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Hsp90 as a capacitor of phenotypic variation


Heat-shock protein 90 (Hsp90) chaperones the maturation of many regulatory proteins and, in the fruitfly Drosophila melanogaster, buffers genetic variation in morphogenetic pathways. Levels and patterns of genetic variation differ greatly between obligatorily outbreeding species such as fruitflies and self-fertilizing species such as the plant Arabidopsis thaliana. Also, plant development is more plastic, being coupled to environmental cues. Here we report that, in Arabidopsis accessions and recombinant inbred lines, reducing Hsp90 function produces an array of morphological phenotypes, which are dependent on underlying genetic variation. The strength and breadth of Hsp90's effects on the buffering and release of genetic variation suggests it may have an impact on evolutionary processes. We also show that Hsp90 influences morphogenetic responses to environmental cues and buffers normal development from destabilizing effects of stochastic processes. Manipulating Hsp90's buffering capacity offers a tool for harnessing cryptic genetic variation and for elucidating the interplay between genotypes, environments and stochastic events in the determination of phenotype.

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Figure 1: Common GDA-dependent phenotypes in Shadara, Col and Ler accessions.
Figure 2: The same RI line-specific phenotypes are uncovered when buffering capacity is challenged by GDA (middle) and by growth at 27 °C (right).
Figure 3: The effect of GDA on developmental plasticity responses differs between 50 Cvi/Ler RI lines and their parents.
Figure 4: F1 progeny of accession crosses exhibit higher diversity and greater phenotype complexity than parental accessions, especially with GDA.
Figure 5: F1 progeny grow more robustly in the presence of 2 µM GDA than do parental accessions.

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We thank H. Oakley, A. Evans and the University of Chicago greenhouse staff for technical help. We are especially grateful to J. Malamy, J. Greenberg, D. Preuss, J. Borevitz, J. Maloof and members of the Lindquist laboratory for advice and discussions, and to N. Patel for use of equipment and comments. We thank the ABRC for seeds. T.A.S. is a Howard Hughes Medical Institute pre-doctoral fellow. S.L. thanks the Howard Hughes Medical Institute and the National Institutes of Health for their support.

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Correspondence to Susan Lindquist.

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Queitsch, C., Sangster, T. & Lindquist, S. Hsp90 as a capacitor of phenotypic variation. Nature 417, 618–624 (2002).

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