Phosphate deficiency alters transcript isoforms via alternative transcription start sites.
ECT4
noncoding RNA
phosphate deficiency
transcription start sites
upstream open reading frame
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
20 Aug 2024
20 Aug 2024
Historique:
revised:
24
05
2024
received:
13
11
2023
accepted:
13
07
2024
medline:
21
8
2024
pubmed:
21
8
2024
entrez:
21
8
2024
Statut:
aheadofprint
Résumé
Alternative transcription start sites (TSS) are widespread in eukaryotes and can alter the 5' UTR length and coding potential of transcripts. Here we show that inorganic phosphate (Pi) availability regulates the usage of several alternative TSS in Arabidopsis (Arabidopsis thaliana). In comparison to phytohormone treatment, Pi had a pronounced and specific effect on the usage of many alternative TSS. By combining short-read RNA sequencing with long-read sequencing of full-length mRNAs, we identified a set of 45 genes showing alternative TSS under Pi deficiency. Alternative TSS affected several processes, such as translation via the exclusion of upstream open reading frames present in the 5' UTR of RETICULAN LIKE PROTEIN B1 mRNA, and subcellular localization via removal of the plastid transit peptide coding region from the mRNAs of HEME OXYGENASE 1 and SULFOQUINOVOSYLDIACYLGLYCEROL 2. Several alternative TSS also generated shorter transcripts lacking the coding potential for important domains. For example, the EVOLUTIONARILY CONSERVED C-TERMINAL REGION 4 (ECT4) locus, which encodes an N
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : CRSII3_154471
Informations de copyright
© 2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Abel, S. (2017) Phosphate scouting by root tips. Current Opinion in Plant Biology, 39, 168–177.
Almagro Armenteros, J.J., Salvatore, M., Emanuelsson, O., Winther, O., von Heijne, G., Elofsson, A. et al. (2019) Detecting sequence signals in targeting peptides using deep learning. Life Science Alliance, 2, e201900429.
Arribas‐Hernández, L., Bressendorff, S., Hansen, M.H., Poulsen, C., Erdmann, S. & Brodersen, P. (2018) An m6A‐YTH module controls developmental timing and morphogenesis in Arabidopsis. The Plant Cell, 30(5), 952–967.
Arribas‐Hernández, L., Rennie, S., Schon, M., Porcelli, C., Enugutti, B., Andersson, R. et al. (2021) The YTHDF proteins ECT2 and ECT3 bind largely overlapping target sets and influence target mRNA abundance, not alternative polyadenylation. eLife, 10, e72377.
Arribas‐Hernández, L., Simonini, S., Hansen, M.H., Botterweg Paredes, E., Bressendorff, S., Dong, Y. et al. (2020) Recurrent requirement for the m6A‐ECT2/ECT3/ECT4 axis in the control of cell proliferation during plant organogenesis. Development, 147, dev189134.
Balzergue, C., Dartevelle, T., Godon, C., Laugier, E., Meisrimler, C., Teulon, J.‐M. et al. (2017) Low phosphate activates STOP1‐ALMT1 to rapidly inhibit root cell elongation. Nature Communications, 8, 15300.
Bazin, J., Baerenfaller, K., Gosai, S.J., Gregory, B.D., Crespi, M. & Bailey‐Serres, J. (2017) Global analysis of ribosome‐associated noncoding RNAs unveils new modes of translational regulation. Proceedings of the National Academy of Sciences of the United States of America, 114, E10018–E10027.
Cartolano, M., Huettel, B., Hartwig, B., Reinhardt, R. & Schneeberger, K. (2016) cDNA library enrichment of full length transcripts for SMRT long read sequencing. PLoS One, 11, 1–10.
Cheng, C., Krishnakumar, V., Chan, A.P., Thibaud‐Nissen, F., Schobel, S. & Town, C.D. (2017) Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. The Plant Journal, 89, 789–804.
Cruz‐Ramírez, A., Oropeza‐Aburto, A., Razo‐Hernández, F., Ramírez‐Chávez, E. & Herrera‐Estrella, L. (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proceedings of the National Academy of Sciences of the United States of America, 103, 6765–6770.
Curtis, M.D. & Grossniklaus, U. (2003) A gateway cloning vector set for high‐throughput functional analysis of genes in plants. Plant Physiology, 133, 462–469.
Davis, S.J., Kurepa, J. & Vierstra, R.D. (1999) The Arabidopsis thaliana HY1 locus, required for phytochrome‐chromophore biosynthesis, encodes a protein related to heme oxygenases. Proceedings of the National Academy of Sciences of the United States of America, 96, 6541–6546.
de Klerk, E. & 't Hoen, P.A. (2015) Alternative mRNA transcription, processing, and translation: insights from RNA sequencing. Trends in Genetics, 31, 128–139.
Deforges, J., Reis, R.S., Jacquet, P., Sheppard, S., Gadekar, V.P., Hart‐Smith, G. et al. (2019) Control of cognate sense mRNA translation by cis‐natural antisense RNAs. Plant Physiology, 180, 305–322.
Deforges, J., Reis, R.S., Jacquet, P., Vuarambon, D.J. & Poirier, Y. (2019) Prediction of regulatory long intergenic non‐coding RNAs acting in trans through base‐pairing interactions. BMC Genomics, 20, 601.
Dong, C., He, F., Berkowitz, O., Liu, J., Cao, P., Tang, M. et al. (2018) Alternative splicing plays a critical role in maintaining mineral nutrient homeostasis in rice (Oryza sativa). Plant Cell, 30, 2267–2285.
Ebina, I., Takemoto‐Tsutsumi, M., Watanabe, S., Koyama, H., Endo, Y., Kimata, K. et al. (2015) Identification of novel Arabidopsis thaliana upstream open reading frames that control expression of the main coding sequences in a peptide sequence‐dependent manner. Nucleic Acids Research, 43, 1562–1576.
Emborg, T.J., Walker, J.M., Noh, B. & Vierstra, R.D. (2006) Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiology, 140, 856–868.
Essigmann, B., Güler, S., Narang, R.A., Linke, D. & Benning, C. (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 95, 1950–1955.
Forrest, A.R.R., Kawaji, H., Rehli, M., Baillie, J.K., De Hoon, M.J.L., Haberle, V. et al. (2014) A promoter‐level mammalian expression atlas. Nature, 507, 462–470.
Franco‐Zorrilla, J.M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio‐Somoza, I. et al. (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics, 39, 1033–1037.
Guo, M., Zhang, Y., Jia, X., Wang, X., Zhang, Y., Liu, J. et al. (2022) Alternative splicing of REGULATOR OF LEAF INCLINATION 1 modulates phosphate starvation signaling and growth in plants. The Plant Cell, 34, 3319–3338.
Gutiérrez‐Alanís, D., Ojeda‐Rivera, J.O., Yong‐Villalobos, L., Cárdenas‐Torres, L. & Herrera‐Estrella, L. (2018) Adaptation to phosphate scarcity: tips from Arabidopsis roots. Trends in Plant Science, 23, 721–730.
Ham, B.‐K., Chen, J., Yan, Y. & Lucas, W.J. (2018) Insights into plant phosphate sensing and signaling. Current Opinion in Biotechnology, 49, 1–9.
Hartley, S.W. & Mullikin, J.C. (2016) Detection and visualization of differential splicing in RNA‐Seq data with JunctionSeq. Nucleic Acids Research, 44, e127.
Hsieh, L.‐C., Lin, S.‐I., Kuo, H.‐F. & Chiou, T.‐J. (2010) Abundance of tRNA‐derived small RNAs in phosphate‐starved Arabidopsis roots. Plant Signaling & Behavior, 5, 537–539.
Jones, P., Binns, D., Chang, H.‐Y., Fraser, M., Li, W., McAnulla, C. et al. (2014) InterProScan 5: genome‐scale protein function classification. Bioinformatics, 30, 1236–1240.
Jung, J.Y., Ried, M.K., Hothorn, M. & Poirier, Y. (2018) Control of plant phosphate homeostasis by inositol pyrophosphates and the SPX domain. Current Opinion in Biotechnology, 49, 156–162.
Kindgren, P., Ard, R., Ivanov, M. & Marquardt, S. (2018) Transcriptional read‐through of the long non‐coding RNA SVALKA governs plant cold acclimation. Nature Communications, 9, 4561.
Knox, K., Wang, P., Kriechbaumer, V., Tilsner, J., Frigerio, L., Sparkes, I. et al. (2015) Putting the squeeze on plasmodesmata: a role for reticulons in primary plasmodesmata formation. Plant Physiology, 168, 1563–1572.
Kurihara, Y., Makita, Y., Kawashima, M., Fujita, T., Iwasaki, S. & Matsui, M. (2018) Transcripts from downstream alternative transcription start sites evade uORF‐mediated inhibition of gene expression in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 115, 7831–7836.
Lagarde, D., Basset, M., Lepetit, M., Conejero, G., Gaymard, F., Astruc, S. et al. (1996) Tissue‐specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. The Plant Journal, 9, 195–203.
Lee, H.Y., Bowen, C.H., Popescu, G.V., Kang, H.G., Kato, N., Ma, S. et al. (2011) Arabidopsis RTNLB1 and RTNLB2 reticulon‐like proteins regulate intracellular trafficking and activity of the FLS2 immune receptor. Plant Cell, 23, 3374–3391.
Li, D., Zhang, H., Hong, Y., Huang, L., Li, X., Zhang, Y. et al. (2014) Genome‐wide identification, biochemical characterization, and expression analyses of the YTH domain‐containing RNA‐binding protein family in Arabidopsis and Rice. Plant Molecular Biology Reporter, 32, 1169–1186.
Li, W., Lin, W.‐D., Ray, P., Lan, P. & Schmidt, W. (2013) Genome‐wide detection of condition‐sensitive alternative splicing in Arabidopsis roots. Plant Physiology, 162, 1750–1763.
Mahawar, L. & Shekhawat, G.S. (2018) Haem oxygenase: a functionally diverse enzyme of photosynthetic organisms and its role in phytochrome chromophore biosynthesis, cellular signalling and defence mechanisms. Plant, Cell & Environment, 41, 483–500.
Misson, J., Raghothama, K.G., Jain, A., Jouhet, J., Block, M.A., Bligny, R. et al. (2005) A genome‐wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proceedings of the National Academy of Sciences of the United States of America, 102, 11934–11939.
Mora‐Macías, J., Ojeda‐Rivera, J.O., Gutiérrez‐Alanís, D., Yong‐Villalobos, L., Oropeza‐Aburto, A., Raya‐González, J. et al. (2017) Malate‐dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proceedings of the National Academy of Sciences of the United States of America, 114, E3563–E3572. Available from: https://doi.org/10.1073/pnas.1701952114
Müller, J., Toev, T., Heisters, M., Teller, J., Moore, K.L., Hause, G. et al. (2015) Iron‐dependent callose deposition adjusts root meristem maintenance to phosphate availability. Developmental Cell, 33, 216–230.
Naumann, C., Müller, J., Sakhonwasee, S., Wieghaus, A., Hause, G., Heisters, M. et al. (2019) The local phosphate deficiency response activates endoplasmic reticulum stress‐dependent autophagy. Plant Physiology, 179, 460–476.
Nielsen, M., Ard, R., Leng, X., Ivanov, M., Kindgren, P., Pelechano, V. et al. (2019) Transcription‐driven chromatin repression of intragenic transcription start sites. PLoS Genetics, 15, e1007969.
Nziengui, H., Bouhidel, K., Pillon, D., Der, C., Marty, F. & Schoefs, B. (2007) Reticulon‐like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Letters, 581, 3356–3362.
Péret, B., Clément, M., Nussaume, L. & Desnos, T. (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends in Plant Science, 16, 442–450.
Poirier, Y., Jaskolowski, A. & Clúa, J. (2022) Phosphate acquisition and metabolism in plants. Current Biology, 32, R623–R629.
Prall, W., Ganguly, D.R. & Gregory, B.D. (2023) The covalent nucleotide modifications within plant mRNAs: what we know, how we find them, and what should be done in the future. The Plant Cell, 35, 1801–1816.
Reis, R.S., Deforges, J., Sokoloff, T. & Poirier, Y. (2020) Modulation of shoot phosphate level and growth by PHOSPHATE1 upstream open reading frame. Plant Physiology, 183, 1145–1156.
Reyes, A. & Huber, W. (2018) Alternative start and termination sites of transcription drive most transcript isoform differences across human tissues. Nucleic Acids Research, 46, 582–592.
Roy, E.D., Richards, P.D., Martinelli, L.A., Coletta, L.D., Lins, S.R.M., Vazquez, F.F. et al. (2016) The phosphorus cost of agricultural intensification in the tropics. Nature Plants, 2, 16043.
Sattari, S.Z., Bouwman, A.F., Martinez Rodríguez, R., Beusen, A.H.W. & van Ittersum, M.K. (2016) Negative global phosphorus budgets challenge sustainable intensification of grasslands. Nature Communications, 7, 10696.
Shao, Y., Wong, C.E., Shen, L. & Yu, H. (2021) N6‐methyladenosine modification underlies messenger RNA metabolism and plant development. Current Opinion in Plant Biology, 63, 102047.
Shekhawat, G.S. & Verma, K. (2010) Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. Journal of Experimental Botany, 61, 2255–2270.
Sherman, B.T., Hao, M., Qiu, J., Jiao, X., Baseler, M.W., Lane, H.C. et al. (2022) DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Research, 50, W216–W221.
Song, P., Wei, L., Chen, Z., Cai, Z., Lu, Q., Wang, C. et al. (2023) m6A readers ECT2/ECT3/ECT4 enhance mRNA stability through direct recruitment of the poly(A) binding proteins in Arabidopsis. Genome Biology, 24, 103.
Srivastava, A.K., Lu, Y., Zinta, G., Lang, Z. & Zhu, J.K. (2018) UTR‐dependent control of gene expression in plants. Trends in Plant Science, 23, 248–259.
Tarkowski, Ł.P., Signorelli, S., Considine, M.J. & Montrichard, F. (2023) Integration of reactive oxygen species and nutrient signalling to shape root system architecture. Plant, Cell & Environment, 46, 379–390.
Teufel, F., Almagro Armenteros, J.J., Johansen, A.R., Gíslason, M.H., Pihl, S.I., Tsirigos, K.D. et al. (2022) SignalP 6.0 predicts all five types of signal peptides using protein language models. Nature Biotechnology, 40, 1023–1025.
Thieffry, A., López‐Márquez, D., Bornholdt, J., Malekroudi, M.G., Bressendorff, S., Barghetti, A. et al. (2022) PAMP‐triggered genetic reprogramming involves widespread alternative transcription initiation and an immediate transcription factor wave. The Plant Cell, 34, 2615–2637.
Tian, P., Lin, Z., Lin, D., Dong, S., Huang, J. & Huang, T. (2021) The pattern of DNA methylation alteration, and its association with the changes of gene expression and alternative splicing during phosphate starvation in tomato. The Plant Journal, 108, 841–858.
Ursache, R., Andersen, T.G., Marhavý, P. & Geldner, N. (2018) A protocol for combining fluorescent proteins with histological stains for diverse cell wall components. The Plant Journal, 93, 399–412.
Ushijima, T., Hanada, K., Gotoh, E., Yamori, W., Kodama, Y., Tanaka, H. et al. (2017) Light controls protein localization through phytochrome‐mediated alternative promoter selection. Cell, 171, 1–10.
Wang, K., Wang, D., Zheng, X., Qin, A., Zhou, J., Guo, B. et al. (2019) Multi‐strategic RNA‐seq analysis reveals a high‐resolution transcriptional landscape in cotton. Nature Communications, 10, 4714.
Wu, H.‐Y.L., Ai, Q., Teixeira, R.T., Nguyen, P.H.T., Song, G., Montes, C. et al. (2024) Improved super‐resolution ribosome profiling reveals prevalent translation of upstream ORFs and small ORFs in Arabidopsis. The Plant Cell, 36, 510–539.
Yoo, S.‐D., Cho, Y.‐H. & Sheen, J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols, 2, 1565–1572.
Yu, B., Xu, C. & Benning, C. (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate‐limited growth. Proceedings of the National Academy of Sciences of the United States of America, 99, 5732–5737.
Zhan, X., Shen, Q., Chen, J., Yang, P., Wang, X. & Hong, Y. (2019) Rice sulfoquinovosyltransferase SQD2.1 mediates flavonoid glycosylation and enhances tolerance to osmotic stress. Plant, Cell & Environment, 42, 2215–2230.
Zhan, X., Shen, Q., Wang, X. & Hong, Y. (2017) The sulfoquinovosyltransferase‐like enzyme SQD2.2 is involved in flavonoid glycosylation, regulating sugar metabolism and seed setting in rice. Scientific Reports, 7, 4685.
Zhang, R., Kuo, R., Coulter, M., Calixto, C.P.G., Entizne, J.C., Guo, W. et al. (2022) A high‐resolution single‐molecule sequencing‐based Arabidopsis transcriptome using novel methods of iso‐seq analysis. Genome Biology, 23, 149.
Zhang, X., Ding, X., Marshall, R.S., Paez‐Valencia, J., Lacey, P., Vierstra, R.D. et al. (2020) Reticulon proteins modulate autophagy of the endoplasmic reticulum in maize endosperm. eLife, 9, e51918.
Zhang, Z., Liao, H. & Lucas, W.J. (2014) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. Journal of Integrative Plant Biology, 56, 192–220.