CoChat
Sign Up
Cited by 26Plant Molecular Biology ResearchPlant Parasitism and ResistancePlant nutrient uptake and metabolism

The ATP-Binding Cassette Transporter ABCB19 Regulates Postembryonic Organ Separation in Arabidopsis

Open access
Zhao, Hongtao, Liu, Lei, Mo, Huixian, Qian, Litao, Cao, Ying, Cui, Sujuan, Li, Xia, Ma, Ligeng·2013·PLoS ONE
DOI 10.1371/journal.pone.0060809PMC PMC3613370
Open this paper in CoChat — free accountOpen PDF

Abstract

The phytohormone auxin plays a critical role in plant development, including embryogenesis, organogenesis, tropism, apical dominance and in cell growth, division, and expansion. In these processes, the concentration gradient of auxin, which is established by polar auxin transport mediated by PIN-FORMED (PIN) proteins and several ATP-binding cassette/multi-drug resistance/P-glycoprotein (ABCB/MDR/PGP) transporters, is a crucial signal. Here, we characterized the function of ABCB19 in the control of Arabidopsis organ boundary development. We identified a new abcb19 allele, abcb19-5, which showed stem-cauline leaf and stem-pedicel fusion defects. By virtue of the DII-VENUS marker, the auxin level was found to be increased at the organ boundary region in the inflorescence apex. The expression of CUP-SHAPED COTYLEDON2 (CUC2) was decreased, while no obvious change in the expression of CUC3 was observed, in abcb19. In addition, the fusion defects were greatly enhanced in cuc3 abcb19-5, which was reminiscent of cuc2 cuc3. We also found that some other organ boundary genes, such as LOF1/2 were down-regulated in abcb19. Together, these results reveal a new aspect of auxin transporter ABCB19 function, which is largely dependent on the positive regulation of organ boundary genes CUC2 and LOFs at the postembryonic organ boundary.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0060809

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • abcb19 mutants displayed increased auxin concentrations in boundaries of the inflorescence meristem, whereas CUC2 and LOF1 expression was decreased.

    “abcb19 mutants displayed increased auxin concentrations in boundaries of the inflorescence meristem, whereas CUC2 and LOF1 expression was found to be decreased (Zhao et al., 2013).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Zhao et al., 2013

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 47

  1. [1]Rast MI, Simon R (2008) The meristem-to-organ boundary: more than an extremity of anything. Curr Opin Genet Dev 18: 287– 294. 18590819
  2. [2]Aida M, Tasaka M (2006) Genetic control of shoot organ boundaries. Curr Opin Plant Biol 9: 72– 77. 16337829
  3. [3]Kwiatkowska D, Dumais J (2003) Growth and morphogenesis at the vegetative shoot apex of Anagallis arvensis L. J Exp Bot. 54: 1585– 1595. 12730267
  4. [4]Kwiatkowska D (2004) Surface growth at the reproductive shoot apex of Arabidopsis thaliana pin-formed 1 and wild type. J Exp Bot 55: 1021– 1032. 15020634
  5. [5]Breuil-Broyer S, Morel P, de Almeida-Engler J, Coustham V, Negrutiu I, et al (2004) High-resolution boundary analysis during Arabidopsis thaliana flower development. Plant J 38: 182– 192. 15053771
  6. [6]Lee DK, Geisler M, Springer PS (2009) LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development 136: 2423– 2432. 19542355
  7. [8]Hibara K, Karim MR, Takada S, Taoka K, Furutani M, et al (2006) Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18: 2946– 2957. 17122068 PMC1693926
  8. [9]Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC (2003) The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15: 1563– 1577. 12837947 PMC165401
  9. [11]Greb T, Clarenz O, Schafer E, Muller D, Herrero R, et al (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17: 1175– 1187. 12730136 PMC196050
  10. [12]Raman S, Greb T, Peaucelle A, Blein T, Laufs P, et al (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55: 65– 76. 18346190
  11. [13]Ha CM, Jun JH, Nam HG, Fletcher JC (2007) BLADE-ON-PETIOLE 1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 19: 1809– 1825. 17601823 PMC1955725
  12. [14]Norberg M, Holmlund M, Nilsson O (2005) The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 132: 2203– 2213. 15800002
  13. [16]Shuai B, Reynaga-Pena CG, Springer PS (2002) The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol 129: 747– 761. 12068116 PMC161698
  14. [17]Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, et al (2012) Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci U S A 109: 21146– 21151. 23213252 PMC3529045
  15. [18]Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127: 5157– 5165. 11060241
  16. [19]Aida M, Vernoux T, Furutani M, Traas J, Tasaka M (2002) Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129: 3965– 3974. 12163400
  17. [20]Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, et al (2004) PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131: 5021– 5030. 15371311
  18. [21]Treml BS, Winderl S, Radykewicz R, Herz M, Schweizer G, et al.. (2005) The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development. 2005/08/19 ed. pp. 4063–4074. 16107478
  19. [23]Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, et al (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226– 2230. 9856939
  20. [24]Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13: 2441– 2454. 11701880 PMC139463
  21. [25]Cho M, Lee SH, Cho HT (2007) P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19: 3930– 3943. 18156217 PMC2217643
  22. [26]Lewis DR, Miller ND, Splitt BL, Wu GS, Spalding EP (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis Multidrug Resistance-Like ABC transporter genes. Plant Cell 19: 1838– 1850. 17557805 PMC1955737
  23. [27]Reinhardt D (2005) Phyllotaxis--a new chapter in an old tale about beauty and magic numbers. Curr Opin Plant Biol 8: 487– 493. 16054863
  24. [28]Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, et al (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426: 255– 260. 14628043
  25. [29]Lewis DR, Miller ND, Splitt BL, Wu G, Spalding EP (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 19: 1838– 1850. 17557805 PMC1955737
  26. [30]Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580: 1094– 1102. 16359667
  27. [31]Wu G, Lewis DR, Spalding EP (2007) Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. Plant Cell 19: 1826– 1837. 17557807 PMC1955722
  28. [32]Wu G, Cameron JN, Ljung K, Spalding EP (2010) A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome 1 and phytochrome B. Plant J. 62: 179– 191. 20088903
  29. [33]Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, et al (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19: 131– 147. 17237354 PMC1820964
  30. [34]Mravec J, Kubes M, Bielach A, Gaykova V, Petrasek J, et al (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135: 3345– 3354. 18787070
  31. [35]Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, et al (2009) ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J 57: 27– 44. 18774968
  32. [36]Geisler M, Kolukisaoglu HU, Bouchard R, Billion K, Berger J, et al (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol Biol Cell 14: 4238– 4249. 14517332 PMC207015
  33. [37]Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, et al (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 281: 30603– 30612. 16887800
  34. [38]Wu G, Otegui MS, Spalding EP (2010) The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. Plant Cell 22: 3295– 3304. 20971896 PMC2990139
  35. [39]Lewis DR, Wu G, Ljung K, Spalding EP (2009) Auxin transport into cotyledons and cotyledon growth depend similarly on the ABCB19 Multidrug Resistance-like transporter. Plant J 60: 91– 101. 19508431
  36. [40]Lin R, Wang H (2005) Two homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. Plant Physiol 138: 949– 964. 15908594 PMC1150410
  37. [41]Rojas-Pierce M, Titapiwatanakun B, Sohn EJ, Fang F, Larive CK, et al (2007) Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem Biol 14: 1366– 1376. 18096505
  38. [42]Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, et al (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 9: e1001076. 21666806 PMC3110179
  39. [43]Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, et al (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7. PMC3167386 21734647
  40. [44]Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, et al (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482: 103– U132. 22246322
  41. [46]Kwon CS, Hibara K, Pfluger J, Bezhani S, Metha H, et al (2006) A role for chromatin remodeling in regulation of CUC gene expression in the Arabidopsis cotyledon boundary. Development 133: 3223– 3230. 16854978
  42. [47]Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, et al (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124: 4481– 4491. 9409666
  43. [48]Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17: 2899– 2910. 16199616 PMC1276018
  44. [49]Hunter C, Willmann MR, Wu G, Yoshikawa M, de la Luz Gutierrez-Nava M, et al (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133: 2973– 2981. 16818444 PMC1610108
  45. [50]Aoyama T, Chua NH (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11: 605– 612. 9107046
  46. [51]Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735– 743. 10069079
  47. [52]Cao Y, Dai Y, Cui S, Ma L (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20: 2586– 2602. 18849490 PMC2590739

Cited by

Sorted by citations

Authors
Zhao, H., Liu, L., Mo, H., Qian, L., Cao, Y., Cui, S., Li, X., & Ma, L.
Affiliations
  • Chinese Academy of Sciences (CN)
  • Hebei Normal University (CN)
Corresponding author
Ma, Ligeng
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-04-01
Volume
8
Issue
4
Pages
e60809
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0060809
PMC
PMC3613370
OpenAlex
W1978863652
Cited by
26
References
4
Citations by year
2026: 2 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 4 · 2020: 3 · 2018: 1 · 2017: 5 · 2016: 1 · 2015: 3 · 2013: 1
FWCI
2.01
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Teva Pharmaceutical Industries
  • University of Pennsylvania
  • Chinese Academy of Sciences
  • Centre National de la Recherche Scientifique
  • Institut National de la Recherche Agronomique
  • Université Claude Bernard Lyon 1
  • National Key Research and Development Program of China (2012CB910900, 2012CB114200)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
Keywords
ABCB19, ABC transporters, auxin transport, CUC2, inflorescence, auxin gradients, Arabidopsis thaliana
MeSH terms
Alleles, Biological Transport, Indoleacetic Acids, Plant Growth Regulators, Seeds, Transcription Factors, Arabidopsis, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Plant Leaves, ATP-Binding Cassette Transporters, Plant Stems, Protein Isoforms, Arabidopsis Proteins, Plant Development

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review