Seeds of Conflict

New research unearths the secrets of the antagonistic forces that shape seedling development.

Courtesy of Cristina Martinez / Deng Lab, Yale University

Every seed begins its life as the subject of a war—between light and gibberellins, a type of plant hormone, which work antagonistically to guide seedling development. In short, gibberellins promote the early elongation of a plant’s stem, while light inhibits it and helps stunt stem growth. Despite nearly 5 decades of research uncovering the two factors’ roles and the nature of their interactions in processes such as germination and leaf development, scientists were unable to fully decipher the mechanisms driving their antagonistic relationship. But the recent side-by-side publication of two studies in Nature identifying key molecular components involved has helped deepen the understanding of plant development and triggered a widespread search for additional regulators.

In 2005, research teams from the Centro Nacional de Biotecnologia–CSIC in...

As part of one of this month’s Hot Papers, Miguel de Lucas and colleagues from the Centro Nacional de Biotecnologia–CSIC set out to test whether DELLA proteins acted on GAs via phytochrome-interacting factors (PIFs), which activate genes involved in light-sensitive development. His team found that DELLA proteins block PIF4’s transcriptional activity by binding to its DNA-recognition domain. Under normal circumstances, PIF4 promotes growth of cells in the stem of Arabidopsis thaliana; when PIF4 is unable to bind with DNA, however, that cell growth does not occur.

In another twist, however, GAs can block this repression of PIF4 by targeting DELLA proteins for degradation by way of the ubiquitin system, says Salome Prat, a plant geneticist at the Centro Nacional de Biotecnologia–CSIC, and corresponding author of the study. With fewer DELLAs in the plant, PIF4’s transcription activity continues undisturbed, and the hypocotyl continues to grow.

“People had been generalizing that DELLA proteins inhibited GA gene expression by binding directly to the promoter region of a gene,” says Prat. “But our research found that they instead interfere with transcription factors—specifically PIF4.”

The team also discovered how light uses PIF4 to inhibit stem growth. Specifically, they found that light turns on phytochrome B, a light photoreceptor, which uses the ubiquitin-proteasome pathway to degrade PIF4’s transcription activity. Therefore, when light is present, PIF4 levels are kept low, which limits hypocotyl elongation.

The study was “the first clear indication of how DELLA works at a molecular level,” says Peter Hedden, a plant biologist at Rothamsted Research in the UK, who was not involved with the research. “It also nicely showed the interaction between light and GA signaling… giving us a clear understanding of how plants interact with their environment,” information that can be used to help improve plant development in various growing conditions.

This and a similar paper were published side by side in January 2008, when they triggered a widespread search for other DELLA targets. PIF4 is a member of a “small, but important class of transcription factors” known to regulate plant development and reproduction, says Hedden; researchers are now trying to map out how other transcription factors in this group interact with DELLA proteins.

Another clue unearthed

At the same time that de Lucas and colleagues were mapping the interactions with PIF4, researchers from Yale University were observing similar interactions between DELLA proteins and another phytochrome-interacting factor, PIF3, during plant development.

In another Hot Paper, Suhua Feng and his colleagues found that, as with PIF4, DELLA proteins prevent PIF3 from binding with its target genes, therefore preventing it from regulating light-mediated gene expression, including hypocotyl growth. Again, just as in the Madrid lab, GAs can use the ubiquitin proteasome pathways to degrade DELLA proteins, allowing PIF3 to accumulate and promote stem elongation. Feng and his colleagues even identified the GA receptor that triggers degradation of the DELLA proteins.

The two teams realized they had similar results while at a conference in Hungary in 2007. “Even after becoming aware of the connection, we continued to work independently,” says Xing Wang Deng, a plant biologist at Yale University and corresponding author of Feng’s paper. “But knowing that another team…had come to similar conclusions was definitely comforting.” Eventually, the two groups of researchers decided to join forces and submit their individual manuscripts to Nature at the same time.

Since the papers appeared, researchers have continued to describe how PIFs play a role in a plant’s ability to adapt to a shaded growing environment,4 temperature-regulated growth,5 and photomorphogenesis.6

And they have continued to try to investigate the interactions between DELLA proteins and the other members of PIF family of transcription factors, but have yet to confirm the specific mechanisms driving them. Scientists, for example, have shown that bHLH proteins, a family of transcription factors that include PIFs, also interact with DELLA proteins, but “the effect this has on function is still being investigated,” says Hedden.

Data derived from the Science Watch/Hot Papers database and the Web of Science (Thomson ISI) show that Hot Papers are cited 50 to 100 times more often than the average paper of the same type and age.
M. de Lucas et al., “A molecular framework for light and gibberellin control of cell elongation,” Nature, 451(7177):480–84, 2008. (Cited in 60 papers)
S. Feng et al., “Coordinated regulation of Arabidopsis thaliana development by light and gibberellins,” Nature, 451(7177):475–79, 2008. (Cited in 65 papers)
1. M. Chen et al., “Light signal transduction in higher plants,” Annu Rev Genet, 38:87–117, 2004.
2. D. Alabadi et al., “Gibberellins repress photomorphogenesis in darkness,” Plant Physiol, 134:1050–57, 2004.
3. T.P. Sun and F. Gubler, “Molecular mechanism of gibberellin signaling in plants,” Annu Rev Plant Biol, 55:197–223, 2004.
4. P. Hornitschek et al., “Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers,” Embo Journal, 28:3893–902, 2009.
5. J.A. Stavang et al., “Hormonal regulation of temperature-induced growth in Arabidopsis,” Plant J, 60:589–601, 2009.
6. S. Zhong et al., “EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings,” Proc Natl Acad Sci, 106:21431–36, 2009.

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