Evolvability of yeast with prions

From: pruest@pop.dplanet.ch
Date: Thu Oct 19 2000 - 14:52:41 EDT

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    Marcio Pie wrote:

    > Date: Mon, 9 Oct 2000 14:24:59 -0400 (EDT)
    > From: Marcio Pie <pie@bu.edu>
    > Subject: interesting article
    >
    > Hi there!
    >
    > An interesting article came out recently in Nature on how a prion may
    > improve the "evolvability" of yeast. This may have some relevance
    > regarding some ID hypotheses. I'd love to hear your comments on this.
    >
    > Best
    >
    > Marcio
    >
    > http://www.nature.com/cgi-taf/DynaPage.taf?file=/nature/journal/v407/n6803/abs/407477a0_fs.html
    >
    > Nature 407, 477 - 483 (2000)
    >
    > A yeast prion provides a mechanism for genetic variation and phenotypic
    > diversity
    >
    > HEATHER L. TRUE AND SUSAN L. LINDQUIST
    >
    > A major enigma in evolutionary biology is that new forms or functions
    > often require the concerted effects of several independent genetic
    > changes. It is unclear how such changes might accumulate when they are
    > likely to be deleterious individually and be lost by selective pressure.
    > The Saccharomyces cerevisiae prion [PSI+] is an epigenetic modifier of the
    > fidelity of translation termination, but its impact on yeast biology has
    > been unclear. Here we show that [PSI+] provides the means to uncover
    > hidden genetic variation and produce new heritable phenotypes. Moreover,
    > in each of the seven genetic backgrounds tested, the constellation of
    > phenotypes produced was unique. We propose that the epigenetic and
    > metastable nature of [PSI+] inheritance allows yeast cells to exploit
    > pre-existing genetic variation to thrive in fluctuating environments.
    > Further, the capacity of [PSI+] to convert previously neutral genetic
    > variation to a non-neutral state may facilitate the evolution of new
    > traits.

    In the same issue of Nature, there is a companion article to this one,
    commenting on it: Linda Partridge & Nicholas H. Barton, "Evolving
    evolvability", Nature 407 (2000), 457-458. But the following comments
    are my own.

    Another mechanism for the activation of cryptic genome sequences has
    been known for a long time. After a gene duplication, one of the copies
    may be inactivated by a mutation producing a stop codon in the open
    reading frame or an inactivating mutation in a control element. From
    then on, the gene is a pseudogene, hidden from the effects of purifying
    selection. That is, it can accumulate any number of mutations which
    might otherwise be lethal. At any time the first (inactivating) mutation
    may be reversed, and the possibly heavily modified gene is activated and
    tested for function by natural selection. It is conceivable that other
    genome sequences, apart from pseudogenes, may suddenly be activated by a
    mutation in a control element, or by the emergence of a new splicing
    signal.

    The prion system, like a mutation in any translation factor, may
    interfere with many genes at once. What makes the prion system a very
    special case is that a prion is autocatalytically produced from its
    "normal" cellular conformer. The yeast prion [PSI+] is a
    self-aggregating conformer of the "natural", non-aggregating translation
    termination factor Sup35. Both forms have the same primary sequence, but
    different tertiary structures. Even one single molecule of the prion
    conformation catalyzes the conformational change of Sup35 molecules into
    the prion form, such that all Sup35 in the cell is transformed into
    prions, which aggregate, disrupting the normal translation termination.
    Within the given cell line, this "epigenetic" change is heritable. But
    it can be reversed by counterselection.

    In their paper, True & Lindquist show many effects of the switch between
    Sup35 [psi-] and prion [PSI+], but in no case it is known how these
    growth and colony morphology changes arose. There is no evidence that
    any new information was used (rather than inactivation or attenuation of
    wild-type functionality or regulatory mechanisms).

    But wether or not any new information is activated, the Sup35-prion
    switch certainly supplies yeast with a useful means of adaptability to
    changing environments. And in case a stop codon "blinded" by the lack of
    Sup35 is mutated while the cell is under prion influence, the epigenetic
    change is genetically fixed, and an evolutionary step has occurred.

    Both the pseudogene and the prion systems, however, can only activate
    something that already exists. If this is to be a new functionality, it
    must have emerged by a mutational random walk in the cryptic state,
    hidden from natural selection. Can we expect really novel
    functionalities to emerge by such random processes extending over
    several mutations, but without intermediate selection?

    This is the question I posed in my post of 22 Sep 2000 13:51:34 +0200
    (asa-digest V1 #1804, 23 Sep 2000 09:20:01 -0000): how many specific
    amino acid substitutions can we reasonably expect in a random mutational
    walk before selection for a newly emerging activity sets in? Up to now,
    no one on this list has tried to deal with it.

    Whether the yeast prion system displays "evolving evolvability" is, at
    present, purely a matter of speculation. In his post of 15 Oct 2000
    16:18:52 +0100, Glenn Morton, "How Irreducibly Complex Systems Evolve.
    Data Behe must deal with", tried to apply it to the spontaneous
    emergence of a combination of interdependent functions, in order to
    invalidate Michael Behe's concept of irreducibly complex systems.
    However, this just augments the number of required mutations that must
    happen independently and without any selection. It is equivalent to the
    set of the total number of independent non-selected mutations required
    for the realization of the entire "irreducibly complex" system, no
    matter whether they have to occur in one or in several genes. The
    probability of occurrence of such a coincidence, however, is not
    increased at all by the prion system. A prion switch might only help the
    cell discover it, once it has occurred.

    Peter Ruest



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