Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

From quantitative trait loci towards mechanisms: Linkage Integration Hypothesis Testing (LIgHT) sheds light on the mechanisms of genetically modulated stress tolerance

Journal Article · · Journal of Experimental Botany
DOI:https://doi.org/10.1093/jxb/eraf323· OSTI ID:2998735
 [1];  [2];  [3];  [4];  [1];  [5];  [5];  [1]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Crops Research Institute, Kumasi (Ghana); Kwame Nkrumah Univ. of Science and Technology (Ghana)
  3. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Jan IngenHousz Institute, Wageningen (Netherlands)
  4. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Univ. of Greenwich (United Kingdom)
  5. Univ. of California, Riverside, CA (United States)

The goal of this work is to assess the mechanistic bases of natural genetic variations in plant responses of photosynthesis to stress. To achieve this goal, we devised the Linkage Integration Hypothesis Testing (LIgHT) approach, comparing chromosomal locations of quantitative trait loci (QTLs) for multiple phenotypes to distinguish between hypothetical mechanisms. As a use case, we explored genetic variations in photosynthesis-related processes under chilling stress in recombinant inbred lines of cowpea (Vigna unguiculata L. Walp.). We focused on photosynthesis-related parameters measurable in high throughput and indicative of proposed chilling responses, including the states of PSI and PSII, photoprotective non-photochemical quenching, PSII photodamage, and nyctinastic leaf movements (NLMs). The patterns of QTL linkages indicated that chilling stress tolerance is genetically controlled by avoiding PSII photodamage rather than PSI damage or NLMs. This model was validated in a separate experiment measuring the rates of PSII photodamage and repair. Additional linkages suggest that chilling-induced damage to PSII is controlled by the thylakoid proton motive force and redox state of PSII. This regulation appears to be modulated by thylakoid fatty acid composition, previously associated with the same genetic loci and now supported by broader mechanistic evidence. We propose that the LIgHT approach can be broadly applied to test mechanisms underlying genetic variations.

Research Organization:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-91ER20021; SC0007101
OSTI ID:
2998735
Alternate ID(s):
OSTI ID: 2998780
Journal Information:
Journal of Experimental Botany, Journal Name: Journal of Experimental Botany; ISSN 1460-2431; ISSN 0022-0957
Publisher:
Oxford University Press (OUP)Copyright Statement
Country of Publication:
United States
Language:
English

References (65)

Chlorophyll Fluorescence as a Probe of Photosynthetic Productivity book
RECORD: a novel method for ordering loci on a genetic linkage map journal December 2005
A major QTL corresponding to the Rk locus for resistance to root-knot nematodes in cowpea (Vigna unguiculata L. Walp.) journal October 2015
Identification of quantitative trait loci for drought tolerance in Bukoba/Kijivu Andean mapping population of common bean journal October 2023
Thioredoxin and germinating barley: targets and protein redox changes journal January 2003
Triose phosphate use limitation of photosynthesis: short-term and long-term effects journal November 2015
Evidence for leaf fold to remedy the deficiency of physiological photoprotection for photosystem II journal December 2011
Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana journal July 2012
Impaired reductive activation of stromal bisphosphatases in tomato leaves following low-temperature exposure at high light journal November 1990
Photoinhibition of Photosystem II. Inactivation, protein damage and turnover journal July 1993
Impacts of chilling temperatures on photosynthesis in warm-climate plants journal January 2001
Energy balance and acclimation to light and cold journal June 1998
Photoinhibition of photosystem II under environmental stress journal June 2007
Photo-oxidative damage of photosystem I by repetitive flashes and chilling stress in cucumber leaves journal November 2024
Disulfide reductase activity of thioredoxin-h2 imparts cold tolerance in Arabidopsis journal September 2021
Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes journal June 2016
QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations journal June 2015
Improving yield by exploiting mechanisms underlying natural variation of photosynthesis journal April 2012
Evidence for the regulation of leaf movement by photosystem II activity journal November 2014
We aren’t good at picking candidate genes, and it’s slowing us down journal April 2020
The Unprecedented Versatility of the Plant‎ Thioredoxin System journal March 2017
Differential Effects of Chilling-Induced Photooxidation on the Redox Regulation of Photosynthetic Enzymes journal May 2000
Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms journal March 2004
Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait journal October 2004
A consensus genetic map of cowpea [Vigna unguiculata (L) Walp.] and synteny based on EST-derived SNPs journal October 2009
In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase journal August 2002
Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. journal July 1995
The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. journal March 1996
The Arabidopsis Plastidial Thioredoxins : NEW FUNCTIONS AND NEW INSIGHTS INTO SPECIFICITY journal April 2003
Genetics as a key to improving crop photosynthesis journal March 2022
Linking photosynthesis and yield reveals a strategy to improve light use efficiency in a climbing bean breeding population journal October 2023
Phenotyping photosynthesis: yes we can journal February 2024
Genetic architecture of photosynthesis in Sorghum bicolor under non-stress and cold stress conditions journal July 2017
Photoinhibition of Photosystem I: Its Physiological Significance in the Chilling Sensitivity of Plants journal April 1996
Singlet Oxygen Production by PSII Under Light Stress: Mechanism, Detection and the Protective role of β-Carotene journal March 2014
Distinct Redox Behaviors of Chloroplast Thiol Enzymes and their Relationships with Photosynthetic Electron Transport in Arabidopsis thaliana journal May 2014
MultispeQ Beta: a tool for large-scale plant phenotyping connected to the open PhotosynQ network journal October 2016
Light potentials of photosynthetic energy storage in the field: what limits the ability to use or dissipate rapidly increased light energy? journal December 2021
Regulation of the photosynthetic apparatus under fluctuating growth light journal December 2012
Expression and Characterization of the Thylakoid Lumen Protease DegP1 from Arabidopsis journal October 2002
Isolation and Characterization of a New Peroxiredoxin from Poplar Sieve Tubes That Uses Either Glutaredoxin or Thioredoxin as a Proton Donor journal November 2001
Increasing Photosynthetic Carbon Assimilation in C 3 Plants to Improve Crop Yield: Current and Future Strategies journal November 2010
Superoxide and Singlet Oxygen Produced within the Thylakoid Membranes Both Cause Photosystem I Photoinhibition journal March 2016
The Thylakoid Lumen Protease Deg1 Is Involved in the Repair of Photosystem II from Photoinhibition in Arabidopsis journal March 2007
Can improvement in photosynthesis increase crop yields? journal March 2006
Determining the limitations and regulation of photosynthetic energy transduction in leaves journal September 2007
Depletion of stromal Pi induces high ‘energy-dependent’ antenna exciton quenching (qE) by decreasing proton conductivity at CFO-CF1 ATP synthase: Depletion of Pi regulates the ATP synthase journal November 2007
The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses: AtGenExpress global abiotic stress data set journal March 2007
A Centennial Celebration for Quantitative Genetics journal April 2007
Light acclimation interacts with thylakoid ion transport to govern the dynamics of photosynthesis in Arabidopsis journal November 2022
NPQ (T) : a chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes : New, rapid probe of non-photochemical quenching journal July 2017
Genetically‐determined variations in photosynthesis indicate roles for specific fatty acid species in chilling responses journal March 2022
A multi‐parent advanced generation inter‐cross ( MAGIC ) population for genetic analysis and improvement of cowpea ( Vigna unguiculata L. Walp.) journal February 2018
The genome of cowpea ( Vigna unguiculata [L.] Walp.) journal March 2019
Plant Thioredoxin Systems Revisited journal June 2000
Automatic measurement of sister chromatid exchange frequency. journal July 1977
Genetic Architecture of Delayed Senescence, Biomass, and Grain Yield under Drought Stress in Cowpea journal July 2013
Epistatic Interactions Among Herbicide Resistances in Arabidopsis thaliana: The Fitness Cost of Multiresistance journal November 2005
The 2007 Eastern US Spring Freeze: Increased Cold Damage in a Warming World? journal March 2008
The Close Relationship between Net Photosynthesis and Crop Yield journal November 1982
Chilling-Induced Limitations on Photosynthesis in Warm Climate Plants: Contrasting Mechanisms. journal January 2002
Genomic Tools in Cowpea Breeding Programs: Status and Perspectives journal June 2016
Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection journal May 2017
Cowpea–Soybean Synteny Clarified through an Improved Genetic Map journal January 2011
Limitations to photosynthesis by proton motive force-induced photosystem II photodamage journal October 2016