Skip to main content
Log in

Genetic control of leaf-blade morphogenesis by the INSECATUS gene in Pisum sativum

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

To understand the role of INSECATUS (INS) gene in pea, the leaf blades of wild-type, ins mutant and seven other genotypes, constructed by recombining ins with uni-tac, af, tl and mfp gene mutations, were quantitatively compared. The ins was inherited as a recessive mutant allele and expressed its phenotype in proximal leaflets of full size leaf blades. In ins leaflets, the midvein development was arrested in distal domain and a cleft was formed in lamina above this point. There was change in the identity of ins leaflets such that the intercalary interrupted midvein bore a leaf blade. Such adventitious blades in ins, ins tl and ins tl mfp were like the distal segment of respective main leaf blade. The ins phenotype was not seen in ins af and ins af uni-tac genotypes. There was epistasis of uni-tac over ins. The ins, tl and mfp mutations interacted synergistically to produce highly pronounced ins phenotype in the ins tl mfp triple mutant. The role(s) of INS in leaf-blade organogenesis are: positive regulation of vascular patterning in leaflets, repression of UNI activity in leaflet primordia for ectopic growth and in leaf-blade primordium for indeterminate growth of rachis, delimitation of proximal leaflet domain and together with TL and MFP homeostasis for meristematic activity in leaflet primordia. The variant apically bifid shape of the affected ins leaflets demonstrated that the leaflet shape is dependent on the venation pattern.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amurrio J. M., deRon A. M. and Escribano M. R. 1992 Evaluation of Pisum sativum landraces from the northwest of the Iberian peninsula and their breeding value. Euphytica 66, 1–10.

    Article  Google Scholar 

  • Barkoulas M., Galinha C., Grigg S. P. and Tsiantis M. 2007 From genes to shape: regulatory interactions in leaf development. Curr. Opin. Plant Biol. 10, 660–666.

    Article  CAS  PubMed  Google Scholar 

  • Berdnikov V. A., Gorel F. L., Bogdanova V. S. and Kosterin O. E. 2000 Interaction of a new leaf mutation ins 2 with af, uni tac and tl w. Pisum Genet. 32, 9–12.

    Google Scholar 

  • Beveridge C. A., Mathesius U., Rose R. J. and Gresshoff P. M. 2007 Common regulatory themes in meristem development and whole-plant homeostasis. Curr. Opin. Plant Biol. 10, 44–51.

    Article  CAS  PubMed  Google Scholar 

  • Blixt S. 1972 Mutation genetics in Pisum. Agri. Hort. Genet. 30, 1–293.

    Google Scholar 

  • Brand U., Fletcher J. C., Hobe M., Meyerowitz E. M. and Simon R. 2000 Dependence of stem cell fate in Arabidopsis in a feedback loop regulated by CLV3 activity. Science 289, 617–619.

    Article  CAS  PubMed  Google Scholar 

  • Burton R. F. 2004 The mathematical treatment of leaf venation: the variation in secondary vein length along the midrib. Ann. Bot. 93, 149–156.

    Article  PubMed  Google Scholar 

  • Carlsbecker A. and Helariutta Y. 2005 Phloem and xylem specification: pieces of the puzzle emerge. Curr. Opin. Plant Biol. 8, 512–517.

    Article  CAS  PubMed  Google Scholar 

  • Champagne C. E. M., Goliber T. E., Wojciechowski M. F., Mei R. W., Townsley B. T., Wang K. et al. 2007 Compound leaf development and evolution in the legumes. Plant Cell 19, 3369–3378.

    Article  CAS  PubMed  Google Scholar 

  • Dalmais M., Schmidt J., Le Signor C., Moussy F., Burstin J., Savois V. et al. 2008 UTILLdp, a Pisum sativum in silico forward and reverse genetics tool. Genome Biol. 9, R43.

    Article  PubMed  Google Scholar 

  • DeMason D. A. 2005 Extending Marx’s isogenic lines in search of Uni function. Pisum Genet. 37, 10–14.

    Google Scholar 

  • DeMason D. A. and Chawla R. 2004 Roles for auxin and Uni in leaf morphogenesis of afila genotype of pea (Pisum sativum). Int. J. Plant Sci. 165, 707–722.

    Article  CAS  Google Scholar 

  • Dengler N. G. and Tsukaya H. 2001 Leaf morphogenesis in dicotyledons: current issues. Int. J. Plant Sci. 162, 459–464.

    Article  Google Scholar 

  • de Vilmorin P. and Bateson W. 1911 A case of gametic coupling in Pisum. Proc. R. Soc. London, Ser. B. Biol. Sci. 84, 9–11.

    Article  Google Scholar 

  • Dolan L. 2009 Body building on land: morphological evolution of land plants. Curr. Opin. Plant Biol. 12, 4–6.

    Article  CAS  PubMed  Google Scholar 

  • Eriksson G. 1929 Erbkomplexe des Rotklees und der Erbsen. Z. Pflanzenzuecht. 40, 445–475.

    Google Scholar 

  • Fiers M., Ku K. L. and Liu C. M. 2007 CLE peptide ligands and their roles in establishing meristems. Curr. Opin. Plant Biol. 10, 39–43.

    Article  CAS  PubMed  Google Scholar 

  • Floyd S. K. and Bowman J. L. 2006 Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Curr. Biol. 16, 1611–1617.

    Article  Google Scholar 

  • Fujita H. and Mochizuki A. 2006 The origin of the diversity of leaf vascular pattern. Dev. Dyn. 235, 2710–2721.

    Article  PubMed  Google Scholar 

  • Goldenberg J. B. 1965 Afila, a new mutant in pea (Pisum sativum L.). Bol. Genet. 1, 27–31.

    Google Scholar 

  • Gourlay C. W., Hofer J. M. I. and Ellis T. H. N. 2000 Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, COCHLEATA, AFILA and TENDRILLESS. Plant Cell 12, 1279–1294.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hecht V., Foucher F., Ferrandiz R., Macknight R., Navarro C., Morin J. et al. 2005 Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 137, 1420–1434.

    Article  CAS  PubMed  Google Scholar 

  • Hecht V., Knowles C. L., Schoor J. K. V., Liew L. C., Jones S. E., Lambert M. J. and Weller J. L. 2007 Pea LATE BLOOMER 1 is GIGANTEA ortholog with roles in photoperiodic flowering, deetiolation, and transcriptional regulation of circadian clock gene homologue. Plant Physiol. 144, 648–661.

    Article  CAS  PubMed  Google Scholar 

  • Heisler M. G. and Jonsson H. 2007 Modelling meristem development in plants. Curr. Opin. Plant Biol. 10, 92–97.

    Article  CAS  PubMed  Google Scholar 

  • Hofer J. M. I. and Ellis T. H. N. 1998 The genetic control of patterning in pea leaves. Trends Plant Sci. 3, 439–444.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hofer J. M. I., Gourlay C. W., Ellis T. H. N. 2001 Genetic control of leaf morphology: a partial view. Ann. Bot. 88, 1129–1139.

    Article  Google Scholar 

  • Hofer J., Turner L., Moreau C., Ambrose M., Isaac P., Butcher S. et al. 2009 Tendril-less regulates tendril formation in pea leaves. Plant Cell 21, 420–428.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi Y. and Weigel D. 2007 Move on up; its time for change-mobile signals controlling photoperiod-dependent flowering. Genes Dev. 21, 2371–2384.

    Article  CAS  PubMed  Google Scholar 

  • Kujala V. 1953 Felderbse bie welcher die ganze Blattspreite in Ranken umgewandelt ist. Arch. Soc. Zoo. Bot. Fennicae ‘Vanamo’ 8, 44–45.

    Google Scholar 

  • Kumar S. and Sharma B. 1986 Mutations in three of the genes determining thiamine biosynthesis in Pisum sativum. Mol. Gen. Genet. 204, 473–476.

    Article  CAS  Google Scholar 

  • Kumar S., Rai S. K., Pandey-Rai S., Srivastava S. and Singh D. 2004 Regulation of unipinnate character in the distal tendrilled domain of compound leaf-blade by the gene MULTIFOLIATE PINNA (MFP) in pea Pisum sativum. Plant Sci. 166, 929–940.

    Article  CAS  Google Scholar 

  • Kumar S., Mishra R. K., Kumar A., Srivastava S. and Chaudhary S. 2009 Regulation of stipule development by COCHLEATA and STIPULE-REDUCED genes in pea Pisum sativum. Planta 230, 449–458.

    Article  CAS  PubMed  Google Scholar 

  • Lamprecht H. 1933 Ein unifoliata Typus von Pisum mit gleichzeitiger Pistilloidie. Hereditas 18, 56–64.

    Article  Google Scholar 

  • Lamprecht H. 1959 Das Merkmal insecatus von Pisum und seine Vererbung sowie einige Koppelungsstudien. Agri. Hortique Genetica 17, 26–36.

    Google Scholar 

  • Marx G. A. 1987 A suit of mutants that modify pattern formation in pea leaves. Plant Mol. Biol. Rep. 5, 311–335.

    Article  Google Scholar 

  • Micol J. L. 2009 Leaf development: time to turn over a new leaf. Curr. Opin. Plant Biol. 12, 9–16.

    Article  CAS  PubMed  Google Scholar 

  • Mishra R. K., Chaudhary S., Kumar A. and Kumar S. 2009 Effects of MULTIFOLIATE-PINNA, AFILA, TENDRIL-LESS and UNIFOLIATA genes on leafblade architecture in Pisum sativum. Planta 230, 177–190

    Article  CAS  PubMed  Google Scholar 

  • Muller R., Broghi L., Kwiatkowska D., Laufs P. and Simon R. 2006 Dynamics and compensatory responses of Arabidopsis shoot and floral meristems to CLV3 signalling. Plant Cell 18, 1188–1198.

    Article  PubMed  Google Scholar 

  • Nardmann J. and Werr W. 2007 The evolution of plant regulatory networks: what Arabidopsis cannot say for itself. Curr. Opin. Plant Biol. 10, 653–659.

    Article  CAS  PubMed  Google Scholar 

  • Prajapati S. and Kumar S. 2001 Role of LLD, a new locus for leaflet/pinna morphogenesis in Pisum sativum. J. Biosci. 26, 607–625.

    Article  CAS  PubMed  Google Scholar 

  • Prajapati S. and Kumar S. 2002 Interaction of the UNIFOLIATATENDRILLED ACACIA gene with AFILA and TENDRIL-LESS genes in the determination of leaf-blade growth and morphology in pea Pisum sativum. Plant Sci. 162, 713–721.

    Article  CAS  Google Scholar 

  • Putterill J., Laurie R. and Macknight R. 2004 It s time to flower. The genetic control of flowering time. BioEssays 26, 363–373.

    Article  CAS  PubMed  Google Scholar 

  • Reddy G. V. and Meyerowitz E. M. 2005 Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310, 663–667.

    Article  CAS  PubMed  Google Scholar 

  • Sablowski R. 2007 The dynamic plant cell niches. Curr. Opin. Plant Biol. 10, 639–664.

    Article  CAS  PubMed  Google Scholar 

  • Scarpella E. and Meijer A. 2004 Pattern formation in the vascular system of monocot and dicot plant species. New Phytol. 164, 209–242.

    Article  CAS  Google Scholar 

  • Schoof H., Lenhard M., Haeker A., Mayer K. F., Jurgens G. and Laux T. 2000 The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644.

    Article  CAS  PubMed  Google Scholar 

  • Singer S., Sollinger J., Maki S., Fishbach J., Short B., Reinke C., et al. 1999 Inflorescence architecture: A developmental genetics approach. Bot. Rev. 65, 385–410.

    Article  Google Scholar 

  • Sharma B. 1972 “Tendrilled acacia”, a new mutation controlling tendril formation in Pisum sativum. Pisum News Lett. 4, 50.

    Google Scholar 

  • Sharma B. and Kumar S. 1981 Discovery of one more allele of the tac-locus of Pisum sativum. Pulse Crops Newslett. 1, 21.

    Google Scholar 

  • Smirnova O. G. 2002 Characteristics and inheritance of the leaf mutation ins. Pisum Genet. 34, 34–35.

    Google Scholar 

  • Wang Z., Luo Y., Li X., Wang L., Xu S., Yang J. et al. 2008 Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proc. Natl. Acad. Sci. USA 105, 10414–10419.

    Article  CAS  PubMed  Google Scholar 

  • Wenden B. and Remeau C. 2009 Systems biology for plant breeding: the example of flowering time in pea. C. R. Biol. 332, 998–1006.

    Article  PubMed  Google Scholar 

  • White D. W. R. 2006 PEAPOD regulates lamina size and curvature in Arabidopsis. Proc. Natl. Acad. Sci. USA 103, 13238–13243.

    Article  CAS  PubMed  Google Scholar 

  • White O. E. 1917 Studies of inheritance in Pisum II. The present state of knowledge of heredity and variation in peas. Proc. Am. Philos. Soc. 56, 487–588.

    Google Scholar 

  • Williams L. and Fletcher J. C. 2005 Stem cell regulation in the Arabidopsis shoot apical meristem. Curr. Opin. Plant Biol. 8, 582–586.

    Article  CAS  PubMed  Google Scholar 

  • Wurschum T., Gross-Hardt R. and Laux T. 2006 APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18, 295–307.

    Article  PubMed  Google Scholar 

  • Yaxley J. L., Jablonski W. and Reid J. B. 2001 Leaf and flower development in pea (Pisum sativum L): mutants cochleata and unifoliata. Ann. Bot. 88, 225–234.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sushil Kumar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kumar, S., Chaudhary, S., Sharma, V. et al. Genetic control of leaf-blade morphogenesis by the INSECATUS gene in Pisum sativum . J Genet 89, 201–211 (2010). https://doi.org/10.1007/s12041-010-0026-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-010-0026-x

Keywords

Navigation