Abstract
Unicellular photoautotrophs adapt to variations in light intensity by changing the abundance of light harvest pigment-protein complexes (LHCs) on time scales of hours to days. This process requires a feedback signal between the plastid (where light intensity is sensed) to the nucleus (where the genes for LHCs are encoded). The signals must include heretofore unidentified transcription factors that modify the expression level of the LHCs. Analysis of the nuclear genome of the model diatom Phaeodactylum tricornutum revealed that all the lhc genes have potential binding sites for transcription factors belonging to the MYB-family proteins. Functional studies involving antisense RNA interference of a hypothetical protein with a MYB DNA-binding domain were performed. The resultant strains with altered photosynthetic and physiological characteristics lost their ability to acclimate to changes in irradiance; i.e., cellular chlorophyll content became independent of growth irradiance. Our results strongly suggest that the inter-organellar signaling cascade was disrupted, and the cell could no longer communicate the environmental signal from the plastid to the nucleus. Here, we identify, for the first time, an LHC Regulating Myb (LRM) transcription factor, which we propose is involved in lhc gene regulation and photoacclimation mechanisms in response to changes in light intensity.
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Abdiche Y, Malashock D, Pinkerton A, Pons J (2008) Determining kinetics and affinities of protein interactions using a parallel real-time label-free biosensor, the octet. Anal Biochem 377(2):209–217. https://doi.org/10.1016/j.ab.2008.03.035
Agarwal A (2021) Inter-organellar signaling in a diatom. 0–181. https://doi.org/10.7282/T3-27SQ-E338.
Albert NW, Lewis DH, Zhang H, Irving LJ, Jameson PE, Davies KM (2009) Light-induced vegetative anthocyanin pigmentation in petunia. J Exp Bot. https://doi.org/10.1093/jxb/erp097
Bailey S, McCarren J, Lieberman SL, Meuser JE, Romano AE, Yee LSD, Brown RC et al (2013) Algal mutants having a locked-in high light acclimated phenoptype. US 2014/0220638 Al, issued 2013
Ballesteros ML, Bolle C, Lois LM, Moore JM, Vielle-Calzada JP, Grossniklaus U, Chua NH (2001) LAF1, a MYB transcription activator for Phytochrome A signaling. Genes Dev. https://doi.org/10.1101/gad.915001
Berner T, Dubinsky Z, Wyman K, Falkowski PG (1989) Photoadaptation and the ‘Package’ effect in Dunaliella tertiolecta (Chlorophyceae) 1. J Phycol 25(1):70–78. https://doi.org/10.1111/J.0022-3646.1989.00070.X
Büchel C (2019) Light harvesting complexes in chlorophyll c-containing algae. Biochim Biophys Acta Bioenergy 1861:148027
Buck JM, Sherman J, Bártulos CR, Serif M, Halder M, Henkel J, Falciatore A et al (2019) Lhcx proteins provide photoprotection via thermal dissipation of absorbed light in the diatom Phaeodactylum tricornutum. Nat Commun 10(1):1–12. https://doi.org/10.1038/s41467-019-12043-6
Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21(13):2933–2942. https://doi.org/10.1093/bioinformatics/bti473
Churin Y, Adam E, Kozma-Bognar L, Nagy F, Börner T (2003) Characterization of two Myb-like transcription factors binding to CAB promoters in wheat and barley. Plant Mol Biol. https://doi.org/10.1023/A:1023934232662
De Martino A, Meichenin A, Shi J, Pan K, Bowler C (2007) Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions 1. J Phycol 43(5):992–1009. https://doi.org/10.1111/j.1529-8817.2007.00384.x
Desai M, Wurihan W, Di R, Fondell JD, Nickels BE, Bao X, Fan H (2018) Role for GrgA in regulation of 28-dependent transcription in the obligate intracellular bacterial pathogen chlamydia trachomatis. J Bacteriol. https://doi.org/10.1128/JB.00298-18
Di R, Huang Q, Stulberg M, Zhao L, Levy L (2016) Detection of plant quarantine pathogen Ralstonia solanacearum race 3 biovar 2 with portable POCKIT™ and BLItz® systems. J Plant Health 1(1):103–111
Dinamarca J, Levitan O, Kenchappa Kumaraswamy G, Lun DS, Falkowski PG (2017) Overexpression of a diacylglycerol acyltransferase gene in Phaeodactylum tricornutum directs carbon towards lipid biosynthesis. J Phycol 53(2):405–414. https://doi.org/10.1111/jpy.12513
Dubinsky Z, Falkowski PG, Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27(7):1335–1349
Durnford DG, Falkowski PG (1997) Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth Res 53(2–3):229–241. https://doi.org/10.1023/a:1005815725371
Escoubas JM, Lomas M, LaRoche J, Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci 92(22):10237–10241. https://doi.org/10.1073/pnas.92.22.10237
Falciatore A, Casotti R, Leblanc C, Abrescia C, Bowler C (1999) Transformation of nonselectable reporter genes in marine diatoms. Mar Biotechnol 1(3):239–251. https://doi.org/10.1007/PL00011773
Falkowski PG, LaRoche J (1991) Acclimation to spectral irradiance in algae. J Phycol. https://doi.org/10.1111/j.0022-3646.1991.00008.x
Falkowski PG, Dubinsky Z, Wyman K (1985) Growth-irradiance relationships in phytoplankton. Limnol Oceanogr 30(2):311–321. https://doi.org/10.4319/lo.1985.30.2.0311
Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The Evolution of Modern Eukaryotic Phytoplankton. Science. https://doi.org/10.1126/science.1095964
Galtier N, Gouy M, Gautier C (1996) Seaview and Phylo_Win: two graphic tools for sequence alignment and molecular phylogeny. Bioinformatics 12(6):543–548. https://doi.org/10.1093/bioinformatics/12.6.543
Gibson DG, Young L, Chuang RY, Craig Venter J, Hutchison CA, Smith HO (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6(5):343–345. https://doi.org/10.1038/nmeth.1318
Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang R-Y, Algire MA, Benders GA et al (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329(5987):52–56. https://doi.org/10.1126/science.1190719
Glatz A, Vass I, Los DA, Vigh L (1999) The synechocystis model of stress: from molecular chaperones to membranes. Plant Physiol Biochem. https://doi.org/10.1016/S0981-9428(99)80061-8
Goldman JC, McCarthy JJ (1978) Steady state growth and ammonium uptake of a fast-growing marine diatom. Limnol Oceanogr 23(4):695–703. https://doi.org/10.4319/lo.1978.23.4.0695
Gorbunov MY, Falkowski PG (2004) Fluorescence induction and relaxation (FIRe) technique and instrumentation for monitoring photosynthetic processes and primary production in aquatic ecosystems. In: Photosynthesis: fundamental aspects to global perspectives-proceedings of the 13th international congress of photosynthesis
Gouy M, Guindon S, Gascuel O (2010) Sea View Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27(2):221–224. https://doi.org/10.1093/molbev/msp259
Grossman AR (2000) Chlamydomonas reinhardtii and photosynthesis: genetics to genomics. Curr Opin Plant Biol. https://doi.org/10.1016/S1369-5266(99)00053-9
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) gran. Can J Microbiol 8(2):229–239. https://doi.org/10.1139/m62-029
Harris EH (2001) Chlamydomonas as a model organism. Annu Rev Plant Biol 52:363–406. https://doi.org/10.1146/annurev.arplant.52.1.363
Hegemann P, Fuhrmann M, Kateriya S (2001) Minireview algal sensory photoreceptors 1. J Phycol 37
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, C1 and C2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167(2):191–194. https://doi.org/10.1016/S0015-3796(17)30778-3
Levitan O, Dinamarca J, Zelzion E, Lun DS, Tiago Guerra L, Kim MK, Kim J, Van Mooy BAS, Bhattacharya D, Falkowski PG (2015) Remodeling of intermediate metabolism in the diatom phaeodactylum tricornutum under nitrogen stress. Proc Natl Acad Sci 112(2):412–417. https://doi.org/10.1073/pnas.1419818112
Liang YK, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM (2005) AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol. https://doi.org/10.1016/j.cub.2005.06.041
Lindemose S, O’Shea C, Jensen MK, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci. https://doi.org/10.3390/ijms14035842
Liu X, Li L, Li M, Liangchen Su, Lian S, Zhang B, Li X, Ge K, Li L (2018) AhGLK1 affects chlorophyll biosynthesis and photosynthesis in peanut leaves during recovery from drought. Sci Rep. https://doi.org/10.1038/s41598-018-20542-7
Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45(1):633–662. https://doi.org/10.1146/ANNUREV.PP.45.060194.003221
Matthijs M, Fabris M, Obata T, Foubert I, Franco-Zorrilla JM, Solano R, Fernie AR, Vyverman W, Goossens A (2017) The transcription factor BZIP14 regulates the TCA cycle in the diatom Phaeodactylum tricornutum. EMBO J 36(11):1559–1576. https://doi.org/10.15252/embj.201696392
McLachlan J (1964) Some considerations of the growth of marine algae in artificial media. Can J Microbiol 10(5):769–782. https://doi.org/10.1139/m64-098
Meyerowitz EM (2001) Prehistory and history of Arabidopsis research. Plant Physiol 125(1):15–19. https://doi.org/10.1104/pp.125.1.15
Nguyen B, Tanious FA, David Wilson W (2007) Biosensor-surface plasmon resonance: quantitative analysis of small molecule-nucleic acid interactions. Methods 42(2):150–161. https://doi.org/10.1016/j.ymeth.2006.09.009
Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol. https://doi.org/10.1146/annurev.arplant.57.032905.105310
Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci. https://doi.org/10.1016/S1360-1385(02)00005-5
Pfannschmidt T, Bräutigam K, Wagner R, Dietzel L, Schröter Y, Steiner S, Nykytenko A (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 103(4):599–607. https://doi.org/10.1093/aob/mcn081
Rayko E, Maumus F, Maheswari U, Jabbari K, Bowler C (2010) Transcription factor families inferred from genome sequences of photosynthetic stramenopiles. New Phytol 188(1):52–66. https://doi.org/10.1111/j.1469-8137.2010.03371.x
Rochaix JD (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet. https://doi.org/10.1146/annurev.ge.29.120195.001233
Soitamo AJ, Piippo M, Allahverdiyeva Y, Battchikova N, Aro EM (2008) Light has a specific role in modulating arabidopsis gene expression at low temperature. BMC Plant Biol. https://doi.org/10.1186/1471-2229-8-13
Sukenik A, Bennett J, Falkowski P (1987) Light-saturated photosynthesis—limitation by electron transport or carbon fixation? Biochim Biophys Acta Bioenerg 891(3):205–215. https://doi.org/10.1016/0005-2728(87)90216-7
Wang ZY, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. https://doi.org/10.1016/S0092-8674(00)81464-6
Zallen DT (1993) The ‘Light’ organism for the job: green algae and photosynthesis research. J Hist Biol 26(2):269–279. https://doi.org/10.1007/BF01061970
Zhou C, Li C (2016) A novel R2R3-MYB transcription factor BpMYB106 of birch (Betula platyphylla) confers increased photosynthesis and growth rate through up-regulating photosynthetic gene expression. Front Plant Sci 7(MAR2016):315. https://doi.org/10.3389/fpls.2016.00315
Zoratti L, Karppinen K, Escobar AL, Häggman H, Jaakola L (2014) Light-controlled flavonoid biosynthesis in fruits. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00534
Acknowledgements
We thank Ehud Zelzion and Nicole Wagner (Rutgers, The State University of New Jersey) for the transcriptome sequencing and its analysis and to Shaun Bailey and Orly Levitan for discussions. This work, in its entirety, was included in the thesis of Agarwal A. (2021), titled “Inter-organellar signaling in a diatom” (Rutgers University 2021).
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This research was supported by the Rutgers University Professional Development Fund, the James G. Gibson (Biodiesel) Fund to PGF, and the Bennett L. Smith Endowment in Business and Natural Resources at Rutgers University to PGF.
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AA and RD designed research. AA and RD performed research. AA, RD and PGF analyzed data. AA wrote first draft of manuscript. All authors contributed to manuscript revision, read, and approved the submitted version.
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Agarwal, A., Di, R. & Falkowski, P.G. Light-harvesting complex gene regulation by a MYB-family transcription factor in the marine diatom, Phaeodactylum tricornutum. Photosynth Res 153, 59–70 (2022). https://doi.org/10.1007/s11120-022-00915-w
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DOI: https://doi.org/10.1007/s11120-022-00915-w