Skip to main content
SpringerLink
Log in

Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum)

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

An Erratum to this article was published on 04 February 2004

Abstract

The goal of this study was to explore the impact of the plant growth regulator auxin on the development of compound leaves in pea. Wildtype (WT) plantlets, as well as those of two leaf mutants, acacia (tl) and tendrilled acacia (uni-tac) of pea (Pisum sativum L.), were grown on media containing the auxin-transport inhibitors 2,3,5-triiodobenzoic acid (TIBA), N-(1-naphthyl)phthalamic acid (NPA), or the auxin antagonist, p-chlorophenoxyisobutyric acid (PCIB). The resulting plantlets were carefully analyzed morphologically, by scanning electron microscopy and for Uni gene expression using quantitative reverse transcription–polymerase chain reaction. Auxin transport was measured in WT leaf parts using [14C]indole-3-acetic acid. Relative Uni gene expression was determined in shoot tips of a range of leaf-form mutants. Morphological abnormalities were observed for all genotypes examined. The terminal tendrils on WT plants were converted to leaflets, stubs or were aborted. The number of pinna pairs produced on leaves was reduced, with the distal forms being eliminated before the proximal ones. Some leaves were converted to simple, including tri-and bilobed, forms. These treatments phenocopy the uni-tac and unifoliata (uni) mutants of pea. In the most extreme situations, leaf blades were completely lost leaving only a pair of stipules or scale leaves. Polar auxin transport was basipetal for all leaf parts. Uni gene expression in shoot tips was significantly reduced in 60 μM NPA and TIBA. Uni mRNA was more abundant in tl, af and af tl and reduced in the uni mutants compared to WT. These results indicate that an auxin gradient plays fundamental roles in controlling morphogenesis in the compound leaves of pea and specifically it: (i) is the driving force for leaf growth and pinna determination; (ii) is necessary for pinna initiation; and (iii) controls subsequent pinna development.

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

Fig. 1a–e.
Fig. 2a–n.
Fig. 3a–c.
Fig. 4a, b.
Fig. 5a–h.
Fig. 6a–f.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.

Similar content being viewed by others

Abbreviations

BAP:

N6-benzylaminopurine

4-Cl-IAA:

4-chloro-indole-3-acetic acid

IAA:

indole-3-acetic acid

MS:

Murashige and Skoog

NPA:

N-(1-naphthyl)phthalamic acid

PCIB:

p-chlorophenoxyisobutyric acid

RT–PCR:

reverse transcription–polymerase chain reaction

SEM:

scanning electron microscopy

TIBA:

2,3,5-triiodobenzoic acid

References

  • Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841–852

    CAS  PubMed  Google Scholar 

  • Blázquez MA (2000) Flower development pathways. J Cell Sci 113:3547–3548

    PubMed  Google Scholar 

  • Blázquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404:889–892

    PubMed  Google Scholar 

  • Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the Leafy promoter. Plant Cell 10:791–800

    PubMed  Google Scholar 

  • Busch MA, Bomblies K, Weigel D (1999) Activation of a floral homeotic gene in Arabidopsis. Science 285:585–587

    CAS  PubMed  Google Scholar 

  • Chen JG, Simomura S, Sitbon F, Sandberg G, Jones A (2001) The role of auxin-binding protein 1 in the expansion of tobacco leaf cells. Plant J 28:607–617

    Article  CAS  PubMed  Google Scholar 

  • DeMason DA, Schmidt RJ (2001) Roles of the Uni gene in shoot and leaf development of pea (Pisum sativum): phenotypic characterization and leaf development in the uni and uni-tac mutants. Int J Plant Sci 162:1033–1051

    Google Scholar 

  • DeMason DA, Villani PJ (2001) Genetic control of leaf development in pea (Pisum sativum). Int J Plant Sci 162:493–511

    CAS  Google Scholar 

  • Doerner P (2000) Root patterning: Does auxin provide positional cues? Curr Biol 10: R201–R203

    CAS  PubMed  Google Scholar 

  • Friml J (2003) Auxin transport — shaping the plant. Cur Opin Plant Biol 6:7–12

    CAS  Google Scholar 

  • Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–673

    CAS  PubMed  Google Scholar 

  • Gälweiler L, Guan CH, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    PubMed  Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Google Scholar 

  • Gocal GFW, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish W, Dennis ES, Weigel D, King RW (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127:1682–1693

    CAS  PubMed  Google Scholar 

  • Gould KS, Cutter EG, Young JPW (1986) Morphogenesis of the compound leaf in three genotypes of the pea, Pisum sativum. Can J Bot 64:1268–1276

    Google Scholar 

  • Gould KS, Cutter EG, Young JPW, Charlton WA (1987) Positional differences in size, morphology and in vitro performance of pea axillary buds. Can J Bot 65:406–411

    Google Scholar 

  • Gould KS, Cutter EG, Young JPW (1991) Modification of pea leaf morphology by 2,3,5-triiodobenzoic acid. Bot Gaz 152:133–138

    CAS  Google Scholar 

  • Gourlay CW, Hofer JMI, Ellis THN (2000) Pea compound leaf architecture is regulated by interactions among the genes Unifoliata, Cochleata, Afila, and Tendril-less. Plant Cell 12:1279–1294

    Article  CAS  PubMed  Google Scholar 

  • Hagemann W, Gleissberg S (1996) Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst Evol 199:121–152

    Google Scholar 

  • Hamann T, U Mayer U, Jürgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126:1387–1395

    CAS  PubMed  Google Scholar 

  • Hamann T, Benkova E, Baurle T, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    CAS  PubMed  Google Scholar 

  • Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7:581–587

    CAS  PubMed  Google Scholar 

  • Lamprecht H (1933) Ein Unifoliata-type von Pisum mit gleichzeitiger Pistilloidie. Hereditas 18:56–64

    Google Scholar 

  • Lohmann JU, Hong R, Hobe M, Busch MA, Parcy F, Simon F, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803

    CAS  PubMed  Google Scholar 

  • Lu B, Villani PJ, Watson JC, DeMason DA, Cooke TJ (1996) The control of pinna morphology in wildtype and mutant leaves of the garden pea (Pisum sativum L). Int J Plant Sci 157:659–673

    Article  Google Scholar 

  • Magnus V, Ozga, JA, Reinecke DM, Pierson GL, Larue TA, Cohen JD, Brenner ML (1997) 4-chloroindole-3-acetic and indole-3-acetic acids in Pisum sativum. Phytochemistry 46:675–681

    Article  CAS  Google Scholar 

  • Marx GA (1986) Tendrilled acacia (tac): an allele at the Uni locus. Pisum Newslett 18:49–52

    Google Scholar 

  • Marx GA (1987) A suite of mutants that modify pattern formation in pea leaves. Plant Mol Biol Rep 5:311–335

    Google Scholar 

  • Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–2991

    CAS  PubMed  Google Scholar 

  • Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 313:1327–1339

    Article  Google Scholar 

  • McRae DH, Bonner J (1953) Chemical structure and antiauxin activity. Physiol Plant 6:485–510

    CAS  Google Scholar 

  • Muday GK, Murphy AS (2002) An emerging model of auxin transport regulation. Plant Cell 14:293–299

    CAS  PubMed  Google Scholar 

  • Nemhauser JL, Feldman LJ, Zambryski PC (2000) Auxin and Ettin in Arabidopsis gynoecium morphogenesis. Development 127:3877–3888

    CAS  PubMed  Google Scholar 

  • Ngo P, Ozga JA, Reinecke DM (2002) Specificity of auxin regulation of gibberellin 20-oxidase gene expression in pea pericarp. Plant Mol Biol 49:439–448

    Article  CAS  PubMed  Google Scholar 

  • O’Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982

    Article  CAS  PubMed  Google Scholar 

  • Okada K, Ueda J, Bell MK, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 11:1073–1080

    Google Scholar 

  • Ozga, JA, Reinecke DM (1999) Interactions of 4-chloroindole-3-acetic acid and gibberellins in early fruit development. Plant Growth Regul 27:33–38

    Article  CAS  Google Scholar 

  • Parcy F, Bomblies K, Weigel D (2002) Interaction of Leafy, Agamous and Terminal Flower in maintaining floral meristem identity in Arabidopsis. Development 129:2519–2527

    CAS  PubMed  Google Scholar 

  • Petrášek J, Černá A, Schwarzerová K, Elčkner M, Morris DA, Zažímalová E (2003) Do phytotropins inhibit auxin efflux my impairing vesicle traffic? Plant Physiol 131:254–263

    PubMed  Google Scholar 

  • Reinecke DM (1999) 4-Chloroindole-3-aceitc acid and plant growth. Plant Growth Reg 27: 3–13

    Article  CAS  Google Scholar 

  • Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518

    CAS  PubMed  Google Scholar 

  • Ross JJ, O’Neill DP, Smith JJ, Huub L, Kerckhoff J, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21:547–552

    CAS  PubMed  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    CAS  PubMed  Google Scholar 

  • Scheres B (2000) Non-linear signaling for pattern formation? Curr Opin Plant Biol 3:412–417

    Google Scholar 

  • Sessions A, Nemhauser JL, McCall A, Roe JL, Feldmann KA, Zambryski PC (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124:4481–4491

    CAS  PubMed  Google Scholar 

  • Sharma B (1972) “Tendrilled acacia”, a new mutation controlling tendril formation in Pisum sativum. Pisum Newslett 4:50

    Google Scholar 

  • Sharma B (1981) Genetic pathway of foliage development in Pisum sativum. Pulse Crops Newslett 1:56–57

    Google Scholar 

  • Sieburth LE (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol 121:1179–1190

    CAS  PubMed  Google Scholar 

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Gälweiler L, Palme K, Jürgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by Gnom ARF GEF. Science 286:316–318

    Google Scholar 

  • Stieger PA, Reinhardt D, Kuhlemeier C (2002) The auxin influx carrier is essential for correct leaf positioning. Plant J 32:509–517

    CAS  PubMed  Google Scholar 

  • Uggla C, Moritz T, Sandberg G, Sundberg C (1996) Auxin as a positional signal in pattern formation in plants. Proc Natl Acad Sci 93:9282–9286

    CAS  PubMed  Google Scholar 

  • van Huizen R, Ozga JA, Reinecke DM (1997) Seed and hormonal regulation of gibberellin 20-oxidase expression in pea pericarp. Plant Physiol 115:123–128

    CAS  PubMed  Google Scholar 

  • Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) Pin-formed1 regulates cell fate at the periphery of the shoot apical meristem. Development 127:5157–5165

    CAS  PubMed  Google Scholar 

  • Villani PJ, DeMason DA (1997) Roles of the Af and Tl genes in pea leaf morphogenesis: characterization of the double mutant (afaftltl). Am J Bot 84:1323–1336

    Google Scholar 

  • Villani PJ, DeMason DA (1999a) The Af gene regulates timing and direction of major developmental events during leaf morphogenesis in garden pea (Pisum sativum). Ann Bot 83:117–128

    CAS  Google Scholar 

  • Villani PJ, DeMason DA (1999b) Roles of the Af and Tl genes in pea leaf morphogenesis: leaf morphology and pinna anatomy of the heterozygotes. Can J Bot 77:611–622

    CAS  Google Scholar 

  • Willemsen, V, Friml J, Grebe M, vanden Toorn A, Palme K, Scheres B (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15:612–625

    CAS  PubMed  Google Scholar 

  • Young GS (1954) The effects of leaf primordia on differentiation in the stem. New Phytol 53:445–460

    Google Scholar 

Download references

Acknowledgements

The authors thank Janet Giles for her technical assistance with the tissue culture experiments and for performing the Uni expression analyses, and Dr. William Thomson for comments on the manuscript. The SEM was done in the Analytical Microscopy Facility at the University of California, Riverside. The pea genotypes used in this study were obtained from the Marx Collection, which currently resides at the USDA–ARS, Pacific West Area. This work was supported by a grant from USDA/CSREES 2001-35304-10958 to the first author.

Author information

Authors and Affiliations

  1. Botany and Plant Sciences, University of California, Riverside, CA 92521, USA

    Darleen A. DeMason & Rekha Chawla

Authors
  1. Darleen A. DeMason
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rekha Chawla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Darleen A. DeMason.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s00425-004-1221-x

Rights and permissions

Reprints and permissions

About this article

Cite this article

DeMason, D.A., Chawla, R. Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 218, 435–448 (2004). https://doi.org/10.1007/s00425-003-1100-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-003-1100-x

Keywords

Search

Navigation