Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus

David Gresham; Renata Usaite; Susanne Manuela Germann; Michael Lisby; David Botstein; Birgitte Regenberg

doi:10.1073/pnas.1014023107

Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus

David Gresham, Renata Usaite, Susanne Manuela Germann, Michael Lisby, David Botstein, Birgitte Regenberg

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

101 Citationer (Scopus)

Abstract

Udgivelsesdato: 2010-Oct

Originalsprog	Engelsk
Tidsskrift	Proceedings of the National Academy of Science of the United States of America
Vol/bind	107
Udgave nummer	43
Sider (fra-til)	18551-6
Antal sider	5
ISSN	0027-8424
DOI	https://doi.org/10.1073/pnas.1014023107
Status	Udgivet - 2010

Adgang til dokumentet

10.1073/pnas.1014023107

Citationsformater

Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. / Gresham, David; Usaite, Renata; Germann, Susanne Manuela et al.
I: Proceedings of the National Academy of Science of the United States of America, Bind 107, Nr. 43, 2010, s. 18551-6.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

@article{978ae930eca011dfb6d2000ea68e967b,

title = "Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus",

abstract = "To study adaptive evolution in defined environments, we performed evolution experiments with Saccharomyces cerevisiae (yeast) in nitrogen-limited chemostat cultures. We used DNA microarrays to identify copy-number variation associated with adaptation and observed frequent amplifications and deletions at the GAP1 locus. GAP1 encodes the general amino acid permease, which transports amino acids across the plasma membrane. We identified a self-propagating extrachromosomal circular DNA molecule that results from intrachromosomal recombination between long terminal repeats (LTRs) flanking GAP1. Extrachromosomal DNA circles (GAP1(circle)) contain GAP1, the replication origin ARS1116, and a single hybrid LTR derived from recombination between the two flanking LTRs. Formation of the GAP1(circle) is associated with deletion of chromosomal GAP1 (gap1¿) and production of a single hybrid LTR at the GAP1 chromosomal locus. The GAP1(circle) is selected following prolonged culturing in L-glutamine-limited chemostats in a manner analogous to the selection of oncogenes present on double minutes in human cancers. Clones carrying only the gap1¿ allele were selected under various non-amino acid nitrogen limitations including ammonium, urea, and allantoin limitation. Previous studies have shown that the rate of intrachromosomal recombination between tandem repeats is stimulated by transcription of the intervening sequence. The high level of GAP1 expression in nitrogen-limited chemostats suggests that the frequency of GAP1(circle) and gap1¿ generation may be increased under nitrogen-limiting conditions. We propose that this genomic architecture facilitates evolvability of S. cerevisiae populations exposed to variation in levels and sources of environmental nitrogen.",

author = "David Gresham and Renata Usaite and Germann, {Susanne Manuela} and Michael Lisby and David Botstein and Birgitte Regenberg",

year = "2010",

doi = "10.1073/pnas.1014023107",

language = "English",

volume = "107",

pages = "18551--6",

journal = "Proceedings of the National Academy of Science of the United States of America",

issn = "0027-8424",

publisher = "The National Academy of Sciences of the United States of America",

number = "43",

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T1 - Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus

AU - Gresham, David

AU - Usaite, Renata

AU - Germann, Susanne Manuela

AU - Lisby, Michael

AU - Botstein, David

AU - Regenberg, Birgitte

PY - 2010

Y1 - 2010

N2 - To study adaptive evolution in defined environments, we performed evolution experiments with Saccharomyces cerevisiae (yeast) in nitrogen-limited chemostat cultures. We used DNA microarrays to identify copy-number variation associated with adaptation and observed frequent amplifications and deletions at the GAP1 locus. GAP1 encodes the general amino acid permease, which transports amino acids across the plasma membrane. We identified a self-propagating extrachromosomal circular DNA molecule that results from intrachromosomal recombination between long terminal repeats (LTRs) flanking GAP1. Extrachromosomal DNA circles (GAP1(circle)) contain GAP1, the replication origin ARS1116, and a single hybrid LTR derived from recombination between the two flanking LTRs. Formation of the GAP1(circle) is associated with deletion of chromosomal GAP1 (gap1¿) and production of a single hybrid LTR at the GAP1 chromosomal locus. The GAP1(circle) is selected following prolonged culturing in L-glutamine-limited chemostats in a manner analogous to the selection of oncogenes present on double minutes in human cancers. Clones carrying only the gap1¿ allele were selected under various non-amino acid nitrogen limitations including ammonium, urea, and allantoin limitation. Previous studies have shown that the rate of intrachromosomal recombination between tandem repeats is stimulated by transcription of the intervening sequence. The high level of GAP1 expression in nitrogen-limited chemostats suggests that the frequency of GAP1(circle) and gap1¿ generation may be increased under nitrogen-limiting conditions. We propose that this genomic architecture facilitates evolvability of S. cerevisiae populations exposed to variation in levels and sources of environmental nitrogen.

AB - To study adaptive evolution in defined environments, we performed evolution experiments with Saccharomyces cerevisiae (yeast) in nitrogen-limited chemostat cultures. We used DNA microarrays to identify copy-number variation associated with adaptation and observed frequent amplifications and deletions at the GAP1 locus. GAP1 encodes the general amino acid permease, which transports amino acids across the plasma membrane. We identified a self-propagating extrachromosomal circular DNA molecule that results from intrachromosomal recombination between long terminal repeats (LTRs) flanking GAP1. Extrachromosomal DNA circles (GAP1(circle)) contain GAP1, the replication origin ARS1116, and a single hybrid LTR derived from recombination between the two flanking LTRs. Formation of the GAP1(circle) is associated with deletion of chromosomal GAP1 (gap1¿) and production of a single hybrid LTR at the GAP1 chromosomal locus. The GAP1(circle) is selected following prolonged culturing in L-glutamine-limited chemostats in a manner analogous to the selection of oncogenes present on double minutes in human cancers. Clones carrying only the gap1¿ allele were selected under various non-amino acid nitrogen limitations including ammonium, urea, and allantoin limitation. Previous studies have shown that the rate of intrachromosomal recombination between tandem repeats is stimulated by transcription of the intervening sequence. The high level of GAP1 expression in nitrogen-limited chemostats suggests that the frequency of GAP1(circle) and gap1¿ generation may be increased under nitrogen-limiting conditions. We propose that this genomic architecture facilitates evolvability of S. cerevisiae populations exposed to variation in levels and sources of environmental nitrogen.

U2 - 10.1073/pnas.1014023107

DO - 10.1073/pnas.1014023107

M3 - Journal article

C2 - 20937885

SN - 0027-8424

VL - 107

SP - 18551

EP - 18556

JO - Proceedings of the National Academy of Science of the United States of America

JF - Proceedings of the National Academy of Science of the United States of America

IS - 43

ER -