DOI: 10.1242/dev.127.23.5157. <i>PIN-FORMED 1</i> regulates cell fate at the periphery of the shoot apical meristem

PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem

10.1242/dev.127.23.5157

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT The process of organ positioning has been addressed, using the pin-formed 1 (pin1) mutant as a tool. PIN1 is a transmembrane protein involved in auxin transport in Arabidopsis. Loss of function severely affects organ initiation, and pin1 mutants are characterised by an inflorescence meristem that does not initiate any flowers, resulting in the formation of a naked inflorescence stem. This phenotype, combined with the proposed role of PIN1 in hormone transport, makes the mutant an ideal tool to study organ formation and phyllotaxis, and here we present a detailed analysis of the molecular modifications at the shoot apex caused by the mutation. We show that meristem structure and function are not severely affected in the mutant. Major alterations, however, are observed at the periphery of the pin1 meristem, where organ initiation should occur. Although two very early markers of organ initiation, LEAFY and AINTEGUMENTA, are expressed at the periphery of the mutant meristem, the cells are not recruited into distinct primordia. Instead a ring-like domain expressing those primordium specific genes is observed around the meristem. This ring-like domain also expresses a boundary marker, CUP-SHAPED COTYLEDON 2, involved in organ separation, showing that the zone at the meristem periphery has a hybrid identity. This implies that PIN1 is not only involved in organ outgrowth, but that it is also necessary for organ separation and positioning. A model is presented in which PIN1 and the local distribution of auxin control phyllotaxis.

Bibliography

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(23), 5157â5165.

Authors 5

Teva Vernoux (first)
Jocelyne Kronenberger (additional)
Olivier Grandjean (additional)
Patrick Laufs (additional)
Jan Traas (additional)

References 47 Referenced 244

10.1105/tpc.9.6.841 / Plant Cell / Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant by Aida (1997)
10.1242/dev.126.8.1563 / Development / Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes by Aida (1999)
{'key': '2023030307464920600_', 'first-page': '1194', 'article-title': 'In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants', 'volume': '316', 'author': 'Bechtold', 'year': '1993', 'journal-title': 'C. R. Acad. Sci. Life Sciences'} / C. R. Acad. Sci. Life Sciences / In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants by Bechtold (1993)
10.1046/j.1365-313X.1995.8040505.x / Plant J / Morphogenesis in pinoid mutants of Arabidopsis thaliana by Bennett (1995)
{'key': '2023030307464920600_', 'first-page': '1188', 'article-title': 'A binary vector based on basta resistance for in planta transformation of Arabidopsis thaliana', 'volume': '316', 'author': 'Bouchez', 'year': '1993', 'journal-title': 'C. R. Acad. Sci. Life Sciences'} / C. R. Acad. Sci. Life Sciences / A binary vector based on basta resistance for in planta transformation of Arabidopsis thaliana by Bouchez (1993)
10.1016/S1360-1385(00)01569-7 / Trends Plant Sci / Formation and maintenance of the shoot apical meristem by Bowman (2000)
10.1073/pnas.95.25.15112 / Proc. Natl. Acad. Sci. USA / The Arabidopsis thaliana AGRAVITROPIC1 gene encodes a component of the polar auxin-transport efflux carrier by Chen (1998)
10.1016/S0092-8674(00)80682-0 / Cell / Regulation of auxin response by the protein kinase PINOID by Christensen (2000)
10.1016/S0092-8674(00)80239-1 / Cell / The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis by Clark (1997)
{'key': '2023030307464920600_', 'first-page': '155', 'article-title': 'AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth', 'volume': '8', 'author': 'Elliott', 'year': '1996', 'journal-title': 'Plant Cell'} / Plant Cell / AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth by Elliott (1996)
10.1126/science.283.5409.1911 / Science / Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot system by Fletcher (1999)
10.1126/science.282.5397.2226 / Science / Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue by Gälweiler (1998)
10.1016/0092-8674(94)90178-3 / Cell / Regulation of the Arabidopsis floral homeotic gene APETALA1 by Gustafson-Brown (1994)
10.1242/dev.125.5.879 / Development / Auxin-induced developmental patterns in Brassica juncea embryos by Hadfi (1998)
10.1093/emboj/17.5.1405 / EMBO J / The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development by Hardtke (1998)
10.1242/dev.124.19.3845 / Development / Floral determination and expression of floral regulatory genes in Arabidopsis by Hempel (1997)
10.1093/pcp/41.1.60 / Plant Cell Physiol / Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana by Ishida (2000)
10.1016/0092-8674(92)90144-2 / Cell / The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS-box and is expressed in petals and stamens by Jack (1992)
{'key': '2023030307464920600_', 'volume-title': 'In situ hybridizationin plants. In Molecular Plant Pathology: a Practical Approach', 'author': 'Jackson', 'year': '1991'} / In situ hybridizationin plants. In Molecular Plant Pathology: a Practical Approach by Jackson (1991)
10.1105/tpc.11.10.1925 / Plant Cell / The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase by Jeong (1999)
10.1002/j.1460-2075.1987.tb02730.x / EMBO J / GUS fusions: β-glucoronidase as a sensitive and versatile gene marker in higher plants by Jefferson (1987)
{'key': '2023030307464920600_', 'first-page': '137', 'article-title': 'The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophytic development is related to the floral homeotic gene APETALA2', 'volume': '8', 'author': 'Klucher', 'year': '1996', 'journal-title': 'Plant Cell'} / Plant Cell / The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophytic development is related to the floral homeotic gene APETALA2 by Klucher (1996)
10.1002/(SICI)1520-6408(1999)25:3<224::AID-DVG5>3.0.CO;2-Y / Dev. Genet / Ectopic expression of AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs by Krizek (1999)
10.1242/dev.125.7.1253 / Development / MGOUN1 and MGOUN2: two genes required for primordium initiation at the shoot apical and floral meristem in Arabidopsis thaliana by Laufs (1998)
10.1016/S1369-5266(99)80009-0 / Curr. Opin. Plant Biol / Shoot meristem formation and maintenance by Lenhard (1999)
10.2307/3869805 / Plant Cell / Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis by Liu (1993)
10.1038/379066a0 / Nature / A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis by Long (1996)
10.1101/gad.12.14.2175 / Genes Dev / EIR1, a root specific protein involved in auxin transport, is required for root gravitropism in Arabidopsis thaliana by Luschnig (1998)
{'key': '2023030307464920600_', 'article-title': 'The shoot Apical Meristem', 'volume-title': 'Cambridge University Press, Cambridge', 'author': 'Lyndon', 'year': '1998'} / Cambridge University Press, Cambridge / The shoot Apical Meristem by Lyndon (1998)
10.1038/360273a0 / Nature / Molecular characterization of the Arabidopsis floral homeotic gene APETALA1 by Mandel (1992)
10.1016/S0092-8674(00)81703-1 / Cell / Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem by Mayer (1998)
10.1073/pnas.97.2.942 / Proc. Natl. Acad. Sci. USA / Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis by Mizukami (2000)
{'key': '2023030307464920600_', 'first-page': '6903', 'volume': '17', 'author': 'Müller', 'year': '1998', 'journal-title': 'AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J'} / AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J by Müller (1998)
10.1016/S1369-5266(99)00036-9 / Curr. Opin. Plant Biol / Three ways to learn the ABCs by Ng (2000)
10.2307/3869249 / Plant Cell / Requirment of the auxin polar trasnport system in early stages of Arabidopsis floral bud formation by Okada (1991)
10.1038/26903 / Nature / A genetic framework for floral patterning by Parcy (1998)
{'key': '2023030307464920600_', 'first-page': '229', 'article-title': 'Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization', 'volume': '200', 'author': 'Prezmeck', 'year': '1996', 'journal-title': 'Planta'} / Planta / Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization by Prezmeck (1996)
10.1105/tpc.12.4.507 / Plant Cell / Auxin regulates the initiation of and radial position of plant lateral organs by Reinhardt (2000)
10.1016/S0092-8674(00)81535-4 / Cell / An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root by Sabatini (1999)
10.1007/BF00203594 / Planta / Use of two dimensional protein pattern analysis for the characterization of Arabidopsis thaliana mutants by Santoni (1994)
10.1016/S0092-8674(00)80700-X / Cell / The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes by Schoof (2000)
10.1038/384059a0 / Nature / Activation of floral meristem identity genes in Arabidopsis by Simon (1996)
10.1046/j.1365-313X.1995.07050785.x / Plant J / A mutation affecting etiolation and cell elongation in Nicotiana plumbaginifolia causes abnormal division plane alignment and pattern formation in the root meristem by Traas (1995)
{'key': '2023030307464920600_', 'first-page': '1111', 'volume': '39', 'author': 'Utsuno', 'year': '1998', 'journal-title': 'AGR, an Agravitropic locus of Arabidopsis thaliana encodes a novel membrane-protein family member. Plant Cell Physiol'} / AGR, an Agravitropic locus of Arabidopsis thaliana encodes a novel membrane-protein family member. Plant Cell Physiol by Utsuno (1998)
{'key': '2023030307464920600_', 'first-page': '582', 'article-title': 'Transcriptional activation of APETALA1 by LEAFY', 'volume': '285', 'author': 'Wagner', 'year': '1999', 'journal-title': 'Nature'} / Nature / Transcriptional activation of APETALA1 by LEAFY by Wagner (1999)
10.1038/377495a0 / Nature / A developmental switch sufficient for flower initiation in diverse plants by Weigel (1995)
10.1016/0092-8674(92)90295-N / Cell / LEAFY controls floral meristem identity in Arabidopsis by Weigel (1992)

Dates

Type	When
Created	4 years, 4 months ago (April 26, 2021, 12:26 a.m.)
Deposited	2 years, 5 months ago (March 3, 2023, 2:47 a.m.)
Indexed	3 weeks, 3 days ago (Aug. 6, 2025, 8:08 a.m.)
Issued	24 years, 8 months ago (Dec. 1, 2000)
Published	24 years, 8 months ago (Dec. 1, 2000)
Published Online	24 years, 8 months ago (Dec. 1, 2000)
Published Print	24 years, 8 months ago (Dec. 1, 2000)

Funders 0

None

BibTeX

@article{Vernoux_2000, title={PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem}, volume={127}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.127.23.5157}, DOI={10.1242/dev.127.23.5157}, number={23}, journal={Development}, publisher={The Company of Biologists}, author={Vernoux, Teva and Kronenberger, Jocelyne and Grandjean, Olivier and Laufs, Patrick and Traas, Jan}, year={2000}, month=dec, pages={5157–5165} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        6
      ]
    ],
    "date-time": "2025-08-06T12:08:39Z",
    "timestamp": 1754482119172
  },
  "reference-count": 47,
  "publisher": "The Company of Biologists",
  "issue": "23",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2000,
            12,
            1
          ]
        ],
        "date-time": "2000-12-01T00:00:00Z",
        "timestamp": 975628800000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://www.biologists.com/user-licence-1-1/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>The process of organ positioning has been addressed, using the pin-formed 1 (pin1) mutant as a tool. PIN1 is a transmembrane protein involved in auxin transport in Arabidopsis. Loss of function severely affects organ initiation, and pin1 mutants are characterised by an inflorescence meristem that does not initiate any flowers, resulting in the formation of a naked inflorescence stem. This phenotype, combined with the proposed role of PIN1 in hormone transport, makes the mutant an ideal tool to study organ formation and phyllotaxis, and here we present a detailed analysis of the molecular modifications at the shoot apex caused by the mutation. We show that meristem structure and function are not severely affected in the mutant. Major alterations, however, are observed at the periphery of the pin1 meristem, where organ initiation should occur. Although two very early markers of organ initiation, LEAFY and AINTEGUMENTA, are expressed at the periphery of the mutant meristem, the cells are not recruited into distinct primordia. Instead a ring-like domain expressing those primordium specific genes is observed around the meristem. This ring-like domain also expresses a boundary marker, CUP-SHAPED COTYLEDON 2, involved in organ separation, showing that the zone at the meristem periphery has a hybrid identity. This implies that PIN1 is not only involved in organ outgrowth, but that it is also necessary for organ separation and positioning. A model is presented in which PIN1 and the local distribution of auxin control phyllotaxis.</jats:p>",
  "DOI": "10.1242/dev.127.23.5157",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T04:26:20Z",
    "timestamp": 1619411180000
  },
  "page": "5157-5165",
  "source": "Crossref",
  "is-referenced-by-count": 244,
  "title": "<i>PIN-FORMED 1</i> regulates cell fate at the periphery of the shoot apical meristem",
  "prefix": "10.1242",
  "volume": "127",
  "author": [
    {
      "given": "Teva",
      "family": "Vernoux",
      "sequence": "first",
      "affiliation": [
        {
          "name": "INRA, Laboratoire de Biologie Cellulaire, Route de Saint Cyr, 78026 Versailles cedex, France"
        }
      ]
    },
    {
      "given": "Jocelyne",
      "family": "Kronenberger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "INRA, Laboratoire de Biologie Cellulaire, Route de Saint Cyr, 78026 Versailles cedex, France"
        }
      ]
    },
    {
      "given": "Olivier",
      "family": "Grandjean",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "INRA, Laboratoire de Biologie Cellulaire, Route de Saint Cyr, 78026 Versailles cedex, France"
        }
      ]
    },
    {
      "given": "Patrick",
      "family": "Laufs",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "INRA, Laboratoire de Biologie Cellulaire, Route de Saint Cyr, 78026 Versailles cedex, France"
        }
      ]
    },
    {
      "given": "Jan",
      "family": "Traas",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        2000,
        12,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "841",
      "DOI": "10.1105/tpc.9.6.841",
      "article-title": "Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant",
      "volume": "9",
      "author": "Aida",
      "year": "1997",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "1563",
      "DOI": "10.1242/dev.126.8.1563",
      "article-title": "Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes",
      "volume": "126",
      "author": "Aida",
      "year": "1999",
      "journal-title": "Development"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "1194",
      "article-title": "In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants",
      "volume": "316",
      "author": "Bechtold",
      "year": "1993",
      "journal-title": "C. R. Acad. Sci. Life Sciences"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "505",
      "DOI": "10.1046/j.1365-313X.1995.8040505.x",
      "article-title": "Morphogenesis in pinoid mutants of Arabidopsis thaliana",
      "volume": "8",
      "author": "Bennett",
      "year": "1995",
      "journal-title": "Plant J"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "1188",
      "article-title": "A binary vector based on basta resistance for in planta transformation of Arabidopsis thaliana",
      "volume": "316",
      "author": "Bouchez",
      "year": "1993",
      "journal-title": "C. R. Acad. Sci. Life Sciences"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "110",
      "DOI": "10.1016/S1360-1385(00)01569-7",
      "article-title": "Formation and maintenance of the shoot apical meristem",
      "volume": "5",
      "author": "Bowman",
      "year": "2000",
      "journal-title": "Trends Plant Sci"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "15112",
      "DOI": "10.1073/pnas.95.25.15112",
      "article-title": "The Arabidopsis thaliana AGRAVITROPIC1 gene encodes a component of the polar auxin-transport efflux carrier",
      "volume": "95",
      "author": "Chen",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "469",
      "DOI": "10.1016/S0092-8674(00)80682-0",
      "article-title": "Regulation of auxin response by the protein kinase PINOID",
      "volume": "100",
      "author": "Christensen",
      "year": "2000",
      "journal-title": "Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "575",
      "DOI": "10.1016/S0092-8674(00)80239-1",
      "article-title": "The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis",
      "volume": "89",
      "author": "Clark",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "155",
      "article-title": "AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth",
      "volume": "8",
      "author": "Elliott",
      "year": "1996",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "1911",
      "DOI": "10.1126/science.283.5409.1911",
      "article-title": "Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot system",
      "volume": "283",
      "author": "Fletcher",
      "year": "1999",
      "journal-title": "Science"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "2226",
      "DOI": "10.1126/science.282.5397.2226",
      "article-title": "Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue",
      "volume": "282",
      "author": "G\u00e4lweiler",
      "year": "1998",
      "journal-title": "Science"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "131",
      "DOI": "10.1016/0092-8674(94)90178-3",
      "article-title": "Regulation of the Arabidopsis floral homeotic gene APETALA1",
      "volume": "76",
      "author": "Gustafson-Brown",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "879",
      "DOI": "10.1242/dev.125.5.879",
      "article-title": "Auxin-induced developmental patterns in Brassica juncea embryos",
      "volume": "125",
      "author": "Hadfi",
      "year": "1998",
      "journal-title": "Development"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "1405",
      "DOI": "10.1093/emboj/17.5.1405",
      "article-title": "The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development",
      "volume": "17",
      "author": "Hardtke",
      "year": "1998",
      "journal-title": "EMBO J"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "3845",
      "DOI": "10.1242/dev.124.19.3845",
      "article-title": "Floral determination and expression of floral regulatory genes in Arabidopsis",
      "volume": "124",
      "author": "Hempel",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "60",
      "DOI": "10.1093/pcp/41.1.60",
      "article-title": "Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana",
      "volume": "41",
      "author": "Ishida",
      "year": "2000",
      "journal-title": "Plant Cell Physiol"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "683",
      "DOI": "10.1016/0092-8674(92)90144-2",
      "article-title": "The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS-box and is expressed in petals and stamens",
      "volume": "68",
      "author": "Jack",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2023030307464920600_",
      "volume-title": "In situ hybridizationin plants. In Molecular Plant Pathology: a Practical Approach",
      "author": "Jackson",
      "year": "1991"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "1925",
      "DOI": "10.1105/tpc.11.10.1925",
      "article-title": "The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase",
      "volume": "11",
      "author": "Jeong",
      "year": "1999",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "3901",
      "DOI": "10.1002/j.1460-2075.1987.tb02730.x",
      "article-title": "GUS fusions: \u03b2-glucoronidase as a sensitive and versatile gene marker in higher plants",
      "volume": "6",
      "author": "Jefferson",
      "year": "1987",
      "journal-title": "EMBO J"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "137",
      "article-title": "The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophytic development is related to the floral homeotic gene APETALA2",
      "volume": "8",
      "author": "Klucher",
      "year": "1996",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "224",
      "DOI": "10.1002/(SICI)1520-6408(1999)25:3&lt;224::AID-DVG5&gt;3.0.CO;2-Y",
      "article-title": "Ectopic expression of AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs",
      "volume": "25",
      "author": "Krizek",
      "year": "1999",
      "journal-title": "Dev. Genet"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "1253",
      "DOI": "10.1242/dev.125.7.1253",
      "article-title": "MGOUN1 and MGOUN2: two genes required for primordium initiation at the shoot apical and floral meristem in Arabidopsis thaliana",
      "volume": "125",
      "author": "Laufs",
      "year": "1998",
      "journal-title": "Development"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "44",
      "DOI": "10.1016/S1369-5266(99)80009-0",
      "article-title": "Shoot meristem formation and maintenance",
      "volume": "2",
      "author": "Lenhard",
      "year": "1999",
      "journal-title": "Curr. Opin. Plant Biol"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "621",
      "DOI": "10.2307/3869805",
      "article-title": "Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis",
      "volume": "5",
      "author": "Liu",
      "year": "1993",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "66",
      "DOI": "10.1038/379066a0",
      "article-title": "A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis",
      "volume": "379",
      "author": "Long",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "2175",
      "DOI": "10.1101/gad.12.14.2175",
      "article-title": "EIR1, a root specific protein involved in auxin transport, is required for root gravitropism in Arabidopsis thaliana",
      "volume": "12",
      "author": "Luschnig",
      "year": "1998",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023030307464920600_",
      "article-title": "The shoot Apical Meristem",
      "volume-title": "Cambridge University Press, Cambridge",
      "author": "Lyndon",
      "year": "1998"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "273",
      "DOI": "10.1038/360273a0",
      "article-title": "Molecular characterization of the Arabidopsis floral homeotic gene APETALA1",
      "volume": "360",
      "author": "Mandel",
      "year": "1992",
      "journal-title": "Nature"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "805",
      "DOI": "10.1016/S0092-8674(00)81703-1",
      "article-title": "Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem",
      "volume": "95",
      "author": "Mayer",
      "year": "1998",
      "journal-title": "Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "942",
      "DOI": "10.1073/pnas.97.2.942",
      "article-title": "Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis",
      "volume": "97",
      "author": "Mizukami",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "6903",
      "volume": "17",
      "author": "M\u00fcller",
      "year": "1998",
      "journal-title": "AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "47",
      "DOI": "10.1016/S1369-5266(99)00036-9",
      "article-title": "Three ways to learn the ABCs",
      "volume": "3",
      "author": "Ng",
      "year": "2000",
      "journal-title": "Curr. Opin. Plant Biol"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "677",
      "DOI": "10.2307/3869249",
      "article-title": "Requirment of the auxin polar trasnport system in early stages of Arabidopsis floral bud formation",
      "volume": "3",
      "author": "Okada",
      "year": "1991",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "561",
      "DOI": "10.1038/26903",
      "article-title": "A genetic framework for floral patterning",
      "volume": "395",
      "author": "Parcy",
      "year": "1998",
      "journal-title": "Nature"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "229",
      "article-title": "Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization",
      "volume": "200",
      "author": "Prezmeck",
      "year": "1996",
      "journal-title": "Planta"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "507",
      "DOI": "10.1105/tpc.12.4.507",
      "article-title": "Auxin regulates the initiation of and radial position of plant lateral organs",
      "volume": "12",
      "author": "Reinhardt",
      "year": "2000",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "463",
      "DOI": "10.1016/S0092-8674(00)81535-4",
      "article-title": "An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root",
      "volume": "99",
      "author": "Sabatini",
      "year": "1999",
      "journal-title": "Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "557",
      "DOI": "10.1007/BF00203594",
      "article-title": "Use of two dimensional protein pattern analysis for the characterization of Arabidopsis thaliana mutants",
      "volume": "192",
      "author": "Santoni",
      "year": "1994",
      "journal-title": "Planta"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "635",
      "DOI": "10.1016/S0092-8674(00)80700-X",
      "article-title": "The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes",
      "volume": "100",
      "author": "Schoof",
      "year": "2000",
      "journal-title": "Cell"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "59",
      "DOI": "10.1038/384059a0",
      "article-title": "Activation of floral meristem identity genes in Arabidopsis",
      "volume": "384",
      "author": "Simon",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "785",
      "DOI": "10.1046/j.1365-313X.1995.07050785.x",
      "article-title": "A mutation affecting etiolation and cell elongation in Nicotiana plumbaginifolia causes abnormal division plane alignment and pattern formation in the root meristem",
      "volume": "7",
      "author": "Traas",
      "year": "1995",
      "journal-title": "Plant J"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "1111",
      "volume": "39",
      "author": "Utsuno",
      "year": "1998",
      "journal-title": "AGR, an Agravitropic locus of Arabidopsis thaliana encodes a novel membrane-protein family member. Plant Cell Physiol"
    },
    {
      "key": "2023030307464920600_",
      "first-page": "582",
      "article-title": "Transcriptional activation of APETALA1 by LEAFY",
      "volume": "285",
      "author": "Wagner",
      "year": "1999",
      "journal-title": "Nature"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "495",
      "DOI": "10.1038/377495a0",
      "article-title": "A developmental switch sufficient for flower initiation in diverse plants",
      "volume": "377",
      "author": "Weigel",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2023030307464920600_",
      "doi-asserted-by": "publisher",
      "first-page": "843",
      "DOI": "10.1016/0092-8674(92)90295-N",
      "article-title": "LEAFY controls floral meristem identity in Arabidopsis",
      "volume": "69",
      "author": "Weigel",
      "year": "1992",
      "journal-title": "Cell"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/127/23/5157/2590430/develop_127_23_5157.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/127/23/5157/2590430/develop_127_23_5157.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        3,
        3
      ]
    ],
    "date-time": "2023-03-03T07:47:38Z",
    "timestamp": 1677829658000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/127/23/5157/41117/PIN-FORMED-1-regulates-cell-fate-at-the-periphery"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        12,
        1
      ]
    ]
  },
  "references-count": 47,
  "journal-issue": {
    "issue": "23",
    "published-print": {
      "date-parts": [
        [
          2000,
          12,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.127.23.5157",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2000,
        12,
        1
      ]
    ]
  }
}