Using Phenomic Analysis of Photosynthetic Function for Abiotic Stress Response Gene Discovery

Monitoring the photosynthetic performance of plants is a major key to understanding how plants adapt to their growth conditions. Stress tolerance traits have a high genetic complexity as plants are constantly, and unavoidably, exposed to numerous stress factors, which limits their growth rates in the natural environment. Arabidopsis thaliana, with its broad genetic diversity and wide climatic range, has been shown to successfully adapt to stressful conditions to ensure the completion of its life cycle. As a result, A. thaliana has become a robust and renowned plant model system for studying natural variation and conducting gene discovery studies. Genome wide association studies (GWAS) in restructured populations combining natural and recombinant lines is a particularly effective way to identify the genetic basis of complex traits. As most abiotic stresses affect photosynthetic activity, chlorophyll fluorescence measurements are a potential phenotyping technique for monitoring plant performance under stress conditions. This review focuses on the use of chlorophyll fluorescence as a tool to study genetic variation underlying the stress tolerance responses to abiotic stress in A. thaliana.

[1]  Stefan Jansson,et al.  A pigment-binding protein essential for regulation of photosynthetic light harvesting , 2000, Nature.

[2]  K. Niyogi,et al.  Non-photochemical quenching. A response to excess light energy. , 2001, Plant physiology.

[3]  Thomas D. Sharkey,et al.  Photosynthetic electron transport and proton flux under moderate heat stress , 2009, Photosynthesis Research.

[4]  Mark G. M. Aarts,et al.  Natural Genetic Variation for Acclimation of Photosynthetic Light Use Efficiency to Growth Irradiance in Arabidopsis1[OPEN] , 2015, Plant Physiology.

[5]  S. Hayat,et al.  Causes of salinity and plant manifestations to salt stress: a review. , 2011, Journal of environmental biology.

[6]  K. Niyogi,et al.  PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. , 1999, Annual review of plant physiology and plant molecular biology.

[7]  S. Leal Genetics and Analysis of Quantitative Traits , 2001 .

[8]  Roberta Croce,et al.  Photosynthetic Quantum Yield Dynamics: From Photosystems to Leaves[W][OA] , 2012, Plant Cell.

[9]  A. Ruban,et al.  Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin , 2014, Journal of experimental botany.

[10]  K. Niyogi,et al.  Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion , 1998, Plant Cell.

[11]  B. Halliwell Photorespiration , 2017, Methods in Molecular Biology.

[12]  K Maxwell,et al.  Chlorophyll fluorescence--a practical guide. , 2000, Journal of experimental botany.

[13]  A. Porcar-Castell,et al.  Thermal energy dissipation and xanthophyll cycles beyond the Arabidopsis model , 2012, Photosynthesis Research.

[14]  R. Munns,et al.  Factors affecting CO2 assimilation, leaf injury and growth in salt-stressed durum wheat. , 2002, Functional plant biology : FPB.

[15]  F. Sato,et al.  Physiological functions of PsbS-dependent and PsbS-independent NPQ under naturally fluctuating light conditions. , 2014, Plant & cell physiology.

[16]  K. Roháček Chlorophyll Fluorescence Parameters: The Definitions, Photosynthetic Meaning, and Mutual Relationships , 2002, Photosynthetica.

[17]  Kevin D. Murray,et al.  TraitCapture: genomic and environment modelling of plant phenomic data. , 2014, Current opinion in plant biology.

[18]  Sandra M. Schmöckel,et al.  A novel protein kinase involved in Na(+) exclusion revealed from positional cloning. , 2013, Plant, cell & environment.

[19]  J. Keurentjes,et al.  The role of natural variation in dissecting genetic regulation of primary metabolism , 2009, Plant signaling & behavior.

[20]  R. Doerge,et al.  Selecting Informative Traits for Multivariate Quantitative Trait Locus Mapping Helps to Gain Optimal Power , 2013, Genetics.

[21]  Hirokazu Kobayashi,et al.  A Recessive Arabidopsis Mutant That Grows Photoautotrophically under Salt Stress Shows Enhanced Active Oxygen Detoxification , 1999, Plant Cell.

[22]  G. Karp Cell and molecular biology : concepts and experiments / Gerald Karp , 1996 .

[23]  Cynthia Weinig,et al.  Shade avoidance and the regulation of leaf inclination in Arabidopsis. , 2006, Plant, cell & environment.

[24]  R. Cheng,et al.  Genetic Variation for Life History Sensitivity to Seasonal Warming in Arabidopsis thaliana , 2013, Genetics.

[25]  R. Knox,et al.  Energy distribution in the photochemical apparatus of Porphyridiumcruentum: Picosecond fluorescence spectroscopy of cells in state 1 and state 2 at 77 K , 2004, Photosynthesis Research.

[26]  Frank Ewert,et al.  Global hot-spots of heat stress on agricultural crops due to climate change , 2013 .

[27]  E H Murchie,et al.  Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. , 2013, Journal of experimental botany.

[28]  Qifa Zhang,et al.  Genome-wide association studies of 14 agronomic traits in rice landraces , 2010, Nature Genetics.

[29]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[30]  O. Loudet,et al.  What does Arabidopsis natural variation teach us (and does not teach us) about adaptation in plants? , 2011, Current opinion in plant biology.

[31]  N. Baker Chlorophyll fluorescence: a probe of photosynthesis in vivo. , 2008, Annual review of plant biology.

[32]  K. Niyogi,et al.  Quantitative Genetic Analysis of Thermal Dissipation in Arabidopsis1[W][OA] , 2009, Plant Physiology.

[33]  Xiao-Ping Li,et al.  PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[34]  L. Santiago,et al.  Consequences of light absorptance in calculating electron transport rate of desert and succulent plants , 2011, Photosynthetica.

[35]  Karsten M. Borgwardt,et al.  Whole-genome sequencing of multiple Arabidopsis thaliana populations , 2011, Nature Genetics.

[36]  M. Tester,et al.  Mechanisms of salinity tolerance. , 2008, Annual review of plant biology.

[37]  A. Korte,et al.  The advantages and limitations of trait analysis with GWAS: a review , 2013, Plant Methods.

[38]  M. Ashraf,et al.  Photosynthesis under stressful environments: An overview , 2013, Photosynthetica.

[39]  T. Sharkey,et al.  High temperature effects on electron and proton circuits of photosynthesis. , 2010, Journal of integrative plant biology.

[40]  Germination variation in Arabidopsis thaliana accessions under moderate osmotic and salt stresses. , 2010, Annals of botany.

[41]  R. Bassi,et al.  Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis. , 2013, The Plant journal : for cell and molecular biology.

[42]  Giorgina Bernasconi,et al.  Natural genetic variation in Arabidopsis: tools, traits and prospects for evolutionary ecology. , 2007, Annals of botany.

[43]  P. Horton,et al.  REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[44]  M. Badger,et al.  Photoprotection in plants: a new light on photosystem II damage. , 2011, Trends in plant science.

[45]  M. Tester,et al.  Image-based phenotyping for non-destructive screening of different salinity tolerance traits in rice , 2014, Rice.

[46]  J. Meurer,et al.  PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis , 2002, Cell.

[47]  Warren L. Butler,et al.  Energy Distribution in the Photochemical Apparatus of Photosynthesis , 1978 .

[48]  Muhammad Ali Amer,et al.  Genome-wide association study of 107 phenotypes in a common set of Arabidopsis thaliana inbred lines , 2010, Nature.

[49]  Detlef Weigel,et al.  Quantitative trait loci controlling light and hormone response in two accessions of Arabidopsis thaliana. , 2002, Genetics.

[50]  J. Beardall,et al.  Photoacclimation in Dunaliella tertiolecta reveals a unique NPQ pattern upon exposure to irradiance , 2011, Photosynthesis Research.

[51]  Masahiro Kasahara,et al.  Chloroplast avoidance movement reduces photodamage in plants , 2002, Nature.

[52]  Karsten M. Borgwardt,et al.  1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana , 2016, Cell.

[53]  Alain Vavasseur,et al.  Arabidopsis OST1 Protein Kinase Mediates the Regulation of Stomatal Aperture by Abscisic Acid and Acts Upstream of Reactive Oxygen Species Production Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007906. , 2002, The Plant Cell Online.

[54]  M. Simon,et al.  Natural Variation in Arabidopsis thaliana as a Tool for Highlighting Differential Drought Responses , 2008, PloS one.

[55]  M. Durand-Tardif,et al.  A Focus on Natural Variation for Abiotic Constraints Response in the Model Species Arabidopsis thaliana , 2009, International journal of molecular sciences.

[56]  Satpal Turan Light Acclimation in Plants: Photoinhibition and Photoprotection , 2013 .

[57]  J. Anderson,et al.  Photoregulation of the Composition, Function, and Structure of Thylakoid Membranes , 1986 .

[58]  The dry facts , 2013, Nature.

[59]  O. Björkman Responses to Different Quantum Flux Densities , 1981 .

[60]  Jeffrey A. Cruz,et al.  Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes. , 2016, Cell systems.

[61]  M. Koornneef,et al.  Naturally occurring genetic variation in Arabidopsis thaliana. , 2004, Annual review of plant biology.

[62]  S. Heckathorn,et al.  The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. , 1998, Plant physiology.

[63]  Celia Miller,et al.  Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+ and Cl- in salt-affected barley and durum wheat. , 2006, Plant, cell & environment.

[64]  O. Loudet,et al.  Bay-0 × Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis , 2002, Theoretical and Applied Genetics.

[65]  J. Bunce Acclimation of photosynthesis to temperature in Arabidopsis thaliana and Brassica oleracea , 2008, Photosynthetica.

[66]  Xuehui Huang,et al.  Natural variations and genome-wide association studies in crop plants. , 2014, Annual review of plant biology.

[67]  S. Muranaka,et al.  A Salt-Tolerant Cultivar of Wheat Maintains Photosynthetic Activity by Suppressing Sodium Uptake , 2002, Photosynthetica.

[68]  T. Kagawa,et al.  Blue light-induced chloroplast relocation. , 2002, Plant & cell physiology.

[69]  D. Delmer,et al.  Annual review of plant physiology and plant molecular biology , 1988 .

[70]  M. Salvucci,et al.  Moderately High Temperatures Inhibit Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (Rubisco) Activase-Mediated Activation of Rubisco , 1998, Plant physiology.

[71]  Detlef Weigel,et al.  Natural Variation in Arabidopsis: From Molecular Genetics to Ecological Genomics1[W][OA] , 2011, Plant Physiology.

[72]  C. Klukas,et al.  Dissecting the Phenotypic Components of Crop Plant Growth and Drought Responses Based on High-Throughput Image Analysis[W][OPEN] , 2014, Plant Cell.

[73]  Qian Qian,et al.  Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm , 2011, Nature Genetics.

[74]  D. Weigel,et al.  Salinity Is an Agent of Divergent Selection Driving Local Adaptation of Arabidopsis to Coastal Habitats1[OPEN] , 2015, Plant Physiology.

[75]  B. Pogson,et al.  A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence , 2008, Plant Methods.

[76]  N. Baker,et al.  Rapid, Noninvasive Screening for Perturbations of Metabolism and Plant Growth Using Chlorophyll Fluorescence Imaging1 , 2003, Plant Physiology.

[77]  E. Govindje,et al.  Sixty-Three Years Since Kautsky: Chlorophyll a Fluorescence , 1995 .

[78]  G. Johnson,et al.  Contrasting Responses of Photosynthesis to Salt Stress in the Glycophyte Arabidopsis and the Halophyte Thellungiella: Role of the Plastid Terminal Oxidase as an Alternative Electron Sink1[C][OA] , 2008, Plant Physiology.

[79]  C. Osmond What is photoinhibition? Some insights from comparisons of shade and sun plants , 1994 .

[80]  K. Taylor,et al.  Genome-Wide Association , 2007, Diabetes.

[81]  Manzoor Qadir,et al.  Economics of salt-induced land degradation and restoration , 2014 .

[82]  A. Nakano,et al.  Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.