TY - JOUR
T1 - Chromosomal duplication is a transient evolutionary solution to stress
AU - Yona, Avihu H.
AU - Manor, Yair S.
AU - Herbst, Rebecca H.
AU - Romano, Gal H.
AU - Mitchell, Amir
AU - Kupiec, Martin
AU - Pilpel, Yitzhak
AU - Dahan, Orna
N1 - Ben May Charitable Trust; Minerva Foundation; Israel Science Foundation; Israeli Ministry of Science and Technology; Machiah Foundation; Safra program for bioinformatics grantWe thank Jasmin Bloch, Sharon Reikhav, and Miri Carmi for assistance with the CGH microarray. Y.P. acknowledges support from the Ben May Charitable Trust, the Minerva Foundation, and the Bikura program of the Israel Science Foundation; Y.P. is an incumbent of the Ben May Professorial Chair. M.K. acknowledges support from the Israel Science Foundation and the Israeli Ministry of Science and Technology. G.H.R. was supported by a Machiah Foundation grant and by a Safra program for bioinformatics grant.
PY - 2012/12/18
Y1 - 2012/12/18
N2 - Aneuploidy, an abnormal number of chromosomes, is a widespread phenomenon found in unicellulars such as yeast, as well as in plants and in mammalians, especially in cancer. Aneuploidy is a genomescale aberration that imposes a severe burden on the cell, yet under stressful conditions specific aneuploidies confer a selective advantage. This dual nature of aneuploidy raises the question of whether it can serve as a stable and sustainable evolutionary adaptation. To clarify this, we conducted a set of laboratory evolution experiments in yeast and followed the long-term dynamics of aneuploidy under diverse conditions. Herewe showthat chromosomal duplications are first acquired as a crude solution to stress, yet only as transient solutions that are eliminated and replaced by more efficient solutions obtained at the individual gene level. These transient dynamics of aneuploidy were repeatedly observed in our laboratory evolution experiments; chromosomal duplications gained under stress were eliminated not only when the stress was relieved, but even if it persisted. Furthermore, when stress was applied gradually rather than abruptly, alternative solutions appear to have emerged, but not aneuploidy. Our findings indicate that chromosomalduplicationis afirst evolutionary line of defense, that retains survivability under strong and abrupt selective pressures, yet it merely serves as a "quick fix," whereas more refined and sustainable solutions take over. Thus, in the perspective of genome evolution trajectory, aneuploidy is a useful yet short-lived intermediate that facilitates further adaptation.
AB - Aneuploidy, an abnormal number of chromosomes, is a widespread phenomenon found in unicellulars such as yeast, as well as in plants and in mammalians, especially in cancer. Aneuploidy is a genomescale aberration that imposes a severe burden on the cell, yet under stressful conditions specific aneuploidies confer a selective advantage. This dual nature of aneuploidy raises the question of whether it can serve as a stable and sustainable evolutionary adaptation. To clarify this, we conducted a set of laboratory evolution experiments in yeast and followed the long-term dynamics of aneuploidy under diverse conditions. Herewe showthat chromosomal duplications are first acquired as a crude solution to stress, yet only as transient solutions that are eliminated and replaced by more efficient solutions obtained at the individual gene level. These transient dynamics of aneuploidy were repeatedly observed in our laboratory evolution experiments; chromosomal duplications gained under stress were eliminated not only when the stress was relieved, but even if it persisted. Furthermore, when stress was applied gradually rather than abruptly, alternative solutions appear to have emerged, but not aneuploidy. Our findings indicate that chromosomalduplicationis afirst evolutionary line of defense, that retains survivability under strong and abrupt selective pressures, yet it merely serves as a "quick fix," whereas more refined and sustainable solutions take over. Thus, in the perspective of genome evolution trajectory, aneuploidy is a useful yet short-lived intermediate that facilitates further adaptation.
KW - Environmental stress
KW - Evolutionary dynamics
KW - Heat tolerance
KW - pH tolerance
UR - http://www.scopus.com/inward/record.url?scp=84871375832&partnerID=8YFLogxK
U2 - 10.1073/pnas.1211150109
DO - 10.1073/pnas.1211150109
M3 - مقالة
C2 - 23197825
SN - 0027-8424
VL - 109
SP - 21010
EP - 21015
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 51
ER -