Localised and non-localised promotion of fruit development by seeds in Arabidopsis

Catherine M. Cox; Stephen M. Swain

doi:10.1071/FP05136

RESEARCH ARTICLE

Previous Next Contents Vol 33(1)

Localised and non-localised promotion of fruit development by seeds in Arabidopsis

Catherine M. Cox ^A ^B and Stephen M. Swain ^B ^C

+ Author Affiliations

- Author Affiliations

^A School of Agricultural Science, La Trobe University, Bundoora, Vic. 3083, Australia.

^B CSIRO Plant Industry, 585 River Ave, South Merbein, Vic. 3505, Australia.

^C Corresponding author. Email: Steve.Swain@csiro.au

^D This paper originates from the Peter Goldacre Award 2004 of the Australian Society of Plant Scientists, received by S. M. Swain.

Functional Plant Biology 33(1) 1-8 https://doi.org/10.1071/FP05136
Submitted: 3 June 2005 Accepted: 29 August 2005 Published: 3 January 2006

Abstract

In Arabidopsis, as in the majority of flowering plants, developing seeds promote fruit growth. One method to investigate this interaction is to use plants with reduced seed set and determine the effect on fruit growth. Plants homozygous for a transgene designed to ectopically express a gene encoding a gibberellin-deactivating enzyme exhibit reduced pollen tube elongation, suggesting that the plant hormone gibberellin is required for this process. Reduced pollen tube growth causes reduced seed set and decreased silique (fruit) size, and this genotype is used to explore the relationship between seed set and fruit elongation. A detailed analysis of seed set in the transgenic line reveals that reduced pollen tube growth decreases the probability of each ovule being fertilised. This effect becomes progressively more severe as the distance between the stigma and the ovule increases, revealing the complex biology underlying seed fertilisation. In terms of seed-promoted fruit growth, major localised and minor non-localised components that contribute to final silique length can be identified. This result demonstrates that despite the relatively small size of the fruit and associated structures, Arabidopsis can be used as a model to investigate fundamental questions in fruit physiology.

Acknowledgments

Thanks to Judy Tisdall (La Trobe University) for cosupervising CMC, Davinder Pal Singh and Richard Storey for the scanning electron microscope image in Fig. 1, and the Cooperative Research Centre for Viticulture and the Grape and Wine Research and Development Corporation (GWRDC) for financial support to CMC. This work was performed in conjunction with CSIRO Plant Industry and La Trobe University as part of Riverlink.

References

Alvarez J, Smyth DR (2002) CRABS CLAW and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana. International Journal of Plant Sciences 163, 17–41.
| Crossref | GoogleScholarGoogle Scholar |

Bowman JL, Baum SF, Eshed Y, Putterill J, Alvarez J (1999) Molecular genetics of gynoecium development in Arabidopsis. Current Topics in Developmental Biology 45, 155–205.
| PubMed |

de Groot P, Weterings K, de Been M, Wittink F, Hulzink R, Custers J, van Herpen M, Wullems G (2004) Silencing of the pollen-specific gene NTP303 and its family members in tobacco affects in vivo pollen tube growth and results in male sterile plants. Plant Molecular Biology 55, 715–726.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Eeuwens CJ, Schwabe WW (1975) Seed and pod wall development in Pisum sativum L. in relation to extracted and applied hormones. Journal of Experimental Botany 26, 1–14.

Garcia-Martinez JL, Marti M, Sabater T, Maldonado A, Vercher Y (1991) Development of fertilized ovules and their role in the growth of the pea pod. Physiologia Plantarum 83, 411–416.
| Crossref | GoogleScholarGoogle Scholar |

Groot SPC, Bruinsma J, Karssen CM (1987) The role of endogenous gibberellin in seed and fruit development of tomato: studies with a gibberellin-deficient mutant. Physiologia Plantarum 71, 184–190.

Hulskamp M, Schneitz K, Pruitt RE (1995) Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. The Plant Cell 7, 57–64.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Ito T, Meyerowitz EM (2000) Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in Arabidopsis. The Plant Cell 12, 1541–1550.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Koltunow, AM , Vivian-Smith, A , Tucker, MR , and Paech, N (2002). The central role of the ovule in apomixis and parthenocarpy. In ‘Plant reproduction. Vol 6.’ pp. 221–256. (Sheffield Academic Press: Sheffield, UK)

Lester DR, Ross JJ, Smith JJ, Elliott RC, Reid JB (1999) Gibberellin 2-oxidation and the SLN gene of Pisum sativum. The Plant Journal 19, 65–73.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Nitsch JP (1952) Plant hormones in the development of fruits. The Quarterly Review of Biology 27, 33–57.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

O’Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiology 130, 1974–1982.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Ozga JA, van Huizen R, Reinecke DM (2002) Hormone and seed-specific regulation of pea fruit growth. Plant Physiology 128, 1379–1389.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Ozga JA, Yu J, Reinecke DM (2003) Pollination-, development-, and auxin-specific regulation of gibberellin 3β-hydroxylase gene expression in pea fruit and seeds. Plant Physiology 131, 1137–1146.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 47–59.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Ross J, O’Neill D (2001) New interactions between classical plant hormones. Trends in Plant Science 6, 2–4.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Shimizu KK, Okada K (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127, 4511–4518.
| PubMed |

Singh DP, Jermakow AM, Swain SM (2002) Gibberellins are required for seed development and pollen tube growth in Arabidopsis. The Plant Cell 14, 3133–3147.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. The Plant Cell 2, 755–767.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Swain SM, Singh DP (2005) Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends in Plant Science 10, 123–129.
| PubMed |

Swain SM, Ross JJ, Reid JB, Kamiya Y (1995) Gibberellins and pea seed development. Expression of the lhi, ls and le5839 mutations. Planta 195, 426–433.
| Crossref | GoogleScholarGoogle Scholar |

Swain SM, Reid JB, Kamiya Y (1997) Gibberellins are required for embryo growth and seed development in pea. The Plant Journal 12, 1329–1338.
| Crossref | GoogleScholarGoogle Scholar |

Swain SM, Muller AJ, Singh DP (2004) The gar2 and rga alleles increase the growth of gibberellin-deficient pollen tubes in Arabidopsis. Plant Physiology 134, 694–705.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Vivian-Smith A, Koltunow AM (1999) Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiology 121, 437–451.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Vivian-Smith A, Luo M, Chaudhury A, Koltunow A (2001) Fruit development is actively restricted in the absence of fertilization in Arabidopsis. Development 128, 2321–2331.
| PubMed |