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Brief Communications Arising

Nature 443, E8 (28 September 2006) | doi:10.1038/nature05251; Published online 27 September 2006

Plant genetics: Increased outcrossing in hothead mutants

Peng Peng1,2, Simon W.-L. Chan2,3, Govind A. Shah2 and Steve E. Jacobsen1,2

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Abstract

Arising from: S. J. Lolle, J. L. Victor, J. M. Young & R. E. Pruitt Nature 434, 505–509 (2005); Lolle et alreply

Lolle et al.1 report that loss-of-function alleles of the HOTHEAD (HTH) gene in Arabidopsis thaliana are genetically unstable, giving rise to wild-type revertants. On the basis of the reversion of many other genetic markers in hth plants, they suggested a model in which a cache of extragenomic information could cause genes to revert to the genotype of previous generations. In our attempts to reproduce this phenomenon, we discovered thathth mutants show a marked tendency to outcross (unlike wild-type A. thaliana, which is almost exclusively self-fertilizing2). Moreover, when hthplants are grown in isolation, their genetic inheritance is completely stable. These results may provide an alternative explanation for the genome wide non-mendelian inheritance reported by Lolle et al.

Initially, we constructed hth-12 gl1-4 double-mutant plants in the Columbia ecotype, reasoning that HTH and GL1 should revert independently because they are on different chromosomes. hth-12 DNA carries a transfer-DNA (T-DNA) insertion (SALK_024611) and gl1-4 is a guanine-to-adenine (G-to-A) transition mutation (like that shown previously to revert1) that changes the start codon of the trichome gene GL1 (ref. 3) from ATG to ATA. Among 1,597 progeny of hth-12 gl1-4 plants, 10 were phenotypically GL1 (normal trichomes). Genotyping based on polymerase chain reaction showed that nine were heterozygous for gl1-4, and one was GL1/GL1. Surprisingly, the nine GL1/gl1-4 plants were also heterozygous for hth-12, and the GL1/GL1 homozygote was homozygous for HTH. These observations are most easily explained by pollen contamination (nine heterozygous plants) and seed contamination (one homozygous plant). We also found a single hth-12 heterozygote that was still homozygous for gl1-4, which could be explained by pollen contamination from nearby gl1-4 plants.

To test whether pollen contamination could be a source of apparent hth genetic reversion, we grew homozygous hth-12 plants either in a mixed population (near to, but not touching, plants with varied genotypes) or in an isolated room containing only hth-12 plants. In one experiment, the progeny of plants grown in the mixed-growth room showed 19/245 revertants (Table 1). Eighteen of nineteen revertants segregated the erectaphenotype in the next generation, suggesting that they arose from pollen contamination by nearby erecta-containing plants.


In a second mixed-population experiment, 18/415 plants were phenotypically HTH. All 18 contained a BIN2-1::GFP transgene4, which was present in other plants grown in the room (Table 1). In contrast, not a single revertant was found among 932 progeny of hth-12 plants grown in isolation.

We repeated these experiments with the originally reported hth-8 and hth-5 alleles in the Landsberg erecta (Ler) ecotype1, 5. We found that hth-8plants grown in mixed populations yielded 156/994 progeny with a HTH phenotype. Most were either ERECTA or contained BIN2-1::GFP (Table 1). However, hth-8 plants grown in isolation gave exclusively hth progeny, none of which was ERECTA (Table 1). Similar results were obtained with hth-5.

Our results indicate that hth mutants are particularly susceptible to pollen contamination, possibly because the hth floral organ fusion defects lead to inefficient self-pollination and exerted stigmas1, or because of changes in cuticle composition5. This tendency to outcross may provide an alternative explanation for the apparent genetic instability of hothead mutants.

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References

  1. Lolle, S. J., Victor, J. L., Young, J. M. & Pruitt, R. E. Nature 434, 505–509 (2005). | Article | PubMed | ISI | ChemPort |
  2. Abbott, R. J. & Gomes, M. F. Heredity 62, 411–418 (1989). | ISI |
  3. Herman, P. L. & Marks, M. D. Plant Cell 1, 1051–1055 (1989). | Article | PubMed | ChemPort |
  4. Li, J. & Nam, K. H. Science 295, 1299–1301 (2002). | PubMed | ISI | ChemPort |
  5. Krolikowski, K. A., Victor, J. L., Wagler, T. N., Lolle, S. J. & Pruitt, R. E. Plant J. 35, 501–511 (2003). | Article | PubMed | ChemPort |
  1. Howard Hughes Medical Institute, University of California, Los Angeles, California 90095, USA
  2. Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, California 90095, USA
  3. Present address: Section of Plant Biology, University of California, Davis, California 95616, USA

Correspondence to: Steve E. Jacobsen1,2 Email: jacobsen@ucla.edu

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