Skip to main content
SpringerLink
Log in

Frontiers in plant RNA research in ICAR2023: from lab to innovative agriculture

  • Meeting Report
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The recent growth in global warming, soil contamination, and climate instability have widely disturbed ecosystems, and will have a significant negative impact on the growth of plants that produce grains, fruits and woody biomass. To conquer this difficult situation, we need to understand the molecular bias of plant environmental responses and promote development of new technologies for sustainable maintenance of crop production. Accumulated molecular biological data have highlighted the importance of RNA-based mechanisms for plant stress responses. Here, we report the most advanced plant RNA research presented in the 33rd International Conference on Arabidopsis Research (ICAR2023), held as a hybrid event on June 5–9, 2023 in Chiba, Japan, and focused on “Arabidopsis for Sustainable Development Goals”. Six workshops/concurrent sessions in ICAR2023 targeted plant RNA biology, and many RNA-related topics could be found in other sessions. In this meeting report, we focus on the workshops/concurrent sessions targeting RNA biology, to share what is happening now at the forefront of plant RNA research.

Key message

The 33rd International Conference on Arabidopsis Research (ICAR2023) had six sessions targeting plant RNA biology. We summarized the latest research there to understand how RNAs contribute to plant responses to changing environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Arribas-Hernández L, Marchais A, Poulsen C, Haase B, Hauptmann J, Benes V, Meister G, Brodersen P (2016) The slicer activity of ARGONAUTE1 is required specifically for the phasing, not production, of trans-acting short interfering RNAs in Arabidopsis. Plant Cell 28:1563–1580

    PubMed  PubMed Central  Google Scholar 

  • Brioudes F, Jay F, Sarazin A, Grentzinger T, Devers EA, Voinnet O (2021) HASTY, the Arabidopsis EXPORTIN5 ortholog, regulates cell-to-cell and vascular microRNA movement. EMBO J 40:e107455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai Q, Qiao L, Wang M, He B, Lin FM, Palmquist J, Huang S-D, Jin H (2018) Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–1129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiang CP, Li JL, Chiou TJ (2023) Dose-dependent long-distance movement of microRNA399 duplex regulates phosphate homeostasis in Arabidopsis. New Phytol 240:802–814

    Article  CAS  PubMed  Google Scholar 

  • Creasey KM, Zhai J, Borges F, Van Ex F, Regulski M, Meyers BC, Martienssen RA (2014) miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508:411–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuerda-Gil D, Slotkin RK (2016) Non-canonical RNA-directed DNA methylation. Nat Plants 2:16163

    Article  CAS  PubMed  Google Scholar 

  • Develtere W, Waegneer E, Debray K, De Saeger J, Van Glabeke S, Maere S, Ruttink T, Jacobs TB (2023) SMAP design: a multiplex PCR amplicon and gRNA design tool to screen for natural and CRISPR-induced genetic variation. Nucleic Acids Res 51:e37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devers EA, Brosnan CA, Sarazin A, Albertini D, Amsler AC, Brioudes F, Jullien PE, Lim P, Schott G, Voinnet O (2020) Movement and differential consumption of short interfering RNA duplexes underlie mobile RNA interference. Nat Plants 6:789–799

    Article  CAS  PubMed  Google Scholar 

  • Dew-Budd KJ, Chow HT, Kendall T, David BC, Rozelle JA, Mosher RA, Beilstein MA (2023) Mating system is associated with seed phenotypes upon loss of RNA-directed DNA methylation in Brassicaceae. Plant Physiol. https://doi.org/10.1093/plphys/kiad622

    Article  Google Scholar 

  • Duncan S, Olsson TSG, Hartley M, Dean C, Rosa S (2016) A method for detecting single mRNA molecules in Arabidopsis thaliana. Plant Methods 12:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Duncan S, Johansson HE, Ding Y (2022) Reference genes for quantitative Arabidopsis single molecule RNA fluorescence in situ hybridization. J Exp Bot 74:2405–2415

    Article  PubMed Central  Google Scholar 

  • Dziasek K, Simon L, Lafon-Placette C, Laenen B, Wärdig C, Santos-González J, Slotte T, Köhler C (2021) Hybrid seed incompatibility in Capsella is connected to chromatin condensation defects in the endosperm. PLoS Genet 17:e1009370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Floyd BE, Mugume Y, Morriss SC, MacIntosh GC, Bassham DC (2017) Localization of RNS2 ribonuclease to the vacuole is required for its role in cellular homeostasis. Planta 245:779–792

    Article  CAS  PubMed  Google Scholar 

  • Floyd BE, Kazibwe Z, Morriss SC, Mugume Y, Liu AY, Ridout V, Luo X, MacIntosh GC, Bassham DC (2021) An active RNA transport mechanism into plant vacuoles. bioRxiv 147:89

    Google Scholar 

  • Grover JW, Kendall T, Baten A, Burgess D, Freeling M, King GJ, Mosher RA (2018) Maternal components of RNA-directed DNA methylation are required for seed development in Brassica rapa. Plant J 94:575–582

    Article  CAS  PubMed  Google Scholar 

  • Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388

    Article  CAS  PubMed  Google Scholar 

  • He B, Cai Q, Qiao L, Huang CY, Wang S, Miao W, Ha T, Wang Y, Jin H (2021) RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles. Nat Plants 7:342–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He B, Wang H, Liu G, Chen A, Calvo A, Cai Q, Jin H (2023) Fungal small RNAs ride in extracellular vesicles to enter plant cells through clathrin-mediated endocytosis. Nat Commun 14:4383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heeney M, Frank MH (2023) The mRNA mobileome: challenges and opportunities for deciphering signals from the noise. Plant Cell 35:1817–1833

    Article  PubMed  PubMed Central  Google Scholar 

  • Hillwig MS, Contento AL, Meyer A, Ebany D, Bassham DC, Macintosh GC (2011) RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants. Proc Natl Acad Sci USA 108:1093–1098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou CY, Lee WC, Chou HC, Chen AP, Chou SJ, Chen HM (2016) Global analysis of truncated RNA ends reveals new insights into ribosome stalling in plants. Plant Cell 28:2398–2416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Patra P, Pisanty O, Shafir A, Belew ZM, Binenbaum J, Ben Yaakov S, Shi B, Charrier L, Hyams G, Zhang Y, Trabolsky M, Caldararu O, Weiss D, Crocoll C, Avni A, Vernoux T, Geisler M, Nour-Eldin HH, Mayrose I, Shani E (2023) Multi-Knock—a multi-targeted genome-scale CRISPR toolbox to overcome functional redundancy in plants. Nat Plants 9:572–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwakawa HO, Lam AYW, Mine A, Fujita T, Kiyokawa K, Yoshikawa M, Takeda A, Iwasaki S, Tomari Y (2021) Ribosome stalling caused by the Argonaute-microRNA-SGS3 complex regulates the production of secondary siRNAs in plants. Cell Rep 35:109300

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Herring G, Oliva M, Fourie E, Zhu JY, Johnston B, Pflüger J, Swain T, Pflüger C, Lloyd J, Secco D, Small I, Kidd B, Lister R (2022) CRISPRi-based circuits for genetic computation in plants. bioRxiv. https://doi.org/10.1101/2022.07.01.498372

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim EY, Wang L, Lei Z, Li H, Fan W, Cho J (2021) Ribosome stalling and SGS3 phase separation prime the epigenetic silencing of transposons. Nat Plants 7:303–309

    Article  CAS  PubMed  Google Scholar 

  • Kitagawa M, Wu P, Balkunde R, Cunniff P, Jackson D (2022) An RNA exosome subunit mediates cell-to-cell trafficking of a homeobox mRNA via plasmodesmata. Science 375:177–182

    Article  CAS  PubMed  Google Scholar 

  • Kurihara Y, Makita Y, Kawauchi M, Kageyama A, Kuriyama T, Matsui M (2022) Intergenic splicing-stimulated transcriptional readthrough is suppressed by nonsense-mediated mRNA decay in Arabidopsis. Commun Biol 5:1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurotani KI, Kawakatsu Y, Kikkawa M, Tabata R, Kurihara D, Honda H, Shimizu K, Notaguchi M (2022) Analysis of plasmodesmata permeability using cultured tobacco BY-2 cells entrapped in microfluidic chips. J Plant Res 135:693–701

    Article  CAS  PubMed  Google Scholar 

  • Lee TA, Nobori T, Illouz-Eliaz N, Xu J, Jow B, Nery JR, Ecker JR (2023) A single-nucleus atlas of seed-to-seed development in Arabidopsis. bioRxiv. https://doi.org/10.1101/2023.03.23.533992

    Article  PubMed  PubMed Central  Google Scholar 

  • Li YR, Liu MJ (2020) Prevalence of alternative AUG and non-AUG translation initiators and their regulatory effects across plants. Genome Res 30:1418–1433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd JPB, Ly F, Gong P, Pflueger J, Swain T, Pflueger C, Fourie E, Khan MA, Kidd B, Lister R (2022) Synthetic memory circuits for stable cell reprogramming in plants. Nat Biotechnol 40:1862–1872

    Article  CAS  PubMed  Google Scholar 

  • Luo KR, Huang NC, Chang YH, Yu TS (2022) Arabidopsis cyclophilins direct plasmodesmata-targeting of mobile mRNA via organelle hitchhiking. Res Sq. https://doi.org/10.21203/rs.3.rs-1088339/v1

    Article  PubMed  PubMed Central  Google Scholar 

  • Mills SC, Enganti R, von Arnim AG (2018) What makes ribosomes tick? RNA Biol 15:44–54

    Article  PubMed  Google Scholar 

  • Notaguchi M, Higashiyama T, Suzuki T (2015) Identification of mRNAs that move over long distances using an RNA-Seq analysis of Arabidopsis/Nicotiana benthamiana heterografts. Plant Cell Physiol 56:311–321

    Article  CAS  PubMed  Google Scholar 

  • Ohtani M (2017) Plant snRNP biogenesis: a perspective from the nucleolus and Cajal bodies. Front Plant Sci 8:2184

    Article  PubMed  Google Scholar 

  • Ohtani M, Wachter A (2019) NMD-based gene regulation—a strategy for fitness enhancement in plants? Plant Cell Physiol 60:1953–1960

    Article  CAS  PubMed  Google Scholar 

  • Oliva M, Stuart T, Tang D, Pflueger J, Poppe D, Jabbari JS, Gigante S, Dragwidge JM, Whelan J, Lewsey MG, Lister R (2022) An environmentally-responsive transcriptional state modulates cell identities during root development. bioRxiv. https://doi.org/10.1101/2022.03.04.483008

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiao L, Niño-Sánchez J, Hamby R, Capriotti L, Chen A, Mezzetti B, Jin H (2023) Artificial nanovesicles for dsRNA delivery in spray-induced gene silencing for crop protection. Summ Plant Biotechnol J 21(4):854–865. https://doi.org/10.1111/pbi.14001

    Article  CAS  Google Scholar 

  • Rigo R, Bazin J, Romero-Barrios N, Moison M, Lucero L, Christ A, Benhamed M, Blein T, Huguet S, Charon C, Crespi M, Ariel F (2020) The Arabidopsis lncRNA ASCO modulates the transcriptome through interaction with splicing factors. EMBO Rep 21:e48977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu K, Kawakatsu Y, Kurotani KI, Kikkawa M, Tabata R, Kurihara D, Honda H, Notaguchi M (2022) Development of microfluidic chip for entrapping tobacco BY-2 cells. PLoS ONE 17:e0266982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang X, Peng Y, Li Z, Guo H, Xia X, Li B, Yin W (2022) The regulation of nitrate reductases in response to abiotic stress in Arabidopsis. Int J Mol Sci 23:1202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W, Yang L, Miñambres M, Walther D, Schulze WX, Paz-Ares J, Scheible WR, Kragler F (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat Plants 1:15025

    Article  CAS  PubMed  Google Scholar 

  • Thomas HR, Gevorgyan A, Frank MH (2023) Anatomical and biophysical basis for graft incompatibility within the Solanaceae. J Exp Bot 74:4461–4470

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui H, Yanagisawa N, Kawakatsu Y, Ikematsu S, Sawai Y, Tabata R, Arata H, Higashiyama T, Notaguchi M (2020) Micrografting device for testing systemic signaling in Arabidopsis. Plant J 103:918–929

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhang X, Greene GH, Xu G, Dong X (2022) PABP/purine-rich motif as an initiation module for cap-independent translation in pattern-triggered immunity. Cell 185:3186-3200.e17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, He B, Wu H, Cai Q, Ramírez-Sánchez O, Abreu-Goodger C, Birch PRJ, Jin H (2024) Plant mRNAs move into a fungal pathogen via extracellular vesicles to reduce infection. Cell Host Microbe 32:93–105

    Article  CAS  PubMed  Google Scholar 

  • Weiberg A, Wang M, Lin F-m, Zhao H, Zhang Z, Kaloshian I, Huang H-D, Jin H (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways RNA on the attack. Science 342(6154):118–123. https://doi.org/10.1126/science.1239705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu HL, Hsu PY (2022) A custom library construction method for super-resolution ribosome profiling in Arabidopsis. Plant Methods 18:115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Li B, Iwakawa HO, Pan Y, Tang X, Ling-Hu Q, Liu Y, Sheng S, Feng L, Zhang H, Zhang X, Tang Z, Xia X, Zhai J, Guo H (2020) Plant 22-nt siRNAs mediate translational repression and stress adaptation. Nature 581:89–93

    Article  CAS  PubMed  Google Scholar 

  • Wu HL, Ai Q, Teixeira RT, Nguyen PHT, Song G, Montes C, Elmore JM, Walley JW, Hsu PY (2023a) Improved super-resolution ribosome profiling revealed prevalent translation of upstream ORFs and small ORFs in Arabidopsis. Plant Cell 13:165

    Google Scholar 

  • Wu HL, Jen J, Hsu PY (2023b) What, where, and how: regulation of translation and the translational landscape in plants. Plant Cell. https://doi.org/10.1093/plcell/koad197

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao C, Li K, Hua J, He Z, Zhang F, Li Q, Zhang H, Yang L, Pan S, Cai Z, Yu Z, Wong KB, Xia Y (2023) Arabidopsis DXO1 activates RNMT1 to methylate the mRNA guanosine cap. Nat Commun 14:202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Mao L, Jittayasothorn Y, Kang Y, Jiao C, Fei Z, Zhong GY (2015) Messenger RNA exchange between scions and rootstocks in grafted grapevines. BMC Plant Biol 15:251

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Wafula EK, Kim G, Shahid S, McNeal JR, Ralph PE, Timilsena PR, Yu WB, Kelly EA, Zhang H, Person TN (2019) Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants. Nat Plants 5:991–1001

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Zhu P, Cheema J, Bloomer R, Mikulski P, Liu Q, Zhang Y, Dean C, Ding Y (2022) In vivo single-molecule analysis reveals COOLAIR RNA structural diversity. Nature 609:394–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Machin F, Wang S, Saplaoura E, Kragler F (2023) Heritable transgene-free genome editing in plants by grafting of wild-type shoots to transgenic donor rootstocks. Nat Biotechnol 41:958–967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, Qi Y, Yang B, Yang X, Ding Y (2023) G4Atlas: a comprehensive transcriptome-wide G-quadruplex database. Nucleic Acids Res 51(D1):D126–D134

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Zheng Y, Ham BK, Chen J, Yoshida A, Kochian LV, Fei Z, Lucas WJ (2016) Vascular-mediated signalling involved in early phosphate stress response in plants. Nat Plants 2:16033

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhong H, Zhang S, Shao X, Ni M, Cai Z, Chen X, Xia Y (2019a) NAD tagSeq reveals that NAD+-capped RNAs are mostly produced from a large number of protein-coding genes in Arabidopsis. Proc Natl Acad Sci USA 116:12072–12077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Yang M, Duncan S, Yang X, Abdelhamid MAS, Huang L, Zhang H, Benfey PN, Waller ZAE, Ding Y (2019b) G-quadruplex structures trigger RNA phase separation. Nucl Acids Res 47:11746–11754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou M, Coruh C, Xu G, Martins LM, Bourbousse C, Lambolez A, Law JA (2022) The CLASSY family controls tissue-specific DNA methylation patterns in Arabidopsis. Nat Commun 13:244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all organizers of session/workshop related to plant RNA researches, Jose Antonio Duarte-Conde (Universidad de Málaga, IHSM-UMA-CSIC), Margaret Frank (Cornell University), Dave Jackson (Cold Spring Harbor Laboratory), Fritz Kragler (Max Planck Institute of Molecular Plant Physiology), Hailing Jin (University of California, Riverside), Catharina Merchante (Universidad de Málaga, IHSM-UMA-CSIC), Michitaka Notaguchi Kyoto University), Gemma Sans-Coll (Universidad de Málaga, IHSM-UMA-CSIC), Eilon Shani (Tel Aviv University), Keith Slotkin (Donald Danforth Plant Science Center and University of Missouri), for their great efforts to make an opportunity for gathering such leading researcher in ICAR2023. We also thank all speakers mentioned in this report for their critical reading of the manuscript. This work was supported in part by JSPS KAKENHI (JP20H03271) and the MEXT KAKENHI (JP25114520, JP15H01235, and JP20H05405) to M.O., and MOST 110-2628-B-001-023, MOST 111-2311-B-001-005 and AS-CDA-111-L06 to M.-J. L.

Funding

This work was supported by Japan Society for the Promotion of Science (Grant No. JP20H03271), MEXT KAKENHI (Grant Nos. JP25114520, JP15H01235, JP20H05405), MOST (Grant Nos. 110-2628-B-001-023 and 111-2311-B-001-005), Academia Sinica (Grant No. AS-CDA-111-L06).

Author information

Authors and Affiliations

  1. Biotechnology Center in Southern Taiwan, Academia Sinica (AS-BCST), Tainan, Taiwan

    Ming-Jung Liu & Jhen-Cheng Fang

  2. Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, 227-8562, Japan

    Ya Ma, Ami Takeuchi, Natsu Takayanagi & Misato Ohtani

  3. Institute of Plant and Microbial Biology, Academia Sinica, Taipei, 115201, Taiwan

    Geeng Loo Chong & Chun-Kai Huang

  4. Division of Biological Science, Graduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, 630-0192, Japan

    Misato Ohtani

  5. RIKEN Center for Sustainable Resource Science, Yokohama, 230-0045, Japan

    Misato Ohtani

Authors
  1. Ming-Jung Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jhen-Cheng Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ya Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Geeng Loo Chong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chun-Kai Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ami Takeuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Natsu Takayanagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Misato Ohtani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors wrote the manuscript.

Corresponding authors

Correspondence to Ming-Jung Liu or Misato Ohtani.

Ethics declarations

Competing interests

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, MJ., Fang, JC., Ma, Y. et al. Frontiers in plant RNA research in ICAR2023: from lab to innovative agriculture. Plant Mol Biol 114, 45 (2024). https://doi.org/10.1007/s11103-024-01436-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11103-024-01436-x

Keywords

Search

Navigation