Plant inheritance mechanism sparks controversy

pruitt-mutant

One of the HOTHEAD mutants of the original study.
(source: Andrea Gawrylewski)

Last month, two papers reawakened a debate dating back to 2005 regarding an unusual non-Mendelian inheritance mechanism in the model plant Arabidopsis thaliana. If true, the proposed mechanism of inheritance would contradict everything we know about how parental traits are passed on to subsequent generations in this model organism. The research was published in the open access online journal F1000 Research, in which peer review occurs post-publication and is available for public comment.

In 2005 Dr Robert Pruitt at Purdue University and his collaborator Susan Lolle, then at Harvard University, found that a parental deleterious version of the HOTHEAD gene, which causes the reproductive parts of the flower to curl up and remain fused together, was reverting to the wild type version at low percentages in the first generation progeny of crosses in which both parents were homozygous for the deleterious mutation. A small fraction of the progeny of parental crosses with the fused, underdeveloped flowers typical of HOTHEAD mutants surprisingly had fully developed flowers. Sequencing the gene demonstrated that the gene itself was reverting back to the ancestral, wild type version.

The research, published in Nature in March 2005, provoked much controversy by suggesting that Arabidopsis plants may be able to rewrite their DNA to replace genes to ancestral versions different from that of their parents. The authors postulated that the reservoir of ancestral genetic information providing the template for such rewriting could be provided by RNA stored in reproductive cells passed down from generation to generation. Experimental data released in 2006 and 2008 from research groups at UCLA and at the French National Institute for Agricultural Research failed to replicate their results, however. The “RNA cache” explanation, which was strongly preferred by Pruitt and Lolle, was questioned by several members of the scientific community who believed the small percentage of revertants to be the result of contamination by foreign pollen from plants that still carried the ancestral gene.

One of the authors of the original study, now a plant geneticist at the University of Waterloo, in Canada, has now published additional evidence confirming this phenomenon. After screening over 300 000 mutant plants that were housed in two separate buildings and on two different floors, the authors believe to have proved beyond any reasonable doubt that the genetic rewriting is actually occurring and is not due to outcrossing of the mutant strain with the wild type strain. A second paper published by an independent group, also in F1000 Research, appears to confirm their findings.

Researchers have known of a similar phenomenon in plants, called paramutation, for nearly 90 years. In maize, for example, a perfectly normal pigmentation gene can act as if it is mutated, simply because one of the plant’s parents carried a mutated version. Paramutation however describes a heritable change of gene expression – an epigenetic change – that is brought about through interactions between homologous chromosomes, and doesn’t involve any actual rewriting of the sequence of the gene. In 2006, a Nature paper by a team of French researchers demonstrated paramutation in mice. A similar process may be active also in humans, as suggested by a 1997 paper which found that a gene may influence type 1 diabetes depending on whether the paternal allele, even if untransmitted, had a specific mutation in it. Information regarding paternal alleles could be stored in the form of RNA, which is present in sperm and is passed on to the next generation.

This post was written by:

Stefano Iantorno Stefano Iantorno View author bio

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