Overexpression of a brassinosteroid biosynthetic gene Dwarf enhances photosynthetic capacity through activation of Calvin cycle enzymes in tomato

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• 作者：Xiao-Jing Li ; Xie Guo ; Yan-Hong Zhou ; Kai Shi ; Jie Zhou ; Jing-Quan Yu…
• 关键词：Brassinosteroids ; 2 ; cystein peroxiredoxins ; Dwarf ; Glutathione ; Photosynthesis ; RuBisCO
• 刊名：BMC Plant Biology
• 出版年：2016
• 出版时间：December 2016
• 年：2016
• 卷：16
• 期：1
• 全文大小：1,617 KB
• 参考文献：1.Rolland F, Baena-Gonzalez E, Sheen J. Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annu Rev Plant Biol. 2006;57:675–709.PubMed CrossRef
  2.Kircher S, Schopfer P. Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis. Proc Natl Acad Sci. 2012;109:11217–21.PubMed PubMedCentral CrossRef
  3.Xiong Y, McCormack M, Li L, Hall Q, Xiang CB, Sheen J. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature. 2013;496:181–7.PubMed PubMedCentral CrossRef
  4.Long SP, Zhu XG, Naidu SL, Ort DR. Can improvement in photosynthesis increase crop yields? Plant Cell Environ. 2006;29:315–30.PubMed CrossRef
  5.von Caemmerer S, Evans JR. Enhancing C-3 Photosynthesis. Plant Physiol. 2010;154:589–92.CrossRef
  6.Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek L. The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci. 2006;11:176–83.PubMed CrossRef
  7.Tholen D, Pons TL, Voesenek LACJ, Poorter H. Ethylene insensitivity results in down-regulation of rubisco expression and photosynthetic capacity in tobacco. Plant Physiol. 2007;144:1305–15.PubMed PubMedCentral CrossRef
  8.Biemelt S, Tschiersch H, Sonnewald U. Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol. 2004;135:254–65.PubMed PubMedCentral CrossRef
  9.Jiang X, Li H, Wang T, Peng C, Wang H, Wu H, et al. Gibberellin indirectly promotes chloroplast biogenesis as a means to maintain the chloroplast population of expanded cells. Plant J. 2012;72:768–80.PubMed CrossRef
  10.Pinheiro C, Chaves MM. Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot. 2011;62:869–82.PubMed CrossRef
  11.Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W, Smirnoff N, et al. The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell. 2009;21:2143–62.PubMed PubMedCentral CrossRef
  12.Khripach V, Zhabinskii V, De Groot A. Twenty years of brassinosteroids: Steroidal plant hormones warrant better crops for the XXI century. Ann Bot. 2000;86:441–7.CrossRef
  13.Vriet C, Russinova E, Reuzeau C. Boosting crop yields with plant steroids. Plant Cell. 2012;24:842–57.PubMed PubMedCentral CrossRef
  14.Clouse SD. Brassinosteroid signal transduction: From receptor kinase activation to transcriptional networks regulating plant development. Plant Cell. 2011;23:1219–30.PubMed PubMedCentral CrossRef
  15.Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, et al. Brassinosteroids regulate grain filling in rice. Plant Cell. 2008;20:2130–45.PubMed PubMedCentral CrossRef
  16.Duan P, Rao Y, Zeng D, Yang Y, Xu R, Zhang B, et al. SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice. Plant J. 2014;77:547–57.PubMed CrossRef
  17.Hu YX, Bao F, Li JY. Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant J. 2000;24:693–701.PubMed CrossRef
  18.Schluter U, Kopke D, Altmann T, Mussig C. Analysis of carbohydrate metabolism of CPD antisense plants and the brassinosteroid-deficient cbb1 mutant. Plant Cell Environ. 2002;25:783–91.CrossRef
  19.Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, et al. A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot. 2004;55:1135–43.PubMed CrossRef
  20.Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, et al. Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta. 2009;230:1185–96.PubMed CrossRef
  21.Yang C, Li H, Zhang J, Luo Z, Gong P, Zhang C, et al. A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci. 2011;108:11836–41.PubMed PubMedCentral CrossRef
  22.von Caemmerer S, Farquhar GD. Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves. Planta. 1981;153:376–87.CrossRef
  23.Ethier GJ, Livingston NJ. On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ. 2004;27:137–53.CrossRef
  24.Baker NR. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu Rev Plant Biol. 2008;59:89–113.PubMed CrossRef
  25.Ding J, Mao LJ, Wang ST, Yuan BF, Feng YQ. Determination of endogenous brassinosteroids in plant tissues using solid-phase extraction with double layered cartridge followed by high-performance liquid chromatography-tandem mass spectrometry. Phytochem Anal. 2013;24:386–94.PubMed CrossRef
  26.Arnon DI. Copper enzymes in isolated chloroplasts-polyphenoloxidase in Beta-vulgaris. Plant Physiol. 1949;24:1–15.PubMed PubMedCentral CrossRef
  27.Muthuramalingam M, Dietz KJ, Stroher E. Thiol-disulfide redox proteomics in plant research. Methods Mol Biol. 2010;639:219–38.PubMed CrossRef
  28.Cheng F, Zhou YH, Xia XJ, Shi K, Zhou J, Yu JQ. Chloroplastic thioredoxin-f and thioredoxin-m1/4 play important roles in brassinosteroids-induced changes in CO2 assimilation and cellular redox homeostasis in tomato. J Exp Bot. 2014;65:4335–47.PubMed PubMedCentral CrossRef
  29.Ward DA, Keys AJ. A comparison between the coupled spectrophotometric and uncoupled radiometric assays for RuBP carboxylase. Photosynth Res. 1989;22:167–71.PubMed CrossRef
  30.Scheibe R, Fickenscher K, Ashton AR. Studies on the mechanism of the reductive activation of NADP-malate dehydrogenase by thioredoxin-m and low-molecular-weight thiols. Biochim Biophys Acta. 1986;870:191–7.CrossRef
  31.Rao MV, Ormrod DP. Ozone exposure decreases UVB sensitivity in a UVB-sensitive flavonoid mutant of Arabidopsis. Photochem Photobiol. 1995;61:71–8.PubMed CrossRef
  32.Nakano Y, Asada K. Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981;22:867–80.
  33.Halliwell B, Foyer CH. Ascorbic-acid, metal-ions and superoxide radical. Biochem J. 1976;155:697–700.PubMed PubMedCentral CrossRef
  34.Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC method. Methods. 2001;25:402–8.PubMed CrossRef
  35.Divi UK, Krishna P. Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotech. 2009;26:131–6.CrossRef
  36.Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, et al. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol. 2006;24:105–9.PubMed CrossRef
  37.Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ. Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ. 2014;37:2036–50.PubMed CrossRef
  38.Xue S, Hu H, Ries A, Merilo E, Kollist H, Schroeder JI. Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO2 signal transduction in guard cell. EMBO J. 2011;30:1645–58.PubMed PubMedCentral CrossRef
  39.Kim TW, Michniewicz M, Bergmann DC, Wang ZY. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature. 2012;482:419–U1526.PubMed PubMedCentral CrossRef
  40.Krumova S, Zhiponova M, Dankov K, Velikova V, Balashev K, Andreeva T, et al. Brassinosteroids regulate the thylakoid membrane architecture and the photosystem II function. J Photochem Photobiol B-Biol. 2013;126:97–104.CrossRef
  41.Zhou J, Wang J, Li X, Xia XJ, Zhou YH, Shi K, et al. H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot. 2014;65:4371–83.PubMed PubMedCentral CrossRef
  42.Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot. 2012;63:1637–61.PubMed CrossRef
  43.Wostrikoff K, Stern D. Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc Natl Acad Sci. 2007;104:6466–71.PubMed PubMedCentral CrossRef
  44.Suzuki Y, Makino A. Translational downregulation of RBCL is operative in the coordinated expression of Rubisco genes in senescent leaves in rice. J Exp Bot. 2013;64:1145–52.PubMed PubMedCentral CrossRef
  45.Suzuki Y, Miyamoto T, Yoshizawa R, Mae T, Makino A. Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS. Plant Cell Environ. 2009;32:417–27.PubMed CrossRef
  46.Cohen I, Knopf JA, Irihimovitch V, Shapira M. A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and its subunit expression. Plant Physiol. 2005;137:738–46.PubMed PubMedCentral CrossRef
  47.Cohen I, Sapir Y, Shapira M. A conserved mechanism controls translation of Rubisco large subunit in different photosynthetic organisms. Plant Physiol. 2006;141:1089–97.PubMed PubMedCentral CrossRef
  48.Rojas-González JA, Soto-Súarez M, García-Díaz Á, Romero-Puertas MC, Sandalio LM, Mérida Á, et al. Disruption of both chloroplastic and cytosolic FBPase genes results in a dwarf phenotype and important starch and metabolite changes in Arabidopsis thaliana. J Exp Bot. 2015;66:2673–89.PubMed CrossRef
  49.Moreno J, Garcia-Murria MJ, Marin-Navarro J. Redox modulation of Rubisco conformation and activity through its cysteine residues. J Exp Bot. 2008;59:1605–14.PubMed CrossRef
  50.Sudhani HPK, Moreno J. Control of the ribulose 1,5-bisphosphate carboxylase/oxygenase activity by the chloroplastic glutathione pool. Arch Biochem Biophys. 2015;567:30–4.PubMed CrossRef
  51.Jiang YP, Cheng F, Zhou YH, Xia XJ, Mao WH, Shi K, et al. Cellular glutathione redox homeostasis plays an important role in the brassinosteroid-induced increase in CO2 assimilation in Cucumis sativus. New Phytol. 2012;194:932–43.PubMed CrossRef
  52.Cejudo FJ, Ferrandez J, Cano B, Puerto-Galan L, Guinea M. The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signaling. FEBS Lett. 2012;586:2974–80.PubMed CrossRef
  53.Nie WF, Wang MM, Xia XJ, Zhou YH, Shi K, Chen ZX, et al. Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H2O2 generation and stress tolerance. Plant Cell Environ. 2013;36:7803.CrossRef
  54.Zhang N, Portis AR. Mechanism of light regulation of Rubisco: A specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci. 1999;96:9438–43.PubMed PubMedCentral CrossRef
  55.Zhang N, Kallis RP, Ewy RG, Portis AR. Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci. 2002;99:3330–4.PubMed PubMedCentral CrossRef
  
• 作者单位：Xiao-Jing Li (1)
  Xie Guo (1)
  Yan-Hong Zhou (1)
  Kai Shi (1)
  Jie Zhou (1)
  Jing-Quan Yu (1) (2)
  Xiao-Jian Xia (1) (2)
  
  1. Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou, 310058, P.R. China
  2. Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou, 310058, China
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background Genetic manipulation of brassinosteroid (BR) biosynthesis or signaling is a promising strategy to improve crop yield and quality. However, the relationships between the BR-promoted growth and photosynthesis and the exact mechanism of BR-regulated photosynthetic capacity are not clear. Here, we generated transgenic tomato plants by overexpressing Dwarf, a BR biosynthetic gene that encodes the CYP85A1, and compared the photosynthetic capacity with the BR biosynthetic mutant d im and wild type.