Traveling with purpose: cell-to-cell transport of plant mRNAs

Munenori Kitagawa1, Thu M. Tran2, David Jackson2
1National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, Huazhong Agricultural University, Wuhan 430070, PR China
2Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 11724 USA

Tài liệu tham khảo

Reagan, 2018, RNA on the move: the plasmodesmata perspective, Plant Sci., 275, 1, 10.1016/j.plantsci.2018.07.001 Maizel, 2020, To move or not to move: roles and specificity of plant RNA mobility, Curr. Opin. Plant Biol., 57, 52, 10.1016/j.pbi.2020.05.005 Kirk, 2022, Plasmodesmata structural components and their role in signaling and plant development, 3 Kehr, 2021, Long-distance transported RNAs: from identity to function, Annu. Rev. Plant Biol., 73, 457, 10.1146/annurev-arplant-070121-033601 Heeney, 2023, The mRNA mobileome: challenges and opportunities for deciphering signals from the noise, Plant Cell, 10.1093/plcell/koad063 Sager, 2018, Plasmodesmata at a glance, J. Cell Sci., 131, jcs209346, 10.1242/jcs.209346 Gundu, 2020, Moving with purpose and direction: transcription factor movement and cell fate determination revisited, Curr. Opin. Plant Biol., 57, 124, 10.1016/j.pbi.2020.08.003 Calderwood, 2016, Transcript abundance explains mRNA mobility data in Arabidopsis thaliana, Plant Cell, 28, 610, 10.1105/tpc.15.00956 Sessions, 2000, Cell–cell signaling and movement by the floral transcription factors LEAFY and APETALA1, Science, 289, 779, 10.1126/science.289.5480.779 Kurata, 2005, Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation, Development, 132, 5387, 10.1242/dev.02139 Daum, 2014, A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis, Proc. Natl. Acad. Sci., 111, 14619, 10.1073/pnas.1406446111 Dong, 2021, An SHR-SCR module specifies legume cortical cell fate to enable nodulation, Nature, 589, 586, 10.1038/s41586-020-3016-z Lucas, 1995, Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata, Science, 270, 1980, 10.1126/science.270.5244.1980 Kitagawa, 2022, An RNA exosome subunit mediates cell-to-cell trafficking of a homeobox mRNA via plasmodesmata, Science, 375, 177, 10.1126/science.abm0840 Luo, 2022, Arabidopsis cyclophilins direct plasmodesmata-targeting of mobile mRNA via organelle hitchhiking, Res. Sq. Luo, 2018, Selective targeting of mobile mRNAs to plasmodesmata for cell-to-cell movement, Plant Physiol., 177, 604, 10.1104/pp.18.00107 Li, 2022, Long-distance transport RNAs between rootstocks and scions and graft hybridization, Planta, 255, 96, 10.1007/s00425-022-03863-w Wang, 2021, RNA motifs and modification involve in RNA long-distance transport in plants, Front. Cell Dev. Biol., 9 Ham, 2009, A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex, Plant Cell, 21, 197, 10.1105/tpc.108.061317 Dai, 2022, PTB: not just a polypyrimidine tract-binding protein, J. Cell. Physiol., 237, 2357, 10.1002/jcp.30716 Cho, 2015, Polypyrimidine tract-binding proteins of potato mediate tuberization through an interaction with StBEL5 RNA, J. Exp. Bot., 66, 6835, 10.1093/jxb/erv389 Zhang, 2016, Vascular-mediated signalling involved in early phosphate stress response in plants, Nat. Plants, 2, 1, 10.1038/nplants.2016.33 Miguel-Tomé, 2021, Broadening the definition of a nervous system to better understand the evolution of plants and animals, Plant Signal. Behav., 16, 1927562, 10.1080/15592324.2021.1927562 Zierer, 2021, Tuber and tuberous root development, Annu. Rev. Plant Biol., 72, 551, 10.1146/annurev-arplant-080720-084456 Thieme, 2015, Endogenous Arabidopsis messenger RNAs transported to distant tissues, Nat. Plants, 1, 15025, 10.1038/nplants.2015.25 Xia, 2020, Long-distance movement of mineral deficiency-responsive mRNAs in Nicotiana benthamiana/tomato heterografts, Plants, 9, 876, 10.3390/plants9070876 Yang, 2023, Non-cell-autonomous HSC70.1 chaperone displays homeostatic feed-back regulation by binding its own mRNA, New Phytol., 237, 2404, 10.1111/nph.18703 Ellison, 2020, Multiplexed heritable gene editing using RNA viruses and mobile single guide RNAs, Nat. Plants, 6, 620, 10.1038/s41477-020-0670-y Uranga, 2021, Efficient Cas9 multiplex editing using unspaced sgRNA arrays engineering in a Potato virus X vector, Plant J., 106, 555, 10.1111/tpj.15164 Lei, 2021, Heritable gene editing using FT mobile guide RNAs and DNA viruses, Plant Methods, 17, 20, 10.1186/s13007-021-00719-4 Yang, 2023, Heritable transgene-free genome editing in plants by grafting of wild-type shoots to transgenic donor rootstocks, Nat. Biotechnol., 10.1038/s41587-022-01585-8 Paultre, 2016, Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts, Plant Cell, 28, 2016, 10.1105/tpc.16.00249 Burjoski, 2021, The landscape of RNA–protein interactions in plants: approaches and current status, Int. J. Mol. Sci., 22, 2845, 10.3390/ijms22062845 Fuchs, 2020, Aiming for the top: non-cell autonomous control of shoot stem cells in Arabidopsis, J. Plant Res., 133, 297, 10.1007/s10265-020-01174-3 Huang, 2022, Function of plasmodesmata in the interaction of plants with microbes and viruses, 23 Kitagawa, 2022, Trafficking and localization of KNOTTED1 related mRNAs in shoot meristems, Commun. Integr. Biol., 15, 158, 10.1080/19420889.2022.2095125 Kim, 2005, A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking, Genes Dev., 19, 788, 10.1101/gad.332805 Kitagawa, 2022, A forward genetic approach to identify plasmodesmal trafficking regulators based on trichome rescue, 393 Carnesecchi, 2022, The Hox transcription factor Ultrabithorax binds RNA and regulates co-transcriptional splicing through an interplay with RNA polymerase II, Nucleic Acids Res., 50, 763, 10.1093/nar/gkab1250 Kim, 2003, Developmental regulation and significance of KNOX protein trafficking in Arabidopsis, Development, 130, 4351, 10.1242/dev.00618 Long, 1996, A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis, Nature, 379, 66, 10.1038/379066a0 Balkunde, 2017, SHOOT MERISTEMLESS trafficking controls axillary meristem formation, meristem size and organ boundaries in Arabidopsis, Plant J., 90, 435, 10.1111/tpj.13504 Xu, 2011, Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function, Science, 333, 1141, 10.1126/science.1205727 Kühn, 1997, Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements, Science, 275, 1298, 10.1126/science.275.5304.1298 Liesche, 2011, Sucrose transporter regulation at the transcriptional, post-transcriptional and post-translational level, J. Plant Physiol., 168, 1426, 10.1016/j.jplph.2011.02.005 Schmitt, 2008, Immunolocalization of solanaceous SUT1 proteins in companion cells and xylem parenchyma: new perspectives for phloem loading and transport, Plant Physiol., 148, 187, 10.1104/pp.108.120410 Liu, 2018, FTIP-dependent STM trafficking regulates shoot meristem development in Arabidopsis, Cell Rep., 23, 1879, 10.1016/j.celrep.2018.04.033 Fal, 2017, Phyllotactic regularity requires the Paf1 complex in Arabidopsis, Development, 144, 4428 Tsuda, 2011, Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice, Plant Cell, 23, 4368, 10.1105/tpc.111.090050 Haimovich, 2021, RNA transfer through tunneling nanotubes, Biochem. Soc. Trans., 49, 145, 10.1042/BST20200113 Landschaft, 2020, Gaps and barriers: gap junctions as a channel of communication between the soma and the germline, Semin. Cell Dev. Biol., 97, 167, 10.1016/j.semcdb.2019.09.002 Menachem, 2016, Intercellular transfer of small RNAs from astrocytes to lung tumor cells induces resistance to chemotherapy, Oncotarget, 7, 12489, 10.18632/oncotarget.7273 Katakowski, 2010, Functional microRNA is transferred between glioma cells, Cancer Res., 70, 8259, 10.1158/0008-5472.CAN-10-0604 Rechavi, 2009, Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs, Genes Dev., 23, 1971, 10.1101/gad.1789609 Valiunas, 2005, Connexin-specific cell-to-cell transfer of short interfering RNA by gap junctions, J. Physiol., 568, 459, 10.1113/jphysiol.2005.090985 Haimovich, 2017, Intercellular mRNA trafficking via membrane nanotube-like extensions in mammalian cells, Proc. Natl. Acad. Sci., 114, E9873, 10.1073/pnas.1706365114 Dasgupta, 2023, Global analysis of contact-dependent human-to-mouse intercellular mRNA and lncRNA transfer in cell culture, eLife, 12, 10.7554/eLife.83584 Zhang, 2023, Syncytin-mediated open-ended membrane tubular connections facilitate the intercellular transfer of cargos including Cas9 protein, eLife, 12, 10.7554/eLife.84391 Tosar, 2021, Revisiting extracellular RNA release, processing, and function, Trends Biochem. Sci., 46, 438, 10.1016/j.tibs.2020.12.008 Prieto-Vila, 2021, Biological functions driven by mRNAs carried by extracellular vesicles in cancer, Front. Cell Dev. Biol., 9, 10.3389/fcell.2021.620498 Bolukbasi, 2012, miR-1289 and “Zipcode”-like sequence enrich mRNAs in microvesicles, Mol. Ther. Nucleic Acids, 1, 10.1038/mtna.2011.2 Szostak, 2014, Sorting signal targeting mRNA into hepatic extracellular vesicles, RNA Biol., 11, 836, 10.4161/rna.29305 Borniego, 2023, Extracellular RNA: mechanisms of secretion and potential functions, J. Exp. Bot., 74, 2389, 10.1093/jxb/erac512 Zand Karimi, 2022, Arabidopsis apoplastic fluid contains sRNA– and circular RNA–protein complexes that are located outside extracellular vesicles, Plant Cell, 34, 1863, 10.1093/plcell/koac043 Cai, 2018, Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes, Science, 360, 1126, 10.1126/science.aar4142 He, 2021, RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles, Nat. Plants, 7, 342, 10.1038/s41477-021-00863-8 Baldrich, 2019, Plant extracellular vesicles contain diverse small RNA species and are enriched in 10-to 17-nucleotide “tiny” RNAs, Plant Cell, 31, 315, 10.1105/tpc.18.00872 Qin, 2023, Molecular characterization reveals no functional evidence for naturally occurring cross-kingdom RNA interference in the early stages of Botrytis cinerea–tomato interaction, Mol. Plant Pathol., 24, 3, 10.1111/mpp.13269 Wong-Bajracharya, 2022, The ectomycorrhizal fungus Pisolithus microcarpus encodes a microRNA involved in cross-kingdom gene silencing during symbiosis, Proc. Natl. Acad. Sci., 119, 10.1073/pnas.2103527119 Dunker, 2020, Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence, Elife, 9, 10.7554/eLife.56096 Weiberg, 2013, Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways, Science, 342, 118, 10.1126/science.1239705 Turck, 2008, Regulation and identity of florigen: FLOWERING LOCUS T moves center stage, Annu. Rev. Plant Biol., 59, 573, 10.1146/annurev.arplant.59.032607.092755 Liu, 2020, Florigen trafficking integrates photoperiod and temperature signals in Arabidopsis, J. Integr. Plant Biol., 62, 1385, 10.1111/jipb.13000 Corbesier, 2007, FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis, Science, 316, 1030, 10.1126/science.1141752 Tamaki, 2007, Hd3a protein is a mobile flowering signal in rice, Science, 316, 1033, 10.1126/science.1141753 Yu, 2021, Mobile FLOWERING LOCUS T RNA – biological relevance and biotechnological potential, Front. Plant Sci., 12 Helariutta, 2000, The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling, Cell, 101, 555, 10.1016/S0092-8674(00)80865-X Nakajima, 2001, Intercellular movement of the putative transcription factor SHR in root patterning, Nature, 413, 307, 10.1038/35095061 Koizumi, 2011, An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor, Curr. Biol., 21, 1559, 10.1016/j.cub.2011.08.013 Spiegelman, 2018, KinG is a plant-specific kinesin that regulates both intra- and intercellular movement of SHORT-ROOT, Plant Physiol., 176, 392, 10.1104/pp.17.01518 Spiegelman, 2019, A role for the endoplasmic reticulum in the cell-to-cell movement of SHORT-ROOT, Protoplasma, 256, 1455, 10.1007/s00709-019-01369-z Liu, 2016, snRNA 3′ end processing by a CPSF73-containing complex essential for development in Arabidopsis, PLoS Biol., 14, 10.1371/journal.pbio.1002571 Winter, 2007, MPB2C, a microtubule-associated protein, regulates non-cell-autonomy of the homeodomain protein KNOTTED1, Plant Cell, 19, 3001, 10.1105/tpc.107.044354 Chen, 2022, Plant and animal small RNA communications between cells and organisms, Nat. Rev. Mol. Cell Biol., 23, 185, 10.1038/s41580-021-00425-y Voinnet, 2022, Revisiting small RNA movement in plants, Nat. Rev. Mol. Cell Biol., 23, 163, 10.1038/s41580-022-00455-0 Fan, 2022, Microtubules promote the non-cell autonomous action of microRNAs by inhibiting their cytoplasmic loading onto ARGONAUTE1 in Arabidopsis, Dev. Cell, 57, 995, 10.1016/j.devcel.2022.03.015 Zang, 2021, A novel plant actin–microtubule bridging complex regulates cytoskeletal and ER structure at ER-PM contact sites, Curr. Biol., 31, 1251, 10.1016/j.cub.2020.12.009 Lange, 2022, Catalytic activities, molecular connections, and biological functions of plant RNA exosome complexes, Plant Cell, 34, 967, 10.1093/plcell/koab310 Kragler, 1998, Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor, Plant J., 15, 367, 10.1046/j.1365-313X.1998.00219.x Mateos, 2022, Toward a systems view on RNA-binding proteins and associated RNAs in plants: guilt by association, Plant Cell, 35, 1708, 10.1093/plcell/koac345 Wu, 2019, A three-dimensional RNA motif mediates directional trafficking of Potato spindle tuber viroid from epidermal to palisade mesophyll cells in Nicotiana benthamiana, PLoS Pathog., 15, 10.1371/journal.ppat.1008147 Li, 2009, A cis element within flowering locus T mRNA determines its mobility and facilitates trafficking of heterologous viral RNA, J. Virol., 83, 3540, 10.1128/JVI.02346-08 Zhang, 2016, tRNA-related sequences trigger systemic mRNA transport in plants, Plant Cell, 28, 1237, 10.1105/tpc.15.01056 Yang, 2019, m5C methylation guides systemic transport of messenger RNA over graft junctions in plants, Curr. Biol., 29, 2465, 10.1016/j.cub.2019.06.042 Das, 2021, Intracellular mRNA transport and localized translation, Nat. Rev. Mol. Cell Biol., 22, 483, 10.1038/s41580-021-00356-8 Gräwe, 2021, RNA-centric methods: toward the interactome of specific RNA transcripts, Trends Biotechnol., 39, 890, 10.1016/j.tibtech.2020.11.011 Denyer, 2022, Crafting a blueprint for single-cell RNA sequencing, Trends Plant Sci., 27, 92, 10.1016/j.tplants.2021.08.016 Yu, 2022, Spinach-based RNA mimicking GFP in plant cells, Funct. Integr. Genom., 22, 423, 10.1007/s10142-022-00835-x Peña, 2021, In vivo imaging of tagged mRNA in plant tissues using the bacterial transcriptional antiterminator BglG, Plant J., 105, 271, 10.1111/tpj.15035