Reciprocal cybrids reveal how organellar genomes affect plant phenotypes

Pádraic J. Flood, Tom P.J.M. Theeuwen, Korbinian Schneeberger, Paul Keizer, Willem Kruijer, Edouard Severing, Evangelos Kouklas, Jos A. Hageman, Raúl Wijfjes, Vanesa Calvo-Baltanas, Frank F.M. Becker, Sabine K. Schnabel, Leo A.J. Willems, Wilco Ligterink, Jeroen Van Arkel, Roland Mumm, José M. Gualberto, Linda Savage, David M. Kramer, Joost J.B. Keurentjes & 5 others Fred Van Eeuwijk, Maarten Koornneef, Jeremy Harbinson, Mark G.M. Aarts, Erik Wijnker

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Assessment of the impact of variation in chloroplast and mitochondrial DNA (collectively termed the plasmotype) on plant phenotypes is challenging due to the difficulty in separating their effect from nuclear-derived variation (the nucleotype). Haploid-inducer lines can be used as efficient plasmotype donors to generate new plasmotype–nucleotype combinations (cybrids)1. We generated a panel comprising all possible cybrids of seven Arabidopsis thaliana accessions and extensively phenotyped these lines for 1,859 phenotypes under both stable and fluctuating conditions. We show that natural variation in the plasmotype results in both additive and epistatic effects across all phenotypic categories. Plasmotypes that induce more additive phenotypic changes also cause more epistatic effects, suggesting a possible common basis for both additive and epistatic effects. On average, epistatic interactions explained twice as much of the variance in phenotypes as additive plasmotype effects. The impact of plasmotypic variation was also more pronounced under fluctuating and stressful environmental conditions. Thus, the phenotypic impact of variation in plasmotypes is the outcome of multi-level nucleotype–plasmotype–environment interactions and, as such, the plasmotype is likely to serve as a reservoir of variation that is predominantly exposed under certain conditions. The production of cybrids using haploid inducers is a rapid and precise method for assessment of the phenotypic effects of natural variation in organellar genomes. It will facilitate efficient screening of unique nucleotype–plasmotype combinations to both improve our understanding of natural variation in these combinations and identify favourable combinations to enhance plant performance.
Original languageEnglish
Pages (from-to)13-21
JournalNature Plants
Volume6
Issue number1
DOIs
Publication statusPublished - 1 Jan 2020

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cybrids
phenotype
haploidy
genome
chloroplast DNA
additive effect
new combination
mitochondrial DNA
Arabidopsis thaliana
screening
environmental factors
methodology

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title = "Reciprocal cybrids reveal how organellar genomes affect plant phenotypes",
abstract = "Assessment of the impact of variation in chloroplast and mitochondrial DNA (collectively termed the plasmotype) on plant phenotypes is challenging due to the difficulty in separating their effect from nuclear-derived variation (the nucleotype). Haploid-inducer lines can be used as efficient plasmotype donors to generate new plasmotype–nucleotype combinations (cybrids)1. We generated a panel comprising all possible cybrids of seven Arabidopsis thaliana accessions and extensively phenotyped these lines for 1,859 phenotypes under both stable and fluctuating conditions. We show that natural variation in the plasmotype results in both additive and epistatic effects across all phenotypic categories. Plasmotypes that induce more additive phenotypic changes also cause more epistatic effects, suggesting a possible common basis for both additive and epistatic effects. On average, epistatic interactions explained twice as much of the variance in phenotypes as additive plasmotype effects. The impact of plasmotypic variation was also more pronounced under fluctuating and stressful environmental conditions. Thus, the phenotypic impact of variation in plasmotypes is the outcome of multi-level nucleotype–plasmotype–environment interactions and, as such, the plasmotype is likely to serve as a reservoir of variation that is predominantly exposed under certain conditions. The production of cybrids using haploid inducers is a rapid and precise method for assessment of the phenotypic effects of natural variation in organellar genomes. It will facilitate efficient screening of unique nucleotype–plasmotype combinations to both improve our understanding of natural variation in these combinations and identify favourable combinations to enhance plant performance.",
author = "Flood, {P{\'a}draic J.} and Theeuwen, {Tom P.J.M.} and Korbinian Schneeberger and Paul Keizer and Willem Kruijer and Edouard Severing and Evangelos Kouklas and Hageman, {Jos A.} and Ra{\'u}l Wijfjes and Vanesa Calvo-Baltanas and Becker, {Frank F.M.} and Schnabel, {Sabine K.} and Willems, {Leo A.J.} and Wilco Ligterink and {Van Arkel}, Jeroen and Roland Mumm and Gualberto, {Jos{\'e} M.} and Linda Savage and Kramer, {David M.} and Keurentjes, {Joost J.B.} and {Van Eeuwijk}, Fred and Maarten Koornneef and Jeremy Harbinson and Aarts, {Mark G.M.} and Erik Wijnker",
year = "2020",
month = "1",
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doi = "10.1038/s41477-019-0575-9",
language = "English",
volume = "6",
pages = "13--21",
journal = "Nature Plants",
issn = "2055-026X",
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Reciprocal cybrids reveal how organellar genomes affect plant phenotypes. / Flood, Pádraic J.; Theeuwen, Tom P.J.M.; Schneeberger, Korbinian; Keizer, Paul; Kruijer, Willem; Severing, Edouard; Kouklas, Evangelos; Hageman, Jos A.; Wijfjes, Raúl; Calvo-Baltanas, Vanesa; Becker, Frank F.M.; Schnabel, Sabine K.; Willems, Leo A.J.; Ligterink, Wilco; Van Arkel, Jeroen; Mumm, Roland; Gualberto, José M.; Savage, Linda; Kramer, David M.; Keurentjes, Joost J.B.; Van Eeuwijk, Fred; Koornneef, Maarten; Harbinson, Jeremy; Aarts, Mark G.M.; Wijnker, Erik.

In: Nature Plants, Vol. 6, No. 1, 01.01.2020, p. 13-21.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

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AU - Flood, Pádraic J.

AU - Theeuwen, Tom P.J.M.

AU - Schneeberger, Korbinian

AU - Keizer, Paul

AU - Kruijer, Willem

AU - Severing, Edouard

AU - Kouklas, Evangelos

AU - Hageman, Jos A.

AU - Wijfjes, Raúl

AU - Calvo-Baltanas, Vanesa

AU - Becker, Frank F.M.

AU - Schnabel, Sabine K.

AU - Willems, Leo A.J.

AU - Ligterink, Wilco

AU - Van Arkel, Jeroen

AU - Mumm, Roland

AU - Gualberto, José M.

AU - Savage, Linda

AU - Kramer, David M.

AU - Keurentjes, Joost J.B.

AU - Van Eeuwijk, Fred

AU - Koornneef, Maarten

AU - Harbinson, Jeremy

AU - Aarts, Mark G.M.

AU - Wijnker, Erik

PY - 2020/1/1

Y1 - 2020/1/1

N2 - Assessment of the impact of variation in chloroplast and mitochondrial DNA (collectively termed the plasmotype) on plant phenotypes is challenging due to the difficulty in separating their effect from nuclear-derived variation (the nucleotype). Haploid-inducer lines can be used as efficient plasmotype donors to generate new plasmotype–nucleotype combinations (cybrids)1. We generated a panel comprising all possible cybrids of seven Arabidopsis thaliana accessions and extensively phenotyped these lines for 1,859 phenotypes under both stable and fluctuating conditions. We show that natural variation in the plasmotype results in both additive and epistatic effects across all phenotypic categories. Plasmotypes that induce more additive phenotypic changes also cause more epistatic effects, suggesting a possible common basis for both additive and epistatic effects. On average, epistatic interactions explained twice as much of the variance in phenotypes as additive plasmotype effects. The impact of plasmotypic variation was also more pronounced under fluctuating and stressful environmental conditions. Thus, the phenotypic impact of variation in plasmotypes is the outcome of multi-level nucleotype–plasmotype–environment interactions and, as such, the plasmotype is likely to serve as a reservoir of variation that is predominantly exposed under certain conditions. The production of cybrids using haploid inducers is a rapid and precise method for assessment of the phenotypic effects of natural variation in organellar genomes. It will facilitate efficient screening of unique nucleotype–plasmotype combinations to both improve our understanding of natural variation in these combinations and identify favourable combinations to enhance plant performance.

AB - Assessment of the impact of variation in chloroplast and mitochondrial DNA (collectively termed the plasmotype) on plant phenotypes is challenging due to the difficulty in separating their effect from nuclear-derived variation (the nucleotype). Haploid-inducer lines can be used as efficient plasmotype donors to generate new plasmotype–nucleotype combinations (cybrids)1. We generated a panel comprising all possible cybrids of seven Arabidopsis thaliana accessions and extensively phenotyped these lines for 1,859 phenotypes under both stable and fluctuating conditions. We show that natural variation in the plasmotype results in both additive and epistatic effects across all phenotypic categories. Plasmotypes that induce more additive phenotypic changes also cause more epistatic effects, suggesting a possible common basis for both additive and epistatic effects. On average, epistatic interactions explained twice as much of the variance in phenotypes as additive plasmotype effects. The impact of plasmotypic variation was also more pronounced under fluctuating and stressful environmental conditions. Thus, the phenotypic impact of variation in plasmotypes is the outcome of multi-level nucleotype–plasmotype–environment interactions and, as such, the plasmotype is likely to serve as a reservoir of variation that is predominantly exposed under certain conditions. The production of cybrids using haploid inducers is a rapid and precise method for assessment of the phenotypic effects of natural variation in organellar genomes. It will facilitate efficient screening of unique nucleotype–plasmotype combinations to both improve our understanding of natural variation in these combinations and identify favourable combinations to enhance plant performance.

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SN - 2055-026X

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