Tầm quan trọng của phản ứng chặt chẽ trong plastid đối với sự phát triển của thực vật trên đất

Plant Growth Regulation - Trang 1-13 - 2024
Mina Goto1, Sousuke Imamura2, Kazuhiro Takaya2, Shinji Masuda1
1Department of Life Science and Technology, Tokyo Institute of Technology, Yokohama, Japan
2Space Environment and Energy Laboratories, Nippon Telegraph and Telephone Corporation, Musashino, Japan

Tóm tắt

Nucleotide điều hòa, guanosine 3′,5′-bis(pyrophosphate) (ppGpp), ban đầu được xác định ở Escherichia coli, kiểm soát quá trình phiên mã, dịch mã và hoạt động enzyme ở vi khuẩn và plastid của tế bào thực vật. Chúng tôi gần đây đã báo cáo rằng cây giống của đột biến sản xuất ppGpp quá mức của Arabidopsis thaliana được trồng trên môi trường đông đặc bằng agar có sinh khối lớn hơn so với loại hoang dã (WT), đặc biệt là trong điều kiện hạn chế dinh dưỡng. Tuy nhiên, khả năng tái tạo của kiểu hình trên đất vẫn chưa được biết đến. Để hiểu rõ hơn về tác động của việc tích lũy ppGpp đối với sự phát triển của thực vật trên đất, kiểu hình của các đột biến liệu không có ppGpp và tích lũy ppGpp của Arabidopsis đã được xác định trên đất giàu nitơ và đất hạn chế nitơ. Chúng tôi nhận thấy rằng mặc dù trọng lượng tươi của đột biến tích lũy ppGpp lớn hơn đáng kể so với WT trong điều kiện hạn chế nitơ, trọng lượng khô của các đột biến là giống như WT, cho thấy rằng tác động của việc tích lũy ppGpp đối với sinh khối thực vật phụ thuộc vào điều kiện tăng trưởng. Những kết quả này xác nhận rằng sự điều chỉnh nhân tạo phản ứng chặt chẽ trong plastid phụ thuộc vào ppGpp có thể góp phần vào sự phát triển của thực vật trên đất để đáp ứng với sự sẵn có của nitơ.

Từ khóa

#ppGpp #Arabidopsis thaliana #plastid #sinh khối #phát triển thực vật #môi trường dinh dưỡng

Tài liệu tham khảo

Anderson BW, Fung DK, Wang JD (2021) Regulatory themes and variations by the stress-signaling nucleotide alarmones (p)ppGpp in bacteria. Annu Rev Genet 55:115–133. https://doi.org/10.1146/annurev-genet-021821-025827 Atkinson GC, Tenson T, Hauryliuk V (2011) The RelA/SpoT homolog (RSH) superfamily: distribution and functional evolution of ppGpp synthetases and hydrolases across the tree of life. PLoS ONE 6:e23479. https://doi.org/10.1371/journal.pone.0023479 Battesti A, Bouveret E (2006) Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Mol Microbiol 62:1048–1063. https://doi.org/10.1111/j.1365-2958.2006.05442.x Cashel M (1969) The control of ribonucleic acid synthesis in Escherichia coli IV. Relevance of unusual phosphorylated compounds from amino acid-starved stringent strains. J Biol Chem 244:3133–3141 Cashel M, Gentry DR, Hernandez VJ, Vinella D (1996) The stringent response. In: Neidhardt FC, Curtiss IR, Ingraham JL et al (eds) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. ASM Press, Washington, pp 1458–1496 Chen Y, Yamori W, Tanaka A et al (2021) Degradation of the photosystem II core complex is independent of chlorophyll degradation mediated by stay-green Mg2+ dechelatase in Arabidopsis. Plant Sci 307:110902. https://doi.org/10.1016/J.PLANTSCI.2021.110902 Chi JT, Zhou P (2023) From magic spot ppGpp to MESH1: stringent response from bacteria to metazoa. PLOS Pathog 19:e1011105. https://doi.org/10.1371/JOURNAL.PPAT.1011105 Dall’Osto L, Bressan M, Bassi R (2015) Biogenesis of light harvesting proteins. Biochim Biophys Acta Bioenerg 1847:861–871. https://doi.org/10.1016/J.BBABIO.2015.02.009 Ding CKC, Rose J, Sun T et al (2020) MESH1 is a cytosolic NADPH phosphatase that regulates ferroptosis. Nat Metab 2:270–277. https://doi.org/10.1038/S42255-020-0181-1 Field B (2018) Green magic: regulation of the chloroplast stress response by (p)ppGpp in plants and algae. J Exp Bot 69:2797–2807. https://doi.org/10.1093/jxb/erx485 Flardh K, Axberg T, Albertson NH, Kjelleberg S (1994) Stringent control during carbon starvation of marine Vibrio sp. strain S14: molecular cloning, nucleotide sequence, and deletion of the relA gene. J Bacteriol 176:5949–5957. https://doi.org/10.1128/JB.176.19.5949-5957.1994 Gallant J, Palmer L, Pao CC (1977) Anomalous synthesis of ppGpp in growing cells. Cell 11:181–185. https://doi.org/10.1016/0092-8674(77)90329-4 Givens RM, Lin MH, Taylor DJ et al (2004) Inducible expression, enzymatic activity and origin of higher plant homologues of bacterial RelA/SpoT stress proteins in Nicotiana tabacum. J Biol Chem 279:7495–7504. https://doi.org/10.1074/jbc.M311573200 Goto M, Oikawa A, Masuda S (2022) Metabolic changes contributing to large biomass production in the Arabidopsis ppGpp-accumulating mutant under nitrogen deficiency. Planta 255:48. https://doi.org/10.1007/S00425-022-03835-0 Honoki R, Ono S, Oikawa A et al (2018) Significance of accumulation of the alarmone (p)ppGpp in chloroplasts for controlling photosynthesis and metabolite balance during nitrogen starvation in Arabidopsis. Photosynth Res 135:299–308. https://doi.org/10.1007/s11120-017-0402-y Inazu M, Nemoto T, Omata Y et al (2023) Complete loss of RelA and SpoT homologs in Arabidopsis reveals the importance of the plastidial stringent response in the interplay between chloroplast metabolism and plant defense response. Plant Cell Physiol. https://doi.org/10.1093/PCP/PCAD136 Irving SE, Choudhury NR, Corrigan RM (2021) The stringent response and physiological roles of (pp)pGpp in bacteria. Nat Rev Microbiol 19:256–271. https://doi.org/10.1038/s41579-020-00470-y Ito D, Ihara Y, Nishihara H, Masuda S (2017) Phylogenetic analysis of proteins involved in the stringent response in plant cells. J Plant Res 130:625–634 Ito D, Kawamura H, Oikawa A et al (2020) ppGpp functions as an alarmone in metazoa. Commun Biol 31(3):1–11. https://doi.org/10.1038/s42003-020-01368-4 Ito K, Ito D, Goto M et al (2022) Regulation of ppGpp synthesis and its impact on chloroplast biogenesis during early leaf development in rice. Plant Cell Physiol 63:919–931. https://doi.org/10.1093/PCP/PCAC053 Jarvis P, López-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802. https://doi.org/10.1038/nrm3702 Li H, Nian J, Fang S et al (2022) Regulation of nitrogen starvation responses by the alarmone (p)ppGpp in rice. J Genet Genomics 49:469–480. https://doi.org/10.1016/J.JGG.2022.02.006 Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1 Lin CC, Ding CKC, Sun T et al (2021) The regulation of ferroptosis by MESH1 through the activation of the integrative stress response. Cell Death Dis 12:727. https://doi.org/10.1038/s41419-021-04018-7 Maekawa M, Honoki R, Ihara Y et al (2015) Impact of the plastidial stringent response in plant growth and stress responses. Nat Plants 1:15167. https://doi.org/10.1038/nplants.2015.167 Masuda S (2012) The stringent response in phototrophs. In: Najafpour M (ed) Advances in photosynthesis. In Tech, London, pp 487–500 Masuda S, Mizusawa K, Narisawa T et al (2008) The bacterial stringent response, conserved in chloroplasts, controls plant fertilization. Plant Cell Physiol 49:135–141. https://doi.org/10.1093/pcp/pcm177 McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37:951–959. https://doi.org/10.1046/j.1529-8817.2001.01126.x Mizusawa K, Masuda S, Ohta H (2008) Expression profiling of four RelA/SpoT-like proteins, homologues of bacterial stringent factors, in Arabidopsis thaliana. Planta 228:553–562. https://doi.org/10.1007/s00425-008-0758-5 Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565. https://doi.org/10.1146/ANNUREV.ARPLANT.57.032905.105350 Ono S, Suzuki S, Ito D et al (2021) Plastidial (p)ppGpp Synthesis by the Ca2+-dependent RelA-SpoT homolog regulates the adaptation of chloroplast gene expression to darkness in Arabidopsis. Plant Cell Physiol 61:2077–2086. https://doi.org/10.1093/PCP/PCAA124 Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394 Romand S, Abdelkefi H, Lecampion C et al (2022) A guanosine tetraphosphate (ppGpp) mediated brake on photosynthesis is required for acclimation to nitrogen limitation in Arabidopsis. Elife 11:e75041. https://doi.org/10.7554/ELIFE.75041 Seyfzadeh M, Keener J, Nomura M (1993) spoT-dependent accumulation of guanosine tetraphosphate in response to fatty acid starvation in Escherichia coli. Proc Natl Acad Sci USA 90:11004–11008. https://doi.org/10.1073/PNAS.90.23.11004 Spira B, Silberstein N, Yagil E (1995) Guanosine 3’,5’-bispyrophosphate (ppGpp) synthesis in cells of Escherichia coli starved for Pi. J Bacteriol 177:4053–4058. https://doi.org/10.1128/JB.177.14.4053-4058.1995 Sugliani M, Abdelkefi H, Ke H et al (2016) An ancient bacterial signaling pathway regulates chloroplast function to influence growth and development in Arabidopsis. Plant Cell 28:661–679 Sun D, Lee G, Lee JH et al (2010) A metazoan ortholog of SpoT hydrolyzes ppGpp and functions in starvation responses. Nat Struct Mol Biol 17:1188–1194. https://doi.org/10.1038/nsmb.1906 Tozawa Y, Nomura Y (2011) Signalling by the global regulatory molecule ppGpp in bacteria and chloroplasts of land plants. Plant Biol (stuttg) 13:699–709. https://doi.org/10.1111/j.1438-8677.2011.00484.x Tozawa Y, Nozawa A, Kanno T et al (2007) Calcium-activated (p)ppGpp synthetase in chloroplasts of land plants. J Biol Chem 282:35536–35545. https://doi.org/10.1074/jbc.M703820200 van der Biezen EA, Sun J, Coleman MJ et al (2000) Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling. Proc Natl Acad Sci 97:3747–3752. https://doi.org/10.1073/pnas.97.7.3747 Vinella D, Albrecht C, Cashel M, D’Ari R (2005) Iron limitation induces SpoT-dependent accumulation of ppGpp in Escherichia coli. Mol Microbiol 56:958–970. https://doi.org/10.1111/J.1365-2958.2005.04601.X