wang P, Grimm B. 2021. Connecting chlorophyll metabolism with accumulation of the photosynthetic apparatus. Trends in Plant Science 26: 484-495.
Woodson JD, Joens MS, Sinson AB, Gilkerson J, Salome PA, Weigel D, Fitzpatrick JA, Chory J. 2015. Ubiquitin facilitates a quality-control pathway that removes damaged chloroplasts. Science 350: 450-454.
Wu H, Ji Y, Du J, Kong D, Liang H, Ling HQ. 2010. ClpC1, an ATP-dependent Clp protease in plastids, is involved in iron homeostasis in Arabidopsis leaves. Annals of Botany 105: 823-833.
Xu Z, Mahmood K, Rothstein SJ. 2017. ROS induces anthocyanin production via late biosynthetic genes and anthocyanin deficiency confers the hypersensitivity to ROS-generating stresses in Arabidopsis. Plant Cell Physiology 58: 1364-1377.
Yoo SD, Cho YH, Sheen J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2: 1565-1572.
Zhong L, Zhou W, Wang H, Ding S, Lu Q, Wen X, Peng L, Zhang L, Lu C. 2013. Chloroplast small heat shock protein HSP21 interacts with plastid nucleoid protein pTAC5 and is essential for chloroplast development in Arabidopsis under heat stress. Plant Cell 25: 2925-2943.

Auteurs

Rudan Geng (R)

Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Xiaoqing Pang (X)

Institute of Biology/Plant Physiology, Humboldt-Universität zu Berlin, Philippstraße 13, Berlin, 10115, Germany.

Xia Li (X)

Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Shanshan Shi (S)

Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Boris Hedtke (B)

Institute of Biology/Plant Physiology, Humboldt-Universität zu Berlin, Philippstraße 13, Berlin, 10115, Germany.

Bernhard Grimm (B)

Institute of Biology/Plant Physiology, Humboldt-Universität zu Berlin, Philippstraße 13, Berlin, 10115, Germany.

Ralph Bock (R)

Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, D-14476, Potsdam-Golm, Germany.

Jirong Huang (J)

Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, 200234, China.

Wenbin Zhou (W)

Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

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