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Review
. 2012 Jun;63(10):3511-22.
doi: 10.1093/jxb/ers065. Epub 2012 Apr 30.

Brassinosteroid Action in Flowering Plants: A Darwinian Perspective

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Free PMC article
Review

Brassinosteroid Action in Flowering Plants: A Darwinian Perspective

Ulrich Kutschera et al. J Exp Bot. .
Free PMC article

Abstract

The year 2012 marks the 150th anniversary of the publication of Charles Darwin's first botanical book, on the fertilization of orchids (1862), wherein he described pollen grains and outlined his evolutionary principles with respect to plant research. Five decades later, the growth-promoting effect of extracts of Orchid pollen on coleoptile elongation was documented. These studies led to the discovery of a new class of phytohormones, the brassinosteroids (BRs) that were isolated from rapeseed (Brassica napus) pollen. These growth-promoting steroids, which regulate height, fertility, and seed-filling in crop plants such as rice (Oryza sativa), also induce stress- and disease resistance in green algae and angiosperms. The origin and current status of BR-research is described here, with reference to BR-action and -signal transduction, and it is shown that modern high-yield rice varieties with erect leaves are deficient in endogenous BRs. Since brassinosteroids induce pathogen resistance in rice plants and hence can suppress rice blast- and bacterial blight-diseases, genetic manipulation of BR-biosynthesis or -perception may be a means to increase crop production. Basic research on BR activity in plants, such as Arabidopsis and rice, has the potential to increase crop yields further as part of a 21th century 'green biotech-revolution' that can be traced back to Darwin's classical breeding experiments. It is concluded that 'Nothing in brassinosteroid research makes sense except in the light of Darwinian evolution' and the value of basic science is highlighted, with reference to the genetic engineering of better food crops that may become resistant to a variety of plant diseases.

Figures

Fig. 1.
Fig. 1.
Side view of the flower of the Bee Ophrys (Ophrys apifera), with the upper sepal and the two upper petals removed (A). This herbaceous perennial angiosperm belongs to the family Orchidaceae and inhabits semi-dry grasslands throughout Europe. A separate pollinium (Po), i.e. a coherent mass of pollen grains (Pg) produced by one anther, is shown at higher magnification (B) (adapted from Darwin, 1862. On the various contrivances by which British and foreign orchids are fertilized by insects. London: John Murray).
Fig. 2.
Fig. 2.
The discovery of growth-promoting substances from pollen extracts of maize (Zea mays) plants using the bean (Phaseolus vulgaris) second internode bioassay. Control experiment (A) and effect of pollen extract on stem- and cell elongation in light-grown pinto beans (B) (adapted from Mitchell and Whitehead, 1941. Response of vegetative parts of plants following application of extracts of pollen from Zea mays. Botanical Gazette 102, 770−791, with permission from the University of Chicago Press).
Fig. 3.
Fig. 3.
Flowering stalk of a rapeseed (Brassica napus) plant (A), pollen grains isolated from the mature stamina (B) and the structure of the steroidal phytohormone brassinolide (C). In 1979, brassinolide was isolated from bee-collected rape pollen and its chemical structure determined by X-ray analysis.
Fig. 4.
Fig. 4.
Brassinosteroids occur in the aquatic unicellular freshwater alga Chlorella vulgaris (A) and in the maize plant Zea mays (B). This complex multicellular terrestrial organism is characterized by the efficient C4-mode of photosynthesis, whereas Chlorella is a C3-photosynthesizer. It is likely that BRs were already present in the last common ancestor of these representative members of the evolutionary green lineage.
Fig. 5.
Fig. 5.
Brassinolide (BL)-induced promotion of leaf bending in etiolated seedlings of rice (Oryza sativa). Thirty-two explants, c. 2.5 cm in length, were cut in the region of the node and collected on distilled water in green safelight. Thereafter, half of the explants (16) were incubated on a shaker either in the absence (−) or presence (+) of BR (1 μmol l−1). After 2 d of incubation (25 °C, darkness), the explants were photographed and the leaf bending angles determined. The results show that in water (control) a significant leaf bending response occurred, which was promoted by a low concentration of BL (data represent means ±sem, n=16).
Fig. 6.
Fig. 6.
Photographs of a tillering-stage wild-type rice (Oryza sativa) plant (A) and the mutant ili1-D (B), grown in soil. Note that, in the rice mutant, the increased lamina inclination phenotype is similar to that caused by treatment of explants from wild-type seedlings with brassinolide (BL) (see Fig. 5) (adapted from a photograph provided by Liying Zhang, Institute of Botany, Chinese Academy of Sciences, Beijing, China, with kind permission from Liying Zhang).
Fig. 7.
Fig. 7.
The phytopathogenic fungus Magnaporthe oryzae, cultivated in a Petri dish on nutrient medium (A), and infected leaves of a barley (Hordeum vulgare) plant (B). Healthy, green leaves were inoculated with the fungus M. oryzae, cultivated, and photographed when the symptoms (red circles) emerged (adapted from Schaffrath and Delventhal, 2011. Wie wird aus Wirt Nichtwirt? Labor and more 7, issue 2, 24−27, with permission from succidia AG).
Fig. 8.
Fig. 8.
The evolution of modern rice (Oryza sativa) cultivars that originated from wild-type like plants. Conventional hybridization and artificial selection led, over many generations, from a wild-type plant (A) to an improved high-yielding high-tillering rice variety with a different phenotype (B). Using the tools of modern biotechnology, rice breeders aim to produce a low-tillering, disease- and stress-resistant ideotype with a higher harvest index than their progenitors (C) (adapted from G S Khush 1999, Green revolution: preparing for the 21st century. Genome 42, 646-655. © 2008 Canadian Science Publishing or its licensors. Reproduction with permission).
Fig. 9.
Fig. 9.
Scheme depicting the cyclical method of induction–deduction in the natural sciences, with respect to basic research and practical applications. Charles Darwin was an eminent 19th century scientist who applied these principles to a variety of research agendas that continue to the present (for instance, studies on brassinosteroid action in green algae and land plants).

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