Science - USA (2022-03-04)

(Maropa) #1

  1. K. Sugimoto, S. P. Gordon, E. M. Meyerowitz, Regeneration in
    plants and animals: Dedifferentiation, transdifferentiation, or
    just differentiation?Trends Cell Biol. 21 , 212–218 (2011).
    doi:10.1016/j.tcb.2010.12.004; pmid: 21236679

  2. G. Wachsman, J. Zhang, M. A. Moreno-Risueno, C. T. Anderson,
    P. N. Benfey, Cell wall remodeling and vesicle trafficking
    mediate the root clock inArabidopsis.Science 370 , 819– 823
    (2020). doi:10.1126/science.abb7250; pmid: 33184208

  3. W. Xuanet al., Cyclic programmed cell death stimulates
    hormone signaling and root development inArabidopsis.
    Science 351 , 384–387 (2016). doi:10.1126/science.aad2776;
    pmid: 26798015

  4. T. van den Berget al., A reflux-and-growth mechanism explains
    oscillatory patterning of lateral root branching sites.Dev. Cell
    56 , 2176–2191.e10 (2021). doi:10.1016/j.devcel.2021.07.005;
    pmid: 34343477

  5. I. De Smetet al., Auxin-dependent regulation of lateral root
    positioning in the basal meristem ofArabidopsis.Development
    134 , 681–690 (2007). doi:10.1242/dev.02753; pmid: 17215297

  6. M. A. Moreno-Risuenoet al., Oscillating gene expression
    determines competence for periodicArabidopsisroot
    branching.Science 329 , 1306–1311 (2010). doi:10.1126/
    science.1191937; pmid: 20829477

  7. A. J. Dickinsonet al., A plant lipocalin promotes retinal-
    mediated oscillatory lateral root initiation.Science 373 ,
    1532 – 1536 (2021). doi:10.1126/science.abf7461;
    pmid: 34446443

  8. K. Esau,Anatomy of Seed Plants(Wiley, 1977).

  9. A. J. Hetherington, L. Dolan, Evolution: Diversification of
    angiosperm rooting systems in the Early Cretaceous.Curr. Biol.
    29 , R1081–R1083 (2019). doi:10.1016/j.cub.2019.08.030;
    pmid: 31639353

  10. P. Groff, D. R. Kaplan, The relation of root systems to shoot
    systems in vascular plants.Bot. Rev. 54 , 387–422 (1988).
    doi:10.1007/BF02858417

  11. C. Bellini, D. I. I. Pacurar, I. Perrone, Adventitious roots and
    lateral roots: Similarities and differences.Annu. Rev. Plant Biol.
    65 , 639–666 (2014). doi:10.1146/annurev-arplant-050213-
    035645 ; pmid: 24555710

  12. K. D. Birnbaum, How many ways are there to make a root?
    Curr. Opin. Plant Biol. 34 , 61–67 (2016). doi:10.1016/
    j.pbi.2016.10.001; pmid: 27780106

  13. L. Chang, E. Ramireddy, T. Schmülling, Cytokinin as a
    positional cue regulating lateral root spacing inArabidopsis.
    J. Exp. Bot. 66 , 4759–4768 (2015). doi:10.1093/jxb/erv252;
    pmid: 26019251

  14. A. Bielachet al., Spatiotemporal regulation of lateral root
    organogenesis inArabidopsisby cytokinin.Plant Cell 24 ,
    3967 – 3981 (2012). doi:10.1105/tpc.112.103044;
    pmid: 23054471

  15. J. Lavenuset al., Lateral root development inArabidopsis: Fifty
    shades of auxin.Trends Plant Sci. 18 , 450–458 (2013).
    doi:10.1016/j.tplants.2013.04.006; pmid: 23701908

  16. C. Galinhaet al., PLETHORA proteins as dose-dependent
    master regulators ofArabidopsisroot development.Nature
    449 , 1053–1057 (2007). doi:10.1038/nature06206;
    pmid: 17960244

  17. Y. Du, B. Scheres, Lateral root formation and the multiple roles
    of auxin.J. Exp. Bot. 69 , 155–167 (2018). doi:10.1093/jxb/
    erx223; pmid: 28992266

  18. H. Hofhuiset al., Phyllotaxis and rhizotaxis inArabidopsisare
    modified by three PLETHORA transcription factors.Curr. Biol.
    23 , 956–962 (2013). doi:10.1016/j.cub.2013.04.048;
    pmid: 23684976

  19. G. Taraminoet al., The maize (Zea maysL.) RTCS gene
    encodes a LOB domain protein that is a key regulator of
    embryonic seminal and post-embryonic shoot-borne root


initiation.Plant J. 50 , 649–659 (2007). doi:10.1111/j.1365-
313X.2007.03075.x; pmid: 17425722


  1. Y. Inukaiet al., Crown rootless1, which is essential for crown
    root formation in rice, is a target of an AUXIN RESPONSE
    FACTOR in auxin signaling.Plant Cell 17 , 1387–1396 (2005).
    doi:10.1105/tpc.105.030981; pmid: 15829602

  2. H. Liuet al., ARL1, a LOB-domain protein required for
    adventitious root formation in rice.Plant J. 43 , 47–56 (2005).
    doi:10.1111/j.1365-313X.2005.02434.x; pmid: 15960615

  3. Y. Kitomiet al., The auxin responsive AP2/ERF transcription
    factor CROWN ROOTLESS5 is involved in crown root initiation
    in rice through the induction of OsRR1, a type-A response
    regulator of cytokinin signaling.Plant J. 67 , 472–484 (2011).
    doi:10.1111/j.1365-313X.2011.04610.x; pmid: 21481033

  4. Y. Zhao, Y. Hu, M. Dai, L. Huang, D.-X. Zhou, The WUSCHEL-
    related homeobox gene WOX11 is required to activate shoot-
    borne crown root development in rice.Plant Cell 21 , 736– 748
    (2009). doi:10.1105/tpc.108.061655; pmid: 19258439

  5. T. Ulmasov, Z. B. Liu, G. Hagen, T. J. Guilfoyle, Composite
    structure of auxin response elements.Plant Cell 7 , 1611– 1623
    (1995). pmid: 7580254

  6. E. Zürcheret al., A robust and sensitive synthetic sensor to
    monitor the transcriptional output of the cytokinin signaling
    network in planta.Plant Physiol. 161 , 1066–1075 (2013).
    doi:10.1104/pp.112.211763; pmid: 23355633

  7. M. Lieberman-Lazarovich, C. Yahav, A. Israeli, I. Efroni, Deep
    conservation ofcis-element variants regulating plant hormonal
    responses.Plant Cell 31 , 2559–2572 (2019). doi:10.1105/
    tpc.19.00129; pmid: 31467248

  8. B. Müller, J. Sheen, Cytokinin and auxin interaction in root
    stem-cell specification during early embryogenesis.Nature
    453 , 1094–1097 (2008). doi:10.1038/nature06943;
    pmid: 18463635

  9. T. Stuartet al., Comprehensive integration of single-cell data.
    Cell 177 , 1888–1902.e21 (2019). doi:10.1016/
    j.cell.2019.05.031; pmid: 31178118

  10. K. Kajalaet al., Innovation, conservation, and repurposing of
    gene function in root cell type development.Cell 184 ,
    3333 – 3348.e19 (2021). doi:10.1016/j.cell.2021.04.024;
    pmid: 34010619

  11. I. Efroni, P.-L. Ip, T. Nawy, A. Mello, K. D. Birnbaum,
    Quantification of cell identity from single-cell gene expression
    profiles.Genome Biol. 16 , 9 (2015). doi:10.1186/s13059-015-
    0580-x; pmid: 25608970

  12. J. Jiet al., WOX4 promotes procambial development.Plant
    Physiol. 152 , 1346–1356 (2010). doi:10.1104/pp.109.149641;
    pmid: 20044450

  13. J. Caoet al., The single-cell transcriptional landscape of
    mammalian organogenesis.Nature 566 , 496–502 (2019).
    doi:10.1038/s41586-019-0969-x; pmid: 30787437

  14. C. Wanget al., The WOX family transcriptional regulator
    SlLAM1 controls compound leaf and floral organ development
    inSolanum lycopersicum.J. Exp. Bot. 72 , 1822–1835 (2021).
    doi:10.1093/jxb/eraa574; pmid: 33277994

  15. Tomato Genome Consortium, The tomato genome sequence
    provides insights into fleshy fruit evolution.Nature 485 ,
    635 – 641 (2012). doi:10.1038/nature11119; pmid: 22660326

  16. A. S. Chanderbali, F. He, P. S. Soltis, D. E. Soltis, Out of the
    water: Origin and diversification of the LBD gene family.
    Mol. Biol. Evol. 32 , 1996–2000 (2015). doi:10.1093/molbev/
    msv080; pmid: 25839188

  17. M. L. Vidoz, E. Loreti, A. Mensuali, A. Alpi, P. Perata, Hormonal
    interplay during adventitious root formation in flooded tomato
    plants.Plant J. 63 , 551–562 (2010). doi:10.1111/j.1365-
    313X.2010.04262.x; pmid: 20497380

  18. S. Kumar, G. Stecher, M. Suleski, S. B. Hedges, TimeTree:
    A resource for timelines, timetrees, and divergence times.


Mol. Biol. Evol. 34 , 1812–1819 (2017). doi:10.1093/molbev/
msx116; pmid: 28387841


  1. P. Sukumar, G. S. Maloney, G. K. Muday, Localized induction
    of the ATP-binding cassette B19 auxin transporter enhances
    adventitious root formation inArabidopsis.Plant Physiol.
    162 , 1392–1405 (2013). doi:10.1104/pp.113.217174;
    pmid: 23677937

  2. C. Sorinet al., Auxin and light control of adventitious rooting in
    Arabidopsisrequire ARGONAUTE1.Plant Cell 17 , 1343– 1359
    (2005). doi:10.1105/tpc.105.031625; pmid: 15829601

  3. C. W. Melnyket al., Transcriptome dynamics atArabidopsis
    graft junctions reveal an intertissue recognition mechanism
    that activates vascular regeneration.Proc. Natl. Acad. Sci. U.S.A.
    115 , E2447–E2456 (2018). doi:10.1073/pnas.1718263115;
    pmid: 29440499

  4. A. Hendelmanet al., Conserved pleiotropy of an ancient plant
    homeobox gene uncovered by cis-regulatory dissection.Cell
    184 , 1724–1739.e16 (2021). doi:10.1016/j.cell.2021.02.001;
    pmid: 33667348

  5. L. Serrano-Ronet al., Reconstruction of lateral root formation
    through single-cell RNA sequencing reveals order of tissue
    initiation.Mol. Plant 14 , 1362–1378 (2021). pmid: 34062316

  6. T. Soyano, Y. Shimoda, M. Kawaguchi, M. Hayashi, A shared
    gene drives lateral root development and root nodule
    symbiosis pathways inLotus.Science 366 , 1021–1023 (2019).
    doi:10.1126/science.aax2153; pmid: 31754003

  7. K. Schiesslet al., NODULE INCEPTION recruits the lateral
    root develop4mental program for symbiotic nodule
    organogenesis inMedicago truncatula.Curr. Biol. 29 ,
    3657 – 3668.e5 (2019). doi:10.1016/j.cub.2019.09.005;
    pmid: 31543454


ACKNOWLEDGMENTS
We thank T. Beeckman, Y. Eshed, Z. Lippman, and S. Savaldi-
Goldstein for comments and discussions; M. De Martino for setting
up the CRISPR system; I. Pri-Tal for tissue culture work; O. Roth
for assistance in etiolated seedlings assay; and M. Chemla for
assistance in library preparation.Funding:I.E. is supported by a
Howard Hughes Medical Institute International Research Scholar
grant (grant no. 55008730) and the Israeli Science Foundation
(grant no. ISF966/17). A.H. is supported by National Science
Foundation grant Plant Genome Research Program grant IOS-
1546837 to Z.B.L.Author contributions:M.O., N.G.-Y., and I.E.
conceived and designed the study and performed the experiments.
C.Y. performed the shoot-borne root quantification and lateral root
RNA-Seq assay. A.H. performed in situ hybridizations. E.S.
performed potato transformation. I.E., N.G.-Y., and M.O. wrote the
manuscript.Competing interests:The authors declare no
competing interests.Data and materials availability:Raw and
processed data are available at the Gene Expression Omnibus
(GEO; single-cell data: GSE159055; lateral root transcriptome data:
GSE159050). All other data are available in the main paper or the
supplementary materials.

SUPPLEMENTARY MATERIALS
science.org/doi/10.1126/science.abf4368
Materials and Methods
Figs. S1 to S14
References ( 47 – 68 )
Tables S1 to S6
MDAR Reproducibility Checklist

2 November 2020; resubmitted 17 October 2021
Accepted 13 January 2022
10.1126/science.abf4368

Omaryet al.,Science 375 , eabf4368 (2022) 4 March 2022 7of7


RESEARCH | RESEARCH ARTICLE

Free download pdf