The polyadenylation factor FIP1 is important for plant development and root responses to abiotic stresses.
5' Untranslated Regions
Abscisic Acid
/ metabolism
Alleles
Arabidopsis
/ drug effects
Arabidopsis Proteins
/ genetics
Cadmium
/ toxicity
Cell Division
/ genetics
Gene Expression Regulation, Plant
/ genetics
Mutation
Phenotype
Plant Roots
/ cytology
Polyadenylation
/ drug effects
Protein Biosynthesis
/ genetics
RNA, Messenger
/ genetics
Salt Stress
/ genetics
mRNA Cleavage and Polyadenylation Factors
/ genetics
Arabidopsis
FIP1
alternative polyadenylation
root development
stem cell maintenance
stress responses
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:
09 2019
09 2019
Historique:
received:
26
03
2019
revised:
03
05
2019
accepted:
14
05
2019
pubmed:
22
5
2019
medline:
2
7
2020
entrez:
22
5
2019
Statut:
ppublish
Résumé
Root development and its response to environmental changes is crucial for whole plant adaptation. These responses include changes in transcript levels. Here, we show that the alternative polyadenylation (APA) of mRNA is important for root development and responses. Mutations in FIP1, a component of polyadenylation machinery, affects plant development, cell division and elongation, and response to different abiotic stresses. Salt treatment increases the amount of poly(A) site usage within the coding region and 5' untranslated regions (5'-UTRs), and the lack of FIP1 activity reduces the poly(A) site usage within these non-canonical sites. Gene ontology analyses of transcripts displaying APA in response to salt show an enrichment in ABA signaling, and in the response to stresses such as salt or cadmium (Cd), among others. Root growth assays show that fip1-2 is more tolerant to salt but is hypersensitive to ABA or Cd. Our data indicate that FIP1-mediated alternative polyadenylation is important for plant development and stress responses.
Substances chimiques
5' Untranslated Regions
0
Arabidopsis Proteins
0
Fip1 protein, Arabidopsis
0
RNA, Messenger
0
mRNA Cleavage and Polyadenylation Factors
0
Cadmium
00BH33GNGH
Abscisic Acid
72S9A8J5GW
Banques de données
GENBANK
['GSE127972']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1203-1219Subventions
Organisme : Howard Hughes Medical Institute
Pays : United States
Informations de copyright
© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.
Références
Addepalli, B. and Hunt, A.G. (2007) A novel endonuclease activity associated with the Arabidopsis ortholog of the 30-kDa subunit of cleavage and polyadenylation specificity factor. Nucleic Acids Res. 35, 4453-4463.
Akman, H.B. and Erson-Bensan, A.E. (2014) Alternative polyadenylation and its impact on cellular processes. Microrna, 3, 2-9.
Anders, S., Reyes, A. and Huber, W. (2012) Detecting differential usage of exons from RNA-seq data. Genome Res. 22, 2008-2017.
Barberon, M., Vermeer, J.E., De Bellis, D. et al. (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell, 164, 447-459.
Blazie, S.M., Geissel, H.C., Wilky, H., Joshi, R., Newbern, J. and Mangone, M. (2017) Alternative polyadenylation directs tissue-specific miRNA targeting in Caenorhabditis elegans somatic tissues. Genetics, 206, 757-774.
Brady, S.M., Orlando, D.A., Lee, J.Y., Wang, J.Y., Koch, J., Dinneny, J.R., Mace, D., Ohler, U. and Benfey, P.N. (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science, 318, 801-806.
Brady, S.M., Zhang, L., Megraw, M. et al. (2011) A stele-enriched gene regulatory network in the Arabidopsis root. Mol. Syst. Biol. 7, 459.
Browning, K.S. and Bailey-Serres, J. (2015) Mechanism of cytoplasmic mRNA translation. Arabidopsis Book, 13, e0176.
Bruno, L., Pacenza, M., Forgione, I., Lamerton, L.R., Greco, M., Chiappetta, A. and Bitonti, M.B. (2017) In Arabidopsis thaliana cadmium impact on the growth of primary root by altering SCR expression and auxin-cytokinin cross-talk. Front. Plant Sci. 8, 1323.
Byrne, M.E. (2009) A role for the ribosome in development. Trends Plant Sci. 14, 512-519.
Byrt, C.S., Munns, R., Burton, R.A., Gilliham, M. and Wege, S. (2018) Root cell wall solutions for crop plants in saline soils. Plant Sci. 269, 47-55.
Chen, M. and Manley, J.L. (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol. 10, 741-754.
Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
De Lorenzo, L., Sorenson, R., Bailey-Serres, J. and Hunt, A.G. (2017) Noncanonical alternative polyadenylation contributes to gene regulation in response to hypoxia. Plant Cell, 29, 1262-1277.
De Smet, I., Signora, L., Beeckman, T., Inze, D., Foyer, C.H. and Zhang, H. (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 33, 543-555.
Deng, X. and Cao, X. (2017) Roles of pre-mRNA splicing and polyadenylation in plant development. Curr. Opin. Plant Biol. 35, 45-53.
Di Giammartino, D.C., Nishida, K. and Manley, J.L. (2011) Mechanisms and consequences of alternative polyadenylation. Mol. Cell, 43, 853-866.
Ding, L., Cao, J., Duan, Y., Li, J., Yang, Y., Yang, G. and Zhou, Y. (2016) Proteomic and physiological responses of Arabidopsis thaliana exposed to salinity stress and N-acyl-homoserine lactone. Physiol. Plant. 158, 414-434.
Dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, D., Pointer, S., Barron, C., Brady, S.M., Schiefelbein, J. and Benfey, P.N. (2008) Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science, 320, 942-945.
Forbes, K.P., Addepalli, B. and Hunt, A.G. (2005) An Arabidopsis Fip1 homologue interacts with RNA and provides conceptual links with a number of other polyadenylation factor subunits. J. Biol. Chem.
Forbes, K.P., Addepalli, B. and Hunt, A.G. (2006) An Arabidopsis Fip1 homolog interacts with RNA and provides conceptual links with a number of other polyadenylation factor subunits. J. Biol. Chem. 281, 176-186.
Forzani, C., Aichinger, E., Sornay, E., Willemsen, V., Laux, T., Dewitte, W. and Murray, J.A. (2014) WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche. Curr. Biol. 24, 1939-1944.
Franco-Zorrilla, J.M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio-Somoza, I., Leyva, A., Weigel, D., Garcia, J.A. and Paz-Ares, J. (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39, 1033-1037.
Fu, H., Yang, D., Su, W., Ma, L., Shen, Y., Ji, G., Ye, X., Wu, X. and Li, Q.Q. (2016) Genome-wide dynamics of alternative polyadenylation in rice. Genome Res. 26, 1753-1760.
Greb, T. and Lohmann, Jan U. (2016) Plant stem cells. Curr. Biol. 26, R816-R821.
Guo, M., Gao, W., Li, L., Li, H., Xu, Y. and Zhou, C. (2014) Proteomic and phosphoproteomic analyses of NaCl stress-responsive proteins in Arabidopsis roots. J. Plant Interact. 9, 396-401.
Guo, C., Spinelli, M., Liu, M., Li, Q.Q. and Liang, C. (2016) A genome-wide study of “non-3UTR” polyadenylation sites in Arabidopsis thaliana. Sci. Rep. 6, 28060.
Helmling, S., Zhelkovsky, A. and Moore, C.L. (2001) Fip1 regulates the activity of Poly(A) polymerase through multiple interactions. Mol. Cell. Biol. 21, 2026-2037.
Hildebrandt, T.M., Nunes Nesi, A., Araújo, W.L. and Braun, H.-P. (2015) Amino acid catabolism in plants. Mol. Plant, 8, 1563-1579.
Hong, L., Ye, C., Lin, J., Fu, H., Wu, X. and Li, Q.Q. (2018) Alternative polyadenylation is involved in auxin-based plant growth and development. Plant J. 93, 246-258.
Hunt, A., Xu, R., Addepalli, B. et al. (2008) Arabidopsis mRNA polyadenylation machinery: comprehensive analysis of protein-protein interactions and gene expression profiling. BMC Genomics, 9, 220.
Hunt, A.G., Xing, D. and Li, Q.Q. (2012) Plant polyadenylation factors: conservation and variety in the polyadenylation complex in plants. BMC Genomics, 13, 641.
Jurado, S., Abraham, Z., Manzano, C., Lopez-Torrejon, G., Pacios, L.F. and Del Pozo, J.C. (2010) The Arabidopsis cell cycle F-box protein SKP2A binds to auxin. Plant Cell, https://doi.org/10.1105/tpc.110.078972.
Kaufmann, I., Martin, G., Friedlein, A., Langen, H. and Keller, W. (2004) Human Fip1 is a subunit of CPSF that binds to U-rich RNA elements and stimulates poly(A) polymerase. EMBO J. 23, 616-626.
Kiegle, E.A., Garden, A., Lacchini, E. and Kater, M.M. (2018) A genomic view of alternative splicing of long non-coding RNAs during rice seed development reveals extensive splicing and lncRNA gene families. Front. Plant Sci. 9, 115.
de Klerk, E. and t Hoen, P.A. (2015) Alternative mRNA transcription, processing, and translation: insights from RNA sequencing. Trends Genet. 31, 128-139.
Kumar, D., Hazra, S., Datta, R. and Chattopadhyay, S. (2016) Transcriptome analysis of Arabidopsis mutants suggests a crosstalk between ABA, ethylene and GSH against combined cold and osmotic stress. Sci. Rep. 6, 36867.
Lackford, B., Yao, C., Charles, G.M. et al. (2014) Fip1 regulates mRNA alternative polyadenylation to promote stem cell self-renewal. EMBO J. 33, 878-889.
Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouze, P. and Rombauts, S. (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30, 325-327.
Lewis, D.R., Olex, A.L., Lundy, S.R., Turkett, W.H., Fetrow, J.S. and Muday, G.K. (2013) A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell, 25, 3329-3346.
Li, J.Y., Fu, Y.L., Pike, S.M. et al. (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell, 22, 1633-1646.
Li, Q., Liu, J., Tan, D., Allan, A.C., Jiang, Y., Xu, X., Han, Z. and Kong, J. (2013) A genome-wide expression profile of salt-responsive genes in the apple rootstock Malus zumi. Int. J. Mol. Sci. 14, 21053-21070.
Li, W., You, B., Hoque, M. et al. (2015) Systematic profiling of poly(A) +transcripts modulated by core 3′ end processing and splicing factors reveals regulatory rules of alternative cleavage and polyadenylation. PLoS Genet. 11, e1005166.
Li, S., Yamada, M., Han, X., Ohler, U. and Benfey, P.N. (2016) High-resolution expression map of the arabidopsis root reveals alternative splicing and lincRNA regulation. Dev. Cell, 39, 508-522.
Li, Z., Wang, R., Gao, Y. et al. (2017) The Arabidopsis CPSF30-L gene plays an essential role in nitrate signaling and regulates the nitrate transceptor gene NRT1.1. New Phytol. 216, 1205-1222.
Lin, W.D., Liao, Y.Y., Yang, T.J., Pan, C.Y., Buckhout, T.J. and Schmidt, W. (2011) Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling. Plant Physiol. 155, 1383-1402.
Liu, M., Xu, R., Merrill, C., Hong, L., Von Lanken, C., Hunt, A.G. and Li, Q.Q. (2015) Integration of developmental and environmental signals via a polyadenylation factor in Arabidopsis. PLoS One, 9, e115779.
Loke, J.C., Stahlberg, E.A., Strenski, D.G., Haas, B.J., Wood, P.C. and Li, Q.Q. (2005) Compilation of mRNA polyadenylation signals in Arabidopsis revealed a new signal element and potential secondary structures. Plant Physiol. 138, 1457-1468.
Lucas, M., Swarup, R., Paponov, I.A. et al. (2011) Short-root regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiol. 155, 384-398.
Luo, X., Chen, Z., Gao, J. and Gong, Z. (2014) Abscisic acid inhibits root growth in Arabidopsis through ethylene biosynthesis. Plant J. 79, 44-55.
Lutz, C.S. and Moreira, A. (2011) Alternative mRNA polyadenylation in eukaryotes: an effective regulator of gene expression. Wiley Interdiscip. Rev. RNA, 2, 23-31.
Malamy, J.E. and Benfey, P.N. (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development, 124, 33-44.
Mandel, C.R., Bai, Y. and Tong, L. (2008) Protein factors in pre-mRNA 3′-end processing. Cell. Mol. Life Sci. 65, 1099-1122.
Manzano, C., Ramirez-Parra, E., Casimiro, I., Otero, S., Desvoyes, B., De Rybel, B., Beeckman, T., Casero, P., Gutierrez, C. and Del Pozo, J.C. (2012) Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiol. 160, 749-762.
Manzano, C., Pallero-Baena, M., Casimiro, I., De Rybel, B., Orman-Ligeza, B., Van Isterdael, G., Beeckman, T., Draye, X., Casero, P. and Del Pozo, J.C. (2014) The emerging role of reactive oxygen species signaling during lateral root development. Plant Physiol. 165, 1105-1119.
Manzano, C., Pallero-Baena, M., Silva-Navas, J. et al. (2017) A light-sensitive mutation in Arabidopsis LEW3 reveals the important role of N-glycosylation in root growth and development. J. Exp. Bot. 68, 5103-5116.
Martin, A.C., del Pozo, J.C., Iglesias, J., Rubio, V., Solano, R., de La Pena, A., Leyva, A. and Paz-Ares, J. (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J. 24, 559-567.
Merchante, C., Stepanova, A.N. and Alonso, J.M. (2017) Translation regulation in plants: an interesting past, an exciting present and a promising future. Plant J. 90, 628-653.
Moreno-Risueno, M.A., Van Norman, J.M., Moreno, A., Zhang, J., Ahnert, S.E. and Benfey, P.N. (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science, 329, 1306-1311.
Moriwaki, T., Miyazawa, Y., Kobayashi, A., Uchida, M., Watanabe, C., Fujii, N. and Takahashi, H. (2011) Hormonal regulation of lateral root development in Arabidopsis modulated by MIZ1 and requirement of GNOM activity for MIZ1 function. Plant Physiol. 157, 1209-1220.
Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M. and Snyder, M. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science, 320, 1344-1349.
Peret, B., Li, G., Zhao, J. et al. (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14, 991-998.
Perianez-Rodriguez, J., Manzano, C. and Moreno-Risueno, M.A. (2014) Post-embryonic organogenesis and plant regeneration from tissues: two sides of the same coin? Front. Plant Sci. 5, 219.
del Pozo, J.C., Diaz-Trivino, S., Cisneros, N. and Gutierrez, C. (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell, 18, 2224-2235.
Ramirez-Parra, E., Perianez-Rodriguez, J., Navarro-Neila, S., Gude, I., Moreno-Risueno, M. and del Pozo, J.C. (2017) The transcription factor OBP4 controls root growth and promotes callus formation. New Phytol. 213, 1787-1801.
Sablowski, R. and Carnier-Dornelas, M. (2014) Interplay between cell growth and cell cycle in plants. J. Exp. Bot. 65, 2703-2714.
Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R. and Laux, T. (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature, 446, 811-814.
Scheres, B. (2005) Stem cells: a plant biology perspective. Cell, 122, 499-504.
Shen, Y., Venu, R.C., Nobuta, K., Wu, X., Notibala, V., Demirci, C., Meyers, B.C., Wang, G.-L., Ji, G. and Li, Q.Q. (2011) Transcriptome dynamics through alternative polyadenylation in developmental and environmental responses in plants revealed by deep sequencing. Genome Res. 21, 1478-1486.
Sherstnev, A., Duc, C., Cole, C., Zacharaki, V., Hornyik, C., Ozsolak, F., Milos, P.M., Barton, G.J. and Simpson, G.G. (2012) Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation. Nat. Struct. Mol. Biol. 19, 845-852.
Shi, Y. and Manley, J.L. (2015) The end of the message: multiple protein-RNA interactions define the mRNA polyadenylation site. Genes Dev. 29, 889-897.
Silva-Navas, J., Moreno-Risueno, M.A., Manzano, C., Téllez-Robledo, B., Navarro-Neila, S., Carrasco, V., Pollmann, S., Gallego, F.J. and del Pozo, J.C. (2016) Flavonols mediate root phototropism and growth through regulation of Proliferation to-Differentiation Transition. Plant Cell, 28, 1372-1387.
Stahl, Y., Wink, R.H., Ingram, G.C. and Simon, R. (2009) A signaling module controlling the stem cell niche in arabidopsis root meristems. Curr. Biol. 19, 909-914.
Sun, H.-X., Li, Y., Niu, Q.-W. and Chua, N.-H. (2017) Dehydration stress extends mRNA 3′ untranslated regions with noncoding RNA functions in Arabidopsis. Genome Res. 27, 1427-1436.
Tabas-Madrid, D., Nogales-Cadenas, R. and Pascual-Montano, A. (2012) GeneCodis3: a non-redundant and modular enrichment analysis tool for functional genomics. Nucleic Acids Res. 40, W478-W483.
Thomas, R.G., Hay, M.J. and Newton, P.C. (2002) A developmentally based categorization of branching in Trifolium repens L.: influence of nodal roots. Ann. Bot. (Lond), 90, 379-389.
Thomas, P.E., Wu, X., Liu, M., Gaffney, B., Ji, G., Li, Q.Q. and Hunt, A.G. (2012) Genome-wide control of polyadenylation site choice by CPSF30 in Arabidopsis. Plant Cell, 24, 4376-4388.
Tian, B. and Manley, J.L. (2016) Alternative polyadenylation of mRNA precursors. Nat. Rev. Mol. Cell Biol. 18, 18.
Toufighi, K., Brady, S.M., Austin, R., Ly, E. and Provart, N.J. (2005) The botany array resource: e-northerns, expression angling, and promoter analyses. Plant J. 43, 153-163.
Ulmasov, T., Murfett, J., Hagen, G. and Guilfoyle, T.J. (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell, 9, 1963-1971.
Wachsman, G., Sparks, E.E. and Benfey, P.N. (2015) Genes and networks regulating root anatomy and architecture. New Phytol. 208, 26-38.
Wang, J., Lan, P., Gao, H., Zheng, L., Li, W. and Schmidt, W. (2013) Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics, 14, 783.
Wang, C., Zhang, W., Li, Z., Li, Z., Bi, Y., Crawford, N.M. and Wang, Y. (2018) FIP1 plays an important role in nitrate signaling and regulates CIPK8 and CIPK23 expression in Arabidopsis. Front. Plant Sci. 9.
Wu, X., Liu, M., Downie, B., Liang, C., Ji, G., Li, Q.Q. and Hunt, A.G. (2011) Genome-wide landscape of polyadenylation in Arabidopsis provides evidence for extensive alternative polyadenylation. Proc. Natl Acad. Sci. USA, 108, 12533-12538.
Wu, X., Gaffney, B., Hunt, A.G. and Li, Q.Q. (2014) Genome-wide determination of poly(A) sites in Medicago truncatula: evolutionary conservation of alternative poly(A) site choice. BMC Genomics, 15, 615.
Yamashita, A. and Takeuchi, O. (2017) Translational control of mRNAs by 3′-Untranslated region binding proteins. BMB Rep. 50, 194-200.
Yoon, O.K. and Brem, R.B. (2010) Noncanonical transcript forms in yeast and their regulation during environmental stress. RNA, 16, 1256-1267.
Yuan, H.-M. and Huang, X. (2016) Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Arabidopsis. Plant Cell Environ. 39, 120-135.
Zhang, J., Addepalli, B., Yun, K.Y., Hunt, A.G., Xu, R., Rao, S., Li, Q.Q. and Falcone, D.L. (2008) A polyadenylation factor subunit implicated in regulating oxidative signaling in Arabidopsis thaliana. PLoS One, 3, e2410.
Zhang, H., Zhou, H., Berke, L., Heck, A.J.R., Mohammed, S., Scheres, B. and Menke, F.L.H. (2013) Quantitative phosphoproteomics after auxin-stimulated lateral root induction identifies an SNX1 protein phosphorylation site required for growth. Mol. Cell. Proteomics, 12, 1158-1169.
Zhu, Y., Wang, X., Forouzmand, E., Jeong, J., Qiao, F., Sowd, G.A., Engelman, A.N., Xie, X., Hertel, K.J. and Shi, Y. (2018) Molecular mechanisms for CFIm-mediated regulation of mRNA alternative polyadenylation. Mol. Cell, 69, 62-74 e64.
Zolla, G., Heimer, Y.M. and Barak, S. (2010) Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J. Exp. Bot. 61, 211-224.