Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana

Oakley, Christopher G.; Savage, Linda; Lotz, Samuel; Larson, G. Rudd; Thomashow, Michael F.; Kramer, David M.; Schemske, Douglas W.

doi:10.1093/jxb/erx437

Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana

Journal Article · 28 December 2017 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/erx437· OSTI ID:1540607

^[1]; Savage, Linda ^[2]; Lotz, Samuel ^[3]; Larson, G. Rudd ^[4]; Thomashow, Michael F. ^[5]; Kramer, David M. ^[6]; Schemske, Douglas W. ^[7]

Department of Plant Biology, Michigan State University, East Lansing, MI, USA
MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, USA
MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, USA; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, USA
MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, USA; Genetics Graduate Program, Michigan State University, East Lansing, MI, USA
MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, USA; Plant Resilience Institute, Michigan State University, East Lansing, MI, USA
Department of Plant Biology, Michigan State University, East Lansing, MI, USA; MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, USA; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, USA
Department of Plant Biology, Michigan State University, East Lansing, MI, USA; W.K. Kellogg Biological Station, Michigan State University, East Lansing, MI, USA

Not provided.

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: FG02-91ER20021

OSTI ID:: 1540607

Journal Information:: Journal of Experimental Botany, Vol. 69, Issue 3; ISSN 0022-0957

Publisher:: Oxford University Press

Country of Publication:: United States

Language:: English

References (65)

A Model Selection Approach for the Identification of Quantitative Trait Loci in Experimental Crosses, Allowing Epistasis Manichaikul, Ani; Moon, Jee Young; Sen, Śaunak Genetics, Vol. 181, Issue 3 https://doi.org/10.1534/genetics.108.094565	journal	December 2008
Differences in light-harvesting, acclimation to growth-light environment, and leaf structural development between Swedish and Italian ecotypes of Arabidopsis thaliana Stewart, Jared J.; Adams, William W.; Cohu, Christopher M. Planta, Vol. 242, Issue 6 https://doi.org/10.1007/s00425-015-2368-3	journal	July 2015
Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes Cruz, Jeffrey A.; Savage, Linda J.; Zegarac, Robert Cell Systems, Vol. 2, Issue 6 https://doi.org/10.1016/j.cels.2016.06.001	journal	June 2016
Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation: Arabidopsis lacking PsbS show photoprotective energy dissipation Johnson, Matthew P.; Ruban, Alexander V. The Plant Journal, Vol. 61, Issue 2 https://doi.org/10.1111/j.1365-313X.2009.04051.x	journal	November 2009
Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes Gehan, Malia A.; Park, Sunchung; Gilmour, Sarah J. The Plant Journal, Vol. 84, Issue 4 https://doi.org/10.1111/tpj.13027	journal	October 2015
Evolutionary genetics of plant adaptation Anderson, Jill T.; Willis, John H.; Mitchell-Olds, Thomas Trends in Genetics, Vol. 27, Issue 7 https://doi.org/10.1016/j.tig.2011.04.001	journal	July 2011
Can improvement in photosynthesis increase crop yields? Long, Stephen P.; Zhu, Xin-Guang; Naidu, Shawna L. Plant, Cell and Environment, Vol. 29, Issue 3 https://doi.org/10.1111/j.1365-3040.2005.01493.x	journal	March 2006
The Population Genetics of Adaptation: the Distribution of Factors Fixed During Adaptive Evolution Orr, H. Allen Evolution, Vol. 52, Issue 4 https://doi.org/10.1111/j.1558-5646.1998.tb01823.x	journal	August 1998
Flowering time QTL in natural populations of Arabidopsis thaliana and implications for their adaptive value Dittmar, Emily L.; Oakley, Christopher G.; Ågren, Jon Molecular Ecology, Vol. 23, Issue 17 https://doi.org/10.1111/mec.12857	journal	August 2014
Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons Demmig-Adams, Barbara; Cohu, Christopher M.; Muller, Onno Photosynthesis Research, Vol. 113, Issue 1-3 https://doi.org/10.1007/s11120-012-9761-6	journal	July 2012
Multiple feedbacks between chloroplast and whole plant in the context of plant adaptation and acclimation to the environment Demmig-Adams, Barbara; Stewart, Jared J.; Adams, William W. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1640 https://doi.org/10.1098/rstb.2013.0244	journal	April 2014
The Importance of Energy Balance in Improving Photosynthetic Productivity Kramer, David M.; Evans, John R. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.166652	journal	November 2010
A Quantitative Survey of Local Adaptation and Fitness Trade‐Offs Hereford, Joe The American Naturalist, Vol. 173, Issue 5 https://doi.org/10.1086/597611	journal	May 2009
Life-History qtls and Natural Selection on Flowering time in Boechera Stricta, a Perennial Relative of Arabidopsis: Flowering time in Boechera Stricta Anderson, Jill T.; Lee, Cheng-Ruei; Mitchell-Olds, Thomas Evolution, Vol. 65, Issue 3 https://doi.org/10.1111/j.1558-5646.2010.01175.x	journal	November 2010
Mutations in Arabidopsis YCF20-like genes affect thermal dissipation of excess absorbed light energy Jung, Hou-Sung; Niyogi, Krishna K. Planta, Vol. 231, Issue 4 https://doi.org/10.1007/s00425-010-1098-9	journal	January 2010
Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus Lowry, David B.; Hall, Megan C.; Salt, David E. New Phytologist, Vol. 183, Issue 3 https://doi.org/10.1111/j.1469-8137.2009.02901.x	journal	August 2009
Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana Agren, J.; Oakley, C. G.; McKay, J. K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 52 https://doi.org/10.1073/pnas.1316773110	journal	December 2013
Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range Ågren, Jon; Schemske, Douglas W. New Phytologist, Vol. 194, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04112.x	journal	March 2012
Photoinhibition of Photosystem II. Inactivation, protein damage and turnover Aro, Eva-Mari; Virgin, Ivar; Andersson, Bertil Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1143, Issue 2 https://doi.org/10.1016/0005-2728(93)90134-2	journal	July 1993
Distinct roles of the photosystem II protein PsbS and zeaxanthin in the regulation of light harvesting in plants revealed by fluorescence lifetime snapshots Sylak-Glassman, Emily J.; Malnoë, Alizée; De Re, Eleonora Proceedings of the National Academy of Sciences, Vol. 111, Issue 49 https://doi.org/10.1073/pnas.1418317111	journal	November 2014
Control of Non-Photochemical Exciton Quenching by the Proton Circuit of Photosynthesis Strand, Deserah D.; Kramer, David M. Advances in Photosynthesis and Respiration https://doi.org/10.1007/978-94-017-9032-1_18	book	October 2014
The effects of phenotypic plasticity on photosynthetic performance in winter rye, winter wheat and Brassica napus Dahal, Keshav; Kane, Khalil; Gadapati, Winona Physiologia Plantarum, Vol. 144, Issue 2 https://doi.org/10.1111/j.1399-3054.2011.01513.x	journal	November 2011
Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants Huner, Norman P. A.; Öquist, Gunnar; Hurry, Vaughan M. Photosynthesis Research, Vol. 37, Issue 1 https://doi.org/10.1007/BF02185436	journal	July 1993
Molecular Basis of Plant Cold Acclimation: Insights Gained from Studying the CBF Cold Response Pathway: Figure 1. Thomashow, Michael F. Plant Physiology, Vol. 154, Issue 2 https://doi.org/10.1104/pp.110.161794	journal	October 2010
Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation Demmig-Adams, Barbara; Adams, William W. New Phytologist, Vol. 172, Issue 1 https://doi.org/10.1111/j.1469-8137.2006.01835.x	journal	October 2006
Chlorophyll fluorescence—a practical guide Maxwell, Kate; Johnson, Giles N. Journal of Experimental Botany, Vol. 51, Issue 345 https://doi.org/10.1093/jexbot/51.345.659	journal	April 2000
Quantitative Genetic Analysis of Thermal Dissipation in Arabidopsis Jung, Hou-Sung; Niyogi, Krishna K. Plant Physiology, Vol. 150, Issue 2 https://doi.org/10.1104/pp.109.137828	journal	April 2009
Improving photosynthesis and crop productivity by accelerating recovery from photoprotection Kromdijk, Johannes; Głowacka, Katarzyna; Leonelli, Lauriebeth Science, Vol. 354, Issue 6314 https://doi.org/10.1126/science.aai8878	journal	November 2016
Limitations to photosynthesis by proton motive force-induced photosystem II photodamage Davis, Geoffry A.; Kanazawa, Atsuko; Schöttler, Mark Aurel eLife, Vol. 5 https://doi.org/10.7554/eLife.16921	journal	October 2016
State transitions: an example of acclimation to low-light stress Mullineaux, C. W. Journal of Experimental Botany, Vol. 56, Issue 411 https://doi.org/10.1093/jxb/eri064	journal	November 2004
New Fluorescence Parameters for the Determination of Q _A Redox State and Excitation Energy Fluxes Kramer, David M.; Johnson, Giles; Kiirats, Olavi Photosynthesis Research, Vol. 79, Issue 2 https://doi.org/10.1023/B:PRES.0000015391.99477.0d	journal	January 2004
Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits Mckay, J. K.; Richards, J. H.; Mitchell-Olds, T. Molecular Ecology, Vol. 12, Issue 5 https://doi.org/10.1046/j.1365-294X.2003.01833.x	journal	May 2003
Chlorophyll Fluorescence as a Tool to Monitor Plant Response to the Environment Adams, William W.; Demmig-Adams, Barbara Chlorophyll a Fluorescence https://doi.org/10.1007/978-1-4020-3218-9_22	book	January 2004
Regulation of the photosynthetic apparatus under fluctuating growth light Tikkanen, Mikko; Grieco, Michele; Nurmi, Markus Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1608 https://doi.org/10.1098/rstb.2012.0067	journal	December 2012
Foliar phloem infrastructure in support of photosynthesis Adams, William W.; Cohu, Christopher M.; Muller, Onno Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00194	journal	January 2013
Genetic architecture of naturally occurring quantitative traits in plants: an updated synthesis Alonso-Blanco, Carlos; Méndez-Vigo, Belén Current Opinion in Plant Biology, Vol. 18 https://doi.org/10.1016/j.pbi.2014.01.002	journal	April 2014
Non-Photochemical Quenching. A Response to Excess Light Energy Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K. Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.1558	journal	April 2001
Photoinhibition at Low Temperature in Chilling-Sensitive and -Resistant Plants Hetherington, Suzan E.; He, Jie; Smillie, Robert M. Plant Physiology, Vol. 90, Issue 4 https://doi.org/10.1104/pp.90.4.1609	journal	August 1989
PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms Thomashow, Michael F. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.571	journal	June 1999
Early life stages contribute strongly to local adaptation in Arabidopsis thaliana Postma, Froukje M.; Ågren, Jon Proceedings of the National Academy of Sciences, Vol. 113, Issue 27 https://doi.org/10.1073/pnas.1606303113	journal	June 2016
Identification of quantitative trait loci and a candidate locus for freezing tolerance in controlled and outdoor environments in the overwintering crucifer B oechera stricta: Freezing tolerance in Boechera Heo, Jae-Yun; Feng, Dongsheng; Niu, Xiaomu Plant, Cell & Environment, Vol. 37, Issue 11 https://doi.org/10.1111/pce.12365	journal	June 2014
Factors influencing the effect size distribution of adaptive substitutions Dittmar, Emily L.; Oakley, Christopher G.; Conner, Jeffrey K. Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1828 https://doi.org/10.1098/rspb.2015.3065	journal	April 2016
Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited Hüner, Norman P. A. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00255	journal	January 2012
Chloroplast Phenomics: Systematic Phenotypic Screening of Chloroplast Protein Mutants in Arabidopsis Lu, Yan; Savage, Linda J.; Last, Robert L. Chloroplast Research in Arabidopsis https://doi.org/10.1007/978-1-61779-237-3_9	book	January 2011
Adaptation to seasonality and the winter freeze Preston, Jill C.; Sandve, Simen R. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00167	journal	January 2013
Quantitative trait loci mapping of freezing tolerance and photosynthetic acclimation to cold in winter two- and six-rowed barley Tyrka, Mirosław; Rapacz, Marcin; Fiust, Anna Plant Breeding, Vol. 134, Issue 3 https://doi.org/10.1111/pbr.12270	journal	May 2015
Natural genetic variation in plant photosynthesis Flood, Pádraic J.; Harbinson, Jeremy; Aarts, Mark G. M. Trends in Plant Science, Vol. 16, Issue 6 https://doi.org/10.1016/j.tplants.2011.02.005	journal	June 2011
Photosynthetic Quantum Yield Dynamics: From Photosystems to Leaves Hogewoning, Sander W.; Wientjes, Emilie; Douwstra, Peter The Plant Cell, Vol. 24, Issue 5 https://doi.org/10.1105/tpc.112.097972	journal	May 2012
Minor loading vein acclimation for three Arabidopsis thaliana ecotypes in response to growth under different temperature and light regimes Cohu, Christopher M.; Muller, Onno; Demmig-Adams, Barbara Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00240	journal	January 2013
Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana : Estimates of selection and QTL mapping: ADAPTIVE DIVERGENCE IN FLOWERING TIME Ågren, Jon; Oakley, Christopher G.; Lundemo, Sverre Evolution, Vol. 71, Issue 3 https://doi.org/10.1111/evo.13126	journal	December 2016
A Small Zinc Finger Thylakoid Protein Plays a Role in Maintenance of Photosystem II in Arabidopsis thaliana Lu, Yan; Hall, David A.; Last, Robert L. The Plant Cell, Vol. 23, Issue 5 https://doi.org/10.1105/tpc.111.085456	journal	May 2011
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo Baker, Neil R. Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092759	journal	June 2008
Fitness Benefits and Costs of Cold Acclimation in Arabidopsis thaliana Zhen, Ying; Dhakal, Preeti; Ungerer, Mark C. The American Naturalist, Vol. 178, Issue 1 https://doi.org/10.1086/660282	journal	July 2011
Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis Nilkens, Manuela; Kress, Eugen; Lambrev, Petar Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 4 https://doi.org/10.1016/j.bbabio.2010.01.001	journal	April 2010
QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs Oakley, Christopher G.; Ågren, Jon; Atchison, Rachel A. Molecular Ecology, Vol. 23, Issue 17 https://doi.org/10.1111/mec.12862	journal	August 2014
Data from: Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana Oakley, Christopher G.; Savage, Linda; Lotz, Samuel Dryad https://doi.org/10.5061/dryad.h2c0c	dataset	January 2018
Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata : GENETIC BASIS OF LOCAL ADAPTATION IN Leinonen, PÄIvi H.; Remington, David L.; LeppÄLÄ, Johanna Molecular Ecology, Vol. 22, Issue 3 https://doi.org/10.1111/j.1365-294X.2012.05678.x	journal	June 2012
Testing Natural Selection vs. Genetic Drift in Phenotypic Evolution Using Quantitative Trait Locus Data Orr, H. Allen Genetics, Vol. 149, Issue 4 https://doi.org/10.1093/genetics/149.4.2099	journal	August 1998
Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana Zhen, Ying; Ungerer, Mark C. New Phytologist, Vol. 177, Issue 2 https://doi.org/10.1111/j.1469-8137.2007.02262.x	journal	November 2007
Phenomenal Phenomics Mak, H. Craig Cell Systems, Vol. 2, Issue 6 https://doi.org/10.1016/j.cels.2016.06.005	journal	June 2016
Digest: Toward predicting evolutionary response to environmental change: The power of integrated experimental and genetic studies* Opedal, Øystein H. Evolution, Vol. 71, Issue 3 https://doi.org/10.1111/evo.13171	journal	January 2017
Local adaptation in The model plant Lowry, David B. New Phytologist, Vol. 194, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04146.x	journal	May 2012
The Population Genetics of Adaptation: The Distribution of Factors Fixed during Adaptive Evolution Orr, H. Allen Evolution, Vol. 52, Issue 4 https://doi.org/10.2307/2411226	journal	August 1998
Associations between the acclimation of phloem-cell wall ingrowths in minor veins and maximal photosynthesis rate Adams III, William W.; Cohu, Christopher M.; Amiard, Véronique Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00024	journal	January 2014
Data from: A quantitative survey of local adaptation and fitness trade-offs Hereford, Joe Dryad https://doi.org/10.5061/dryad.315	dataset	January 2009

Cited By (8)

Combining population genomics and fitness QTLs to identify the genetics of local adaptation in Arabidopsis thaliana Price, Nicholas; Moyers, Brook T.; Lopez, Lua Proceedings of the National Academy of Sciences, Vol. 115, Issue 19 https://doi.org/10.1073/pnas.1719998115	journal	April 2018
Elevated temperature increases meiotic crossover frequency via the interfering (Type I) pathway in Arabidopsis thaliana Modliszewski, Jennifer L.; Wang, Hongkuan; Albright, Ashley R. PLOS Genetics, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pgen.1007384	journal	May 2018
Plant biodiversity and regulation of photosynthesis in the natural environment Sello, Simone; Meneghesso, Andrea; Alboresi, Alessandro Planta, Vol. 249, Issue 4 https://doi.org/10.1007/s00425-018-03077-z	journal	January 2019
Exploration of Plant Biodiversity to Investigate Regulation of Photosynthesis in Natural Environment Sello, Simone; Alboresi, Alessandro; Baldan, Barbara https://doi.org/10.1101/368852	posted_content	July 2018
Genetic and physiological mechanisms of freezing tolerance in locally adapted populations of a winter annual Sanderson, Brian J.; Park, Sunchung; Jameel, M. Inam American Journal of Botany, Vol. 107, Issue 2 https://doi.org/10.1002/ajb2.1385	journal	November 2019
Less photoprotection can be good in some genetic and environmental contexts Demmig-Adams, Barbara; Stewart, Jared J.; Adams, William W. Biochemical Journal, Vol. 476, Issue 14 https://doi.org/10.1042/bcj20190328	journal	July 2019
Data from: Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana Oakley, Christopher G.; Savage, Linda; Lotz, Samuel Dryad https://doi.org/10.5061/dryad.h2c0c	dataset	January 2018
Optimization of Photosynthetic Productivity in Contrasting Environments by Regulons Controlling Plant Form and Function Demmig-Adams, Barbara; Stewart, Jared; Baker, Christopher International Journal of Molecular Sciences, Vol. 19, Issue 3 https://doi.org/10.3390/ijms19030872	journal	March 2018

Similar Records

Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana

Journal Article · 2017 · Journal of Experimental Botany · OSTI ID:1602771

Oakley, Christopher G.; Savage, Linda; Lotz, Samuel; +4 more

Data from: Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana

Dataset · 2018 · OSTI ID:1873985

Oakley, Christopher G.; Savage, Linda; Lotz, Samuel; +4 more

Natural variation in the C‐repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes

Journal Article · 2015 · The Plant Journal · OSTI ID:1401396

Gehan, Malia A.; Park, Sunchung; Gilmour, Sarah J.; +3 more

Related Subjects

Plant Sciences

Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana

Citation Formats

References (65)

Cited By (8)

Similar Records

Related Subjects