On the potential for evolutionary change in meristematic cell lineages through intraorganismal selection

Abstract

In the absence of sexual recombination somatic mutations represent the only source of genetic variation in clonally propagating plants. We analyse the probability of such somatic mutations in the shoot apical meristem being fixed in descendant generations of meristems. A model of meristem cell dynamics is presented for the unstratified shoot apical meristem. The fate of one mutant initial is studied for a two‐ and three‐celled shoot apical meristem. The main parameters of the model are the number of apical initials, the time between selection cycles, number of selection cycles and cell viability of the mutant genotype. As the number of mitotic divisions per selection cycle and number of selection cycles increases the chimeric state dissipates and the probability of mutation fixation approaches an asymptote. The value of this fixation asymptote depends primarily on cell viability, while the time to reach it is mainly influenced by the total number of mitotic divisions as well as the number of initials. In contrast to the presumed operation of Muller’s Ratchet in plants the chimeric state may represent an opportunity for deleterious mutations to be eliminated through intraorganismal selection or random drift. We conclude that intraorganismal selection not only can be a substantial force for the elimination of deleterious mutations, but also can have the potential to confer an evolutionary change through a meristematic cell lineage alone.

Cell Lineage Dynamics in Stratified Shoot Apical Meristems

“…Previous works on the cell dynamics of unstratified SAMs have shown that by virtue of the small number of initials, the probability of a mutant lineage rapidly going to fixation through drift is high (Pineda-Krch & Fagerstro¨m, 1999). By devising a general, spatially explicit, model of a stratified SAM, we addressed two main aspects of the dynamics: the probability of a mutant lineage going to fixation and the time it takes.…”

“…If a genetic change occurs in a meristematic cell, the ensuing ramet or branch may become genetically heterogeneous encompassing multiple genetically distinct lineages. The fate of the mutant lineage depends on several factors such as the organization and dynamics of the meristem, drift, intraorganismal selection (Pineda-Krch & Fagerstro¨m, 1999) as well as details of the life cycle, e.g. ploidy (Poore & Fagerstro¨m, 2000).…”

“…the module level and organism level), it may reach fixation by n replacing the wild-type lineage. Previous works on the fate of mutant lineages in SAMs have shown that there is a high probability for a mutant lineage to rapidly replace the wild type through intraorganismal selection or through drift even when the mutant lineage is deleterious (Klekowski, 1988;Pineda-Krch & Fagerstro¨m, 1999). Most of these models have assumed the meristem to be composed of a spatially unstructured population of cells, i.e.…”

Plant individuality: a solution to the demographer’s dilemma

“…Stochastic meristems, which are found in gymnosperms (Cycads, conifers and Gingkos) do support a limited amount of between-cell selection because there is a pool of meristem cells which divide several times before the ones destined to differentiate are picked stochastically. Mutants which divide faster can easily spread through the pool of meristems and gain themselves better than average chances of being picked to remain in the germ line (Klekowski and Kazarinova-Fukshansky 1984;Pineda-Krch and Fagerström 1999).…”

Ecology and Evolutionary Biology of Clonal Plants

“…If evolutionary change can occur without sexual reproduction, it is conceivable that genetically different individuals have originated from a succession of genetically different ramet generations without involving sexual reproduction (Fagerstrom et al, 1998;Pineda-Krch and Fagerstrom, 1999), as in the case of C. taxi/olia. In marine macroalgae, the production of mitotically derived and genetically different individuals can occur during different phases (diploid and haploid) of their life cycle, so we can expect that intraclonal variation will contribute substantially to levels of genetic variation of each phase and of the general population Fagerstrom, 2000, 2001).…”