Science in Society Archive

View from MADS House

New opportunities for manipulating flowering in plants set the stage for extensive alteration of crop geography. Prof. Joe Cummins

MADS-box genes are a large family of genes coding for protein transcription-factors that recognize short stretches of DNA - the MADS-box - to which they bind directly to regulate transcription. MADS-boxes and transcription factors are present in all multi-cellular eukaryotes from fungi to plants and humans where they regulate developmental pathways. The MADS-box transcription factors bend DNA at the site of transcription initiation to juxtapose transcription factors on adjacent sites (boxes) [1].

In plants, the MADS-box gene families are conserved among gymnosperms, angiosperms, ferns and mosses. They serve a wide range of functions from floral development to root formation, but the range of effects is not yet fully explored [2,3]. The controls of floral development pathways and time of flowering have a common evolutionary origin [4]. Flowering plants prefer transcription from chromosomes of maternal rather than paternal origin and even that epigenetic effect is mediated through MADS-box controls [5].

The discovery of the MADS-box gene families has had an instant impact on agriculture and forestry. A wide array of inventions to control flowering, seed production as well as other growth modifications has not yet reached commercial farms and forests, but many modifications have been reported and others have been patented. The main commercial transgenic crops now available are modified for herbicide resistance or insect resistance, the MADS-box constructions are modified with flowering controls or flowering timing, even alterations in yield are contemplated. Agronomy, horticulture and forestry will all be greatly affected by the genetic modifications involving the MADS-box.

Much of the initial work on the plant MADS-box transcription factors was done using the tiny mustard plant Arabidopsis. Recently a floral transcription factor was found to control the agronomic traits of seed yield and seed mass [6,7]. Of course, such trait in Arabidopsis would mainly please a few voles, but the trait can easily be manipulated in grain crops such as maize, rice and wheat. In rice, for example, MADS-box genes have been identified which control the timing of flowering. As flowering time determines regional adaptability of rice varieties, manipulating that timing will allow greater use of regional varieties [8,9]. Genes determining rice floral morphology have been identified allowing rice spikelet development to be manipulated [10].

Vernalization is the long winter cold treatment required for flowering in grain and some oil crops. Usually, the crops requiring vernalization have spring planted cultivars that do not require the cold treatment so they can be planted in spring rather than autumn. Nevertheless, the winter requiring varieties have desirable traits that are not present in the spring varieties. In wheat, vernalization is controlled by the MADS-box gene WAP1 [11]. Unlocking vernalization should allow quality wheat to be produced in warm climates. Bolting is another aspect of cold temperature-induced flowering. Exposing the germinating seeds or plantlets to a range of low temperatures accelerates flowering causing cabbage or lettuce to lose commercial value. An anti-bolting MADS-box gene has been identified in Chinese cabbage [12]. The stage is set for extensive alterations in crop geography.

The MADS-box genes expressed during tomato seed and fruit development have been identified [13]. Such findings may lead to commercial applications.

An anther-specific MADS-box was identified in peas and is expressed also in a number of other plant species [14]. The anther-specific transcription regulator can be manipulated to produce male-sterile varieties used to produce high value hybrid seeds.

A root nodule-specific MADS-box gene was identified in alfalfa root nodules [15]. Transferring nitrogen-fixing ability to non-legumes has been discussed for decades, and this discovery may spur developments in that area.

The MADS-box gene DAL1 was identified as a mediator of juvenile to adult transition in Norway spruce [16]. Hastening floral development in forest trees can accelerate breeding programs.

The first of many patents on MADS-box related functions have begun to appear, all of them broad patents covering reproductive development in plants in general. United States Patent 6 828 478 provides the surprising finding that ectopic expression of certain MADS-box-containing gene products, such as SEP1, SEP2, SEP3 or AGL24, combined with the ectopic expression of AP1, CAL or LFY gene products, result in modulated reproductive development. Thus, this invention provides plants comprising such ectopically expressible gene products as well as methods of modulating the timing of reproductive development in plants [17].

US patent 6 693 228 deals with the flowering locus (FLC) to delay or advance flowering [18], and US patent 6 713 663, with FT protein that modulates flowering in plants and dominant negative mutations of that protein (dominant negative mutations usually disrupt the function of a wild type gene by producing peptides that inactivate the wild type product) [19]. A Canadian patent application deals with floral homeotic genes for manipulation of flowering in poplar [20], and involves ablation of reproductive cells using toxins activated by promoters for the flower specific transcription factors, or by inhibiting the transcription factors with genetic anti-sense or dominant negative mutants. In the patents described above, the genes involved all originate from plants, but selectable markers and synthetic genes are also used to modulate the plant genes.

The discovery of MADS-box transcription regulators has open doors to modulating a wide array of agronomical properties of which the control of flowering and seed production is only the first. Other properties include nitrogen fixation, plant growth and disease resistance. The potential benefits from such manipulation must be evaluated alongside the safety considerations, including the genetic modifications themselves, which may involve synthetic genes and ablation toxins that pose a threat to animals [21, 22]. Indeed, the homology between plant and animal MADS-box genes should receive special attention.

Article first published 09/03/05


References

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  2. Ng M and Yanofsky M. Function and evolution of the plant MADS-box gene family. Nature reviews genetics 2001, 2,186-96
  3. DeBodt S, Raes J, VandePeer Y and Theissen G. And then there were many: MADS goes genomic. Trends in Plant science 2003, 8, 475-83.
  4. Lawton-Rauh A, Alvarez-Buylla E and Purugganan M. Molecular evolution of follower development. Trends in Ecology and Evolution 2000, 15,144-9.
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  7. Ohto M, Fischer R,Goldgerg R, Nakamura K and Harada J. Control of seed mass by APETALA2 2005 Proc. Natl. Acad.Sci.USA 2005, 102, 3123-8.
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  9. Lee S, Kim J, Han J, Han M and An G. Functional analyses of the flowering time gene OsMADS50, the putative suppressor of overexpression of CO 1/agamous-like 20(SOC1/AGL20) ortholog in rice. The Plant Journal 2004, 38 754-64.
  10. Sentoku N, Kato H, Kitano H and Imai1 R. OsMADS22, an STMADS11-like MADS-box gene of rice, is expressed in non-vegetative tissues and its ectopic expression induces spikelet meristem indeterminacy. Molecular Genetics and Genomics, in press, 2005.doi 10.1007/s00438-004-1093-6
  11. Trevaskis B, Bagnall D, Ellis M, Peacock W and Dennis E. MADS box genes control vernalization-induced flowering in cereals. Proc Natnl Acad Sc USA 2003, 100, 13099-104.
  12. Lia Z, Zhaoa L, Cuib C, Kaia G, Zhanga L, Sunc X and Tanga K. Molecular cloning and characterization of an anti-bolting related gene (BrpFLC) from Brassica rapa ssp. Pekinensis. Plant Science 2005, 168, 407-13.
  13. Busi M, Bustamante C, D'Angelo C, Hidalgo-Cuevas M, Boggio S, Valle E and Zabalet E. MADS-box genes expressed during tomato seed and fruit development. Plant Molecular Biology 2003, 52, 801-15.
  14. Gomez M, Beltran J and Canas L. The pea END1 promoter drives anther specific gene expression in different plant species. Planta 2004, 219, 967-81.
  15. Zucchero J, Caspi,M and Dunn K. ngl9: A Third MADS Box gene expressed in alfalfa root nodules. Molecular Plant-Microbe Interactions 2001, 14, 1463-7.
  16. Carlsbecker A, Tandre K, Johanson U, Englund M and Engstro P. The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). The Plant Journal 2004, 40, 546-57
  17. Yanofsky M, Pelaz S and Ditta G. Combination of genes for producing seed plants exhibiting modulated reproductive development 2004 United States patent 6 828 478
  18. Amasino R, Schomberg F, Michaels S, Sung S and Scortecci K. Altering of flowering in plants 2004 United States patent 6 693 228
  19. Weigel D and Kardailsky I. Flowering locus T9FT and genetically modified plants having delayed flower development 2004 United States patent 6 713 663
  20. Strauss S, Rottman W, Brunner A and Sheppard L. Floral homeotic genes for manipulation of flowering poplar trees and other plant species Canadian patent application 2 319 853.
  21. Ho MW and Cummins J. Terminate the terminators! I-SIS Report July 12, 2001 https://www.i-sis.org.uk/terminator.php
  22. Ho MW and Cummins J. Chronicle of an ecological disaster foretold. I-SIS report 2/02/03 https://www.i-sis.org.uk/CEDF.php; also Science in Society 2003, 18, 26-27 https://www.i-sis.org.uk/isisnews.php

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