Novelty and Convergence in Adaptation to Whole Genome
Duplication

J 2021

Novelty and Convergence in Adaptation to Whole Genome Duplication

BOHUTINSKA, M., M. ALSTON, P. MONNAHAN, Terezie MALÍK MANDÁKOVÁ, S. BRAY et. al.

Basic information

Original name

Novelty and Convergence in Adaptation to Whole Genome Duplication

Authors

BOHUTINSKA, M., M. ALSTON, P. MONNAHAN, Terezie MALÍK MANDÁKOVÁ (203 Czech Republic, guarantor, belonging to the institution), S. BRAY, P. PAAJANEN, F. KOLAR and L. YANT

Edition

Molecular Biology and Evolution, OXFORD, OXFORD UNIV PRESS, 2021, 0737-4038

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10611 Plant sciences, botany

Country of publisher

United Kingdom of Great Britain and Northern Ireland

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 8.800

RIV identification code

RIV/00216224:14740/21:00119674

Organization unit

Central European Institute of Technology

DOI

http://dx.doi.org/10.1093/molbev/msab096

UT WoS

000693664800031

Keywords in English

polyploidy; convergence; genome duplication; adaptation

Abstract

V originále

Whole genome duplication (WGD) can promote adaptation but is disruptive to conserved processes, especially meiosis. Studies in Arabidopsis arenosa revealed a coordinated evolutionary response to WGD involving interacting proteins controlling meiotic crossovers, which are minimized in an autotetraploid (within-species polyploid) to avoid missegregation. Here, we test whether this surprising flexibility of a conserved essential process, meiosis, is recapitulated in an independent WGD system, Cardamine amara, 17 My diverged from A. arenosa. We assess meiotic stability and perform population-based scans for positive selection, contrasting the genomic response to WGD in C. amara with that of A. arenosa. We found in C amara the strongest selection signals at genes with predicted functions thought important to adaptation to WGD: meiosis, chromosome remodeling, cell cycle, and ion transport. However, genomic responses to WGD in the two species differ: minimal ortholog-level convergence emerged, with none of the meiosis genes found in A. arenosa exhibiting strong signal in C amara. This is consistent with our observations of lower meiotic stability and occasional clonal spreading in diploid C amara, suggesting that nascent C. amara autotetraploid lineages were pre-adapted by their diploid lifestyle to survive while enduring reduced meiotic fidelity. However, in contrast to a lack of ortholog convergence, we see process-level and network convergence in DNA management, chromosome organization, stress signaling, and ion homeostasis processes. This gives the first insight into the salient adaptations required to meet the challenges of a WGD state and shows that autopolyploids can utilize multiple evolutionary trajectories to adapt to WGD.

Links

GA19-03442S, research and development project

Name: Geny pro ribozomální RNA - cestovatelé v čase a genomech

Investor: Czech Science Foundation, Ribosomal RNA genes - travellers in time and the genomes

GA19-06632S, research and development project

Name: Vliv hybridizace a alopolyploidizace na diverzitu ve třech tribech čeledi Brassicaceae

Investor: Czech Science Foundation, How hybridisation and allopolyploidisation affect the diversity in three Brassicaceae tribes

LM2018140, research and development project

Name: e-Infrastruktura CZ (Acronym: e-INFRA CZ)

Investor: Ministry of Education, Youth and Sports of the CR

LQ1601, research and development project

Name: CEITEC 2020 (Acronym: CEITEC2020)

Investor: Ministry of Education, Youth and Sports of the CR

Citovat

BOHUTINSKA, M., M. ALSTON, P. MONNAHAN, Terezie MALÍK MANDÁKOVÁ, S. BRAY, P. PAAJANEN, F. KOLAR and L. YANT. Novelty and Convergence in Adaptation to Whole Genome Duplication. Molecular Biology and Evolution. OXFORD: OXFORD UNIV PRESS, 2021, vol. 38, No 9, p. 3910-3924. ISSN 0737-4038. Available from: https://dx.doi.org/10.1093/molbev/msab096.

@article{1837982,
   author = {Bohutinska, M. and Alston, M. and Monnahan, P. and Malík Mandáková, Terezie and Bray, S. and Paajanen, P. and Kolar, F. and Yant, L.},
   article_location = {OXFORD},
   article_number = {9},
   doi = {http://dx.doi.org/10.1093/molbev/msab096},
   keywords = {polyploidy; convergence; genome duplication; adaptation},
   language = {eng},
   issn = {0737-4038},
   journal = {Molecular Biology and Evolution},
   title = {Novelty and Convergence in Adaptation to Whole Genome Duplication},
   url = {https://academic.oup.com/mbe/article/38/9/3910/6203814},
   volume = {38},
   year = {2021}
}

TY  - JOUR
ID  - 1837982
AU  - Bohutinska, M. - Alston, M. - Monnahan, P. - Malík Mandáková, Terezie - Bray, S. - Paajanen, P. - Kolar, F. - Yant, L.
PY  - 2021
TI  - Novelty and Convergence in Adaptation to Whole Genome Duplication
JF  - Molecular Biology and Evolution
VL  - 38
IS  - 9
SP  - 3910-3924
EP  - 3910-3924
PB  - OXFORD UNIV PRESS
SN  - 07374038
KW  - polyploidy
KW  - convergence
KW  - genome duplication
KW  - adaptation
UR  - https://academic.oup.com/mbe/article/38/9/3910/6203814
N2  - Whole genome duplication (WGD) can promote adaptation but is disruptive to conserved processes, especially meiosis. Studies in Arabidopsis arenosa revealed a coordinated evolutionary response to WGD involving interacting proteins controlling meiotic crossovers, which are minimized in an autotetraploid (within-species polyploid) to avoid missegregation. Here, we test whether this surprising flexibility of a conserved essential process, meiosis, is recapitulated in an independent WGD system, Cardamine amara, 17 My diverged from A. arenosa. We assess meiotic stability and perform population-based scans for positive selection, contrasting the genomic response to WGD in C. amara with that of A. arenosa. We found in C amara the strongest selection signals at genes with predicted functions thought important to adaptation to WGD: meiosis, chromosome remodeling, cell cycle, and ion transport. However, genomic responses to WGD in the two species differ: minimal ortholog-level convergence emerged, with none of the meiosis genes found in A. arenosa exhibiting strong signal in C amara. This is consistent with our observations of lower meiotic stability and occasional clonal spreading in diploid C amara, suggesting that nascent C. amara autotetraploid lineages were pre-adapted by their diploid lifestyle to survive while enduring reduced meiotic fidelity. However, in contrast to a lack of ortholog convergence, we see process-level and network convergence in DNA management, chromosome organization, stress signaling, and ion homeostasis processes. This gives the first insight into the salient adaptations required to meet the challenges of a WGD state and shows that autopolyploids can utilize multiple evolutionary trajectories to adapt to WGD.
ER  -

BOHUTINSKA, M., M. ALSTON, P. MONNAHAN, Terezie MALÍK MANDÁKOVÁ, S. BRAY, P. PAAJANEN, F. KOLAR and L. YANT. Novelty and Convergence in Adaptation to Whole Genome Duplication. \textit{Molecular Biology and Evolution}. OXFORD: OXFORD UNIV PRESS, 2021, vol.~38, No~9, p.~3910-3924. ISSN~0737-4038. Available from: https://dx.doi.org/10.1093/molbev/msab096.

Detailed Information on Publication Record