Low light intensity elongates period and defers peak time of photosynthesis: a computational approach to circadian-clock-controlled photosynthesis in tomato

Ting Huang , Hui Liu , Jian-Ping Tao , Jia-Qi Zhang , Tong-Min Zhao , Xi-Lin Hou , Ai-Sheng Xiong , Xiong You

Horticulture Research ›› 2023, Vol. 10 ›› Issue (6) : 077

PDF (2983KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (6) :077 DOI: 10.1093/hr/uhad077
Article
research-article
Low light intensity elongates period and defers peak time of photosynthesis: a computational approach to circadian-clock-controlled photosynthesis in tomato
Author information +
History +
PDF (2983KB)

Abstract

Photosynthesis is involved in the essential process of transforming light energy into chemical energy. Although the interaction between photosynthesis and the circadian clock has been confirmed, the mechanism of how light intensity affects photosynthesis through the circadian clock remains unclear. Here, we propose a first computational model for circadian-clock-controlled photosynthesis, which consists of the light-sensitive protein P, the core oscillator, photosynthetic genes, and parameters involved in the process of photosynthesis. The model parameters were determined by minimizing the cost function (δ = 8.56), which is defined by the errors of expression levels, periods, and phases of the clock genes (CCA1, PRR9, TOC1, ELF4, GI, and RVE8). The model recapitulates the expression pattern of the core oscillator under moderate light intensity (100 μmol m−2 s−1). Further simulation validated the dynamic behaviors of the circadian clock and photosynthetic outputs under low (62.5 μmol m−2 s−1) and normal (187.5 μmol m−2 s−1) intensities. When exposed to low light intensity, the peak times of clock and photosynthetic genes were shifted backward by 1–2 hours, the period was elongated by approximately the same length, and the photosynthetic parameters attained low values and showed delayed peak times, which confirmed our model predictions. Our study reveals a potential mechanism underlying the circadian regulation of photosynthesis by the clock under different light intensities in tomato.

Cite this article

Download citation ▾
Ting Huang, Hui Liu, Jian-Ping Tao, Jia-Qi Zhang, Tong-Min Zhao, Xi-Lin Hou, Ai-Sheng Xiong, Xiong You. Low light intensity elongates period and defers peak time of photosynthesis: a computational approach to circadian-clock-controlled photosynthesis in tomato. Horticulture Research, 2023, 10 (6) : 077 DOI:10.1093/hr/uhad077

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was partially supported by the National Natural Science Foundation of China (11171155, 11871268), the National Natural Science Foundation of Jiangsu Province, China (BK20171370, BK20221009), the Jiangsu Agricultural Science and Technology Innovation Fund [CX (21) 3025], the China Postdoctoral Science Foundation (2021 M701742), and the Priority Academic Program Development of Jiangsu Higher Education Institution Project (PAPD).

Author Contributions

X.Y. and A.S.X. designed the research; T.H. built the computational model and made numerical simulations; T.H., H.L., J.P.T., and J.Q.Z. performed the experiments; T.H., H.L., and J.P.T. analyzed the data and wrote the paper; T.M.Z. and X.L.H. provided English language editing; and X.Y. and A.S.X. revised the paper.

Data availability

Data are available in figures of the article and its supplementary materials.

Conflict of interest

The authors declare no competing interests.

Compliance with ethics requirement

This article does not contain any studies with human or animal subjects.

References

[1]

Han N, Fan S, Zhang T et al. SlHY5 is a necessary regulator of the cold acclimation response in tomato. Plant Growth Regul. 2020; 91: 1-12.

[2]

Lu T, Meng Z, Zhang G et al. Sub-high temperature and high light intensity induced irreversible inhibition on photosynthesis system of tomato plant (Solanum lycopersicum L.). Front Plant Sci. 2017; 08: 365.

[3]

Johnson MP . Photosynthesis. Essays Biochem. 2016; 60: 255-73.

[4]

Zournas A, Mani K, Dismukes GC . Cyclic electron flow around photosystem II in silico: how it works and functions in vivo. Photosynth Res. 2023; 156: 129-45.

[5]

Berry JO, Yerramsetty P, Zielinski AM et al. Photosynthetic gene expression in higher plants. Photosynth Res. 2013; 117: 91-120.

[6]

Lu J, Pan C, Li X et al. OBV (obscure vein), a C2H2 zinc finger transcription factor, positively regulates chloroplast development and bundle sheath extension formation in tomato (Solanum lycopersicum) leaf veins. Hortic Res. 2021; 8: 230.

[7]

Pietrzykowska M, Suorsa M, Semchonok DA et al. The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis. Plant Cell. 2014; 26: 3646-60.

[8]

Tamim SA, Li F, Wang Y et al. Effect of shading on ascorbic acid accumulation and biosynthetic gene expression during tomato fruit development and ripening. Veget Res. 2022; 2: 1-8.

[9]

Wang X, Chen G, Du S et al. Light intensity influence on growth and photosynthetic characteristics of Horsfieldia hainanensis. Front Ecol Evol. 2021; 9: 636804.

[10]

Khurshid G, Abbassi AZ, Khalid MF et al. A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants. Sci Rep. 2020; 10: 20879.

[11]

Von Caemmerer S. Steady-state models of photosynthesis. Plant Cell Environ. 2013; 36: 1617-30.

[12]

Zhu XG, de Sturler E, Long SP . Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol. 2007; 145: 513-26.

[13]

Xin CP, Tholen D, Devloo V et al. The benefits of photorespiratory bypasses: how can they work? Plant Physiol. 2015; 167: 574-85.

[14]

Poolman MG, Fell DA, Thomas S . Modelling photosynthesis and its control. J Exp Bot. 2000; 51: 319-28.

[15]

Ebenhöh O, Fucile G, Finazzi G et al. Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model. Phil Trans R Soc B. 2014; 369: 20130223.

[16]

Dodd AN, Belbin FE, Frank A et al. Interactions between circadian clocks and photosynthesis for the temporal and spatial coordination of metabolism. Front Plant Sci. 2015; 6: 245.

[17]

Nakamichi N, Yamaguchi J, Sato A et al. Chemical biology to dissect molecular mechanisms underlying plant circadian clocks. New Phytol. 2022; 235: 1336-43.

[18]

Xu X, Yuan L, Xie Q . The circadian clock ticks in plant stress responses. Stress Biol. 2022; 2: 15.

[19]

Harmer SL, Fankhauser C, Webb AAR . Focus on circadian rhythms. Plant Physiol. 2022; 190: 921-3.

[20]

Torii K, Inoue K, Bekki K et al. A guiding role of the Arabidopsis circadian clock in cell differentiation revealed by time-series single-cell RNA sequencing. Cell Rep. 2022; 40: 111059.

[21]

Román Á, Li X, Deng D et al. Superoxide is promoted by sucrose and affects amplitude of circadian rhythms in the evening. Proc Natl Acad Sci USA. 2021; 118: e2020646118.

[22]

Creux N, Harmer S . Circadian rhythms in plants. Cold Spring Harb Perspect Biol. 2019; 11: a034611.

[23]

Hsu PY, Devisetty UK, Harmer SL . Accurate timekeeping is controlled by a cycling activator in Arabidopsis. eLife. 2013; 2: e00473.

[24]

De Caluwé J, Xiao Q, Hermans C et al. A compact model for the complex plant circadian clock. Front Plant Sci. 2016; 7: 74.

[25]

Hsu PY, Harmer SL . Wheels within wheels: the plant circadian system. Trends Plant Sci. 2014; 19: 240-9.

[26]

Nakamichi N, Kiba T, Henriques R et al. PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell. 2010; 22: 594-605.

[27]

Xie Q, Wang P, Liu X et al. LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell. 2014; 26: 2843-57.

[28]

Pokhilko A, Fernández AP, Edwards KD et al. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol. 2012; 8: 574.

[29]

Kim WY, Fujiwara S, Suh SS et al. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature. 2007; 449: 356-60.

[30]

Haydon MJ, Mielczarek O, Robertson FC et al. Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature. 2013; 502: 689-92.

[31]

Frank A, Matiolli CC, Viana AJC et al. Circadian entrainment in Arabidopsis by the sugar-responsive transcription factor bZIP63. Curr Biol. 2018; 28: 2597-2606.e6.

[32]

Xu X, Yuan L, Yang X et al. Circadian clock in plants: linking timing to fitness. J Integr Plant Biol. 2022; 64: 792-811.

[33]

Hwang Y, Han S, Yoo CY et al. Anterograde signaling controls plastid transcription via sigma factors separately from nuclear photosynthesis genes. Nat Commun. 2022; 13: 7440.

[34]

Liu Z, Yu C, Xiang B et al. Processing tomato chlorophyll a/b-binding protein 1C interacts with CMV 2b protein. Physiol Mol Plant Pathol. 2022; 120: 101857.

[35]

Zhuang K, Kong F, Zhang S et al. Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation. New Phytol. 2019; 221: 1998-2012.

[36]

Martin-Avila E, Lim Y-L, Birch R et al. Modifying plant photosynthesis and growth via simultaneous chloroplast transformation of rubisco large and small subunits. Plant Cell. 2020; 32: 2898-916.

[37]

Zhuang K, Wang J, Jiao B et al. WHIRLY1 maintains leaf photosynthetic capacity in tomato by regulating the expression of RbcS1 under chilling stress. J Exp Bot. 2020; 71: 3653-63.

[38]

Gong C, Cheng M, Li J et al. The α-subunit of the chloroplast ATP synthase of tomato reinforces resistance to gray mold and broad-spectrum resistance in transgenic tobacco. Phytopathology 2021; 111: 485-495.

[39]

Liu T, Duan W, Chen Z Enhanced photosynthetic activity in pak choi hybrids is associated with increased grana thylakoids in chloroplasts. Plant J. 2020; 103: 2211-24.

[40]

Wang ZY, Tobin EM. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. 1998; 93: 1207-17.

[41]

Cha JY, Lee D, Ali I et al. Arabidopsis GIGANTEA negatively regulates chloroplast biogenesis and resistance to herbicide butafenacil. Plant Cell Rep. 2019; 38: 793-801.

[42]

Müller NA, Wijnen CL, Srinivasan A et al. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nat Genet. 2016; 48: 89-93.

[43]

Greenwood M, Tokuda IT, Locke JCW . A spatial model of the plant circadian clock reveals design principles for coordinated timing. Mol Syst Biol. 2022; 18: e10140.

[44]

Rawat R, Takahashi N, Hsu PY et al. REVEILLE8 and PSEUDO-RESPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLoS Genet. 2011; 7: e1001350.

[45]

Huang H, Nusinow DA . Into the evening: complex interactions in the Arabidopsis circadian clock. Trends Genet. 2016; 32: 674-86.

[46]

Nohales MA, Kay SA . Molecular mechanisms at the core of the plant circadian oscillator. Nat Struct Mol Biol. 2016; 23: 1061-9.

[47]

Locke JCW, Kozma-Bognár L, Gould PD et al. Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol. 2006; 2: 59.

[48]

Gould PD, Locke JCW, Larue C et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell. 2006; 18: 1177-87.

[49]

Kidokoro S, Hayashi K, Haraguchi H et al. Posttranslational regulation of multiple clock-related transcription factors triggers cold-inducible gene expression in Arabidopsis. Proc Natl Acad Sci USA. 2021; 118: e2021048118.

[50]

Michael TP . Core circadian clock and light signaling genes brought into genetic linkage across the green lineage. Plant Physiol. 2022; 190: 1037-56.

[51]

Aschoff J . Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Ethology. 1979; 49: 225-49.

[52]

Gil K, Park C . Thermal adaptation and plasticity of the plant circadian clock. New Phytol. 2019; 221: 1215-29.

[53]

Andronis C, Barak S, Knowles SM et al. The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol Plant. 2008; 1: 58-67.

[54]

Green RM, Tobin EM . Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. Proc Natl Acad Sci USA. 1999; 96: 4176-9.

[55]

Pogson BJ, Albrecht V . Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol. 2011; 155: 1545-51.

[56]

Moualeu-Ngangue DP, Chen T, Stützel H . A new method to estimate photosynthetic parameters through net assimilation rate-intercellular space CO2 concentration (a-Ci) curve and chlorophyll fluorescence measurements. New Phytol. 2017; 213: 1543-54.

[57]

Dixon LE, Knox K, Kozma-Bognar L et al. Temporal repression of core circadian genes is mediated through EARLY FLOWERING 3 in Arabidopsis. Curr Biol. 2011; 21: 120-5.

[58]

Sorkin ML, Tzeng SC, King S et al. COLD REGULATED GENE 27 and 28 antagonize the transcriptional activity of the RVE8/LNK1/LNK2 circadian complex. Plant Physiol 2023; kiad210.

[59]

Xing H, Wang P, Cui X et al. LNK1 and LNK2 recruitment to the evening element require morning expressed circadian related MYB-like transcription factors. Plant Signal Behav. 2015; 10: e1010888.

[60]

Yan J, Kim YJ, Somers DE . Post-translational mechanisms of plant circadian regulation. Genes. 2021; 12: 325.

[61]

Fujiwara S, Wang L, Han L et al. Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. J Biol Chem. 2008; 283: 23073-83.

[62]

Han X, Huang X, Deng XW . The photomorphogenic central repressor COP1: conservation and functional diversification during evolution. Plant Commun. 2020; 1: 100044.

[63]

Wang F, Zhang L, Chen X et al. SlHY5 integrates temperature, light, and hormone signaling to balance plant growth and cold tolerance. Plant Physiol. 2019; 179: 749-60.

[64]

Kung JE, Jura N . The pseudokinase TRIB 1 toggles an intramolecular switch to regulate COP 1 nuclear export. EMBO J. 2019; 38: e99708.

[65]

Zhang L, Jiang X, Liu Q et al. The HY5 and MYB15 transcription factors positively regulate cold tolerance in tomato via the CBF pathway. Plant Cell Environ. 2020; 43: 2712-26.

[66]

Wang W, Wang P, Li X et al. The transcription factor SlHY5 regulates the ripening of tomato fruit at both the transcriptional and translational levels. Hortic Res. 2021; 8: 83.

[67]

Li G, Siddiqui H, Teng Y et al. Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat Cell Biol. 2011; 13: 616-22.

[68]

Lau OS, Deng XW . Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol. 2010; 13: 571-7.

[69]

Gangappa SN, Botto JF . The multifaceted roles of HY5 in plant growth and development. Mol Plant. 2016; 9: 1353-65.

[70]

Burko Y, Seluzicki A, Zander M et al. Chimeric activators and repressors define HY5 activity and reveal a light-regulated feedback mechanism. Plant Cell. 2020; 32: 967-83.

[71]

King S. Luminous intensity of an LED as a function of input power. J Phys. 2008; 2: 1-4.

[72]

Peeters JCH, Eilers P . The relationship between light intensity and photosynthesis-a simple mathematical model. Hydrobiol Bull. 1978; 12: 134-6.

[73]

Pay ML, Kim DW, Somers DE et al. Modelling of plant circadian clock for characterizing hypocotyl growth under different light quality conditions. In Silico Plants. 2022; 4: diac001.

[74]

Keily J, MacGregor DR, Smith RW et al. Model selection reveals control of cold signalling by evening-phased components of the plant circadian clock. Plant J. 2013; 76: 247-57.

[75]

Resco de Dios V, Gessler A . Circadian regulation of photosynthesis and transpiration from genes to ecosystems. Environ Exp Bot. 2018; 152: 37-48.

[76]

Wimalasekera R. Effect of light intensity on photosynthesis. In: Ahmad P, Abass Ahanger M, Nasser Alyemeni M et al. (eds), Photosynthesis, Productivity, and Environmental Stress. Wiley-Blackwell, Hoboken, New Jersey, United States; 2019, 65-73.

[77]

Dodd AN, Kusakina J, Hall A et al. The circadian regulation of photosynthesis. Photosynth Res. 2014; 119: 181-90.

[78]

Jiang Q, Xu ZS, Wang F et al. Correlating effects of abiotic stresses with the expression of Lhcb1 gene and photosynthetic activity in Oenanthe javanica and Apium graveolens. Biol Plant. 2014; 58: 256-64.

[79]

Dodd AN, Parkinson K, Webb AAR . Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol. 2004; 162: 63-70.

[80]

Resco de Dios V. Circadian regulation and diurnal variation in gas exchange. Plant Physiol. 2017; 175: 3-4.

[81]

Resco de Dios V, Loik ME, Smith R et al. Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth. Plant Cell Environ. 2016; 39: 3-11.

[82]

Ross O, Geider R . New cell-based model of photosynthesis and photo-acclimation: accumulation and mobilisation of energy reserves in phytoplankton. Mar Ecol Prog Ser. 2009; 383: 53-71.

[83]

Bernardi A, Perin G, Sforza E et al. An identifiable state model to describe light intensity influence on microalgae growth. Ind Eng Chem Res. 2014; 53: 6738-49.

[84]

Arnon DI . The light reactions of photosynthesis. Proc Natl Acad Sci USA. 1971; 68: 2883-92.

[85]

Liu JX, Jiang Q, Tao JP et al. Integrative genome, transcriptome, microRNA and degradome analysis of water dropwort (Oenanthe javanica) in response to water stress. Hortic Res. 2021; 8: 26.

[86]

Avello PA, Davis SJ, Ronald J et al. Heat the clock: entrainment and compensation in Arabidopsis circadian rhythms. J Circadian Rhythms. 2019; 17: 5.

[87]

Lu X, Zhou Y, Fan F et al. Coordination of light, circadian clock with temperature: the potential mechanisms regulating chilling tolerance in rice. J Integr Plant Biol. 2020; 62: 737-60.

[88]

Teo J, Mohan R, Zhang S et al. Optimization of light and temperature in indoor farming to boost anthocyanin biosynthesis and accumulation in Indigo Rose tomato. Veget Res. 2022; 2: 1-11.

[89]

Zhang RQ, Gonze D, Hou XL et al. A computational model for the cold response pathway in plants. Front Physiol. 2020; 11: 591073.

[90]

Locke JCW, Millar AJ, Turner MS . Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. J Theor Biol. 2005; 234: 383-93.

PDF (2983KB)

83

Accesses

0

Citation

Detail

Sections
Recommended

/