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Relieving DELLA Restraint

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Science  21 Mar 2003:
Vol. 299, Issue 5614, pp. 1853-1854
DOI: 10.1126/science.1083217

According to an old English nursery rhyme: “Oats and beans and barley grow, …, nor you nor I nor anyone knows how oats and beans and barley grow.” On page 1896 of this issue, Sasaki et al. (1) bring us closer to understanding the age-old mystery of plant growth.

The phytohormone gibberellin (GA) controls plant growth. Mutant plants deficient in GA are dwarfed, and treating these plants with GA restores normal growth (2). It is unclear exactly how plant cells detect GA, but our understanding of downstream GA signaling events is more advanced. A family of proteins, the DELLA proteins, are key intracellular repressors of GA responses (3, 4). The “relief-of-restraint” model proposes that DELLA proteins restrain plant growth, and that growth is promoted by a GA signal that relieves plants of DELLA-mediated growth restraint (2, 3).

Recent advances have put some biochemical and cellular flesh on the bones of the restraint model. For example, DELLA proteins are known to be localized in the nucleus of plant cells but disappear rapidly in response to GA (5, 6). In addition, the disappearance of the DELLA proteins induced by GA requires both protein phosphorylation and a functional 26S proteasome, the cellular organelle that degrades proteins (7).

Targeted degradation of regulatory proteins by the proteasome is an important mechanism for controlling cellular and developmental signaling in a wide variety of organisms. For example, the phytohormone auxin regulates plant development through proteasome-mediated degradation of members of the AUX/IAA family of auxin signaling proteins (8). Sasaki et al. (1) now rewrite the relief-of-restraint model in terms of specific GA-promoted targeting of DELLA proteins to the proteasome. First, they describe the properties of rice gid2 mutants. These mutants exhibit a dwarf phenotype resembling that conferred by GA deficiency. However, unlike GA-deficient rice mutants, gid2 mutants exhibit reduced GA responses and do not resume normal growth when treated with GA.

Molecular cloning revealed that the GID2 gene encodes a protein containing an F-box domain. F-box domains are found in specific components of the multisubunit SCF E3 ubiquitin ligase complex. This enzyme complex targets proteins for destruction in the proteasome by tagging them with a chain of ubiquitin molecules. GID2 may be part of an SCF complex and may interact with another SCF complex component called OsSkp2. In addition, GID2 turns out to be a rice ortholog of the SLY1 gene of Arabidopsis. SLY1 also encodes a positive regulator of GA signaling (9), which suggests that GID2 and SLY1 have similar functions.

Now that GID2 is established as a likely candidate component in a GA-specific SCF E3 ligase complex, what is the substrate of this complex? Could it be the rice DELLA protein SLR1 (6)? Sasaki et al. (1) show that in rice gid2-1 mutants SLR1 accumulates to high levels and is resistant to GA-induced degradation. Furthermore, the loss-of-function slr1-1 mutation suppressed the dwarf phenotype conferred by the gid2-1 allele, indicating that gid2 mutants are dwarfed because they accumulate SLR1. Finally, a ubiquitinated form of SLR1 could be detected in wild-type plants but not in gid2-1 mutants. Taken together, these results suggest that SLR1 is indeed the target of the presumed SCFGID2 E3 ubiquitin ligase complex. In many organisms, proteins targeted for ubiquitination by SCF E3 ubiquitin ligases are themselves first subjected to an initial modification, commonly phosphorylation. In further experiments, Sasaki et al. (1) reveal that phosphorylated SLR1 accumulates in gid2-1 mutant plants, and that GA can stimulate this accumulation.

These investigators outline the potential mechanics of the restraint model (see the figure). Through an unknown protein kinase, GA stimulates the phosphorylation of DELLA proteins. The SCFGID2 complex then polyubiquitinates phosphorylated DELLA proteins, which are subsequently degraded in the 26S proteasome. If correct, their proposal identifies the first case in plants of protein phosphorylation marking out a protein as a future substrate of an SCF E3 ubiquitin ligase.

A restraining order for plants.

The DELLA proteins, such as SLR1 in rice, restrain plant growth. In response to a GA signal, the DELLA proteins are first phosphorylated, then targeted for destruction in the proteasome by polyubiquitination. The addition of a polyubiquitin chain is catalyzed by the SCFGID2 E3 ligase. Degradation of the DELLA proteins releases the restraint on plant growth.

What's next? Immediate questions arise about the phosphorylation of the DELLA proteins. Which amino acid residues are phosphorylated in response to GA and which kinase is involved? How does GA stimulate phosphorylation? But for an overall understanding of plant growth regulation, we need to integrate our emerging understanding of GA signaling into the broader picture. One possible clue is the observation that auxin, as well as GA, controls growth through effects on the properties of DELLA proteins (10).

Sasaki and co-workers provide a biochemical definition of the relief-of- restraint model of plant growth regulation. The fact that both DELLA proteins and the GID2/SLY1 proteins have been highly conserved throughout evolution suggests that the discoveries outlined by Sasaki and colleagues advance our understanding of the growth of rice and Arabidopsis, of “oats and beans and barley” and indeed of higher plants in general.

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