Abstract
Increase in atmospheric carbon dioxide (CO2) has a significant effect on plant growth and development. To explore the elevated-CO2 response, we generated transcriptional profiles over a time course (2 h–14 days) of exposure to elevated CO2 in Arabidopsis thaliana. Genes related to photosynthesis were down-regulated and circadian rhythm-related genes were abnormally regulated in the early to middle phase of elevated CO2 exposure. To understand the novel mechanism of elevated CO2 signaling, we focused on 42 unknown small coding genes that showed differential expression patterns under elevated CO2 conditions. Four transgenic plants overexpressing the small coding gene exhibited a growth-defective phenotype under elevated CO2 but not under current CO2. Transcriptome analysis showed that circadian rhythm-related genes were commonly regulated in four transgenic plants. These circadian rhythm-related genes were transcribed in the dark when CO2 concentrations in the leaf was high. Taken together, our identified four small coding genes are likely to participate in elevated CO2 signaling to the circadian rhythm.
Key Message
Transcriptome analysis was performed under elevated CO2 condition in Arabidopsis thaliana. We identified small coding genes associated with signal molecules from elevated CO2 to circadian rhythm genes.


Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Availability of data and material
The raw unfiltered microarray results are available in the Gene Expression Omnibus (GEO) database under the subseries entry GSE49960.
Code availability
Not applicable.
Abbreviations
- ABA:
-
Abscisic acid
- ANOVA:
-
One-way analysis of variance
- FACE:
-
Free-air CO2 enrichment
- FDR:
-
False discovery rate
- GEO:
-
Gene expression omnibus
- GO:
-
Gene ontology
- GUS:
-
β-Glucuronidase
- LIMMA:
-
Linear models for microarray data
- sORFs:
-
Small open reading frames
- X-gluc:
-
5-Bromo-4-chloro-3-indolyl-β-d-glucuronic acid
References
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2 Elizabeth. New Phytol 165:351–372. https://doi.org/10.1111/j.1469-8137.2004.01224.x
Ainsworth EA, Rogers A, Vodkin LO, Walter A, Schurr U (2006) The effects of elevated CO2 concentration on soybean gene expression. An analysis of growing and mature leaves. Plant Physiol 142:135–147. https://doi.org/10.1104/pp.106.086256
Andrews SJ, Rothnagel JA (2014) Emerging evidence for functional peptides encoded by short open reading frames. Nat Rev Genet 15:193–204. https://doi.org/10.1038/nrg3520
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium -mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Coupe SA, Palmer BG, Lake JA, Overy SA, Oxborough K, Woodward FI, Gray JE, Quick WP (2005) Systemic signalling of environmental cues in Arabidopsis leaves. J Exp Bot 57:329–341. https://doi.org/10.1093/jxb/erj033
Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:R130. https://doi.org/10.1186/gb-2008-9-8-r130
Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469. https://doi.org/10.1104/pp.103.027979
Dyrløv Bendtsen J, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795. https://doi.org/10.1016/j.jmb.2004.05.028
Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JCW, Lynn JR, Straume M, Smith JQ, Millar AJ (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18:639–650. https://doi.org/10.1105/tpc.105.038315
Hanada K, Akiyama K, Sakurai T, Toyoda T, Shinozaki K, Shiu S-H (2009) sORF finder: a program package to identify small open reading frames with high coding potential. Bioinformatics 26:399–400. https://doi.org/10.1093/bioinformatics/btp688
Hanada K, Higuchi-Takeuchi M, Okamoto M, Yoshizumi T, Shimizu M, Nakaminami K, Nishi R, Ohashi C, Iida K, Tanaka M, Horii Y, Kawashima M, Matsui K, Toyoda T, Shinozaki K, Seki M, Matsui M (2013) Small open reading frames associated with morphogenesis are hidden in plant genomes. Proc Natl Acad Sci USA 110:2395–2400. https://doi.org/10.1073/pnas.1213958110
Hanada K, Zhang X, Borevitz JO, Li W-H, Shiu S-H (2007) A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res 17:632–640. https://doi.org/10.1101/gr.5836207.632
Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T (2007) The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21:1720–1725. https://doi.org/10.1101/gad.1550707
Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89. https://doi.org/10.1016/j.pbi.2009.09.007
Kaplan F, Zhao W, Richards JT, Wheeler RM, Guy CL, Levine LH (2012) Transcriptional and metabolic insights into the differential physiological responses of Arabidopsis to optimal and supraoptimal atmospheric CO2. PLoS ONE 7:e43583
Kinoshita T, Ono N, Hayashi Y, Morimoto S, Nakamura S, Soda M, Kato Y, Ohnishi M, Nakano T, Inoue S, Shimazaki K (2011) FLOWERING LOCUS T regulates stomatal opening. Curr Biol 21:1232–1238. https://doi.org/10.1016/j.cub.2011.06.025
Lake JA, Quick WP, Beerling DJ, Woodward FI (2001) Signals from mature to new leaves. Nature 411:154. https://doi.org/10.1038/35075660
Lee IT, Chang AS, Manandhar M, Shan Y, Fan J, Izumo M, Ikeda Y, Motoike T, Dixon S, Seinfeld JE, Takahashi JS, Yanagisawa M (2015) Neuromedin s-producing neurons act as essential pacemakers in the suprachiasmatic nucleus to couple clock neurons and dictate circadian rhythms. Neuron 85:1086–1102. https://doi.org/10.1016/j.neuron.2015.02.006
Lepistö A, Rintamäki E (2012) Coordination of plastid and light signaling pathways upon development of Arabidopsis leaves under various photoperiods. Mol Plant 5:799–816. https://doi.org/10.1093/mp/ssr106
Li P, Ainsworth EA, Leakey ADB, Ulanov A, Lozovaya V, Ort DR, Bohnert HJ (2008) Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated CO2. Plant Cell Environ 31:1673–1687. https://doi.org/10.1111/j.1365-3040.2008.01874.x
Liu T, Carlsson J, Takeuchi T, Newton L, Farré EM (2013) Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J 76:101–114. https://doi.org/10.1111/tpj.12276
Matsubayashi Y, Sakagami Y (2006) Peptide hormones in plants. Annu Rev Plant Biol 57:649–674. https://doi.org/10.1146/annurev.arplant.56.032604.144204
Matsushita T (2011) A versatile method to prevent transcriptional gene silencing in Arabidopsis thaliana. Plant Biotechnol 28:515–519. https://doi.org/10.5511/plantbiotechnology.11.1028a
McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408:716–720. https://doi.org/10.1038/35047079
Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM, Givan SA, McEntee C, Kay SA, Chory J (2007) The diurnal project: diurnal and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb Symp Quant Biol 72:353–363. https://doi.org/10.1101/sqb.2007.72.006
Murphy E, Smith S, De Smet I (2012) Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198–3217. https://doi.org/10.1105/tpc.112.099010
Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T (2005) SEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46:686–698. https://doi.org/10.1093/pcp/pci086
Nakaminami K, Okamoto M, Higuchi-Takeuchi M, Yoshizumi T, Yamaguchi Y, Fukao Y, Shimizu M, Ohashi C, Tanaka M, Matsui M, Shinozaki K, Seki M, Hanada K (2018) AtPep3 is a hormone-like peptide that plays a role in the salinity stress tolerance of plants. Proc Natl Acad Sci USA 115:5810–5815. https://doi.org/10.1073/pnas.1719491115
Negi J, Hashimoto-Sugimoto M, Kusumi K, Iba K (2013) New approaches to the biology of stomatal guard cells. Plant Cell Physiol 55:241–250. https://doi.org/10.1093/pcp/pct145
Porra RJ, Thompson WA, Kriedemann PE (1989) Determinations 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
Reyes-Fox M, Steltzer H, Trlica MJ, McMaster GS, Andales AA, LeCain DR, Morgan JA (2014) Elevated CO2 further lengthens growing season under warming conditions. Nature 510:259–262. https://doi.org/10.1038/nature13207
Rugnone ML, Faigón Soverna A, Sanchez SE, Schlaen RG, Hernando CE, Seymour DK, Mancini E, Chernomoretz A, Weigel D, Más P, Yanovsky MJ (2013) LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. Proc Natl Acad Sci USA 110:12120–12125. https://doi.org/10.1073/pnas.1302170110
Stocker TF, Qin D, Plattner GK, Tignor MMB, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (2013) Climate change 2013 the physical science basis: Working Group I contribution to the fifth assessment report of the intergovernmental panel on climate change. Clim Chang 2013 Phys Sci Basis Work Gr I Contrib to Fifth Assess Rep Intergov Panel Clim Chang 9781107057:1–1535. doi:10.1017/CBO9781107415324
Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445. https://doi.org/10.1073/pnas.1530509100
Takahashi F, Hanada K, Kondo T, Shinozaki K (2019) Hormone-like peptides and small coding genes in plant stress signaling and development. Curr Opin Plant Biol 51:88–95. https://doi.org/10.1016/j.pbi.2019.05.011
Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K (2018) A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556:235–238. https://doi.org/10.1038/s41586-018-0009-2
Taylor G, Street NR, Tricker PJ, Sjödin A, Graham L, Skogström O, Calfapietra C, Scarascia-Mugnozza G, Jansson S (2005) The transcriptome of Populus in elevated CO2. New Phytol 167:143–154. https://doi.org/10.1111/j.1469-8137.2005.01450.x
Terashima I, Yanagisawa S, Sakakibara H (2014) Plant responses to CO2: background and perspectives. Plant Cell Physiol 55:237–240. https://doi.org/10.1093/pcp/pcu022
Valdés AE, Övernäs E, Johansson H, Rada-Iglesias A, Engström P (2012) The homeodomain-leucine zipper (HD-Zip) class I transcription factors ATHB7 and ATHB12 modulate abscisic acid signalling by regulating protein phosphatase 2C and abscisic acid receptor gene activities. Plant Mol Biol 80:405–418. https://doi.org/10.1007/s11103-012-9956-4
Wen J, Lease KA, Walker JC (2004) DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J 37:668–677. https://doi.org/10.1111/j.1365-313X.2003.01994.x
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718
Yannielli PC, Harrington ME (2001) Neuropeptide Y in the mammalian circadian system: effects on light-induced circadian responses. Peptides 22:547–556. https://doi.org/10.1016/S0196-9781(01)00356-4
Yoshii T, Wülbeck C, Sehadova H, Veleri S, Bichler D, Stanewsky R, Helfrich-Förster C (2009) The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila’s clock. J Neurosci 29:2597–2610. https://doi.org/10.1523/JNEUROSCI.5439-08.2009
Acknowledgements
We thank Dr H. Sakakibara, Dr T. Kiba and Dr K. Kusumi for use of the CO2 chambers. This work was supported by the Program for Promotion of Basic and Applied Research for Innovations in Bio-oriented Industry (BRAIN, to M.H. and K.H.), Grants-in-Aid for Scientific Research 19H05348, 19K22313, 18H02420, 18KK0176, 17H03727 (to K.H.), 16K00593 (to M. H.) and the Core Research for Evolutional Science and Technology (CREST) Program “Creation of essential technologies to utilize carbon dioxide as a resource through the enhancement of plant productivity and the exploitation of plant products” of the Japan Science and Technology Agency (JST, JPMJCR11B3 to K.H.).
Author information
Authors and Affiliations
Contributions
M. H.-T. and K. H. conceived the study and obtained funding. M. H.-T., T. K., M. S. and Y. K. performed experiments. K. H. conducted informatics analyses. M. H.-T., T. K. and K. H. wrote the paper. K.S. participated in the experimental design and coordination, and helped to draft the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Higuchi-Takeuchi, M., Kondo, T., Shimizu, M. et al. Effect of small coding genes on the circadian rhythms under elevated CO2 conditions in plants. Plant Mol Biol 104, 55–65 (2020). https://doi.org/10.1007/s11103-020-01023-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-020-01023-w


