Abstract
De novo genes created in the plant mitochondrial genome have frequently been transferred into the nuclear genome via intergenomic gene transfer events. Therefore, plant mitochondria might be a source of de novo genes in the nuclear genome. However, the functions of de novo genes originating from mitochondria and the evolutionary fate remain unclear. Here, we revealed that an Arabidopsis thaliana specific small coding gene derived from the mitochondrial genome regulates floral transition. We previously identified 49 candidate de novo genes that induce abnormal morphological changes on overexpression. We focused on a candidate gene derived from the mitochondrial genome (sORF2146) that encodes 66 amino acids. Comparative genomic analyses indicated that the mitochondrial sORF2146 emerged in the Brassica lineage as a de novo gene. The nuclear sORF2146 emerged following an intergenomic gene transfer event in the A. thaliana after the divergence between Arabidopsis and Capsella. Although the nuclear and mitochondrial sORF2146 sequences are the same in A. thaliana, only the nuclear sORF2146 is transcribed. The nuclear sORF2146 product is localized in mitochondria, which may be associated with the pseudogenization of the mitochondrial sORF2146. To functionally characterize the nuclear sORF2146, we performed a transcriptomic analysis of transgenic plants overexpressing the nuclear sORF2146. Flowering transition-related genes were highly regulated in the transgenic plants. Subsequent phenotypic analyses demonstrated that the overexpression and knockdown of sORF2146 in transgenic plants resulted in delayed and early flowering, respectively. These findings suggest that a lineage-specific de novo gene derived from mitochondria has an important regulatory effect on floral transition.
Key message
A large-scale intergenomic gene transfer event involving the nuclear and mitochondrial genomes in the Arabidopsis thaliana lineage created a small coding gene that regulates floral timing.
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Data availability
The raw unfiltered microarray results and the normalized data generated during and/or analyzed during the current study are available in the Gene Expression Omnibus (GEO) repository under the subseries entry GSE184689, https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE184689. The sORF2146 full-length transcript sequence generated during and/or analyzed during the current study will be available in the DNA Data Bank of Japan (DDBJ) repository under the subseries entry LC718385 on December 1st 2022, https://getentry.ddbj.nig.ac.jp/getentry/na/LC718385?filetype=html
References
Adams KL, Palmer JD (2003) Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 29:380–395. https://doi.org/10.1016/S1055-7903(03)00194-5
Akhter S, Uddin MN, Jeong IS, Kim DW, Liu X-M, Bahk JD (2016) Role of Arabidopsis AtPI4Kγ3, a type II phosphoinositide 4-kinase, in abiotic stress responses and floral transition. Plant Biotechnol J 14:215–230. https://doi.org/10.1111/pbi.12376
Almagro Armenteros JJ, Sønderby CK, Sønderby SK, Nielsen H, Winther O (2017) DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics 33:3387–3395. https://doi.org/10.1093/bioinformatics/btx431
Alonso-Blanco C, Andrade J, Becker C, Bemm F, Bergelson J, Borgwardt KM, Cao J, Chae E, Dezwaan TM, Ding W, Ecker JR, Exposito-Alonso M, Farlow A, Fitz J, Gan X, Grimm DG, Hancock AM, Henz SR, Holm S, Horton M, Jarsulic M, Kerstetter RA, Korte A, Korte P, Lanz C, Lee C-R, Meng D, Michael TP, Mott R, Muliyati NW, Nägele T, Nagler M, Nizhynska V, Nordborg M, Novikova PY, Picó FX, Platzer A, Rabanal FA, Rodriguez A, Rowan BA, Salomé PA, Schmid KJ, Schmitz RJ, Seren Ü, Sperone FG, Sudkamp M, Svardal H, Tanzer MM, Todd D, Volchenboum SL, Wang C, Wang G, Wang X, Weckwerth W, Weigel D, Zhou X (2016) 1,135 Genomes reveal the global pattern of polymorphism in arabidopsis thaliana. Cell 166:481–491. https://doi.org/10.1016/j.cell.2016.05.063
Andersson DI, Jerlström-Hultqvist J, Näsvall J (2015) Evolution of new functions de novo and from preexisting genes. Cold Spring Harb Perspect Biol 7:a017996. https://doi.org/10.1101/cshperspect.a017996
Arendsee ZW, Li L, Wurtele ES (2014) Coming of age: orphan genes in plants. Trends Plant Sci 19:698–708. https://doi.org/10.1016/j.tplants.2014.07.003
Arimura S, Ayabe H, Sugaya H, Okuno M, Tamura Y, Tsuruta Y, Watari Y, Yanase S, Yamauchi T, Itoh T, Toyoda A, Takanashi H, Tsutsumi N (2020) Targeted gene disruption of ATP synthases 6–1 and 6–2 in the mitochondrial genome of Arabidopsis thaliana by mitoTALENs. Plant J 104:1459–1471. https://doi.org/10.1111/tpj.15041
Basrai MA, Hieter P, Boeke JD (1997) Small open reading frames: beautiful needles in the haystack. Genome Res 7:768–771. https://doi.org/10.1101/gr.7.8.768
Berg OG, Kurland CG (2000) Why mitochondrial genes are most often found in nuclei. Mol Biol Evol 17:951–961. https://doi.org/10.1093/oxfordjournals.molbev.a026376
Blevins WR, Ruiz-Orera J, Messeguer X, Blasco-Moreno B, Villanueva-Cañas JL, Espinar L, Díez J, Carey LB, Albà MM (2021) Uncovering de novo gene birth in yeast using deep transcriptomics. Nat Commun 12:604. https://doi.org/10.1038/s41467-021-20911-3
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Cai J, Zhao R, Jiang H, Wang W (2008) De Novo origination of a new protein-coding gene in Saccharomyces cerevisiae. Genetics 179:487–496. https://doi.org/10.1534/genetics.107.084491
Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, Wang X, Ott F, Müller J, Alonso-Blanco C, Borgwardt K, Schmid KJ, Weigel D (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43:956–963. https://doi.org/10.1038/ng.911
Carlsson J, Leino M, Sohlberg J, Sundström JF, Glimelius K (2008) Mitochondrial regulation of flower development. Mitochondrion 8:74–86. https://doi.org/10.1016/j.mito.2007.09.006
Chen L, DeVries AL, Cheng C-HC (1997) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci 94:3811–3816. https://doi.org/10.1073/pnas.94.8.3811
Chen S, Krinsky BH, Long M (2013) New genes as drivers of phenotypic evolution. Nat Rev Genet 14:645–660. https://doi.org/10.1038/nrg3521
Cheng-Guo D, Chun-Han W, Rong-Xiang F, Hui-Shan G (2008) Artificial microRNAs highly accessible to targets confer efficient virus resistance in plants. J Virol 82:11084–11095. https://doi.org/10.1128/JVI.01377-08
Christensen AC (2013) Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome Biol Evol 5:1079–1086. https://doi.org/10.1093/gbe/evt069
Chuah J-A, Yoshizumi T, Kodama Y, Numata K (2015) Gene introduction into the mitochondria of Arabidopsis thaliana via peptide-based carriers. Sci Rep 5:7751. https://doi.org/10.1038/srep07751
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
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291–294. https://doi.org/10.1093/molbev/msz189
Deng C, Cheng C-HC, Ye H, He X, Chen L (2010) Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proc Natl Acad Sci 107:21593–21598. https://doi.org/10.1073/pnas.1007883107
Ding ZJ, Yan JY, Xu XY, Yu DQ, Li GX, Zhang SQ, Zheng SJ (2014) Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79:13–27. https://doi.org/10.1111/tpj.12538
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. https://doi.org/10.1093/bioinformatics/bts635
Donoghue MTA, Keshavaiah C, Swamidatta SH, Spillane C (2011) Evolutionary origins of Brassicaceae specific genes in Arabidopsis thaliana. BMC Evol Biol 11:47. https://doi.org/10.1186/1471-2148-11-47
Emami H, Kempken F (2019) PRECOCIOUS1 (POCO1), a mitochondrial pentatricopeptide repeat protein affects flowering time in Arabidopsis thaliana. Plant J 100:265–278. https://doi.org/10.1111/tpj.14441
Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, Kahles A, Bohnert R, Jean G, Derwent P, Kersey P, Belfield EJ, Harberd NP, Kemen E, Toomajian C, Kover PX, Clark RM, Rätsch G, Mott R (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477:419–423. https://doi.org/10.1038/nature10414
Gu X, Le C, Wang Y, Li Z, Jiang D, Wang Y, He Y (2013) Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat Commun 4:1947. https://doi.org/10.1038/ncomms2947
Hanada K, Zhang X, Borevitz JO, Li WH, Shiu SH (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. https://doi.org/10.1101/gr.5836207
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
Ihaka R, Gentleman R (1996) R: A language for data analysis and graphics. J Comput Graph Stat 5:299–314. https://doi.org/10.1080/10618600.1996.10474713
Ito E, Ebine K, Choi S, Ichinose S, Uemura T, Nakano A, Ueda T (2018) Integration of two RAB5 groups during endosomal transport in plants. Elife 7:e34064. https://doi.org/10.7554/eLife.34064
Jing Y, Shi L, Li X, Zheng H, Gao J, Wang M, He L, Zhang W (2019) OXS2 is required for salt tolerance mainly through associating with salt inducible genes, CA1 and Araport11, in Arabidopsis. Sci Rep 9:20341. https://doi.org/10.1038/s41598-019-56456-1
Kazan K, Lyons R (2016) The link between flowering time and stress tolerance. J Exp Bot 67:47–60. https://doi.org/10.1093/jxb/erv441
Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Kumar A, Gates PB, Czarkwiani A, Brockes JP (2015) An orphan gene is necessary for preaxial digit formation during salamander limb development. Nat Commun 6:8684. https://doi.org/10.1038/ncomms9684
Li C-Y, Zhang Y, Wang Z, Zhang Y, Cao C, Zhang P-W, Lu S-J, Li X-M, Yu Q, Zheng X, Du Q, Uhl GR, Liu Q-R, Wei L (2010) A human-specific de novo protein-coding gene associated with human brain functions. PLoS Comput Biol 6:e1000734. https://doi.org/10.1371/journal.pcbi.1000734
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. https://doi.org/10.1093/bioinformatics/btt656
Liberatore KL, Dukowic-Schulze S, Miller ME, Chen C, Kianian SF (2016) The role of mitochondria in plant development and stress tolerance. Free Radic Biol Med 100:238–256. https://doi.org/10.1016/j.freeradbiomed.2016.03.033
Lin X, Kaul S, Rounsley S, Shea TP, Benito M-I, Town CD, Fujii CY, Mason T, Bowman CL, Barnstead M, Feldblyum TV, Buell CR, Ketchum KA, Lee J, Ronning CM, Koo HL, Moffat KS, Cronin LA, Shen M, Pai G, Van Aken S, Umayam L, Tallon LJ, Gill JE, Adams MD, Carrera AJ, Creasy TH, Goodman HM, Somerville CR, Copenhaver GP, Preuss D, Nierman WC, White O, Eisen JA, Salzberg SL, Fraser CM, Venter JC (1999) Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402:761–768. https://doi.org/10.1038/45471
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
McLysaght A, Guerzoni D (2015) New genes from non-coding sequence: the role of de novo protein-coding genes in eukaryotic evolutionary innovation. Philos Trans R Soc B Biol Sci 370:20140332. https://doi.org/10.1098/rstb.2014.0332
Mileshina D, Niazi AK, Weber-Lotfi F, Gualberto J, Dietrich A (2015) Mitochondrial genetic manipulation
Mouille G, Witucka-Wall H, Bruyant M-P, Loudet O, Pelletier S, Rihouey C, Lerouxel O, Lerouge P, Höfte H, Pauly M (2006) Quantitative trait loci analysis of primary cell wall composition in arabidopsis. Plant Physiol 141:1035–1044. https://doi.org/10.1104/pp.106.079384
Nagai K, Mori Y, Ishikawa S, Furuta T, Gamuyao R, Niimi Y, Hobo T, Fukuda M, Kojima M, Takebayashi Y, Fukushima A, Himuro Y, Kobayashi M, Ackley W, Hisano H, Sato K, Yoshida A, Wu J, Sakakibara H, Sato Y, Tsuji H, Akagi T, Ashikari M (2020) Antagonistic regulation of the gibberellic acid response during stem growth in rice. Nature 584:109–114. https://doi.org/10.1038/s41586-020-2501-8
Naito Y, Yoshimura J, Morishita S, Ui-Tei K (2009) siDirect 2.0: updated software for designing functional siRNA with reduced seed-dependent off-target effect. BMC Bioinformatics 10:392. https://doi.org/10.1186/1471-2105-10-392
Noutsos C, Kleine T, Armbruster U, DalCorso G, Leister D (2007) Nuclear insertions of organellar DNA can create novel patches of functional exon sequences. Trends Genet 23:597–601. https://doi.org/10.1016/j.tig.2007.08.016
O’Conner S, Li L (2020) Mitochondrial fostering: the mitochondrial genome may play a role in plant orphan gene evolution. Front Plant Sci 11:1855
Ogasawara Y, Ishizaki K, Kohchi T, Kodama Y (2013) Cold-induced organelle relocation in the liverwort Marchantia polymorpha L. Plant Cell Environ 36:1520–1528. https://doi.org/10.1111/pce.12085
Osaki Y, Kodama Y (2017) Particle bombardment and subcellular protein localization analysis in the aquatic plant Egeria densa. PeerJ 5:e3779. https://doi.org/10.7717/peerj.3779
Qi M, Zheng W, Zhao X, Hohenstein JD, Kandel Y, O’Conner S, Wang Y, Du C, Nettleton D, MacIntosh GC, Tylka GL, Wurtele ES, Whitham SA, Li L (2019) QQS orphan gene and its interactor NF-YC4 reduce susceptibility to pathogens and pests. Plant Biotechnol J 17:252–263. https://doi.org/10.1111/pbi.12961
Ren H, Wu X, Zhao W, Wang Y, Sun D, Gao K, Tang W (2022) Heat shock-induced accumulation of the glycogen synthase kinase 3-like kinase BRASSINOSTEROID INSENSITIVE 2 promotes early flowering but reduces thermotolerance in arabidopsis. Front Plant Sci. https://doi.org/10.3389/fpls.2022.838062
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47–e47. https://doi.org/10.1093/nar/gkv007
Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, Alix A, McCosh RB, Chen H, Schork NJ, Ecker JR (2013) Patterns of population epigenomic diversity. Nature 495:193–198. https://doi.org/10.1038/nature11968
Sheldon CC, Finnegan EJ, Rouse DT, Tadege M, Bagnall DJ, Helliwell CA, Peacock WJ, Dennis ES (2000) The control of flowering by vernalization. Curr Opin Plant Biol 3:418–422. https://doi.org/10.1016/S1369-5266(00)00106-0
Shirai K, Matsuda F, Nakabayashi R, Okamoto M, Tanaka M, Fujimoto A, Shimizu M, Shinozaki K, Seki M, Saito K, Hanada K (2017) A highly specific genome-wide association study integrated with transcriptome data reveals the contribution of copy number variations to specialized metabolites in arabidopsis thaliana accessions. Mol Biol Evol 34:3111–3122. https://doi.org/10.1093/molbev/msx234
Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LEV, Loudet O, Colot V, Vincentz M (2013) Extensive natural epigenetic variation at a De Novo originated gene. PLOS Genet 9:e1003437
Storey JD, Taylor JE, Siegmund D (2004) Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach. J Royal Sta Soc B 66:187–205. https://doi.org/10.1111/j.1467-9868.2004.00439.x
Takeno K (2016) Stress-induced flowering: the third category of flowering response. J Exp Bot 67:4925–4934. https://doi.org/10.1093/jxb/erw272
Tautz D, Domazet-Lošo T (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12:692–702. https://doi.org/10.1038/nrg3053
Ushijima T, Hanada K, Gotoh E, Yamori W, Kodama Y, Tanaka H, Kusano M, Fukushima A, Tokizawa M, Yamamoto YY, Tada Y, Suzuki Y, Matsushita T (2017) Light controls protein localization through phytochrome-mediated alternative promoter selection. Cell 171:1316-132515.e12. https://doi.org/10.1016/j.cell.2017.10.018
Whittaker C, Dean C (2017) The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu Rev Cell Dev Biol 33:555–575. https://doi.org/10.1146/annurev-cellbio-100616-060546
Wynn EL, Christensen AC (2019) Repeats of unusual size in plant mitochondrial genomes identification, incidence and evolution. G3 Genes|genomes|genetics 9:549–559. https://doi.org/10.1534/g3.118.200948
Xiao W, Liu H, Li Y, Li X, Xu C, Long M, Wang S (2009) A rice gene of De Novo origin negatively regulates pathogen-induced defense response. PLoS ONE 4:e4603
Yu C-W, Chang K-Y, Wu K (2016) Genome-wide analysis of gene regulatory networks of the FVE-HDA6-FLD complex in arabidopsis. Front Plant Sci 7:555. https://doi.org/10.3389/fpls.2016.00555
Zhang L, Ren Y, Yang T, Li G, Chen J, Gschwend AR, Yu Y, Hou G, Zi J, Zhou R, Wen B, Zhang J, Chougule K, Wang M, Copetti D, Peng Z, Zhang C, Zhang Y, Ouyang Y, Wing RA, Liu S, Long M (2019) Rapid evolution of protein diversity by de novo origination in Oryza. Nat Ecol Evol 3:679–690. https://doi.org/10.1038/s41559-019-0822-5
Zhao L, Saelao P, Jones CD, Begun DJ (2014) Origin and spread of de Novo genes in drosophila melanogaster populations. Science 80(343):769–772. https://doi.org/10.1126/science.1248286
Zhao N, Wang Y, Hua J (2018) The roles of mitochondrion in intergenomic gene transfer in plants: a source and a pool. Int J Mol Sci. https://doi.org/10.3390/ijms19020547
Acknowledgements
This study was supported by Grants-in-Aid for Scientific Research and the Asahi Glass Foundation. We thank the National Institute of Genetics of the Research Organization of Information and Systems for providing excellent supercomputer services. We also thank Edanz ( https://jp.edanz.com/ac) for editing a draft of this manuscript.
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This study was supported by JSPS KAKENHI (JP22H02675 to K.H, JP20H03317 to K.H., JP18H02420 to K.H., JP22K14870 to K.S.), MEXT KAKENHI (JP21H05724 to K.H., JP20H05905 to K.H. JP20H05906 to K.H., JP22H05731 to K.S.), and the Asahi Glass" Foundation (to K.H.).).
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TT, KS, and KH. conceived the project; TT, Y-WK, MH-T, TK, TU, MS, and TM performed the experiments; TT and KS conducted the bioinformatics analysis; TT and KH wrote the article.
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Takeda, T., Shirai, K., Kim, Yw. et al. A de novo gene originating from the mitochondria controls floral transition in Arabidopsis thaliana. Plant Mol Biol 111, 189–203 (2023). https://doi.org/10.1007/s11103-022-01320-6
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DOI: https://doi.org/10.1007/s11103-022-01320-6