Great leap forward? Transposable elements, small interfering RNA and adaptive Lamarckian evolution

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(Author for correspondence: tel +1 516 367 8466; fax +1 516 367 8369; email martiens@cshl.edu)

The botanist and philosopher Lamarck famously proposed that environmental challenges suffered in one generation could influence phenotypic outcomes in the next. At the turn of the 19th century, the passing of life experiences to future generations seemed part of the natural order, explaining perhaps the acclimation of new species imported from exotic locales and the perceived increase in biological complexity over generations. Lamarckian principles influenced Darwin's vision of natural selection, but were ultimately overturned by this very vision. With the rediscovery of Mendel's laws, Lamarckian mechanisms became less plausible, and with the advent of molecular genetics, the writing was on the wall. How could the environment influence germ cells in such a way that genes were altered in a directed and heritable way? In this issue of New Phytologist, Hilbricht et al. (pp. 877–887) provide a potential example of environmental influence on evolution and inheritance, in the desiccation-tolerant ‘resurrection’ plant Craterostigma plantagineum. They provide evidence that desiccation induces a family of non-Long Terminal Repeat (LTR) retrotransposons that encode a small RNA which promotes the expression of dehydration genes in transformed callus. They propose that transposition, on the one hand, and small RNA, on the other, have driven the evolution of this remarkable property (Fig. 1).

Figure 1.

Effect of desiccation treatment on the ‘resurrection’ plant Craterostigma plantagineum: fully turgid (a), desiccated (b) and rehydrated (c). The timescale for the rehydration shown is 12 h (see Bartels et al., 1990). Image courtesy of D. Bartels, Bonn, Germany.

‘... a combination of the two stress response mechanisms – amplification of the transposon on the one hand, and triggering stress tolerance on the other – presents an interesting case for students of Lamarck.’

In most animals the germline differentiates within a few days after fertilization of the egg, long before adult cell types. As a result, any environmental influence on the adult must modify genetic material in cells that are already committed to germline fate. In long-lived flowering plants, however, germ cells can differentiate hundreds of years after embryogenesis is complete. This is because the germline is set aside very late in development, differentiating from inflorescence meristems that in this respect resemble adult rather than germline stem cell lineages. This makes plants uniquely sensitive to environmental effects (Walbot & Evans, 2003).

Even so, many of these effects are transient and are not captured in the germline. Examples include vernalization, in which adult plant cells experience cold during winter and trigger flowering the following spring. This is accomplished by silencing key regulatory genes through histone modification (Dennis & Peacock, 2007). Vernalization requires long exposure to the stimulus, and only dividing cells respond. It is thought that RNA interference may mediate some of these cues. Importantly, vernalization is erased during meiosis so that the next generation can respond to cold at the appropriate time. However, some epigenetic changes are heritable in plants: for example, many transposable elements are also very sensitive to temperature, but silent transposons can be stably inherited from generation to generation (Slotkin & Martienssen, 2007).

Epigenetic mechanisms allow alternative chromosomal (and even nonchromosomal) states to be inherited from cell to cell and from generation to generation. When these states are influenced by the environment, progeny adopt their parents’ response without necessarily being subject to the same stimulus. While perhaps not the deterministic mechanism imagined by Lamarck, such epigenetic mechanisms open up the possibility of the environment directing evolution. An interesting example is provided by paramutation in maize: the R locus encodes a gene family interrupted by transposable elements. Silencing of one of these genes occurs progressively during development, but is delayed at high temperatures. By the time germ cells develop from the inflorescence meristem, few of them contain silent genes, but those that remain silent are passed on to the next generation (Chandler et al., 2000). Interestingly, this temperature-sensitive phenomenon depends on RNA interference (Chandler, 2007).

Craterostigma plantagineum is a desert succulent that can lose up to 96% of its water but still recover just hours after rehydration (Fig. 1). This property is not shared by callus, which needs a supply of exogenous abscisic acid (ABA) to recover from dehydration. The authors isolated genes that could bypass this ABA requirement through activation tagging – the callus was transformed with transfer DNA (T-DNA) carrying a strong promoter and then subjected to dehydration in the absence of ABA. Survivors were examined to see which gene was responsible for the control of desiccation tolerance. Surprisingly, the first such gene to be identified, CDT-1, did not encode a functional protein. Worse, it was found in multiple copies and terminated with a polyA tail, flanked by direct repeats. These are hallmarks of non-LTR retrotransposons, or short interspersed elements (SINEs). One redeeming feature was that CDT-1 was induced by ABA and dehydration in normal callus, supporting its role in desiccation tolerance.

How could a transposon influence desiccation tolerance? Deletions indicated that only half of the element, including the polyA tail, was required for high levels of transcript accumulation and for desiccation tolerance. A second gene detected by T-DNA insertion, CDT-2, shared this region. Abundant short interfering RNA was found on both strands and was narrowed down to a 21-nucleotide sequence reminiscent of a micro RNA or perhaps a trans-acting or tasiRNA. Protoplast transfection was used to show that this small RNA alone was capable of inducing dehydration genes, an important step in desiccation tolerance, to the same extent as exogenous application of the hormone ABA.

The expression of transposons under environmental stress is well known: the resulting transposition is thought to increase chances of inheritance by the next generation, ensuring survival of the transposon (Slotkin & Martienssen, 2007). This response seems to have been co-opted during evolution, such that CDT-1 transposons now encode a small RNA that is required for desiccation tolerance and is induced by dehydration. However, a combination of the two stress response mechanisms – amplification of the transposon on the one hand, and triggering stress tolerance on the other – presents an interesting case for students of Lamarck: this is because, over generations, plants with an increased CDT copy number might be more desiccation tolerant. Unlike other transposons, non-LTR retrotransposons are difficult to remove from the genome. This is because they undergo widespread transposition but cannot undergo excision like Class II elements, or recombination between homologous LTRs like other Class I transposons. When co-opted in this way they may take their host on a journey of no return (Dover, 2002). A great leap forward indeed.

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