Plant biology

Witchcraft and destruction

The discovery of a protein that is targeted for degradation by the 'witch' hormones called strigolactones reveals a mechanism by which shoot architecture is controlled in rice plants. See Articles p.401 & p.406

The mythical old hag Striga gained succour by drawing the life force from her young victims. Today, she lends her name to the witchweeds of the genus Striga and to the strigolactone compounds that trigger these plants to parasitize their unsuspecting host plants. But these compounds typically play a more positive part in plant biology — as hormones that control the development of roots and shoots to coordinate the capture of mineral nutrients from the soil with that of carbon from the atmosphere. The strigolactone receptor is a curious protein because it simultaneously perceives and destroys the hormone. In two papers1,2 published on Nature's website today, a target of this receptor in rice is reported to be the novel protein DWARF53, the strigolactone-dependent destruction of which blocks the outgrowth of secondary shoots.

Strigolactones were first discovered in root exudates through their ability to stimulate seed germination of the root-parasitic plant Striga hermonthica3. The compounds were later shown to promote the formation of mutually beneficial symbioses between plant roots and fungi4. More recently, it was discovered that strigolactones are involved in the control of plant development5,6. In response to nutrient limitation, strigolactones are produced in the roots7, where they promote the growth of lateral roots and root hairs, and they are transported to the shoots, where they repress the outgrowth of lateral buds or secondary shoots8. These outcomes increase the capture of mineral nutrients by the roots, while at the same time reducing the shoots' demand for resources.

Mutant plants that are strigolactone deficient or insensitive have multiple secondary shoots and often a short primary stem. In rice, these plants are typically described as dwarf mutants. Genetic analysis of these plants has led to the identification of enzymes involved in strigolactone biosynthesis9 and of the rice strigolactone receptor DWARF14 (D14)10. The receptor is an α/β-fold hydrolase enzyme that uses a catalytic triad of amino acids to simultaneously perceive and hydrolyse strigolactones, in conjunction with an F-box protein11 that in rice is known as DWARF3 (D3)3. Because the function of F-box proteins is to select other proteins for degradation, this interaction suggests that D14 and D3 might form a complex that targets other proteins for removal. Just such a target protein has now been identified.

Jiang et al.1 (page 401) and Zhou et al.2 (page 406) studied a rice dwarf mutant known as d53, which was described 36 years ago12. Both groups of authors show that these plants are strigolactone insensitive, and they have succeeded in the difficult task of identifying the mutated gene. They show that the D53 protein has sequence similarities to Clp ATPase enzymes and to heat-shock protein 101, which suggests that it has a role in protein–protein interactions. They also reveal that the d53 mutation involves the deletion of five amino acids and substitution of one other in the D53 protein, which could potentially cause the protein to malfunction.

Both papers present evidence for strigolactone-dependent interactions between D53 and D14, and between D14 and D3, and show that the catalytic triad of D14 is essential for this strigolactone function. Interaction between the three proteins leads to D53 being tagged with ubiquitin — a regulatory protein that marks proteins for destruction — and destroyed (Fig. 1). In the absence of D14 or strigolactone, D53 and D3 can still interact, but this does not lead to destruction of D53. Furthermore, the mutant D53 protein is neither ubiquitinated nor degraded even in the presence of D14 and strigolactone, which seems to explain why d53 plants produce multiple secondary shoots (tillers).

Figure 1: Repression of secondary-shoot growth by strigolactones.
figure1

a, Strigolactone hormones can inhibit the outgrowth of secondary shoots when nutrients are in short supply. Jiang et al.1 and Zhou et al.2 have found that, in rice, this is achieved by destruction of the protein D53, which otherwise promotes secondary-shoot growth. b, The authors show that binding and hydrolysis of strigolactone by its receptor D14 leads to the recruitment of D53 into a complex of D14 and another protein, D3. These protein interactions result in the ubiquitination (indicated by Ub) and subsequent destruction of D53.

Both groups go on to show that D53 is located in the nucleus and that it contains putative EAR sequences; these are thought to interact with proteins of the TOPLESS family, which are involved in repression of gene transcription in several plant-hormone signalling pathways. Indeed, Jiang et al. show that D53 interacts with two rice TOPLESS proteins, raising the possibility that D53 in concert with TOPLESS proteins could regulate the expression of genes that determine shoot architecture. The d53 mutant also exhibits downregulation of the gene FC1, an orthologue of the maize (corn) TB1 and thale cress (Arabidopsis) BRC1 genes, which are known to repress secondary-shoot growth. Thus, it seems likely that D53 acts in the nucleus to regulate the expression of genes involved in secondary-shoot growth.

Strigolactones control numerous aspects of plant development, so might D53 have a broader role? D53 belongs to a small gene family, other members of which could regulate different aspects of development. Support for this idea comes from a recent study of Arabidopsis13. MAX2 is the Arabidopsis orthologue of D3 and is required not only for the control of shoot development, in conjunction with the Arabidopsis D14, but also for seedling growth, together with the D14-like protein KAI2. A gene (SMAX1) has been identified13 that encodes a protein that works in conjunction with MAX2 and is required for seedling growth but not for secondary-shoot growth; SMAX1 is a homologue of D53, indicating that these genes provide examples of functional specialization within a gene family.

Although Jiang et al. indicate that D53 acts as a repressor of strigolactone action, it is conceptually easier to think of strigolactones as repressors of D53. What is remarkable is that nutrient limitation in the roots does not simply limit shoot growth by default, but instead the root dispatches the strigolactone signal to impose a brake on shoot growth by destroying the D53 protein. These findings reveal remarkable similarities between strigolactones and their receptors, and the perception and signalling mechanisms of several other classes of plant hormone, including auxins, jasmonates and gibberellins. For example, the rice gibberellin receptor GID1 is also a member of the α/β-fold hydrolase family, and by binding the protein SLR1 recruits it into a complex with an F-box protein (SLY1) for ubiquitination and destruction. Another twist to the story comes from the recent report14 that rice D14 exhibits strigolactone-dependent interaction with SLR1, suggesting a mechanism for the coordination of strigolactone and gibberellin signalling during the control of shoot development. This will be an exciting area for further research.

The discovery that strigolactones have a central role in regulating resource allocation and growth in plants has far-reaching consequences. Agriculturalists need to boost yields while decreasing their dependency on finite resources, such as phosphate, and on fossil fuels for nitrogen-based fertilizers. We have already seen the development of higher-yielding nitrogen-dependent crop varieties with modified gibberellin action. It is now clear that strigolactones might be exploited to generate crop varieties with improved resource allocation under nutrient-limiting conditions.

References

  1. 1

    Jiang, L. et al. Nature 504, 401–405 (2013).

    ADS  CAS  Article  Google Scholar 

  2. 2

    Zhou, F. et al. Nature 504, 406–410 (2013).

    ADS  CAS  Article  Google Scholar 

  3. 3

    Xie, X., Yoneyama, K. & Yoneyama, K. Annu. Rev. Phytopathol. 48, 93–117 (2010).

    CAS  Article  Google Scholar 

  4. 4

    Akiyama, K., Matsuzaki, K. & Hayashi, H. Nature 435, 824–827 (2005).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Umehara, M. et al. Nature 455, 195–200 (2008).

    ADS  CAS  Article  Google Scholar 

  6. 6

    Gomez-Roldan, V. et al. Nature 455, 189–194 (2008).

    ADS  CAS  Article  Google Scholar 

  7. 7

    Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N. & Yamaguchi, S. Plant Cell Physiol. 51, 1118–1126 (2010).

    CAS  Article  Google Scholar 

  8. 8

    Brewer, P. B., Koltai, H. & Beveridge, C. A. Mol. Plant 6, 18–28 (2013).

    CAS  Article  Google Scholar 

  9. 9

    Alder, A. et al. Science 335, 1348–1351 (2012).

    ADS  CAS  Article  Google Scholar 

  10. 10

    Arite, T. et al. Plant Cell Physiol. 50, 1416–1424 (2009).

    CAS  Article  Google Scholar 

  11. 11

    Hamiaux, C. et al. Curr. Biol. 22, 2032–2036 (2012).

    CAS  Article  Google Scholar 

  12. 12

    Iwata, N., Satoh, H. & Omura, T. Japan. J. Breed. 27 (suppl. 1), 250–251 (1977).

    Google Scholar 

  13. 13

    Stanga, J. P., Smith, S. M., Briggs, W. R. & Nelson, D. C. Plant Physiol. 163, 318–330 (2013).

    CAS  Article  Google Scholar 

  14. 14

    Nakamura, H. et al. Nature Commun. 4, 2613 10.1038/ncomms3613 (2013).

    ADS  CAS  Article  Google Scholar 

Download references

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Correspondence to Steven M. Smith.

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Smith, S. Witchcraft and destruction. Nature 504, 384–385 (2013). https://doi.org/10.1038/nature12843

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