Heritability of the structures and 13C fractionation in tomato leaf wax alkanes: a genetic model system to inform paleoenvironmental reconstructions

Leaf wax n-alkanes are broadly used to reconstruct paleoenvironmental information. However, the utility of n-alkanes as a paleoenvironmental proxy may be modulated by the extent to which biological as well as environmental factors influence the structural and isotopic variability of leaf waxes. In paleoclimate applications, there is usually an implicit assumption that most variation of leaf wax traits through a time series can be attributed to environmental change and that biological sources of variability within plant communities are small. For example, changes in hydrology affect the δ2H of waxes via rainwater and the δ13C of leaf waxes by changing plant communities. We measured the degree of genetic control over δ13C variation in leaf waxes within closely related species with an experimental greenhouse growth study. We measured the proportion of variability in structural and isotopic leaf wax traits that is attributable to genetic variation using a set of 76 introgression lines (ILs) between two interfertile Solanum (tomato) species: S. lycopersicum cv M82 (hereafter cv M82) and S. pennellii. Leaves of S. pennellii, a wild desert tomato relative, produced significantly more iso-alkanes than cv M82, a domesticated tomato cultivar adapted to water-replete conditions. We report a methylation index to summarize the ratio of branched (iso- and anteiso-) to total alkanes. Between S. pennellii and cv M82, the iso-alkanes were found to be enriched in 13C by 1.2–1.4‰ over n-alkanes. The broad-sense heritability values (H2) of leaf wax traits describe the degree to which genetic variation contributes to variation of these traits. Variation of individual carbon isotopic compositions of alkanes were of low heritability (H2 = 0.13–0.19), suggesting that most variation in δ13C of leaf waxes in this study can be attributed to environmental variance. This supports the interpretation that variation in the δ13C of wax compounds recorded in sediments reflects paleoenvironmental and vegetation changes. Average chain length (ACL) values of n-alkanes were of intermediate heritability (H2 = 0.30), suggesting that ACL values are more strongly influenced by genetic cues.

[1]  Jeffrey K. Conner,et al.  A Primer of Ecological Genetics , 2004 .

[2]  W. D'Andrea,et al.  Uncertainty in paleohydrologic reconstructions from molecular δD values , 2014 .

[3]  Geoffrey Eglinton,et al.  Leaf Epicuticular Waxes , 1967, Science.

[4]  M. Pagani,et al.  A 35 Myr North American leaf-wax compound-specific carbon and hydrogen isotope record: Implications for C4 grasslands and hydrologic cycle dynamics , 2010 .

[5]  G. Eglinton,et al.  Even carbon number predominance of plant wax n-alkanes: a correction , 2000 .

[6]  Marie E. Bolger,et al.  Identification of Enzyme Activity Quantitative Trait Loci in a Solanum lycopersicum × Solanum pennellii Introgression Line Population1[W][OA] , 2011, Plant Physiology.

[7]  P. deMenocal,et al.  A comparison of biomarker records of northeast African vegetation from lacustrine and marine sediments (ca. 3.40 Ma) , 2007 .

[8]  G. Haug,et al.  Strengthening of North American dust sources during the late Pliocene (2.7 Ma) , 2012 .

[9]  P. Kolattukudy,et al.  Plant waxes , 2006, Lipids.

[10]  Howard Griffiths,et al.  Carbon isotopes and water use efficiency: sense and sensitivity , 2008, Oecologia.

[11]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[12]  W. D'Andrea,et al.  Evidence for water use efficiency as an important factor in determining the δD values of tree leaf waxes , 2007 .

[13]  G. Farquhar,et al.  Biosynthetic and environmental effects on the stable carbon isotopic compositions of anteiso- (3-methyl) and iso- (2-methyl) alkanes in tobacco leaves. , 2008, Phytochemistry.

[14]  K. Mueller,et al.  Global patterns in leaf 13C discrimination and implications for studies of past and future climate , 2010, Proceedings of the National Academy of Sciences.

[15]  F. A. McInerney,et al.  The Paleocene-Eocene Thermal Maximum: A Perturbation of Carbon Cycle, Climate, and Biosphere with Implications for the Future , 2011 .

[16]  P. deMenocal,et al.  Biomarker records of late Neogene changes in northeast African vegetation , 2005 .

[17]  R. Pancost,et al.  12.15 – Biomarkers for Terrestrial Plants and Climate , 2013 .

[18]  R. Evershed,et al.  Variations in the stable carbon isotope compositions of individual lipids from the leaves of modern angiosperms: implications for the study of higher land plant-derived sedimentary organic matter , 1997 .

[19]  S. Boissinot,et al.  Evolutionary Biology , 2000, Evolutionary Biology.

[20]  S. Warnock.  Natural Habitats of Lycopersicon Species , 1991 .

[21]  Michael F. Covington,et al.  A Quantitative Genetic Basis for Leaf Morphology in a Set of Precisely Defined Tomato Introgression Lines[C][W][OPEN] , 2013, Plant Cell.

[22]  M. Simpson,et al.  Biomarker assessment of organic matter sources and degradation in Canadian High Arctic littoral sediments , 2010 .

[23]  T. Filley,et al.  Late Quaternary vegetation history of southeast Africa: The molecular isotopic record from Lake Malawi , 2009 .

[24]  J. Selbig,et al.  Mode of Inheritance of Primary Metabolic Traits in Tomato[W][OA] , 2008, The Plant Cell Online.

[25]  D. Zamir,et al.  An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. , 1995, Genetics.

[26]  T. Dawson,et al.  Molecular Paleohydrology: Interpreting the Hydrogen-Isotopic Composition of Lipid Biomarkers from Photosynthesizing Organisms , 2012 .

[27]  R. Jetter,et al.  Composition of Plant Cuticular Waxes , 2007 .

[28]  Kazuo Fukushima,et al.  Implications of long-chain anteiso compounds in acidic freshwater lake environments: Inawashiro-ko in Fukushima Prefecture, Japan , 2005 .

[29]  U. Roessner,et al.  Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement , 2006, Nature Biotechnology.

[30]  Stefan Schouten,et al.  Wet phases in the Sahara/Sahel region and human migration patterns in North Africa , 2009, Proceedings of the National Academy of Sciences.

[31]  F. A. McInerney,et al.  Leaf wax n-alkane distributions in and across modern plants: Implications for paleoecology and chemotaxonomy , 2013 .

[32]  James R. Ehleringer,et al.  Correlations between carbon isotope ratio and microhabitat in desert plants , 1988, Oecologia.

[33]  A. Diefendorf,et al.  Extracting the most from terrestrial plant-derived n-alkyl lipids and their carbon isotopes from the sedimentary record: A review , 2017 .

[34]  Zhonghua Wang,et al.  The fruit cuticles of wild tomato species exhibit architectural and chemical diversity, providing a new model for studying the evolution of cuticle function. , 2012, The Plant journal : for cell and molecular biology.

[35]  T. Juenger,et al.  The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana , 2013, Photosynthesis Research.

[36]  E. Candès,et al.  Controlling the false discovery rate via knockoffs , 2014, 1404.5609.

[37]  A. Fernie,et al.  Metabolic Profiling of a Mapping Population Exposes New Insights in the Regulation of Seed Metabolism and Seed, Fruit, and Plant Relations , 2012, PLoS genetics.

[38]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[39]  M. Pagani,et al.  δ13C and δD compositions of n-alkanes from modern angiosperms and conifers: An experimental set up in central Washington State, USA , 2008 .

[40]  B. E. Torkelson,et al.  A revised carbon preference index , 1993 .

[41]  S. Wing,et al.  Leaf wax composition and carbon isotopes vary among major conifer groups , 2015 .

[42]  J. Mudd,et al.  Epicuticular Lipid Accumulation on the Leaves of Lycopersicon pennellii (Corr.) D'Arcy and Lycopersicon esculentum Mill. , 1985, Plant physiology.

[43]  G. Eglinton,et al.  Composition, age, and provenance of organic matter in NW African dust over the Atlantic Ocean , 2002 .

[44]  F. A. McInerney,et al.  Influence of temperature and C4 abundance on n-alkane chain length distributions across the central USA , 2015 .

[45]  B. Schubert,et al.  The effect of atmospheric CO2 concentration on carbon isotope fractionation in C3 land plants , 2012 .

[46]  Marleen de Bruijne,et al.  A Genome-Wide Association Study Identifies Five Loci Influencing Facial Morphology in Europeans , 2012, PLoS genetics.

[47]  H. Graham,et al.  Production of n-alkyl lipids in living plants and implications for the geologic past , 2011 .

[48]  C. D. Kemp,et al.  Density Estimation for Statistics and Data Analysis , 1987 .

[49]  J. Ehleringer,et al.  Carbon Isotope Discrimination and Photosynthesis , 1989 .